Hormones and Reproduction of Vertebrates - Volume 4: Birds

Hormones and Reproduction Hormones and Reproduction Hormones and Reproduction Hormones and Reproduction Hormones and Re...

Author: David O. Norris | Kristin H. Lopez

169 downloads 1090 Views 7MB Size Report

This content was uploaded by our users and we assume good faith they have the permission to share this book. If you own the copyright to this book and it is wrongfully on our website, we offer a simple DMCA procedure to remove your content from our site. Start by pressing the button below!

Report copyright / DMCA form

DOWNLOAD PDF

Hormones and Reproduction Hormones and Reproduction Hormones and Reproduction Hormones and Reproduction Hormones and Reproduction

of Vertebrates, of Vertebrates, of Vertebrates, of Vertebrates, of Vertebrates,

Volume 1dFishes Volume 2dAmphibians Volume 3dReptiles Volume 4dBirds Volume 5dMammals

Hormones and Reproduction of Vertebrates Volume 4: Birds

David O. Norris Department of Integrative Physiology University of Colorado Boulder, Colorado

Kristin H. Lopez Department of Integrative Physiology University of Colorado Boulder, Colorado

AMSTERDAM BOSTON HEIDELBERG LONDON NEW YORK OXFORD PARIS SAN DIEGO SAN FRANCISCO SINGAPORE SYDNEY TOKYO Academic Press is an imprint of Elsevier

Academic Press is an imprint of Elsevier 32 Jamestown Road, London NW1 7BY, UK 30 Corporate Drive, Suite 400, Burlington, MA 01803, USA 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA First edition 2011 Copyright Ó 2011 Elsevier Inc. All rights reserved Cover images Front cover image: Amphiprion percula, the orange clownfish. Courtesy of iStockphoto: Image 6571184. Back cover image: Atlantic hagfish (Myxine glutinosa) eggs. Courtesy of Stacia A. Sower, University of New Hampshire, Durham, NH, USA and Scott I. Kavanaugh, University of Colorado, Boulder, CO, USA. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone (+44) (0) 1865 843830; fax (+44) (0) 1865 853333; email: [email protected]. Alternatively, visit the Science and Technology Books website at www.elsevierdirect.com/rights for further information. Notice No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made. British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library. Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress. ISBN: ISBN: ISBN: ISBN: ISBN: ISBN:

978-0-12-374932-1 978-0-12-375009-9 978-0-12-374931-4 978-0-12-374930-7 978-0-12-374929-1 978-0-12-374928-4

(Set) (Volume (Volume (Volume (Volume (Volume

1) 2) 3) 4) 5)

For information on all Academic Press publications visit our website at elsevierdirect.com Typeset by TNQ Books and Journals Pvt Ltd. www.tnq.co.in Printed and bound in United States of America 10 11 12 13 14 15 10 9 8 7 6 5 4 3 2 1

Dedication

Richard Evan Jones

This series of five volumes on the hormones and reproduction of vertebrates is appropriately dedicated to our friend and colleague of many years, Professor Emeritus Richard Evan Jones, who inspired us to undertake this project. Dick spent his professional life as a truly comparative reproductive endocrinologist who published many papers on hormones and reproduction in fishes, amphibians, reptiles, birds, and mammals. Additionally, he published a number of important books including The Ovary (Jones, 1975, Plenum Press), Hormones and Reproduction in Fishes, Amphibians, and Reptiles (Norris and Jones, 1987, Plenum Press), and a textbook, Human Reproductive Biology (Jones & Lopez, 3rd edition 2006, Academic Press). Throughout his productive career he consistently stressed the importance of an evolutionary perspective to understanding reproduction and reproductive endocrinology. His enthusiasm for these subjects inspired all with whom he interacted, especially the many graduate students he fostered, including a number of those who have contributed to these volumes.

v

Preface

Hormones and Reproduction of Vertebrates Preface to the Series Every aspect of our physiology and behavior is either regulated directly by hormones or modified by their actions, as exemplified by the essential and diverse roles of hormones in reproductive processes. Central to the evolutionary success of all vertebrates are the regulatory chemicals secreted by cells that control sexual determination, sexual differentiation, sexual maturation, reproductive physiology, and reproductive behavior. To understand these processes and their evolution in vertebrates, it is necessary to employ an integrated approach that combines our knowledge of endocrine systems, genetics and evolution, and environmental factors in a comparative manner. In addition to providing insight into the evolution and physiology of vertebrates, the study of comparative vertebrate reproduction has had a considerable impact on the biomedical sciences and has provided a useful array of model systems for investigations that are of fundamental importance to human health. The purpose of this series on the hormones and reproduction of vertebrates is to bring together our current knowledge of comparative reproductive endocrinology in one place as a resource for scientists involved in reproductive endocrinology and for students who are just becoming interested in this field. In this series of five volumes, we have selected authors with broad perspectives on reproductive endocrinology from a dozen countries. These authors are especially knowledgeable in their specific areas of interest and are familiar with both the historical aspects of their fields and the cutting edge of today’s research. We have intentionally included many younger scientists in an effort to bring in fresh viewpoints. Topics in each volume include sex determination, neuroendocrine regulation of the hypothalamuse pituitaryegonadal (HPG) axis, separate discussions of testicular and ovarian functions and control, stress and reproductive function, hormones and reproductive behaviors, and comparisons of reproductive patterns. Emphasis on the use of model species is balanced throughout the series with comparative treatments of reproductive cycles in major taxa.

Chemical pollution and climate change pose serious challenges to the conservation and reproductive health of wildlife populations and humans in the twenty-first century, and these issues must be part of our modern perspective on reproduction. Consequently, we have included chapters that specifically deal with the accumulation of endocrinedisrupting chemicals (EDCs) in the environment at very low concentrations that mimic or block the critical functions of our reproductive hormones. Many authors throughout the series also have provided information connecting reproductive endocrinology to species conservation. The series consists of five volumes, each of which deals with a major traditional grouping of vertebrates: in volume order, fishes, amphibians, reptiles, birds, and mammals. Each volume is organized in a similar manner so that themes can be easily followed across volumes. Terminology and abbreviations have been standardized by the editors to reflect the more common usage by scientists working with this diverse assembly of organisms we identify as vertebrates. Additionally, we have provided indices that allow readers to locate terms of interest, chemicals of interest, and particular species. A glossary of abbreviations used is provided with each chapter. Finally, we must thank the many contributors to this work for their willingness to share their expertise, for their timely and thoughtful submissions, and for their patience with our interventions and requests for revisions. Their chapters cite the work of innumerable reproductive biologists and endocrinologists whose efforts have contributed to this rich and rewarding literature. And, of course, our special thanks go to our editor, Patricia Gonzalez of Academic Press, for her help with keeping us all on track and overseeing the incorporation of these valuable contributions into the work. David O. Norris Kristin H. Lopez

xiii

Preface

Preface to Volume 4 Birds Birds are unique among vertebrates in that they are highly adapted for flight in terms of their anatomy, physiology, and behavior. Further, they are possibly the most visible vertebrate species to humans in being strongly diurnal, often brightly colored, and extremely easy to observe in their natural habitats. Consequently, birds have been a favorite target for biologists interested in studying the relationships among hormones, natural environmental factors, and reproduction in wild vertebrates. Distributed in a wide range of habitats globally, all birds are characterized physiologically by endothermy, internal fertilization, and obligate oviparity. Females produce relatively small numbers of large yolky eggs, and embryonic development generally requires elevated temperatures, provided by brooding. Thus, considerable parental care is involved in the successful reproduction of most bird species.

This avian volume on hormones and reproduction focuses both on bird species in wild populations and on captive birds, in which reproductive physiology and behavior may be studied relatively easily. We begin with a chapter on the neuroendocrine regulation of reproduction and follow with chapters on testicular and ovarian functions. Following is a discussion of the maternal role in determining the hormonal and nutrient composition of the egg and its significance for successful reproduction. Chapters on the hormones involved in stress, courtship and mating behavior, parental behavior, and migration and reproductive cycles represent the emphases of the study of bird reproduction over the past several decades. Finally, the importance of endocrine disruption in bird populations by anthropogenic chemicals is discussed.

xv

Contributors

Sarah J. Alger, University of Wisconsin, Madison, WI, USA

Moira McKernan

George E. Bentley, University of California at Berkeley, Berkeley,

Mary Ann Ottinger, University of Maryland, College Park, MD,

CA, USA

USA

Creagh W. Breuner, University of Montana, Missoula, MT, USA

Michael J. Quinn, Jr.

Karen Dean

Marilyn Ramenofsky, University of California, Davis, CA, USA

Pierre Deviche, Arizona State University, Tempe, AZ, USA

Takayoshi Ubuka, University of California at Berkeley, Berkeley,

H. Bobby Fokidis, Arizona State University, Tempe, AZ, USA

CA, USA

Ton G.G. Groothuis, University of Groningen, Haren,

Lauren V. Riters, University of Wisconsin, Madison, WI, USA

The Netherlands

Carol M. Vleck, Iowa State University, Ames, IA, USA

Laura L. Hurley, Arizona State University, Tempe, AZ, USA

David Vleck, Iowa State University, Ames, IA, USA

A.L. Johnson, The Pennsylvania State University, University Park,

Nikolaus von Engelhardt, University of Bielefeld, Bielefeld,

PA, USA

Germany

xvii

Chapter 1

Neuroendocrine Control of Reproduction in Birds Takayoshi Ubuka and George E. Bentley University of California at Berkeley, Berkeley, CA, USA

SUMMARY Reproductive physiology and behavior of birds are ultimately controlled by the hypothalamusehypophysial system. Hypothalamic neurons integrate internal and external signals, controlling reproduction by releasing neurohormones to the adenohypophysis (anterior pituitary). Reproductive activation occurs via gonadotropin-releasing hormone (GnRH) stimulation of adenohypophysial gonadotropin secretion. Gonadotropins (GTHs) (luteinizing hormone (LH), follicle-stimulating hormone (FSH)) act on the gonads to stimulate gametogenesis and sex steroid production. Gonadotropin-inhibiting hormone (GnIH) may inhibit gonadotropin secretion directly or indirectly by decreasing the activity of GnRH neurons. Another adenohypophysial hormone that plays an important role in avian reproduction is prolactin (PRL). The secretion of PRL is thought to be regulated by a hypothalamic neuropeptide, vasoactive intestinal peptide. Arginine vasotocin (AVT) is released from the neurohypophysis (posterior pituitary) and regulates oviposition by directly inducing uterine contraction. Several mechanisms are discussed in terms of how the brain perceives and translates external environmental information into internal hormonal signals to time seasonal reproduction.

1. INTRODUCTION Birds (class Aves) are bipedal, homeothermic oviparous vertebrate animals. Modern birdsdcomprising nearly 10 000 living speciesdare divided basally into two clades, Palaeognathae and Neognathae (Harshman, 2006). Palaeognathae includes the ratites (e.g. ostrich (Struthio camelus), emu (Dromaius novaehollandiae), and kiwis (Apteryx)) and tinamous. Neognathae is divided into Galloanserae and Neoaves. Galloanserae consist of the sister orders Anseriformes (e.g., ducks, geese, and swans) and Galliformes (e.g., turkeys, grouse, chickens, quail, and pheasants). Neoaves consist of 24 orders, including Columbiformes (pigeons, doves) and Passeriformes. Hormones and Reproduction of Vertebrates, Volume 4dBirds Copyright Ó 2011 Elsevier Inc. All rights reserved.

Passeriformes include all songbirds, and contain more than half of all bird species (Sibley & Monroe, 1990). Reproductive activities of birds consist of multiple stages in their life history. Typically, males establish territories after the initiation of gonadal maturation and form pairs with females. Male and female birds mature their gonads and engage in courtship, construct nests, and copulate, and female birds ovulate and lay eggs. After incubating their eggs, they feed nestlings and fledglings. Finally, the reproductive system regresses and the next life-history stage follows, e.g., molt (Wingfield et al., 1999). Many passerine species that breed at high latitudes incorporate two migratory periods between nonbreeding and breeding stages (Wingfield & Farner, 1980). Reproductive physiology and behavior of birds are governed by the hypothalamic (neuroendocrine) control of pituitary hormone secretion (hypothalamusepituitary system (HPS)). Accordingly, this chapter will start with a brief summary of the anatomy of the HPS and the neurohormones involved in avian reproduction. Gonadotropins (GTHs) (luteinizing hormone (LH), folliclestimulating hormone (FSH)) are important anterior pituitary hormones that control avian reproduction by inducing gametogenesis (spermatogenesis, oogenesis) and sex steroidogenesis (androgens, estrogens, progestogens) in the gonad. Accordingly, investigation of how the hypothalamic neurohormones control GTH secretion from the pituitary is imperative to understand the neuroendocrine control of reproduction. Two hypothalamic neuropeptides, gonadotropin-releasing hormone (GnRH) and gonadotropin-inhibitory hormone (GnIH), which have opposite effects on GTH secretion, will be introduced. Ovulation and egg-laying (oviposition) are highly orchestrated female reproductive actions that involve various hormones. Another hypothalamic neurohormone, arginine vasotocin (AVT), is released directly from the neurohypophysis and induces oviposition. After 1

2

oviposition, incubation of the eggs and feeding of the offspring are the typical next stages in avian life history. These parental behaviors seem to be controlled by another anterior pituitary hormone, prolactin (PRL). Hypothalamic vasoactive intestinal peptide (VIP) is thought to regulate PRL secretion from the anterior pituitary. Many birds reproduce seasonally. How do birds perceive and translate external environmental information into internal hormonal signals to time reproduction? If reproductive physiology and behavior of birds are ultimately controlled by the HPS, how does this system control seasonal reproductive activities of birds? Does the hypothalamus detect the external environmental signals itself, or are they detected by other organs and the information transduced to the hypothalamic neuronal system to control pituitary hormone secretion? These interesting topics will be discussed in Section 3. Finally, we will investigate the lines of research that will be necessary in the future to reveal a more complete picture of the neuroendocrine control mechanism of avian reproduction.

Hormones and Reproduction of Vertebrates

2. THE HYPOTHALAMUSePITUITARY SYSTEM (HPS) Reproductive activity of birds is controlled by the HPS. Hypothalamic neurons somehow integrate external (light, temperature, sound, etc.) and internal (water, nutrition, hormones, etc.) information, and regulate the reproductive physiology and behavior of the bird by releasing neurohormones to the pituitary. Figure 1.1 shows the generalized anatomical structure of the hypothalamus and pituitary in the avian brain (Stokes, Leonard, & Nottebohm, 1974; Foster, Plowman, Goldsmith, & Follett, 1987; Matsumoto & Ishii, 1992). Table 1.1 summarizes the molecular structures and the known functions of the identified key neurohormones that control reproduction in birds. The neuroendocrine system controlling reproduction of birds is summarized in Figure 1.2. Various neurohormones that seem to play important roles in reproduction, such as GnRH, GnIH, VIP, and AVT, are synthesized in the brain nuclei of the hypothalamus. Gonadotropin-releasing hormone, GnIH, and VIP are

FIGURE 1.1 Generalized anatomical structure of the hypothalamus and pituitary in the midsagittal section of the avian brain. The hypothalamus is in the anterior part of the diencephalon, which is located between the telencephalon and midbrain (MB) (inset). Neuronal cell bodies with a common function often cluster in specific brain nuclei in the hypothalamus. The pituitary gland consists of the anterior pituitary including the pars distalis (PD) and pars tuberalis (PT), and the posterior pituitary (pars nervosa (PN)). There is either no pars intermedia in the adult avian pituitary, or it is highly reduced (Norris, 2007). AHA, anterior hypothalamic area; AHP, posterior hypothalamic area; CA, anterior commissure; CO, optic chiasm; IN, infundibular nucleus; ME, median eminence; MM, medial mammillary nucleus; NIII, nervus oculomotorius; POD, dorsal preoptic nucleus; POM, medial preoptic area; PVN, paraventricular nucleus; PVO, paraventricular organ; SC, suprachiasmatic nucleus; TSM, septomesencephalic tract. Reconstructed from Stokes, Leonard, and Nottebohm (1974); Foster, Plowman, Goldsmith, and Follett (1987); Matsumoto and Ishii (1992).

Chapter | 1

3

Neuroendocrine Control of Reproduction in Birds

TABLE 1.1 Molecular structure and function of neurohormones controlling reproduction in birds Structure

Species

Function

aGnRH-I

pEHWSYGLQPG-NH2 (chicken, turkey, goose, dove, zebra finch, European starling)

Chicken (King & Millar, 1982; Miyamoto et al., 1982; Dunn et al., 1993); turkey (Kang et al., 2006); goose (Huang et al., 2008); dove (Mantei et al., 2008); zebra finch (Stevenson et al., 2009; Ubuka & Bentley, 2009); European starling (Sherwood et al., 1988; Stevenson et al., 2009; Ubuka et al., 2009)

Stimulation of LH and FSH release (Millar & King, 1983; Hattori et al., 1985)

aGnRH-II

pEHWSHGWYPG-NH2 (chicken)

Chicken (Miyamoto et al., 1984)

Stimulation of LH and FSH release (Hattori et al., 1986); stimulation of copulation solicitation (Maney et al., 1997b)

GnIH

SIRPSAYLPLRF-NH2 (chicken); SIKPSAYLPLRF-NH2 (quail); SIKPFSNLPLRF-NH2 (white-crowned sparrow, zebra finch); SIKPFANLPLRFNH2 (European starling)

Quail (Tsutsui et al., 2000; Satake et al., 2001); white-crowned sparrow (Osugi et al., 2004); zebra finch (Tobari et al., 2010); European starling (Ubuka et al., 2008a)

Inhibition of LH and FSH release (Tsutsui et al., 2000; Ciccone et al., 2004; Osugi et al., 2004; Bentley et al., 2006; Ubuka et al., 2006); inhibition of copulation solicitation (Bentley et al., 2006)

VIP

HSDAVFTDNYSRFRKQMAVKKYLNSVLTNH2 (chicken, turkey)

Chicken (Nilsson, 1975; Talbot et al., 1995); turkey (You et al., 1995)

Stimulation of PRL release (Macnamee et al., 1986; Opel & Proudman, 1988; Proudman & Opel, 1988)

AVT

CYIQNCPRG-NH2 (chicken, goose, turkey, ostrich)

Chicken (Acher et al., 1970); goose (Acher et al., 1970); turkey (Acher et al., 1970); ostrich (Rouille´ et al., 1986)

Induction of oviposition (Shimada et al., 1986; Saito & Koike, 1992); stimulation of sexual behavior (Kihlstro¨m & Danninge, 1972; Maney et al., 1997a; Castagna et al., 1998; Goodson, 1998a; 1998b; Goodson & Adkins-Reagan, 1999)

FSH, follicle-stimulating hormone; LH, luteinizing hormone; PRL, prolactin.

thought to be transmitted through neuronal axons and released into the portal vessels in the median eminence (ME). Other mechanisms may exist to orchestrate the actions of various neurohormones, such as direct interactions of neurohormones in the hypothalamus. Neurohormones released at the ME are directly conveyed to the anterior pituitary (adenohypophysis) in the blood and stimulate or inhibit anterior pituitary hormone secretion. Six adenohypophysial hormones have been identified in birds: LH, FSH, PRL, thyrotropin (TSH), corticotropin (ACTH), and growth hormone (GH) (Scanes, 1986). Hypothalamic neurohormones, such as AVT and mesotocin (MST), which are produced in magnocellular neurons in the hypothalamus, are transmitted through their axons and released at the neural lobe of the pituitary, which is called the posterior pituitary or pars nervosa (Oksche & Farner, 1974). Anterior pituitary hormones and hypothalamic neurohormones, which are released at the posterior pituitary, travel in the general circulation and regulate the physiology and behavior of the bird.

3. MECHANISMS AND PATHWAYS REGULATING GONADOTROPIN (GTH) SECRETION 3.1. Gonadotropin-releasing Hormone (GnRH) Reproductive activities of vertebrates are primarily regulated by hypothalamic GnRHs. This decapeptide was originally isolated from mammals (Matsuo, Baba, Nair, Arimura, & Schally, 1971; Burgus et al., 1972) and subsequently from chickens (King & Millar, 1982; Miyamoto et al., 1982). The molecular structure of the originally isolated mammalian GnRH (mGnRH-I) is pEHWSYGLRPG-NH2. Chicken GnRH-I (cGnRH-I) (pEHWSYGLQPG-NH2) differs by one amino acid from mGnRH-I in that glutamine is substituted for arginine at position eight. Specific genes encoding the same cGnRH-I peptide have been identified by cDNA cloning in Galliformes (chicken, quail, turkey) (Dunn, Chen, Hook, Sharp, &

4

Hormones and Reproduction of Vertebrates

FIGURE 1.2 The neuroendocrine system controlling reproduction of birds. Environmental information, such as light, food availability, predation pressure, and social interactions, are perceived by the brain. Hypothalamic neurohormones integrate external and internal signals to Thyroid Stress control pituitary function. The activity of gonadotropinMelatonin hormone hormone inhibiting hormone (GnIH) is likely to be stimulated by the action of melatonin and stress. Gonadotropin-inhibiting hormone may suppress reproductive activities of Brain birds by directly inhibiting gonadotropin (GTH) (luteinizing hormone (LH) and follicle-stimulating hormone (FSH)) secretion from the pars distalis (PD), or by GnIH aGnRH-I aGnRH-II inhibiting the actions of avian gonadotropin-releasing hormone (aGnRH-I and aGnRH-II) neurons. The stimBiological AVT ulatory action of aGnRH-I on GTH secretion may be clock accelerated by the action of triiodothyronine (T3) on the reduction of glial processes encasing aGnRH-I nerve T4 VIP terminals at the median eminence. Triiodothyronine is converted from thyroxine (T4) by the action of DII, which DII is induced by thyrotropin (TSH). Thyrotropin is syntheT3 sized in the pars tuberalis (PT) by photostimulation. LH TSH PRL Gonadotropins act on the gonads to induce steroidogenFSH esis and gametogenesis. Sex steroids act on various PT PD PD PN organs including the brain to organize and activate sex characteristics. Ovulation in females seems to occur by Sexual behavior the synergistic actions of progesterone (P4), aGnRH-I, Aggression Gonads and LH. Cell bodies containing aGnRH-II are found in Courtship Sex steroid the midbrain. It is more likely that aGnRH-II regulates Copulation synthesis, release sexual behavior rather than stimulating GTH secretion. Spermatogenesis The neurohypophysial hormone arginine vasotocin Oviposition Oogenesis (AVT) produced in magnocellular neurons is released Ovulation Parental behavior from the pars nervosa (PN) to induce oviposition. ParIncubation vocellular AVT neurons are likely to regulate various Feeding male sexual behaviors. Vasoactive intestinal peptide (VIP) is released at the median eminence (ME) to stimulate prolactin (PRL) release from the PD. Prolactin induces parental behaviors, such as incubation and feeding of the young. The seasonal reproductive cycle of birds is initiated by the interactions of biological clocks and neurohormones, the actions of which are modified by various external and internal signals.

Environmental information (light, food availability, predation pressure etc.) Social interactions (sight, sound, contact etc.)

Sang, 1993; Kang et al., 2006), Anseriformes (goose, duck) (Huang, Shi, Z. Liu, Y. Liu, & Li, 2008), and Columbiformes (dove) (Mantei, Ramakrishnan, Sharp, & Buntin, 2008). Although the existence of the same cGnRH-I peptide was unknown in passerine birds for a long time, the mRNA encoding cGnRH-I was recently identified in zebra finches (Ubuka & Bentley, 2009; Stevenson, Lynch, Lamba, Ball, & Bernard, 2009) and in European starlings (Ubuka, Cadigan, Wang, Liu, & Bentley, 2009; Stevenson et al., 2009). The expression of cGnRH-I peptide in songbirds also has been suggested from its high-performance liquid chromatography (HPLC) elution pattern and its cross-reactivity with various GnRH antisera (Sherwood, Wingfield, Ball, & Dufty, 1988). Accordingly, cGnRH-I could be called avian GnRH-I (aGnRH-I) and we will use this naming in this chapter. There is a second form of GnRH, which is called chicken GnRH-II (cGnRH-II). Chicken GnRH-II was first found in chickens and subsequently in mammals (Miyamoto et al., 1984; King, Mehl, Tyndale-Biscoe, Hinds, & Millar, 1989; Morgan & Millar, 2004; Millar, 2005) and eventually in all vertebrate groups

(Norris, 2007; see also Volume 1, Chapter 2; Volume 2, Chapter 2; Volume 5, Chapter 2). The structure of cGnRHII (pEHWSHGWYPG-NH2) differs by three amino acids from mGnRH-I or aGnRH-I at positions five, seven, and eight. We will also refer to cGnRH-II as avian GnRH-II (aGnRH-II) to be consistent with the naming of aGnRH-I. Note that aGnRH-I and -II were formerly named cGnRH-I and -II, respectively. Specific antibodies against avian GnRH peptides (aGnRH-I and aGnRH-II) have been made, and the histological localization of aGnRHs has been studied in the chicken and quail (Mikami, Yamada, Hasegawa, & Miyamoto, 1988; Van Gils et al., 1993). In mammals, the GnRHI neurons originate at the olfactory placode and migrate to preoptic-septal nuclei during embryonic development (Wray, Grant, & Gainer, 1989; Schwanzel-Fukuda & Pfaff, 1989). The migration of aGnRH-I neurons from the olfactory placode to the forebrain along the olfactory nerve also has been observed in chickens (Norgren & Lehman, 1991; Akutsu, Takada, Ohki-Hamazaki, Murakami, & Arai, 1992; Yamamoto, Uchiyama, Ohki-Hamazaki, Tanaka, &

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

Ito, 1996). In adult birds, aGnRH-I-immunoreactive (-ir) cell bodies are found in a fairly wide area covering the hypothalamic preoptic area (POA) to the thalamic region. On the other hand, magnocellular aGnRH-II-ir cell bodies were found in the area dorsomedial to the nervus oculomotorius in the midbrain. Fibers immunoreactive for aGnRH-I or aGnRH-II were widely distributed in the telencephalon, diencephalon, and mesencephalon (midbrain). In sharp contrast to the existence of abundant aGnRH-I-ir fibers in the external layer of the ME, aGnRHII-ir fibers were absent or less prominent in this area, suggesting that the major GnRH controlling pituitary function is aGnRH-I (Mikami et al., 1988; Van Gils et al., 1993). Specific radioimmunoassays (RIAs) for chicken LH (Follett, Scanes, & Cunningham, 1972), turkey LH (Burke, Licht, Papkoff, & Bona-Gallo, 1979), and chicken FSH (Scanes, Godden, & Sharp, 1977; Sakai & Ishii, 1980) have been developed and used to measure the effect of GnRH on GTH release. The action of aGnRH-I on LH release from chicken anterior pituitary cells was first shown in vitro (Millar & King, 1983). Subsequently, the activities of aGnRH-I on LH and FSH release was shown both in vivo and in vitro in quail (Hattori et al., 1985). The activity of aGnRH-I on LH release was more marked than that on FSH release both in vivo and in vitro (Hattori et al., 1985). The activity of aGnRH-II (Miyamoto et al., 1984) on LH and FSH release was also shown in vivo and in vitro (Hattori, Ishii, & Wada, 1986). The activity of aGnRH-II on LH and FSH release was almost equal to that of aGnRH-I. Again, the activity of aGnRH-II on LH release was more marked than on FSH release both in vivo and in vitro. No synergism was observed between aGnRH-I and aGnRH-II on LH or FSH release in vitro (Hattori et al., 1986). The physiological roles of aGnRH-I and aGnRH-II on LH release also have been investigated in chickens (Sharp et al., 1990). Egg laying of somatically mature hens is regulated by strain differences and environmental conditions. As ovulation is controlled by the preovulatory LH surge (as described in Section 4.1), the activity of GnRH may be higher in laying hens. The amount of aGnRH-I in the ME was higher in laying than in out-of-lay hens, as measured by RIA. Avian GnRH-II was not detected in the ME. The amount of aGnRH-I in the hypothalamus increased in cockerels at the onset of puberty, but the amount of aGnRH-II did not change. Active immunization of laying hens against aGnRH-I but not against aGnRH-II resulted in the complete regression of the reproductive system. Accordingly, it was concluded that GTH secretion in chickens is more likely to be controlled by aGnRH-I (Sharp et al., 1990). On the other hand, aGnRH-II may be involved in the control of sexual behaviors in various animals (Millar, 2003). Indeed aGnRH-II, but not aGnRH-I, administered to the brain increased copulation

5

solicitation display, a female courtship behavior, in female white-crowned sparrows (Maney, Richardson, & Wingfield, 1997). Three GnRH receptor (GnRH-R) subtypes (types I, II, and III) have been identified, each with distinct distributions and functions in vertebrates (Millar et al., 2004). These receptor subtypes belong to the G-protein-coupled receptor (GPCR) superfamily. Two receptor subtypes have been identified in chickens: type I (GnRH-R-I) (Sun et al., 2001a; 2001b) and type III (GnRH-R-III) (Shimizu & Be´de´carrats, 2006), according to the classification by Millar et al. (2004). GnRH-R-I is widely expressed, and aGnRH-II has a higher binding affinity to this receptor and is more potent in stimulating accumulation of inositol trisphosphate, a secondary messenger molecule that can induce GTH release, than aGnRH-I (Sun et al., 2001a; 2001b). Inositol trisphosphate accumulation in response to aGnRH-II binding to GnRH-R-III was also more marked than in response to aGnRH-I. As fully processed GnRH-RIII mRNA was exclusively expressed in the pituitary, and its mRNA level was positively correlated with reproductive states in both sexes, it is likely that GnRH-R-III plays a role in the regulation of GTH secretion by pituitary gonadotropes (Shimizu & Be´de´carrats, 2006). Despite the implication here that aGnRH-II is more effective in regulation of gonadotrope function, the current opinion is that aGnRH-I, and not aGnRH-II, is the dominant regulator of GTH release.

3.2. Gonadotropin-inhibiting Hormone (GnIH) A hypothalamic neuropeptide, GnIH, has been found to be an inhibiting factor for LH release from the quail anterior pituitary (Tsutsui et al., 2000). Gonadotropin-inhibiting hormone-ir neuronal cell bodies are located in the paraventricular nucleus (PVN) in quail (Ubuka, Ueno, Ukena, & Tsutsui, 2003; Ukena, Ubuka, & Tsutsui, 2003). These neurons project to the ME, thus providing a functional anatomical infrastructure that regulates anterior pituitary function. A cDNA encoding the GnIH precursor polypeptide has been cloned from the brains of quail (Satake et al., 2001), white-crowned sparrows (Osugi et al., 2004), European starlings (Ubuka et al., 2008a), and zebra finches (Tobari et al., 2010). The expression of GnIH precursor mRNA also has been observed in the PVN of these birds. Gonadotropin-inhibiting hormone homologs are present in the brains of other vertebrates, such as mammals, amphibians, and fishes (Tsutsui & Ukena, 2006; Fukusumi, Fujii, & Hinuma, 2006). These peptides, categorized as RFamide-related peptides (RFRPs), possess a characteristic LPXRF-amide (X ¼ L or Q) motif at their C-termini in all vertebrates tested. Three LPXRF-amide (X ¼ L or Q)

6

peptide sequences are encoded in the GnIH precursor polypeptide, designated GnIH-related peptide-1 (GnIH-RP1), GnIH, and GnIH-RP-2. Quail GnIH (SIKPSAYLPLRFamide), quail GnIH-RP-2 (SSIQSLLNLPQRF-amide), starling GnIH (SIKPFANLPLRF-amide), and zebra finch GnIH (SIKPFSNLPLRF-amide) have been identified as mature endogenous peptides by mass spectrometric analyses (Satake et al., 2001; Ubuka et al., 2008a, Tobari et al., 2010). The receptor for quail GnIH has been identified and its binding activities have been investigated (Yin, Ukena, Ubuka, & Tsutsui, 2005). Structural analysis of the quail GnIH receptor revealed that it belongs to the GPCR superfamily. A crude membrane fraction of COS-7 cells transfected with the quail GnIH receptor cDNA specifically bound GnIH, GnIH-RP-1, and GnIH-RP-2 in a concentration-dependent manner. The identified quail GnIH receptor mRNA was expressed in the pituitary as well as in various parts of the brain. The mammalian homolog of GnIH receptor is GPR147 (OT7T022, NPFF-1), and the mechanism of RFRP action on mammalian cellular events has been investigated (Fukusumi et al., 2006). RFamide-related peptides suppressed the production of cyclic-3’,5’-adenosine monophosphate (cAMP) in Chinese hamster ovarian cells transfected with GPR147, suggesting that the receptor couples to the a-subunit of the inhibitory G-protein (Gai). GPR147 mRNA is also expressed in various parts of the mammalian brain as well as in the pituitary, suggesting that there are multiple actions of GnIH within the central nervous system (Hinuma et al., 2000). The actual release of GnIH into the hypothalamusehypophysial portal system has not been reported in any vertebrate. However, the dense population of GnIH-ir fibers in the ME in quail (Tsutsui et al., 2000; Ubuka et al., 2003; Ukena et al., 2003), house sparrows and song sparrows (Bentley, Perfito, Ukena, Tsutsui, & Wingfield, 2003), and European starlings (Ubuka et al., 2008a) suggests a role for GnIH in the regulation of pituitary function, at least in these birds. The same is true for white-crowned sparrows. The fact that GnIH inhibits release of GTHs from cultured quail and chicken anterior pituitary provides strong support for this function (Tsutsui et al., 2000; Ciccone et al., 2004). Gonadotropin-inhibitory hormone administration to cultured chicken anterior pituitary inhibits not only the release of GTHs but also the synthesis of GTH subunit mRNAs (Ciccone et al., 2004). Nevertheless, direct regulation of pituitary function by GnIH may be regulated in a different way in some bird species either developmentally or temporally because there is no apparent GnIH-ir material in the ME in adult male Rufous-winged sparrows (Small et al., 2008), although GnIH receptor is expressed in the pituitary gland in this species (McGuire, Ubuka, Perfito, & Bentley, 2009). In other words, GnIH may directly inhibit pituitary function only during certain periods before sexual maturation or in response to stress, as described in Section 7.

Hormones and Reproduction of Vertebrates

To clarify the functional significance of GnIH in the control of avian reproduction, Ubuka, Ukena, Sharp, Bentley, and Tsutsui (2006) investigated the action of GnIH on the hypothalamicepituitaryegonadal (HPG) axis in male quail. It is generally accepted that in avian species LH stimulates the formation of testosterone (T) by Leydig cells. Follicle-stimulating hormone and T stimulate growth, differentiation, and spermatogenetic activity of the testis (Follett, 1984; Johnson, 1986). Luteinizing hormone is a protein complex, which is made of GTH common a and LHb subunits, whereas FSH is a complex of GTH common a and FSHb subunits. Peripheral administration of GnIH to mature quail via osmotic pumps for two weeks decreased the expression of GTH common a and LHb subunit mRNAs in the pituitary. Concentrations of plasma LH and T were also decreased dose-dependently. Further, administration of GnIH to mature birds induced testicular apoptosis and decreased spermatogenetic activity in the testis. In immature birds, daily administration of GnIH for two weeks suppressed testicular growth and the rise in the concentration of plasma T. An inhibition of molt by juveniles also occurred after GnIH administration. These results show that GnIH may inhibit gonadal development and maintenance and also sexual development of birds by decreasing the synthesis and release of GTHs (Ubuka et al., 2006). Although a dense population of GnIH neuronal cell bodies was found only in the PVN, GnIH-ir fibers were widely distributed in the diencephalic and mesencephalic regions in the Japanese quail (Ukena et al., 2003). Thus, it was hypothesized that GnIH may participate not only in the regulation of pituitary function, but also in behavioral and autonomic mechanisms. Immunohistochemical studies using light and confocal microscopy indicate that GnIH-ir axon terminals are in probable contact with aGnRH-I neurons in birds (Bentley et al., 2003). Thus, there is potential for the direct regulation of aGnRH-I neurons by GnIH neurons. Recently, Ubuka et al. (2008a) investigated the interaction of GnIH and aGnRH-I neurons in the European starling brain. Double-label immunocytochemistry showed GnIH axon terminals on aGnRH-I and aGnRH-II neurons (Bentley et al., 2003; Ubuka et al., 2008a). Further, in-situ hybridization of European starling GnIH receptor mRNA combined with immunocytochemistry of aGnRHs showed the expression of GnIH receptor mRNA in both aGnRH-I and aGnRH-II neurons (Ubuka et al., 2008a). Central administration of GnIH inhibits the release of GTHs in white-crowned sparrows (Bentley et al., 2006a) in a manner similar to peripheral administration of GnIH (Osugi et al., 2004; Ubuka et al., 2006). Accordingly, GnIH may inhibit the secretion of GTHs by decreasing aGnRH-I neuronal activity in addition to regulating the release of pituitary GTHs directly. Central administration of GnIH also inhibits reproductive behavior of females in white-crowned sparrows

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

(Bentley et al., 2006a). It is known that aGnRH-II enhances copulation solicitation in estrogen-primed female whitecrowned sparrows exposed to male song (Maney et al., 1997b). As a result of the putative contact of GnIH neurons with aGnRH-II neurons in white-crowned sparrows (Bentley et al., 2003), Bentley et al. (2006a) investigated the effect of GnIH on copulation solicitation in females of this species. Centrally administered GnIH inhibited copulation solicitation in estrogen-primed female whitecrowned sparrows exposed to the song of males without affecting locomotor activity. The result suggests that GnIH inhibits reproductive physiology and behavior not only by inhibiting the secretion of GTHs from the pituitary but also by directly inhibiting aGnRH-I and -II neuronal activity within the brain (Ubuka, McGuire, Calisi, Perfito, & Bentley, 2008). Many hormones that are classified as neuropeptides are synthesized in vertebrate gonads in addition to the brain. Recently, GnIH and its receptor were found to be expressed in the gonads and accessory reproductive organs in Passeriformes and Galliformes (Bentley et al., 2008). Immunocytochemistry detected GnIH peptide in ovarian thecal and granulosa cells, testicular interstitial cells and germ cells, and pseudostratified columnar epithelial cells in the epididymis. Binding sites for GnIH were initially identified using in-vivo and in-vitro receptor fluorography, and were localized in ovarian granulosa cells as well as in the interstitial layer and seminiferous tubules of the testis. Insitu hybridization of GnIH-R mRNA in testes produced a strong reaction product that was localized to the germ cells and interstitium. In the epididymis, the product was also localized in the pseudostratified columnar epithelial cells. Similar data have been gathered from chickens, and estradiol (E2) and/or progesterone (P4) treatment of sexually immature chickens significantly decreased ovarian GnIH-R mRNA abundance (Maddineni, Oco´n-Grove, Krzysik-Walker, Hendricks, Ramachandran, 2008). Further, GnIH decreased LH-induced T release from cultured dispersed testis (McGuire et al., 2009). The distributions and action of GnIH and its receptor suggest a role for GnIH in autocrine/paracrine regulation of gonadal steroid production and possibly germ cell differentiation and maturation in birds.

4. MECHANISMS AND PATHWAYS REGULATING OVULATION AND OVIPOSITION 4.1. Regulation of Ovulation A hierarchy of developing follicles exists in the ovary of birds, and the largest follicle is ovulated at regular intervals. Many birds normally lay one egg each day during the breeding season. They usually lay two to ten eggs (two to

7

ten days) in a sequence (clutch), but the actual number varies greatly among species. Between the clutches there are one or more pause days. Generally clutch size is smaller and the interval between eggs is longer in species producing large eggs. Many birds lay a fixed number of eggs in a clutch (determinate layers), but others can continue laying for long periods (indeterminate layers) (Follett, 1984). Clutch size also tends to increase with latitude (Ricklefs, 1970). In domestic chickens, ovulation occurs six to eight hours after the preovulatory LH surge and the egg spends about 24 hours in the oviduct before it is laid. The next ovulation occurs 15 to 75 minutes after the oviposition, except after the last oviposition in a clutch. As a result of this temporal relationship, the time of oviposition is a practical index of the time of ovulation. Under lightedark cycles of 14L : 10D, chickens usually lay their eggs in the first half of the photophase whereas quail lay late in the day and early in the night. In both cases, the preovulatory surge of LH occurs six hours plus one day before the egg is laid. Under continuous light, the oviposition rhythms are freerunning, and egg laying occurs throughout the 24 hours (Warren & Scott, 1936; Morris, 1961; Wilson & Cunningham, 1981). Normally, the lightedark cycle entrains the rhythm, with dusk being the primary cue in chickens (Bhatti & Morris, 1978a; 1978b) and dawn in Japanese quail (Tanabe, 1977). Other factors such as feeding, temperature changes, and bright/dim light are capable of entrainment when hens are illuminated constantly (Morris & Bhatti, 1978). Ovulation depends on a surge of LH four to eight hours earlier, as determined by studies employing injection of LH or GnRH in intact birds or hypophysectomy (Fraps, 1970; Van Tienhoven & Schally, 1972). A surge in plasma LH occurs four to eight hours before ovulation in chickens (Wilson & Sharp, 1973; Etches & Cunningham, 1977), turkeys (Mashaly, Birrenkott, El-Begearmi, & Wentworth, 1976), and quail (Tanabe, 1977), and presumably other species. A constant relationship of about 30 hours exists between the peak of LH and the resulting oviposition, and the LH peak is absent on the last day of a sequence. Plasma FSH shows only minor changes during the ovulatory cycle (Scanes et al., 1977), although there is a small increase 14 to 15 hours before ovulation. Prolactin levels appear to be inversely related to LH (Scanes, Chadwick, & Bolton, 1976). As P4, but not estrogens, can induce premature ovulation in the hen, Fraps (1955; 1970) proposed that P4 triggers the preovulatory LH surge by a positive feedback mechanism. A single major peak of P4 coincides with that of LH (Furr, Bonney, England, & Cunningham, 1973; Senior & Cunningham, 1974; Etches & Cunningham, 1977). This peak is delayed by two to three hours each day in a laying sequence and is absent when no ovulation takes place.

8

A preovulatory peak of E2 occurs with that of LH but ovulation can take place in its absence (Lague¨, Van Tienhoven, & Cunningham, 1975). The effects of various steroids on the LH surge and ovulation have been tested. Progesterone almost always triggers an LH surge that begins 15 to 45 minutes after intramuscular injection, peaks within two hours, and lasts for about six hours. Gonadotropin-releasing hormone seems to relay the effect of P4 on the LH surge, because anti-GnRH antibody administration blocks the effect of P4 (Fraser & Sharp, 1978). Intrahypothalamic injections of P4 also trigger ovulation (Ralph & Fraps, 1960). In summary, the P4 surge appears to be important for initiating ovulation. The ovulated egg is captured by the ostium of the oviduct. Fertilization and deposition of the first layer of albumen occur here. The ovum passes down the oviduct through highly differentiated regions that have specific functions. Further albumen is laid down in the magnum, and membranes surround the developing egg in the isthmus. On reaching the shell gland (also known as the uterus), a shell and pigment are deposited (Solomon, 1983). Finally, oviposition occurs through the vagina and cloaca. Note that since there is only one ovary and one oviduct, further ovulations cannot occur unless oviposition has occurred (Sharp, 1980).

4.2. Regulation of Oviposition Oviposition means expulsion of the egg from the oviduct to the external environment and is a common phenomenon in vertebrates other than eutherian mammals. Avian oviposition is thought to be regulated by a neurohypophysial hormone, AVT, together with ovarian hormones and prostaglandins (PGs) through the induction of uterine contractions (Munsick, Sawyar, & Van Dyke, 1960; Rzasa & Ewy, 1970; Hertelendy, 1972; Wechsung & Houvenaghel, 1976; Olson, Biellier, & Hertelendy, 1978; Toth, Olson, & Hertelendy, 1979; Takahashi, Kawashima, Kamiyoshi, & Tanaka, 1992). Regulation of oviposition by the sympathetic nervous system using galanin as a neurotransmitter seems to exist in quail (Li, Tsutsui, Muneoka, Minakata, & Nomoto, 1996; Tsutsui, Azumaya, Muneoka, Minakata, & Nomoto, 1997; Tsutsui, Li, Ukena, Kikuchi, & Ishii, 1998; Sakamoto et al., 2000). The expression of galanin in the sympathetic ganglia is regulated by ovarian sex steroids (Ubuka, Sakamoto, Li, Ukena, & Tsutsui, 2001). The neurohypophysial hormones AVT and MST represent the nonmammalian homologs to arginine vasopressin and oxytocin, respectively (Acher, Chauvet, & Chauvet, 1970). However, in birds, the oxytocic effect of AVT is greater than that of MST (Saito & Koike, 1992; Barth et al., 1997). Plasma AVT increases sharply at the time of oviposition to induce uterine contraction (Nouwen et al., 1984; Tanaka, Goto, Yoshioka, Terao, & Koga, 1984;

Hormones and Reproduction of Vertebrates

Shimada, Neldon, & Koike, 1986) and decreases within 30 minutes of an egg being laid (Koike, Shimada, & Cornett, 1988). Elevation of plasma AVT at the time of oviposition is accompanied by a depletion of AVT concentration in the neurohypophysis (Sasaki, Shimada, & Saito, 1998). Magnocellular neurons producing AVT are found in the preoptic nucleus, the supraoptic nucleus, and the PVN of the hypothalamus. A sexually dimorphic population of parvocellular AVT neurons is observed from the mediocaudal part of the preoptic region to the dorsolateral part of the bed nucleus of stria terminalis in male birds, suggesting a role in the control of male sexual behaviors (Jurkevich & Grossmann, 2003). Effects of AVT on various male reproductive behaviors, such as aggressive and courtship behaviors, including song production, have been documented (Kihlstro¨m & Danninge, 1972; Maney, Goode, & Wingfield, 1997; Castagna, Absil, Foidart, & Balthazart, 1998; Goodson, 1998a; 1998b; Goodson & Adkins-Regan, 1999). There is also a role for AVT, along with corticotropin-releasing hormone (CRH), in ACTH release from the anterior pituitary (Castro, Estivariz, & Iturriza, 1986; Romero, Soma, & Wingfield, 1998; Madison, Jurkevich, & Kuenzel, 2008).

5. MECHANISMS AND PATHWAYS REGULATING PROLACTIN (PRL) SECRETION A period of egg incubation occurs in the vast majority of birds (Drent, 1975). Brood patches develop in virtually all birds and seem to be used to transfer body heat to the eggs. The changes in the brood pouch skin are substantial, involving hyperplasia of the epidermis, an edema leading to wrinkling of the skin, and extra vascularization. The whole process is thought to be controlled by a synergism between PRL and the sex steroids (Jones, 1971; Drent, 1975). Estrogens and P4 are the active agents in the female, but where males incubate these are replaced by androgens. Injections of PRL induce chickens to incubate eggs (Riddle, Bates, & Lahr, 1935; Sharp, Macnamee, Sterling, Lea, & Pedersen, 1988), and maintain readiness of ring doves to incubate their clutches (Lehrman & Brody, 1964; Janik & Buntin, 1985). In species that hatch precocial young, PRL levels rise slightly during egg-laying, but then increase markedly throughout incubation and fall immediately when the chicks have hatched. In female birds that fail to incubate, as well as in males, PRL never rises above baseline concentrations (mallards (Goldsmith & Williams, 1980)). In species that produce altricial young, PRL is also very high during incubation but it often stays high whilst the young are fed in the nest (canary (Goldsmith, 1982)). In ring doves and other Columbiformes, PRL causes growth of the crop gland and production of crop milk for feeding of

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

young for the first few days after hatch. In these birds, plasma levels of PRL do not rise during egg-laying and the early part of incubation but are high at the end of incubation and when the squabs are being fed (Goldsmith, Edwards, Koprucu, & Silver, 1981). It has been suggested that in female turkeys the action of PRL on incubation behavior is facilitated by the combined action of E2 and P4 (El Halawani, Silsby, Behnke, & Fehrer, 1986). In birds, PRL secretion is actively stimulated by release of VIP from the ME. Mammalian VIP specifically stimulated PRL release in vivo and in vitro in bantam hens (Macnamee, Sharp, Lea, Sterling, & Harvey, 1986) and turkeys (Opel & Proudman, 1988; Proudman & Opel, 1988), while immunohistochemical studies showed the presence of VIP-ir nerve terminals in the ME in quail (Yamada, Mikami, & Yanaihara, 1982), bantam hens (Macnamee et al., 1986), and pigeons (Pe´czely & Kiss, 1988). The structure of hypothalamic chicken and turkey VIP is regarded as the same as that isolated from the chicken gut, which is a 28amino-acid peptide differing from mammalian VIP in four amino acids (Nilsson, 1975). Both chicken and turkey VIP cDNAs have been sequenced (Talbot, Dunn, Wilson, Sang, & Sharp, 1995; You, Silsby, Farris, Foster, & El Halawani, 1995). Immunization against VIP inhibits PRL secretion in bantam hens (Sharp, Sterling, Talbot, & Huskisson, 1989) and turkeys (El Halawani, Pitts, Sun, Silsby, & Sivanandan, 1996). Daily injections of anti-VIP caused incubating bantam hens to desert their nests. On the other hand, disruption of incubation behavior with anti-VIP was prevented by concomitant administration of ovine PRL (Sharp et al., 1989). The amount of VIP was significantly higher in the ME and cell bodies in the medial basal hypothalamus in incubating as compared to actively laying hens (Sharp et al., 1989). Vasoactive intestinal peptide mRNA and peptide levels were low in nonphotostimulated turkeys, higher in laying hens, and highest in incubating hens. Changes in VIP paralleled the changes in plasma PRL levels (Chaiseha, Tong, Youngren, & El Halawani, 1998). Dopaminergic control of PRL secretion also has been suggested in turkeys (Youngren, Pitts, Phillips, & El Halawani, 1996; Youngren, Chaiseha, & El Halawani, 1998). The peak in PRL concentrations coincides with a decrease in LH concentrations and coincident gonadal regression in many bird species (Sharp & Sreekumar, 2001), which suggests a role for PRL in the termination of breeding. However, this is unlikely because administration of exogenous PRL does not on its own cause the onset of photorefractoriness (Goldsmith, 1985). Further, active immunization of starlings against VIP completely blocks PRL secretion but does not prevent gonadal regression (Dawson & Sharp, 1998). The timing of high levels of PRL is also closely linked to molt, premigratory fattening, and migration (Meier & MacGregor, 1972; Meier, 1972; Dawson & Goldsmith, 1983).

9

6. MECHANISMS AND PATHWAYS REGULATING SEASONAL REPRODUCTION 6.1. Seasonal Reproduction in Birds Birds have presumably evolved the timing of their breeding so that they can maximize the production of offspring, and laying is normally timed so that young are in the nest when there is enough food for them to be raised (Lack, 1968). Baker (1938) suggested that seasonal breeding is controlled by two sets of environment factors: ‘ultimate’ and ‘proximate’ factors. The most important ultimate factor for birds is the availability of an adequate food supply for the hatchlings as well as for the mother during the final stages of ovarian development. Other ultimate factors operating in special situations are competition, nesting conditions, predation pressure, and climate factors. However, these ultimate factors are often not those that trigger and regulate the secretion of reproductive hormones, because it is necessary to anticipate the hatching date and to begin preparations for breeding some weeks or months ahead of the time when young must be produced. In birds living in mid and high latitudes, there is excellent experimental evidence that the annual change in day length controls the timing of breeding, and it may be assumed that photoperiod is a proximate factor for birds living in such regions (Follett, 1984). Other environmental factors are also used to accelerate or retard photoperiodically induced gonadal growth (Farner & Follett, 1979). These include the presence of males for stimulating ovarian development (Marshall, 1936; Hinde, 1965; Cheng, 1979), ambient temperature (Perrins, 1973), and rainfall (Leopold, Erwin, Oh, & Browning, 1976). It is thought that photoperiod is not the proximate factor for many tropical and desert species (Marshall, 1970). Reproduction of tropical birds, such as African stonechats (Gwinner & Scheuerlein, 1999) and zebra finches (Bentley, Spar, MacDougallShackleton, Hahn, & Ball, 2000) can respond to changing photoperiod although the experimental length of the photoperiods used in these studies exceeded that of the tropics. However, studies on spotted antbirds suggest that tropical birds can respond to natural slight photoperiodic changes (Hau, Wikelski, & Wingfield, 1998; Beebe, Bentley, & Hau, 2005). The proximate factors used to time breeding in tropical birds remain largely unknown although correlative analyses suggest rainfall, territory, nest site availability, nest materials, and food supply as being involved (Immelmann, 1971; Zann, Morton, Jones, & Burley, 1995). Stonechats may respond to low light intensity as a predictive cue for rainfall (Gwinner & Scheuerlein, 1999). The reproductive axis of tropical birds may remain in a state of ‘readiness to breed,’ and full functionality may be triggered by the relevant proximate cues (Perfito, Bentley, & Hau, 2006; Perfito, Kwong, Bentley, & Hau,

10

2008). Although crossbills live in high latitudes, breeding can occur opportunistically at any time between January and August in response to their food supply. They feed on the seeds of coniferous trees, which are produced in different amounts in different years, and at unpredictable times of the year. However, they have a short, fixed nonbreeding period in fall when they appear to be photorefractory (Hahn, 1998). The vast majority of temperate-zone passerines undergo dynamic seasonal changes in their reproductive activities. Gonadal development occurs in spring in response to increasing day length (photostimulation). However, the gonads are maintained in a functional condition only for a short period, and they spontaneously regress after extended exposure to long day lengths (absolute photorefractoriness). After becoming photorefractory, exposure to short day length is required to regain photosensitivity and thus allow for photostimulation (Wingfield & Farner, 1980). Photorefractoriness seems to have evolved to minimize the costs of reproducing in the rapidly deteriorating environmental conditions of fall and winter (Follett, 1984). The only well-studied birds that do not become photorefractory are some species of pigeon and dove (Murton & Westwood, 1977). A condition similar to absolute photorefractoriness is relative photorefractoriness. The main difference is that, once relative photorefractoriness has been induced and the gonads have regressed, a subsequent substantial increase in day length will once more initiate reproductive maturationdwithout the need for a short-day-length ‘sensitization,’ or photosensitive, stage (Robinson & Follett, 1982). For example, if Japanese quail experience day lengths of over 11.5 hours, rapid gonadal development occurs. After about three months, and when (in the wild) day length decreases below 14.5 hours, complete gonadal regression occursdin a similar manner to absolute photorefractoriness (Nicholls, Goldsmith, & Dawson, 1988). However, if the day length is subsequently artificially increased further, a full return to reproductive maturity occurs. Indeed, if quail are maintained on any constant long day length, no form of photorefractoriness will be elicited unless they experience a decrease in day length, e.g., from 23 to 16 hours (Nicholls et al., 1988). This suggests a shift in the critical day length in birds that are relatively photorefractoryda shift that appears to depend on the photoperiodic history of such birds (Robinson & Follett, 1982). There does not seem to be any change in critical day length in birds that exhibit absolute photorefractoriness, regardless of their photoperiodic history (Dawson, 1987). Song sparrows and house sparrows show characteristics of both absolute and relative photorefractoriness (Dawson, King, Bentley, & Ball, 2001). Song sparrows (Wingfield, 1983) and house sparrows (Dawson, 1998a) eventually become photorefractory during exposure to long

Hormones and Reproduction of Vertebrates

photoperiods, but the timing can vary widely among individuals. If the photophase is decreased slightly, gonadal regression occurs sooner and is more synchronized among individuals. Moreover, song sparrows can show renewed gonadal maturation before exposure to short photoperiods (Wingfield, 1993). Seasonal changes in reproductive activities are correlated with GTH secretion. The primary effect of long day lengths on stimulating GTH secretion has been shown in quail (Follett, 1976), white-crowned sparrows (Wingfield & Farner, 1980), tree sparrows (Wilson & Follett, 1974), canaries (Nicholls, 1974), ducks (Balthazart, Hendrick, & Deviche, 1977), starlings (Dawson & Goldsmith, 1983), and many other birds. If male quail are transferred from short day lengths (8L : 16D) to long day lengths (20L : 4D), the levels of FSH and LH rise substantially during the first week of photostimulation. Testicular growth and steroidogenesis begin and maturity is reached in about five weeks (Follett & Robinson, 1980). Gonadal steroids affect GTH secretion by negative feedback (King et al., 1989a; Dunn & Sharp, 1999). Gonadal steroids also induce sexual behavior, development of secondary sexual characteristics, and spermatogenesis (Follett & Robinson, 1980). Female quail also grow their ovaries as a result of increased GTH secretion induced by long day lengths (20L : 4D). Gonadotropin levels becomes basal after transferring quail from long days to short days (8L : 16D) (Gibson, Follett, & Gledhill, 1975). On the other hand, in most of the temperate-zone passerine birds, which undergo spontaneous photorefractoriness after exposure to long days, GTH secretion is diminished and gonadal collapse occurs after a species-specific number of long days (Follett, 1984). Seasonality continues in the absence of the gonads. Castrated or intact quail show an identical time-course in LH and FSH secretion under natural photoperiods over two consecutive years, the difference being that in summer the GTH levels in castrated birds are higher, as a result of lack of negative feedback from gonadal steroids (Follett, 1984). A similar annual cycle of LH secretion has been observed in the plasma of intact and castrated white-crowned sparrows (Mattocks, Farner, & Follett, 1976). It is also thought that gonads are not required for photorefractoriness to develop, because castrated white-crowned sparrows (Wingfield, Follett, Matt, & Farner, 1980), canaries (Storey, Nicholls, & Follett, 1980), and starlings (Dawson & Goldsmith, 1984) show a spontaneous fall in GTH level under long days. Castration of photorefractory canaries does not cause enhanced LH secretion, but when photosensitivity is regained under short days there is an immediate rise in plasma LH (Nicholls & Storey, 1976). Birds seem to measure daylength using their circadian clock. In a classic experiment, white-crowned sparrows held on short day lengths (8L : 16D) were placed in continuous darkness. When birds were exposed to a single

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

eight-hour photophase, an increase in LH occurred only if the photophase coincided with a time period 12e20 hours after the subjective dawn, as judged by the circadian rhythms of the birds (Follett, Mattocks, & Farner, 1974). These data imply that a circadian rhythm of sensitivity to light, or photoinducibility, exists in the photoperiodic time measurement system of these birds. There are two possible models of how circadian rhythms might be involved in photoperiodic time measurement in birds (Goldman, 2001). The ‘external coincidence model’ assumes the organism possesses a circadian rhythm of ‘photosensitivity’. If coincidence between this rhythm and light occurs under long days, it induces GTH secretion. The ‘internal coincidence model’ assumes the induction to occur when coincidence is established between two separate circadian oscillators (usually dawn and dusk oscillators). As a consequence of using a circadian clock for photoperiodic time measurement, light is not required throughout the day to induce gonadal growth, but pulses of light simulating dawn and dusk can cause induction if one of the pulses coincides with the phase of photosensitivity (Follett, 1973). As with white-crowned sparrows, when 15-minute pulses of light were given at different times in the night to quail on the basic photoperiod of 6L : 18D, induction occurred only if the pulses were within 12 to 16 hours of dawn (Follett & Sharp, 1969). Light intensity can also modify the reproductive responses of birds under the same photoperiod (Bissonnette, 1931; Bartholomew, 1949). In the experiment conducted by Bentley, Goldsmith, Dawson, Briggs, and Pemberton (1998), photosensitive starlings transferred from short days to long days of different light intensities underwent graded reproductive responses according to the light intensities they experienced. Interestingly, the responses observed, such as the growth in their testes size and the development of photorefractoriness, were similar to those seen in starlings exposed to different photoperiods. At face value, these data contradict the external coincidence model in that light falling in the photoinducible phase should cause a long-day response. However, this discrepancy might be explained by the possibility that low light intensities only weakly entrain the circadian oscillations of the photoinducible phase, so that light is experienced in only part of the photoinducible phase.

6.2. Seasonal Changes in Gonadotropinreleasing Hormone (GnRH) Radioimmunoassay and immunocytochemistry (ICC) using GnRH antisera have numerous times demonstrated cyclic changes in GnRH in songbirds in response to changing photoperiod. Radioimmunoassay revealed that hypothalamic GnRH content did not increase significantly

11

during the first six weeks of photostimulation in female starlings. However, by 12 weeks after the onset of photostimulation, as birds became photorefractory, GnRH had decreased to levels significantly lower than those before photostimulation (Dawson, Follett, Goldsmith, & Nicholls, 1985). Immunocytochemistry with quantitative image analyses for both GnRH and its precursor, proGnRH-GAP, was performed after a photoperiodically induced reproductive cycle in male starlings (Parry, Goldsmith, Millar, & Glennie, 1997). The size of cells staining for GnRH and proGnRH-GAP increased during gonadal maturation. A reduction in the number of cells staining for GnRH and the size of cells staining for both GnRH and proGnRH-GAP occurred during gonadal regression, though staining for GnRH and proGnRH-GAP in the ME remained high. Staining for GnRH and proGnRH-GAP was reduced significantly after gonadal regression. These observations suggest that photorefractoriness is promoted by a reduction in pro-GnRH-GAP and GnRH synthesis (Parry et al., 1997). Changes in aGnRH-I in the POA and mediobasal hypothalamus (MBH) including the ME have been measured in starlings during the recovery of photosensitivity under short days, and following photostimulation at various times during the recovery of photosensitivity (Dawson & Goldsmith, 1997). During exposure of longday photorefractory starlings to short days for 10 days, there was a significant increase in aGnRH-I in the POA but not in the MBH. Photostimulation after 20 short days caused an immediate increase in aGnRH-I in the POA, a delayed increase in the MBH, but no increase in plasma LH. Photostimulation after 30 short days caused an immediate increase in aGnRH-I in the POA and the MBH and in plasma LH. These results show that the recovery of photosensitivity is gradual and the first measurable change occurs in the POA, consistent with photosensitivity being due to renewed aGnRH-I synthesis (Dawson & Goldsmith, 1997). Recently, the complete sequence of aGnRH-I precursor mRNA was identified in songbirds: starlings (Ubuka et al., 2009; Stevenson et al., 2009) and zebra finches (Ubuka & Bentley, 2009; Stevenson et al., 2009). The expression of aGnRH-I precursor mRNA was found to be regulated as a function of age and reproductive condition in zebra finches (Ubuka & Bentley, 2009). In starlings, there was regulation of aGnRH-I precursor mRNA expression as a function of season (Ubuka et al., 2009) and photoperiod (Stevenson et al., 2009). Photostimulation of short-day-exposed chickens and turkeys can also increase aGnRH-I precursor mRNA expression (Dunn & Sharp, 1999; Kang et al., 2006). What is the molecular mechanism regulating aGnRH-I synthesis and release? Is GTH secretion solely controlled by aGnRH-I? If photoperiod is the proximate factor controlling seasonal reproduction, how is the photoperiodic information acquired and processed in the brain?

12

Photoreceptors to perceive light and a biological clock to process photoperiodic information seem necessary to time seasonal reproduction. How autonomous are the seasonal reproductive activities? In other words, does external information such as day length need to be sensed through the whole year to time seasonal reproduction? Does the daily melatonin (MEL) rhythm control reproductive cycles of birds? Thyroid hormones seem to be required to achieve seasonal reproduction, but what is the mechanism involved? Studies on the potential mechanisms controlling seasonal reproduction of birds will be discussed in the following sections.

6.3. Photoreceptor It is believed that light can affect the activity of birds via three different pathways: the eyes, the pineal, and the deep brain (Underwood, Steele, & Zivkovic, 2001). The avian eye is not only a functional photoreceptor, but also contains a circadian clock and produces a circadian rhythm of MEL release (Binkley, Reilly, & Hryschchyshyn, 1980; Hamm & Menaker, 1980). The principal cell types within the pineal of most nonmammalian vertebrates have characteristics of a photosensory cell, including the presence of an outer segment composed of stacked disks containing photopigments (Collin & Oksche, 1981). The avian pineal organ is directly photosensitive and it is also the locus of a circadian pacemaker (Takahashi & Menaker, 1984; Okano & Fukada, 2001). The location of the extrapinealeextraretinal photoreceptors mediating circadian entrainment in birds has not been established. In a study using opsin antibodies, cerebrospinal fluid-contacting cells were labeled in the septal and the tuberal areas in the ring dove (Silver et al., 1988), and lateral septum in the pigeon (Wada, Okano, & Fukada, 2000). Light and confocal microscopy revealed interactions of GnRH-ir and opsin-ir materials in the POA and in the ME, suggesting a direct communication between these putative deep brain photoreceptors and GnRH neurons (Saldanha, Silverman, & Silver, 2001).

6.4. Biological Clock The circadian system of birds is composed of several interacting sites, including the pineal organ, the suprachiasmatic nucleus (SCN) of the hypothalamus, and eyes, in at least some species. Each of these sites may contain a circadian clock (Underwood et al., 2001). Significant variation can occur among birds in the relative roles that the pineal, the SCN, and the eyes play within the circadian system. For example, in the house sparrow, circadian pacemakers in the pineal play the predominant role, whereas in the pigeon circadian pacemakers in both the pineal and eyes play a significant role. In Japanese quail, ocular pacemakers play the predominant role. There has

Hormones and Reproduction of Vertebrates

been controversy concerning the precise location of the avian homologs of the mammalian SCN. The medial hypothalamic nucleus (MHN) (also termed the medial SCN) and the lateral hypothalamic retinorecipient nucleus (LHRN) (also termed the visual SCN) are the possible homologs of the mammalian SCN (Norgren & Silver, 1989; 1990; Shimizu, Cox, Karten, & Britto, 1994; Cassone & Moore, 1987). The self-sustaining circadian oscillation in any organism is thought to be generated by a transcriptionetranslation feedback loop of clock genes, the presence of which appears to be a conserved property from fruit flies to humans. Clock and Period homologs (qClock, qPer2, and qPer3) have been cloned in the Japanese quail. qPer2 and qPer3 showed robust circadian oscillations in the eye and in the pineal gland, although qClock mRNA was expressed throughout the day. In addition, qPer2 mRNA was induced by light, whereas qClock or qPer3 were not (Yoshimura et al., 2000). These clock genes were expressed in the MHN, but not in the LHRN in quail (Yoshimura et al., 2001). On the other hand, Per2 mRNA is expressed both in the MHN and in the LHRN with rhythmic expression patterns in the house sparrow (Abraham, Albrecht, Gwinner, & Brandsta¨tter, 2002). Clock genes such as Per, Cry, Clock, Bmal, and E4bp4 are all expressed and differentially oscillate in quail and chicken pineal glands (Doi, Nakajima, Okano, & Fukada, 2001; Okano et al., 2001; Yamamoto, Okano, & Fukada, 2001; Fukada & Okano, 2002; Yasuo, Watanabe, Okabayashi, Ebihara, & Yoshimura, 2003). The avian pineal gland seems to possess a functional circadian oscillator composed of a transcription-/translation-based autoregulatory feedback loop, as in the mammalian SCN (Fukada & Okano, 2002). Thus, multiple oscillators are present in birds, and they are somehow coordinated to convey circadian rhythmicity. Annual seasonal activities of birds, such as reproduction, molt, and migration, can persist for many cycles, with a period deviating from 12 months under constant conditions. These cycles have been named ‘circannual rhythms’ (Gwinner, 2003), although many of them deviate significantly from a 12-month period. These cycles have been experimentally demonstrated for at least 20 species of bird under specific lighting conditions (Gwinner, 1986; Gwinner & Dittami, 1990; C. Guyomarc’h & J. Guyomarc’h, 1995). In European starlings, a cycle of reproduction composed of photosensitive and photorefractory phases continues in constant photoperiods close to 12 hours (Gwinner, 1996; Dawson, 1997). Under photoperiods longer than 12 hours, starlings remain in the photorefractory state, whereas under shorter photoperiods they remain in the photosensitive state (Gwinner, 1996). Castrated starlings exposed to 12L : 12D did not exhibit cyclic rhythms of this type (Dawson & McNaughton, 1993). Accordingly, the reproductive cycle that was observed for intact birds under this specific

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

constant photoperiod (12L : 12D) might be generated as a result of complex interactions within the HPG axis, rather than as a result of a circannual ‘calendar’ in the brain.

6.5. Melatonin (MEL) The pineal glands of all vertebrates show daily rhythms in the activity of the enzymes in the indolamine-synthesizing pathway that produces MEL. Levels of MEL are higher at night in both diurnal and nocturnal animals. In the pineal gland, serotonin (5-HT) is converted by the action of Nacetyltransferase (NAT) to N-acetylserotonin, and then by hydroxyindole-O-methyltransferase (HIOMT) to MEL. Invitro rhythms of melatonin synthesis and release from the pineal gland occur in pigeons, house sparrows, quail, and chickens. Circadian rhythms in MEL secretion from the cultured pineal gland can persist under constant conditions and they can be entrained by 24-hour lightedark cycles (Murakami, Nakamura, Nishi, Marumoto, & Nasu, 1994; Barrett & Takahashi, 1997; Brandsta¨tter, Kumar, Abraham, & Gwinner, 2000; Brandsta¨tter, Kumar, Van’t Hof, & Gwinner, 2001). The eyes can contribute significantly (up to 30%) to blood MEL levels in pigeons and Japanese quail (Underwood, Binkley, Siopes, & Mosher, 1984; Oshima, Yamada, Goto, Soto, & Ebihara, 1989). The eyes of Japanese quail show a rhythm in MEL content that can be entrained by light directed exclusively to the eyes, which is high at scotophase and low at photophase (Underwood, Barrett, & Siopes, 1990). Circadian pacemakers in the pineal and in the eyes of some species are thought to communicate with the hypothalamic pacemakers via the rhythmic synthesis and release of MEL (Chabot & Menaker, 1992; Underwood et al., 2001). Three MEL receptor (MEL-R) subtypes, Mel1a, Mel1b, and Mel1c, have been identified in birds. These are G-protein-coupled receptors (Reppert, Weaver, Cassone, Godson, & Kolakowski, 1995). Mel1a and Mel1c receptors are present in the LHRN in the chicken brain (Reppert et al., 1995). Contrary to the MEL rhythm, which exhibits higher MEL secretion during the scotophase, [125I]-iodomelatonin binding in the brain is higher during the photophase and lower during the scotophase in chickens (Yuan & Pang, 1992), quail (Yuan & Pang, 1990), and pigeons (Yuan & Pang, 1991). Sex differences and the effect of photoperiod on [125I]-iodomelatonin binding also have been observed in the avian brain (Aste, Cozzi, Stankov, & Panzica, 2001; Panzica et al., 1994). Higher densities of MEL binding sites in males than in females were detected in some telencephalic nuclei of songbirds, as well as in the visual pathways and in the POA of quail (Aste et al., 2001). Japanese quail under short days exhibited higher MEL-R density in the optic tectum and nucleus triangularis, whereas long-day birds had a higher density of MEL-R in the hyperstriatum and nucleus preopticus dorsalis (Panzica et al., 1994). Seasonal

13

changes in the volumes of song control nuclei are at least partly regulated by MEL binding to these brain nuclei (Bentley, Van’t Hof, & Ball, 1999; Bentley & Ball, 2000). Photoperiodic mammals rely on the annual cycle of changes in nocturnal secretion of MEL to drive their reproductive responses (Bronson, 1990). In contrast, a dogma exists that birds do not use seasonal changes in MEL secretion to time their reproductive effort, and a role for MEL in birds has remained enigmatic. The effects of pinealectomy (Px), bilateral orbital enucleation (Ex), and Px þ Ex on seasonal regulation of reproduction were tested in tree sparrows, a highly photoperiodic species (Wilson, 1991). Although there was an accelerating effect of Ex on the changes in their testicular size, Px, Ex, and Px þ Ex birds exhibited photostimulation, photorefractoriness, and recovery of photosensitivity in the same way as did the intact birds. The effects of artificial extension of the duration of circulating MEL on reproductive status were tested using Japanese quail by exogenous MEL injection (Juss, Meddle, Servant, & King, 1993). Male quail reared under nonstimulatory short days (8L : 16D) were switched to 12L : 12D and given daily MEL injections at the time of lights-on or before and at the time of lights-off or for three weeks. Contrary to the prediction, MEL injection resulted in significant stimulation of LH concentration and testicular size. Despite the accepted dogma, there is increasing evidence that MEL is involved in the regulation of seasonal reproductive processes. Male Japanese quail reared under nonstimulatory short days (8L : 16D) were used to test the effect of anti-MEL antibody (anti-MEL) administration on the reproductive status (Ohta, Kadota, & Konishi, 1989). Intravenous injection of anti-MEL just before lights-off for three days significantly increased T concentration and testicular size after two weeks even if quail were kept under the same nonstimulatory photoperiod (8L : 16D). There are also reports showing inhibitory effects of MEL on seasonal recrudescence in quail (Guyomarc’h, Lumineau, VivienRoels, Richard, & Deregnaucourt, 2001) and on LH secretion in chickens (Rozenboim, Aharony, & Yahav, 2002). In light of these reports and considering GnIH’s inhibitory effects on the secretion of GTH, Ubuka, Bentley, Ukena, Wingfield, and Tsutsui (2005) hypothesized that MEL may be involved in the induction of GnIH expression, thus influencing gonadal activity. As the pineal gland and eyes are the major sources of MEL in the quail (Underwood et al., 1984), Ubuka et al. (2005) analyzed the effects of Px and Ex on the expression of GnIH precursor mRNA and GnIH peptide. Subsequently, MEL was administered to Px þ Ex birds. Pinealectomy þ Ex decreased the expression of GnIH precursor mRNA and the content of GnIH peptide in the hypothalamus. Further, MEL administration to Px þ Ex birds caused a dose-dependent increase in the expression of GnIH precursor mRNA and the production of the mature

14

peptide. The expression of GnIH was photoperiodically controlled and increased under short-day photoperiods, when the duration of MEL secretion increases. A MEL-R subtype, Mel1c mRNA, was expressed in GnIH-ir neurons in the PVN. Autoradiography of MER-Rs further revealed specific binding of [125I]-MEL in the PVN. Accordingly, MEL appears to act directly on GnIH neurons through its receptor to induce GnIH expression. Recently, it was shown that MEL also stimulates the release of GnIH from the quail hypothalamus (Chowdhury et al., 2010). Gonadotropininhibiting hormone may transduce photoperiodic information by means of changes in the MEL signal, and thus influences the reproductive activities of birds (Ubuka et al., 2005). Although Px þ Ex treatment for one week eliminated MEL concentration in the plasma, there was a substantial amount of MEL-immunoreactive (ir) material remaining in the quail diencephalon (Ubuka et al., 2005). Recently, a group of neurons that synthesize both dopamine (DA) and MEL were identified in the premammillary nucleus of the turkey hypothalamus (Kang, Thayananuphat, Bakken, & El Halawani, 2007; El Halawani, Kang, Leclerc, Kosonsiriluk, & Chaiseha, 2009). These neurons express clock genes and a photoreceptor, melanopsin. Dopamine-MEL neurons are activated when a light pulse is given during the photosensitive phase, associated with an upregulation of GnRH-I mRNA expression. The expression of tryptophan hydroxylase-1 (TPH1) (5-HT-synthesizing enzyme) mRNA level is low during the photophase and high during the scotophase, and tyrosine hydroxylase (TH) (rate-limiting DAsynthesizing enzyme) mRNA shows the opposite cycle. These hypothalamic DAeMEL neurons may provide a novel role for MEL in the regulation of seasonal reproductive cycles in birds.

6.6. Thyroid Hormones It has been known for many decades that thyroid hormones can affect reproductive function, but the effects of thyroidectomy on seasonal breeding were often contradictory (Dawson et al., 2001). Gonadal regression caused by photorefractoriness is normally prevented by thyroidectomy, but in some studies photorefractoriness appears to have been accelerated (Dawson & Thapliyal, 2001). Treatment with one of the thyroid hormones, thyroxine (T4), can mimic the effects of long photoperiods (Follett & Nicholls, 1988; Goldsmith & Nicholls, 1992; Wilson & Reinert, 1995). Reinert and Wilson (1996) argue that, in tree sparrows, the increase in plasma T4 concentrations following photostimulation (Dawson, 1984; Sharp & Klandorf, 1981) serves to program the subsequent gonadal cycle and molt. The contrary view is taken by Bentley et al. (1997). When they maintained T4 concentrations at subphysiological levels by treating thyroidectomized starlings

Hormones and Reproduction of Vertebrates

held on long days with appropriate amounts of T4, these birds became photorefractory and molted. This suggests that T4 simply has to be present for the appropriate responses to photoperiod to occur. The site(s) of action of thyroid hormones may lie within the central nervous system since, in starlings and sparrows, the prevention of photorefractoriness by thyroidectomy is associated with maintenance of high levels of aGnRH-I, typical of photosensitive birds (Dawson et al., 1985; Reinert & Wilson, 1996; Dawson, 1998b), and thyroidectomy of photorefractory birds results in an increase in aGnRH-I (Dawson, Goldsmith, Nicholls, & Follett, 1986). Central administration of thyroid hormones to thyroidectomized tree sparrows restores all of the photoperiodic responses, with the effects of T4 being more potent than triiodothyronine (T3) (Wilson & Reinert, 2000). Chronic thyroidectomy appears to render starlings ‘photoperiodically blind,’ because the GnRH response to an increase or a decrease in photoperiod is greatly attenuated (Bentley, Dawson, & Goldsmith, 2000a). In house sparrows, the effects of thyroidectomy are very different. Again, thyroidectomized birds appear to be photoperiodically blind; testicular size and GnRH-I are the same whether birds are on long or short photoperiods (Dawson, 1998b). However, although GnRH-I remains high, which is typical of photosensitive birds, testicular size remains minimal, which is typical of photorefractory birds. Thyroid hormone may have different effects on GnRH-I synthesis and release, which may account for the apparently contradictory results regarding the effects of thyroidectomy on reproductive processes. Recent molecular analyses suggest that local thyroid hormone activation in the hypothalamus may play a critical role in the regulation of seasonal reproduction in birds (Nakao, Ono, & Yoshimura, 2008b). If the light exposure occurs around 11 to 16 hours after dawn (photoinducible phase), the first detectable change in GTH secretion begins around 22 hours after dawn in Japanese quail (Follett & Sharp, 1969), and a wave of GTH secretion occurs over the next few days (Follett, Davies, & Gledhill, 1977; Nicholls, Follett, & Robinson, 1983). Meddle and Follett (1997) examined the effect of the first long day on expression of a transcription factor, Fos, in the basal tuberal hypothalamus, a brain area that includes GnRH-I neuronal terminals. Transfer of short-day (6L : 18D) quail to long days induced Fos-ir in neuronal cells in the infundibular nucleus (IFN) and glial cells in the ME by 18 hours of the first long day. This activation of specific brain areas was followed by the first rise in LH, 20 hours after dawn (Meddle & Follett, 1997). Fos-ir in the IFN, and LH release were also stimulated by subcutaneous N-methyl-D-aspartate administration in the white-crowned sparrow (Meddle, Maney, & Wingfield, 1999). Yoshimura et al. (2003) hypothesized that important molecular events would be triggered in the

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

MBH, when light was given to quail during the photoinducible phase. Acute induction of type 2 iodothyronine deiodinase (DII) mRNA expression was observed in the ependymal cells of the MBH and in the IFN by long-day treatments. Type 2 iodothyronine deiodinase is an enzyme that catalyzes the conversion of T4 to T3, whereas type 3 iodothyronine deiodinase (DIII) catalyzes the conversion of T4 and T3 to their inactive forms. Interestingly, the expression of DIII was downregulated under long-day conditions, when DII was upregulated (Yasuo et al., 2005). Central administration of DII inhibitor, iopanoic acid, reduced testicular growth of quail that were transferred from short- to long-day conditions (Yoshimura et al., 2003). Triiodothyronine implantation to the MBH caused testicular growth and reduced encasement of nerve terminals by glial processes in the ME of quail (Yamamura, Yasuo, Hirunagi, Ebihara, & Yoshimura, 2006). The glial processes do not physically occupy and block space in between axon terminals and capillaries of the portal system in the ME of photostimulated white-crowned sparrows, but they do in photorefractory birds (Bern, Nishioka, Mewaldt, & Farner, 1966; Mikami, Oksche, Farner, & Vitums, 1970). As GnRH nerve terminals are also in closer proximity to the basal lamina of the ME in long-day quail (Yamamura, Hirunagi, Ebihara, & Yoshimura, 2004), Yamamura et al. (2006) suggest a role for T3 in the regulation of photoperiodic GnRH secretion via neuroeglial plasticity in the ME. In a more recent study, functional genomic analysis was performed using a chicken high-density oligonucleotide microarray during photoinduction in quail (Nakao et al., 2008a). The microarray detected two waves of gene expression in the MBH. Interestingly, thyrotropin b subunit (TSHb) mRNA expression peaked around 14 hours after dawn, and upregulation of DII and downregulation of DIII occurred around 18e19 hours after dawn of the first long day. Spatiotemporal expression analyses of the genes revealed that the first wave events occurred in the pars tuberalis (PT) of the pituitary gland, whereas the second wave events occurred in the ependymal cells in the ventrolateral walls of the third ventricle in the MBH. Glycoprotein-a mRNA, which codes for the common subunit for TSH, LH, and FSH, was cyclically expressed in the PT. TSH receptor also was observed in the ependymal cells in the ventrolateral walls of the third ventricle in the MBH, where the second wave genes were expressed, and the binding of [125I]-TSH was further observed. Intracerebroventricular administration of TSH induced the expression of DII, whereas anti-TSHb antibody reduced DII expression (Nakao et al., 2008a). Although the mechanism of TSHb mRNA induction by the first long day was not identified in this study, the removal of the inhibitory effect of melatonin on TSHb mRNA expression is a possible mechanism, because MEL-R (Mel1c) mRNA is expressed in the PT in chickens (Kameda, Miura, &

15

Maruyama, 2002). Glycoprotein-a is also expressed in the PT in chickens, and Px induces glycoprotein-a subunit mRNA expression in the PT (Kameda et al., 2002). Thus, local induction of thyroid hormones caused by changes in MEL signaling might well be involved in at least the initial photoperiodic response.

7. FUTURE RESEARCH DIRECTIONS The neuroendocrine system controlling reproductive activities of birds is summarized in Figure 1.2. The functional significance of each action may vary among species and between sexes, developmental processes, and reproductive stages. It is important to continue searching for unidentified hypothalamic and pituitary hormones and/or networks to reveal the whole picture of neuroendocrine mechanisms that control avian reproduction. Chicken (Galliformes) and zebra finch (Passeriformes) genomes have been published recently. A functional genomic analysis such as microarray is a powerful tool to identify important genes and molecules related to reproductive processes. Gene silencing of target substances by RNAi, and physiological administration of the gene products, are powerful approaches that will provide greater understanding of the reproductive processes. Reproduction in birds consists of various stages that are timed to maximize the survival of the species. Birds have amazing abilities to adjust their physiology and behavior appropriately to the external environment. As annual changes in photoperiod are the most reliable predictor of seasonal change outside the tropics, most birds have an ability to respond to changing photoperiods. In this chapter, we have described many studies on the effects of photoperiod on reproductive activities of birds. However, social interactions also have dramatic effects on reproductive physiology in birds (Hinde, 1965; Lehrman, 1965; Wingfield, Whaling, & Marler, 1994). For example, male courtship behaviors can greatly enhance the development of reproductive physiology and behaviors of female birds (Crews & Silver, 1985; Searcy, 1992; Bentley, Wingfield, Morton, & Ball, 2000; Stevenson et al., 2008). To maximize reproductive success, some bird species categorized as opportunistic breeders integrate various environmental cues, such as temperature, rainfall, and food availability, independently from, or in addition to, photoperiodic changes to initiate breeding (Immelmann, 1971; Zann et al., 1995; Perfito et al., 2008). These indispensable factors for reproduction, such as the establishment of territory, interactions with the opposite sex, and food availability, are obviously very important to the timing of breeding. Our knowledge of how this type of environmental information and social interactions are processed and integrated in the HPG axis is minimal. For example, there is experimental evidence that sounds including vocalization

16

Hormones and Reproduction of Vertebrates

of birds can stimulate the HPG axis during the scotophase of the lightedark cycle (Millam, El Halawani, & Burke, 1985; Li & Burke, 1987). This brings about the question of whether there is a circadian rhythm of audioinducibility, just as there is for photoinducibility. Stress can also modify the reproductive activity of birds. Inhibitory effects of stress on reproductive function may be mediated via the hypothalamic GnIH system (Calisi, Rizzo, & Bentley, 2008). Activation of the immune system can also impair reproductive function in birds (Owen-Ashley & Wingfield, 2007). Coordination of several neural mechanisms is necessary to translate various environmental information and social interactions and produce appropriately timed changes in the reproductive physiology and behavior of birds (Figure 1.2). For each mechanism that we wish to study, it is important to use an appropriate model animal and analysis. However, reductionism can lead us to emphasize only one aspect of a specific mechanism that may be applicable to a specific avian species or only in certain artificial situations. Accordingly, whole-animal experiments have a great deal to offer in terms of our understanding of these complex biological systems, as do experiments in real-world environments. Only when we integrate studies from the molecular and cellular levels into the physiological, behavioral, and ecological levels can we begin to reveal the whole picture of neuroendocrine control of avian reproduction.

ABBREVIATIONS 5-HT ACTH aGnRH-I aGnRH-II anti-MEL AVT cAMP cGnRH-I cGnRH-II CRH DA DII DIII E2 Ex FSH Gai GH GnIH GnIH-RP GnRH GnRH-R GPCR GTH HIOMT

Serotonin Corticotropin Avian gonadotropin-releasing hormone-I Avian gonadotropin-releasing hormone-II Anti-melatonin antibody Arginine vasotocin Cyclic-3’,5’-adenosine monophosphate Chicken gonadotropin-releasing hormone-I Chicken gonadotropin-releasing hormone-II Corticotropin-releasing hormone Dopamine Type 2 iodothyronine deiodinase Type 3 iodothyronine deiodinase Estradiol Bilateral orbital enucleation Follicle-stimulating hormone a-subunit of the inhibitory G-protein Growth hormone Gonadotropin-inhibiting hormone Gonadotropin-inhibiting hormone-related peptide Gonadotropin-releasing hormone Gonadotropin-releasing hormone receptor G-protein-coupled receptor Gonadotropin Hydroxyindole-O-methyltransferase

HPG HPLC HPS ICC IFN ir LH LHRN MBH ME MEL MEL-R mGnRH-I MHN MST NAT P4 PG PN POA PRL proGnRH-GAP PT PVN Px RFRP RIA SCN T T3 T4 TH TPH1 TSH TSHb VIP

Hypothalamicepituitaryegonadal High performance liquid chromatography Hypothalamusepituitary system Immunocytochemistry Infundibular nucleus Immunoreactive Luteinizing hormone Lateral hypothalamic retinorecipient nucleus Mediobasal hypothalamus Median eminence Melatonin Melatonin receptor Mammalian gonadotropin-releasing hormone Medial hypothalamic nucleus Mesotocin N-acetyltransferase Progesterone Prostaglandin Pars nervosa Preoptic area Prolactin Precursor protein of gonadotropin-releasing hormone Pars tuberalis Paraventricular nucleus Pinealectomy RFamide-related peptide Radioimmunoassay Suprachiasmatic nucleus Testosterone Triiodothyronine Thyroxine Tyrosine hydroxylase Tryptophan hydroxylase-1 Thyrotropin Thyrotropin b subunit Vasoactive intestinal peptide

REFERENCES Abraham, U., Albrecht, U., Gwinner, E., & Brandsta¨tter, R. (2002). Spatial and temporal variation of passer Per2 gene expression in two distinct cell groups of the suprachiasmatic hypothalamus in the house sparrow (Passer domesticus). Eur. J. Neurosci., 16, 429e436. Acher, R., Chauvet, J., & Chauvet, M. T. (1970). Phylogeny of the neurohypophysial hormones. The avian active peptides. Eur. J. Biochem., 17, 509e513. Akutsu, S., Takada, M., Ohki-Hamazaki, H., Murakami, S., & Arai, Y. (1992). Origin of luteinizing hormone-releasing hormone (LHRH) neurons in the chick embryo: effect of the olfactory placode ablation. Neurosci. Lett., 142, 241e244. Aste, N., Cozzi, B., Stankov, B., & Panzica, G. (2001). Sexual differences and effect of photoperiod on melatonin receptor in avian brain. Microsc. Res. Tech., 55, 37e47. Baker, J. R. (1938). The evolution of breeding seasons. In G. R. de Beer (Ed.), Evolution. Essays on Aspects of Evolutionary Biology (pp. 161e177). London, UK: Oxford University Press.

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

Balthazart, J., Hendrick, J. C., & Deviche, P. (1977). Diurnal variations of plasma gonadotrophins in male domestic ducks during the sexual cycle. Gen. Comp. Endocrinol., 32, 376e389. Barrett, R. K., & Takahashi, J. S. (1997). Lability of circadian pacemaker amplitude in chick pineal cells: a temperature-dependent process. J. Biol. Rhythms, 12, 309e318. Barth, S. W., Bathgate, R. A., Mess, A., Parry, L. J., Ivell, R., & Grossmann, R. (1997). Mesotocin gene expression in the diencephalon of domestic fowl: cloning and sequencing of the MT cDNA and distribution of MT gene expressing neurons in the chicken hypothalamus. J. Neuroendocrinol., 9, 777e787. Bartholomew, G. A., Jr. (1949). The effect of light intensity and day length on reproduction in the English sparrow. Bull. Mus. Comp. Zoo. (Harvard), 101, 433e476. Beebe, K., Bentley, G. E., & Hau, M. (2005). A seasonally breeding tropical bird lacks absolute photorefractoriness in the wild, despite high photosensitivity. Funct. Ecol., 19, 505e512. Bentley, G. E., & Ball, G. F. (2000). Photoperiod-dependent and -independent regulation of melatonin receptors in the forebrain of songbirds. J. Neuroendocrinol., 12, 745e752. Bentley, G. E., Dawson, A., & Goldsmith, A. R. (2000a). Lack of gonadotrophin-releasing hormone (GnRH) neuron response to decreasing photoperiod in thyroidectomized male starlings (Sturnus vulgaris). J. Exp. Zool., 287, 74e79. Bentley, G. E., Goldsmith, A. R., Dawson, A., Briggs, C., & Pemberton, M. (1998). Decreased light intensity alters the perception of day length by male European starlings (Sturnus vulgaris). J. Biol. Rhythms, 13, 148e158. Bentley, G. E., Goldsmith, A. R., Dawson, A., Glennie, L. M., Talbot, R. T., & Sharp, P. J. (1997). Photorefractoriness in European starlings (Sturnus vulgaris) is not dependent upon the long-dayinduced rise in plasma thyroxine. Gen. Comp. Endocrinol., 107, 428e438. Bentley, G. E., Jensen, J. P., Kaur, G. J., Wacker, D. W., Tsutsui, K., & Wingfield, J. C. (2006a). Rapid inhibition of female sexual behavior by gonadotropin-inhibitory hormone (GnIH). Horm. Behav., 49, 550e555. Bentley, G. E., Perfito, N., Ukena, K., Tsutsui, K., & Wingfield, J. C. (2003). Gonadotropin-inhibitory peptide in song sparrows (Melospiza melodia) in different reproductive conditions, and in house sparrows (Passer domesticus) relative to chicken-gonadotropin-releasing hormone. J. Neuroendocrinol., 15, 794e802. Bentley, G. E., Spar, B. D., MacDougall-Shackleton, S. A., Hahn, T. P., & Ball, G. F. (2000b). Photoperiodic regulation of the reproductive axis in male zebra finches, Taeniopygia guttata. Gen. Comp. Endocrinol., 117, 449e455. Bentley, G. E., Ubuka, T., McGuire, N. L., Chowdhury, V. S., Morita, Y., Yano, T., et al. (2008). Gonadotropin-inhibitory hormone and its receptor in the avian reproductive system. Gen. Comp. Endocrinol., 156, 34e43. Bentley, G. E., Van’t Hof, T. J., & Ball, G. F. (1999). Seasonal neuroplasticity in the songbird telencephalon: a role for melatonin. Proc. Natl. Acad. Sci. USA, 13, 4674e4679. Bentley, G. E., Wingfield, J. C., Morton, M. L., & Ball, G. F. (2000c). Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song. Horm. Behav., 37, 179e189. Bern, H. A., Nishioka, R. S., Mewaldt, L. R., & Farner, D. S. (1966). Photoperiodic and osmotic influences on the ultrastructure of

17

the hypothalamic neurosecretory system of the white-crowned sparrow, Zonotrichia leucophrys gambelii. Z. Zellforsch, 69, 198e227. Bhatti, B. M., & Morris, T. R. (1978a). Entrainment of oviposition in the fowl using light-dark cycles. Br. Poult. Sci., 19, 333e340. Bhatti, B. M., & Morris, T. R. (1978b). The relative importance of sunrise and sunset for entrainment of oviposition in the fowl. Br. Poult. Sci., 19, 365e371. Binkley, S., Reilly, K. B., & Hryschchyshyn, M. (1980). N-acetyltransferase in the chick retina. I. Circadian rhythms controlled by environmental lighting are similar to those in the pineal gland. J. Comp. Physiol., 139, 103e108. Bissonnette, T. H. (1931). Studies on the sexual cycle in birds. V. Effects of light of different intensities upon the testis activity of the European starling (Sturnus vulgaris). Physiol. Zool., 4, 542e574. Brandsta¨tter, R., Kumar, V., Abraham, U., & Gwinner, E. (2000). Photoperiodic information acquired and stored in vivo is retained in vitro by a circadian oscillator, the avian pineal gland. Proc. Natl. Acad. Sci. USA, 97, 12324e12328. Brandsta¨tter, R., Kumar, V., Van’t Hof, T. J., & Gwinner, E. (2001). Seasonal variations of in-vivo and in-vitro melatonin production in a passeriform bird, the house sparrow (Passer domesticus). J. Pineal. Res., 31, 120e126. Bronson, F. H. (1990). Mammalian Reproductive Biology. Chicago, IL: University of Chicago Press. Burgus, R., Butcher, M., Amoss, M., Ling, N., Monahan, M., Rivier, J., et al. (1972). Primary structure of the ovine hypothalamic luteinizing hormone-releasing factor (LRF) (LH-hypothalamus-LRF-gas chromatography-mass spectrometry-decapeptide-Edman degradation). Proc. Natl. Acad. Sci. USA, 69, 278e282. Burke, W. H., Licht, P., Papkoff, H., & Bona-Gallo, A. (1979). Isolation and characterization of luteinizing hormone and follicle-stimulating hormone from pituitary glands of the turkey (Meleagris gallopavo). Gen. Comp. Endocrinol., 37, 508e520. Calisi, R. M., Rizzo, N. O., & Bentley, G. E. (2008). Seasonal differences in hypothalamic EGR-1 and GnIH expression following capturehandling stress in house sparrows (Passer domesticus). Gen. Comp. Endocrinol., 158, 283e287. Cassone, V. M., & Moore, R. Y. (1987). Retinohypothalamic projection and suprachiasmatic nucleus of the house sparrow, Passer domesticus. J. Comp. Neurol., 266, 171e182. Castagna, C., Absil, P., Foidart, A., & Balthazart, J. (1998). Systemic and intracerebroventricular injections of vasotocin inhibit appetitive and consummatory components of male sexual behavior in Japanese quail. Behav. Neurosci., 112, 233e250. Castro, M. G., Estivariz, F. E., & Iturriza, M. J. (1986). The regulation of the corticomelanotropic cell activity in Aves: II. Effect of various peptides on the release of ACTH from dispersed, perfused duck pituitary cells. Comp. Biochem. Physiol. A, 83, 71e75. Chabot, C. C., & Menaker, M. (1992). Effects of physiological cycles of infused melatonin on circadian rhythmicity in pigeons. J. Comp. Physiol. A, 170, 615e622. Chaiseha, Y., Tong, Z., Youngren, O. M., & El Halawani, M. E. (1998). Transcriptional changes in hypothalamic vasoactive intestinal peptide during a photo-induced reproductive cycle in the turkey. J. Mol. Endocrinol., 21, 267e275. Cheng, M. F. (1979). Progress and prospect in ring dove research: a personal view. In J. S. Rosenblatt, R. A. Hinde, C. Beer, &

18

M. C. Busnel (Eds.), Advances in the Study of Behavior, Vol. 9 (pp. 97e129). New York, NY: Academic Press. Chowdhury, V. S., Yamamoto, K., Ubuka, T., Bentley, G. E., Hattori, A., & Tsutsui, K. (2010). Melatonin stimulates the release of gonadotropin-inhibitory hormone by the avian hypothalamus. Endocrinology, 151, 271e280. Ciccone, N. A., Dunn, I. C., Boswell, T., Tsutsui, K., Ubuka, T., Ukena, K., et al. (2004). Gonadotrophin inhibitory hormone depresses gonadotrophin alpha and follicle-stimulating hormone beta subunit expression in the pituitary of the domestic chicken. J. Neuroendocrinol., 16, 999e1006. Collin, J. P., & Oksche, A. (1981). Structural and functional relationships in the nonmammalian pineal gland. In R. J. Reiter (Ed.), The pineal gland v.1. Anatomy and biochemistry (pp. 27e67). Boca Raton, FL: CRC press. Crews, D., & Silver, R. (1985). Reproductive physiology and behavior interactions in non-mammalian vertebrates. In N. Adler, D. Pfaff, & R. Goy (Eds.), Handbook of Behavioral Neurobiology, Vol. 7 (pp. 101e182). New York, NY: Plenum. Dawson, A. (1984). Changes in plasma thyroxine concentrations in male and female starlings (Sturnus vulgaris) during a photo-induced gonadal cycle. Gen. Comp. Endocrinol., 56, 193e197. Dawson, A. (1987). Photorefractoriness in European starlings: critical daylength is not affected by photoperiodic history. Physiol. Zool., 60, 722e729. Dawson, A. (1997). Plasma-luteinizing hormone and prolactin during circannual rhythms of gonadal maturation and molt in male and female European starlings. J. Biol. Rhythms, 12, 371e377. Dawson, A. (1998a). Photoperiodic control of the termination of breeding and the induction of moult in house sparrows Passer domesticus. Ibis, 140, 35e40. Dawson, A. (1998b). Thyroidectomy of house sparrows (Passer domesticus) prevents photo-induced testicular growth but not the increased hypothalamic gonadotrophin-releasing hormone. Gen. Comp. Endocrinol., 110, 196e200. Dawson, A., & Goldsmith, A. R. (1983). Plasma prolactin and gonadotrophins during gonadal development and the onset of photorefractoriness in male and female starlings (Sturnus vulgaris) on artificial photoperiods. J. Endocrinol., 97, 253e260. Dawson, A., & Goldsmith, A. R. (1984). Effects of gonadectomy on seasonal changes in plasma LH and prolactin concentrations in male and female starlings (Sturnus vulgaris). J. Endocrinol., 100, 213e218. Dawson, A., & Goldsmith, A. R. (1997). Changes in gonadotrophinreleasing hormone (GnRH-I) in the pre-optic area and median eminence of starlings (Sturnus vulgaris) during the recovery of photosensitivity and during photostimulation. J. Reprod. Fertil., 111, 1e6. Dawson, A., Follett, B. K., Goldsmith, A. R., & Nicholls, T. J. (1985). Hypothalamic gonadotrophin-releasing hormone and pituitary and plasma FSH and prolactin during photostimulation and photorefractoriness in intact and thyroidectomized starlings (Sturnus vulgaris). J. Endocrinol., 105, 71e77. Dawson, A., & McNaughton, F. J. (1993). Circannual rhythms in starlings: response of castrated birds to 12-hr days depends on photoperiodic history. J. Biol. Rhythms, 8, 141e150. Dawson, A., & Sharp, P. J. (1998). The role of prolactin in the development of reproductive photorefractoriness and postnuptial molt in the European starling (Sturnus vulgaris). Endocrinology, 139, 485e490.

Hormones and Reproduction of Vertebrates

Dawson, A., & Thapliyal, J. P. (2001). The thyroid and photoperiodism. In A. Dawson, & C. M. Chatruvedi (Eds.), Avian endocrinology (pp. 141e151). New Delhi, India: Narosa. Dawson, A., Goldsmith, A. R., Nicholls, T. J., & Follett, B. K. (1986). Endocrine changes associated with the termination of photorefractoriness by short daylengths and thyroidectomy in starlings (Sturnus vulgaris). J. Endocrinol., 110, 73e79. Dawson, A., King, V. M., Bentley, G. E., & Ball, G. F. (2001). Photoperiodic control of seasonality in birds. J. Biol. Rhythms, 16, 365e380. Doi, M., Nakajima, Y., Okano, T., & Fukada, Y. (2001). Light-induced phase-delay of the chicken pineal circadian clock is associated with the induction of cE4bp4, a potential transcriptional repressor of cPer2 gene. Proc. Natl. Acad. Sci. USA, 98, 8089e8094. Drent, R. (1975). Incubation. In D. S. Farner, & J. R. King (Eds.), Avian Biology, Vol. 5 (pp. 333e420). New York, NY: Academic Press. Dunn, I. C., & Sharp, P. J. (1999). Photo-induction of hypothalamic gonadotrophin releasing hormone-I mRNA in the domestic chicken: a role for oestrogen? J. Neuroendocrinol., 11, 371e375. Dunn, I. C., Chen, Y., Hook, C., Sharp, P. J., & Sang, H. M. (1993). Characterization of the chicken preprogonadotrophin-releasing hormone-I gene. J. Mol. Endocrinol., 11, 19e29. El Halawani, M. E., Kang, S. W., Leclerc, B., Kosonsiriluk, S., & Chaiseha, Y. (2009). Dopamine-melatonin neurons in the avian hypothalamus and their role as photoperiodic clocks. Gen. Comp. Endocrinol. (In press). El Halawani, M. E., Pitts, G. R., Sun, S., Silsby, J. L., & Sivanandan, V. (1996). Active immunization against vasoactive intestinal peptide prevents photo-induced prolactin secretion in turkeys. Gen. Comp. Endocrinol., 104, 76e83. El Halawani, M. E., Silsby, J. L., Behnke, E. J., & Fehrer, S. C. (1986). Hormonal induction of incubation behavior in ovariectomized female turkeys (Meleagris gallopavo). Biol. Reprod., 35, 59e67. Etches, R. J., & Cunningham, F. J. (1977). The plasma concentrations of testosterone and LH during the ovulation cycle of the hen (Gallus domesticus). Acta Endocrinol. (Copenh.), 84, 357e566. Farner, D. S., & Follett, B. K. (1979). In E. J. W. Barrington (Ed.), Hormones and Evolution. Reproductive periodicity in birds, Vol. 2 (pp. 829e872). New York: Academic Press. Follett, B. K. (1973). Circadian rhythms and photoperiodic time measurement in birds. J. Reprod. Fertil. Suppl., 19, 5e18. Follett, B. K. (1976). Plasma follicle-stimulating hormone during photoperiodically induced sexual maturation in male Japanese quail. J. Endocrinol., 69, 117e126. Follett, B. K. (1984). In G. E. Lamming (Ed.), Marshall’s physiology of reproduction 4th Edition. Birds, Vol. 1 (pp. 283e350). New York, NY: Churchill-Livingstone. Follett, B. K., & Nicholls, T. J. (1988). Acute effect of thyroid hormones in mimicking photoperiodically induced release of gonadotropins in Japanese quail. J. Comp. Physiol. B, Biochem. Syst. Environ. Physiol., 157, 837e843. Follett, B. K., & Robinson, J. E. (1980). Photoperiod and gonadotrophin secretion in birds. In R. J. Reiter, & B. K. Follett (Eds.), Seasonal Reproduction in Higher Vertebrates. Progress in Reproductive Biology, Vol. 5 (pp. 39e61). Follett, B. K., & Sharp, P. J. (1969). Circadian rhythmicity in photoperiodically induced gonadotrophin release and gonadal growth in the quail. Nature, 223, 968e971.

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

Follett, B. K., Davies, D. T., & Gledhill, B. (1977). Photoperiodic control of reproduction in Japanese quail: changes in gonadotrophin secretion on the first day of induction and their pharmacological blockade. J. Endocrinol., 74, 449e460. Follett, B. K., Mattocks, P. W., & Farner, D. S. (1974). Circadian function in the photoperiodic induction of gonadotropin secretion in the whitecrowned sparrow. Proc. Natl. Acad. Sci. USA, 71, 1666e1669. Follett, B. K., Scanes, C. G., & Cunningham, F. J. (1972). A radioimmunoassay for avian luteinizing hormone. J. Endocrinol., 52, 359e378. Foster, R. G., Plowman, G., Goldsmith, A. R., & Follett, B. K. (1987). Immunohistochemical demonstration of marked changes in the LHRH system of photosensitive and photorefractory European starlings (Sturnus vulgaris). J. Endocrinol., 115, 211e220. Fraps, R. M. (1955). Egg production and fertility in poultry. In J. Hammond (Ed.), Progress in the physiology of farm animals. (pp. 661e740). London, UK: Butterworth. Fraps, R. M. (1970). Photoregulation in the ovulation cycle of the domestic fowl. In J. Benoit, & I. Assenmacher (Eds.), La photoregulation de la reproduction chez les oiseaux ex les mammiferes (pp. 281e306). Paris, France: CNRS. Fraser, H. M., & Sharp, P. J. (1978). Prevention of positive feedback in the hen (Gallus domesticus) by antibodies to luteinizing hormone releasing hormone. J. Endocrinol., 76, 181e182. Fukusumi, S., Fujii, R., & Hinuma, S. (2006). Recent advances in mammalian RFamide peptides: the discovery and functional analyses of PrRP, RFRPs and QRFP. Peptides, 27, 1073e1086. Fukada, Y., & Okano, T. (2002). Circadian clock system in the pineal gland. Mol. Neurobiol., 25, 19e30. Furr, B. J., Bonney, R. C., England, R. J., & Cunningham, F. J. (1973). Luteinizing hormone and progesterone in peripheral blood during the ovulatory cycle of the hen Gallus domesticus. J. Endocrinol., 57, 159e169. Gibson, W. R., Follett, B. K., & Gledhill, B. (1975). Plasma levels of luteinizing hormone in gonadectomized Japanese quail exposed to short or to long daylengths. J. Endocrinol., 64, 87e101. Goldman, B. D. (2001). Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement. J. Biol. Rhythms, 16, 283e301. Goldsmith, A. R. (1982). Plasma concentrations of prolactin during incubation and parental feeding throughout repeated breeding cycles in canaries (Serinus canarius). J. Endocrinol., 94, 51e59. Goldsmith, A. R. (1985). Prolactin in avian reproduction: incubation and the control of seasonal breeding. In R. M. Macleod, U. Scapagnini, & M. O. Thorner (Eds.), Prolactin. Fidia Research Series, Vol. 1 (pp. 411e429). Berlin, Germany: Liviana Press, Padova and SpringerVerlag. Goldsmith, A. R., & Nicholls, T. J. (1992). Thyroxine effects upon reproduction, prolactin secretion and plumage moult in thyroidectomised European starlings Sturnus vulgaris. Ornis. Scand., 23, 398e404. Goldsmith, A. R., & Williams, D. M. (1980). Incubation in mallards (Anas platyrhynchos): changes in plasma levels of prolactin and luteinizing hormone. J. Endocrinol., 86, 371e379. Goldsmith, A. R., Edwards, C., Koprucu, M., & Silver, R. (1981). Concentrations of prolactin and luteinizing hormone in plasma of doves in relation to incubation and development of the crop gland. J. Endocrinol., 90, 437e443.

19

Goodson, J. L. (1998a). Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm. Behav., 34, 67e77. Goodson, J. L. (1998b). Vasotocin and vasoactive intestinal polypeptide modulate aggression in a territorial songbird, the violet-eared waxbill (Estrildidae: Uraeginthus granatina). Gen. Comp. Endocrinol., 111, 233e244. Goodson, J. L., & Adkins-Regan, E. (1999). Effect of intraseptal vasotocin and vasoactive intestinal polypeptide infusions on courtship song and aggression in the male zebra finch (Taeniopygia guttata). J. Neuroendocrinol., 11, 19e25. Guyomarc’h, C., & Guyomarc’h, J. C. (1995). Moulting cycles in European quail (Coturnix coturnix coturnix) under constant photoperiodic conditions. Biol. Rhythm Res., 26, 292e305. Guyomarc’h, C., Lumineau, S., Vivien-Roels, B., Richard, J., & Deregnaucourt, S. (2001). Effect of melatonin supplementation on the sexual development in European quail (Coturnix coturnix). Behav. Processes., 53, 121e130. Gwinner, E. (1986). Circannual Clocks. Berlin, Germany: SpringerVerlag. Gwinner, E. (1996). Circannual clocks in avian reproduction and migration. Ibis, 138, 47e63. Gwinner, E. (2003). Circannual rhythms in birds. Curr. Opin. Neurobiol., 13, 770e778. Gwinner, E., & Dittami, J. (1990). Endogenous reproductive rhythms in a tropical bird. Science, 249, 906e908. Gwinner, E., & Scheuerlein, A. (1999). Photoperiodic responsiveness of equatorial and temperate-zone stonechats. Condor, 101, 347e359. Hahn, T. P. (1998). Reproductive seasonality in an opportunistic breeder, the red crossbill. Loxia curvirostra. Ecology, 79, 2363e2375. Hamm, H. E., & Menaker, M. (1980). Retinal rhythms in chicks: circadian variation in melantonin and serotonin N-acetyltransferase activity. Proc. Natl. Acad. Sci. USA, 77, 4998e5002. Harshman, J. (2006). Classification and phylogeny of birds. In G. M. Jamieson (Ed.), Reproductive biology and phylogeny, Vol. 6A (pp. 1e35). Enfield, NH: Science Publishers. Hattori, A., Ishii, S., & Wada, M. (1986). Effects of two kinds of chicken luteinizing hormone-releasing hormone (LH-RH), mammalian LHRH and its analogs on the release of LH and FSH in Japanese quail and chicken. Gen. Comp. Endocrinol., 64, 446e455. Hattori, A., Ishii, S., Wada, M., Miyamoto, K., Hasegawa, Y., Igarashi, M., et al. (1985). Effects of chicken (Gln8)- and mammalian (Arg8)-luteinizing hormone-releasing hormones on the release of gonadotrophins in vitro and in vivo from the adenohypophysis of Japanese quail. Gen. Comp. Endocrinol., 59, 155e161. Hau, M., Wikelski, M., & Wingfield, J. C. (1998). A neotropical bird can measure changes in tropical photoperiod. Proc. R. Soc. London B., 265, 89e95. Hertelendy, F. (1972). Prostaglandin-induced premature oviposition in the coturnix quail. Prostaglandins, 2, 269e279. Hinde, R. A. (1965). Interaction of internal and external factors in integration of canary reproduction. In F. A. Beach (Ed.), Sex and Behavior (pp. 381e415). New York, NY: John Wiley. Hinuma, S., Shintani, Y., Fukusumi, S., Iijima, N., Matsumoto, Y., Hosoya, M., et al. (2000). New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat. Cell Biol., 2, 703e708.

20

Huang, Y. M., Shi, Z. D., Liu, Z., Liu, Y., & Li, X. W. (2008). Endocrine regulations of reproductive seasonality, follicular development and incubation in Magang geese. Anim. Reprod. Sci., 104, 344e358. Immelmann, K. (1971). Ecological aspects of photoperiodic reproduction. In D. S. Farner, & J. R. King (Eds.), Avian Biology, Vol. 1 (pp. 341e389). New York, NY: Academic Press. Janik, D. S., & Buntin, J. D. (1985). Behavioural and physiological effects of prolactin in incubating ring doves. J. Endocrinol., 105, 201e209. Johnson, A. L. (1986). Reproduction in the male. In P. D. Sturkie (Ed.), Avian Physiology 4th Edition (pp. 432e451). New York, NY: Springer-Verlag. Jones, R. E. (1971). The incubation patch of birds. Biol. Rev., 46, 315e339. Jurkevich, A., & Grossmann, R. (2003). Vasotocin and reproductive functions of the domestic chicken. Domest. Anim. Endocrinol., 25, 93e99. Juss, T. S., Meddle, S. L., Servant, R. S., & King, V. M. (1993). Melatonin and photoperiodic time measurement in Japanese quail (Coturnix coturnix japonica). Proc. Biol. Sci., 254, 21e28. Kameda, Y., Miura, M., & Maruyama, S. (2002). Effect of pinealectomy on the photoperiod-dependent changes of the specific secretory cells and alpha-subunit mRNA level in the chicken pars tuberalis. Cell Tissue Res., 308, 121e130. Kang, S. W., Thayananuphat, A., Bakken, T., & El Halawani, M. E. (2007). Dopamine-melatonin neurons in the avian hypothalamus controlling seasonal reproduction. Neuroscience, 150, 223e233. Kang, S. W., Thayananuphat, A., Rozenboim, I., Millam, J. R., Proudman., J. A., & El Halawani, M. E. (2006). Expression of hypothalamic GnRH-I mRNA in the female turkey at different reproductive states and following photostimulation. Gen. Comp. Endocrinol., 146, 91e99. Kihlstro¨m, J. E., & Danninge, I. (1972). Neurohypophysial hormones and sexual behavior in males of the domestic fowl (Gallus domesticus l.) and the pigeon (Columba livia gmel.). Gen. Comp. Endocrinol., 18, 115e120. King, J. A., & Millar, R. P. (1982). Structure of chicken hypothalamic luteinizing hormone-releasing hormone. II. Isolation and characterization. J. Biol. Chem., 257, 10729e10732. King, J. A., Davidson, J. S., Mehl, A. E., Wakefield, I. K., Andersson, P. B., & Millar, R. P. (1989a). Gonadal steroid modulation of signal transduction and luteinizing hormone release in cultured chicken pituitary cells. Endocrinology, 124, 1830e1840. King, J. A., Mehl, A. E., Tyndale-Biscoe, C. H., Hinds, L., & Millar, R. P. (1989b). A second form of gonadotropin-releasing hormone (GnRH), with chicken GnRH II-like properties, occurs together with mammalian GnRH in marsupial brains. Endocrinology, 125, 2244e2252. Koike, T. I., Shimada, K., & Cornett, L. E. (1988). Plasma levels of immunoreactive mesotocin and vasotocin during oviposition in chickens: relationship to oxytocic action of the peptides in vitro and peptide interaction with myometrial membrane binding sites. Gen. Comp. Endocrinol., 70, 119e126. Lack, D. (1968). Ecological adaptations for breeding in birds. London, UK: Methuen. Lague¨, P. C., Van Tienhoven, A., & Cunningham, F. J. (1975). Concentrations of estrogens, progesterone and LH during the ovulatory cycle of the laying chicken [Gallus domesticus]. Biol. Reprod., 12, 590e598.

Hormones and Reproduction of Vertebrates

Lehrman, D. S. (1965). Interaction between internal and external environments in the regulation of the reproductive cycle of the ring dove. In F. Beach (Ed.), Sex and Behavior (pp. 355e380). New York, NY: Wiley. Lehrman, D. S., & Brody, P. N. (1964). Effect of prolactin on established incubation behavior in the ringdove. J. Comp. Physiol. Psychol., 57, 161e165. Leopold, A. S., Erwin, M., Oh, J., & Browning, B. (1976). Phytoestrogens: adverse effects on reproduction in California quail. Science, 191, 98e100. Li, D., Tsutsui, K., Muneoka, Y., Minakata, H., & Nomoto, K. (1996). An oviposition-inducing peptide: isolation, localization, and function of avian galanin in the quail oviduct. Endocrinology, 137, 1618e1626. Li, Z. Z., & Burke, W. H. (1987). Influence of 12 hours of sound stimuli on gonad development and plasma luteinizing hormone in Japanese quail (Coturnix coturnix japonica) exposed to 6 hours of daily light. Poult. Sci., 66, 1045e1052. Macnamee, M. C., Sharp, P. J., Lea, R. W., Sterling, R. J., & Harvey, S. (1986). Evidence that vasoactive intestinal polypeptide is a physiological prolactin-releasing factor in the bantam hen. Gen. Comp. Endocrinol., 62, 470e478. Maddineni, S. R., Oco´n-Grove, O. M., Krzysik-Walker, S. M., Hendricks, G. L., 3rd, & Ramachandran, R. (2008). Gonadotropininhibitory hormone (GnIH) receptor gene is expressed in the chicken ovary: potential role of GnIH in follicular maturation. Reproduction, 135, 267e274. Madison, F. N., Jurkevich, A., & Kuenzel, W. J. (2008). Sex differences in plasma corticosterone release in undisturbed chickens (Gallus gallus) in response to arginine vasotocin and corticotropin releasing hormone. Gen. Comp. Endocrinol., 155, 566e573. Maney, D. L., Goode, C. T., & Wingfield, J. C. (1997a). Intraventricular infusion of arginine vasotocin induces singing in a female songbird. J. Neuroendocrinol., 9, 487e491. Maney, D. L., Richardson, R. D., & Wingfield, J. C. (1997b). Central administration of chicken gonadotropin-releasing hormone-II enhances courtship behavior in a female sparrow. Horm. Behav., 32, 11e18. Mantei, K. E., Ramakrishnan, S., Sharp, P. J., & Buntin, J. D. (2008). Courtship interactions stimulate rapid changes in GnRH synthesis in male ring doves. Horm. Behav., 54, 669e675. Marshall, A. J. (1970). Environmental factors other than light involved in the control of sexual cycle in birds and mammals. In J. Benoit, & I. Assenmacher (Eds.), La Photore´gulation de la Reproduction chez les Oiseaux et les Mammife´res (pp. 53e65). Paris, France: CNRS. Marshall, F. H. A. (1936). Sexual periodicity and the causes which determine it. Philos. Trans. R. soc. Lond. B, 226, 423e456. Mashaly, M. M., Birrenkott, G. P., El-Begearmi, M. M., & Wentworth, B. C. (1976). Plasma LH progesterone concentrations in the turkey hen during the ovulatory cycle. Poult. Sci., 55, 1226e1234. Matsumoto, A., & Ishii, S. (1992). Atlas of Endocrine Organs: Vertebrates and Invertebrates. Berlin, Germany: Springer-Verlag. Matsuo, H., Baba, Y., Nair, R. M., Arimura, A., & Schally, A. V. (1971). Structure of the porcine LH- and FSH-releasing hormone. I. The proposed amino acid sequence. Biochem. Biophys. Res. Commun., 43, 1334e1339. Mattocks, P. W., Jr., Farner, D. S., & Follett, B. K. (1976). The annual cycle in luteinizing hormone in the plasma of intact and castrated

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

white-crowned sparrows, Zonotrichia leucophrys gambelii. Gen. Comp. Endocrinol., 30, 156e161. McGuire, N. L., Ubuka, T., Perfito, N., & Bentley, G. E. (2009). A Novel Neuropeptide System Within the Gonads: GnIH and GnIH-R in Passerine Songbirds. Boston, MA: Paper presented at the Annual Meeting for the Society for Integrative and Comparative Biology. Meddle, S. L., & Follett, B. K. (1997). Photoperiodically driven changes in Fos expression within the basal tuberal hypothalamus and median eminence of Japanese quail. J. Neurosci., 17, 8909e8918. Meddle, S. L., Maney, D. L., & Wingfield, J. C. (1999). Effects of N-methyl-D-aspartate on luteinizing hormone release and Foslike immunoreactivity in the male white-crowned sparrow (Zonotrichia leucophrys gambelii). Endocrinology, 140, 5922e5928. Meier, A. H. (1972). Temporal synergism of prolactin and adrenal steroids in the regulation of fat storage. Gen. Comp. Endocrinol. Suppl., 3, 499e508. Meier, A. H., & MacGregor, R. (1972). Temporal organization in avian reproduction. Am. Zool., 12, 257e271. Mikami, S.-I., Oksche, A., Farner, D. S., & Vitums, A. (1970). Fine structure of the vessels of the hypohysial portal system of the whitecrowned sparrow, Zonotrichia leucophrys gambelii. Zeitschrift fu¨r Z. Zellforsch, 106, 155e174. Mikami, S., Yamada, S., Hasegawa, Y., & Miyamoto, K. (1988). Localization of avian LHRH-immunoreactive neurons in the hypothalamus of the domestic fowl, Gallus domesticus, and the Japanese quail. Coturnix coturnix. Cell Tissue Res., 251, 51e58. Millam, J. R., El Halawani, M. E., & Burke, W. H. (1985). Effect of cyclic sound cues on sexual development in nonphotostimulated Japanese quail. Poult. Sci., 64, 169e175. Millar, R. P. (2003). GnRH II and type II GnRH receptors. Trends Endocrinol. Metab., 14, 35e43. Millar, R. P. (2005). GnRHs and GnRH receptors. Anim. Reprod. Sci., 88, 5e28. Millar, R. P., & King, J. A. (1983). Synthesis and biological activity of [D-Trp6] chicken luteinizing hormone-releasing hormone. Peptides, 4, 425e429. Millar, R. P., Lu, Z. L., Pawson, A. J., Flanagan, C. A., Morgan, K., & Maudsley, S. R. (2004). Gonadotropin-releasing hormone receptors. Endocr. Rev., 25, 235e275. Miyamoto, K., Hasegawa, Y., Minegishi, T., Nomura, M., Takahashi, Y., Igarashi, M., et al. (1982). Isolation and characterization of chicken hypothalamic luteinizing hormone-releasing hormone. Biochem. Biophys. Res. Commun., 107, 820e827. Miyamoto, K., Hasegawa, Y., Nomura, M., Igarashi, M., Kangawa, K., & Matsuo, H. (1984). Identification of the second gonadotropinreleasing hormone in chicken hypothalamus: evidence that gonadotropin secretion is probably controlled by two distinct gonadotropinreleasing hormones in avian species. Proc. Natl. Acad. Sci. USA, 81, 3874e3878. Morgan, K., & Millar, R. P. (2004). Evolution of GnRH ligand precursors and GnRH receptors in protochordate and vertebrate species. Gen. Comp. Endocrinol., 139, 191e197. Morris, J. A. (1961). The effect of continuous light and continuous noise on pullets held in a sealed chamber. Poult. Sci., 40, 995e1000. Morris, T. R., & Bhatti, B. M. (1978). Entrainment of oviposition in the fowl using bright and dim light cycles. Br. Poult. Sci., 19, 341e348.

21

Munsick, R. A., Sawyar, W. H., & Van Dyke, H. B. (1960). Avian neurohypophysial hormone: pharmacological properties and tentative identification. Endocrinology, 66, 860e871. Murakami, N., Nakamura, H., Nishi, R., Marumoto, N., & Nasu, T. (1994). Comparison of circadian oscillation of melatonin release in pineal cells of house sparrow, pigeon and Japanese quail, using cell perfusion systems. Brain Res., 651, 209e214. Murton, R. K., & Westood, N. J. (1977). Avian Breeding Cycles. Oxford, UK: Clarendon Press. Nakao, N., Ono, H., Yamamura, T., Anraku, T., Takagi, T., Higashi, K., et al. (2008a). Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature, 452, 317e322. Nakao, N., Ono, H., & Yoshimura, T. (2008b). Thyroid hormones and seasonal reproductive neuroendocrine interactions. Reproduction, 136, 1e8. Nicholls, T. J. (1974). Changes in plasma LH levels during a photoperiodically controlled reproductive cycle in the canary (Serinus canarius). Gen. Comp. Endocrinol., 24, 442e445. Nicholls, T. J., & Storey, C. R. (1976). The effects of castration on plasma LH levels in photosensitive and photorefractory canaries (Serinus canarius). Gen. Comp. Endocrinol., 29, 170e174. Nicholls, T. J., Follett, B. K., & Robinson, J. E. (1983). A photoperiodic response in gonadectomized Japanese quail exposed to a single long day. J. Endocrinol., 97, 121e126. Nicholls, T. J., Goldsmith, A. R., & Dawson, A. (1988). Photorefractoriness in birds and comparison with mammals. Physiol. Rev., 68, 133e176. Nilsson, A. (1975). Structure of the vasoactive intestinal octacosapeptide from chicken intestine. The amino acid sequence. FEBS Lett., 60, 322e326. Norgren, R. B, Jr., & Lehman, M. N. (1991). Neurons that migrate from the olfactory epithelium in the chick express luteinizing hormonereleasing hormone. Endocrinology, 128, 1676e1678. Norgren, R. B, Jr., & Silver, R. (1989). Retinohypothalamic projections and the suprachiasmatic nucleus in birds. Brain Behav. Evol., 34, 73e83. Norgren, R. B, Jr., & Silver, R. (1990). Distribution of vasoactive intestinal peptide-like and neurophysin-like immunoreactive neurons and acetylcholinesterase staining in the ring dove hypothalamus with emphasis on the question of an avian suprachiasmatic nucleus. Cell Tissue Res., 259, 331e339. Norris, D. O. (2007). Vertebrate Endocrinology (4th ed.). New York, NY: Academic press. Nouwen, E. J., Decuypere, E., Ku¨hn, E. R., Michels, H., Hall, T. R., & Chadwick, A. (1984). Effect of dehydration, haemorrhage and oviposition on serum concentrations of vasotocin, mesotocin and prolactin in the chicken. J. Endocrinol., 102, 345e351. Ohta, M., Kadota, C., & Konishi, H. (1989). A role of melatonin in the initial stage of photoperiodism in the Japanese quail. Biol. Reprod., 40, 935e941. Okano, T., & Fukada, Y. (2001). Photoreception and circadian clock system of the chicken pineal gland. Microsc. Res. Tech., 53, 72e80. Okano, T., Yamamoto, K., Okano, K., Hirota, T., Kasahara, T., Sasaki, M., et al. (2001). Chicken pineal clock genes: implication of BMAL2 as a bidirectional regulator in circadian clock oscillation. Genes Cells, 6, 825e836. Oksche, A., & Farner, D. S. (1974). Neurohistological studies of the hypothalamoehypophysial system of Zonotrichia leucophrys gambelii. Adv. Anat. Embryol. Cell Biol., 48, 1e136.

22

Olson, D. M., Biellier, H. V., & Hertelendy, F. (1978). Shell gland responsiveness to prostaglandin F2a in relation to oviposition in the domestic hen (Gallus domesticus). Biol. Reprod., 24, 496e504. Opel, H., & Proudman, J. A. (1988). Stimulation of prolactin release in turkeys by vasoactive intestinal peptide. Proc. Soc. Exp. Biol. Med., 187, 455e460. Oshima, I., Yamada, H., Goto, M., Soto, K., & Ebihara, S. (1989). Pineal and retinal melatonin is involved in the control of circadian locomotor activity and body temperature rhythms in the pigeon. J. Comp. Physiol. A, 166, 217e226. Osugi, T., Ukena, K., Bentley, G. E., O’Brien, S., Moore, I. T., Wingfield, J. C., et al. (2004). Gonadotropin-inhibitory hormone in Gambel’s white-crowned sparrow (Zonotrichia leucophrys gambelii): cDNA identification, transcript localization and functional effects in laboratory and field experiments. J. Endocrinol., 182, 33e42. Owen-Ashley, N. T., & Wingfield, J. C. (2007). Acute phase responses of passerine birds: characterization and seasonal variation. J. Ornithol., 148(Suppl 2), S583eS591. Panzica, G. C., Fraschini, F., Aste, N., Lucini, V., Viglietti-Panzica, C., Cozzi, B., et al. (1994). The density of melatonin receptors is dependent upon the prevailing photoperiod in the Japanese quail (Coturnix japonica). Neurosci. Lett., 173, 111e114. Parry, D. M., Goldsmith, A. R., Millar, R. P., & Glennie, L. M. (1997). Immunocytochemical localization of GnRH precursor in the hypothalamus of European starlings during sexual maturation and photorefractoriness. J. Neuroendocrinol., 9, 235e243. Pe´czely, P., & Kiss, J. Z. (1988). Immunoreactivity to vasoactive intestinal polypeptide (VIP) and thyrotropin-releasing hormone (TRH) in hypothalamic neurons of the domesticated pigeon (Columba livia). Alterations following lactation and exposure to cold. Cell Tissue Res., 251, 485e494. Perfito, N., Bentley, G., & Hau, M. (2006). Tonic activation of brain GnRH immunoreactivity despite reduction of peripheral reproductive parameters in opportunistically breeding zebra finches. Brain Behav. Evol., 67, 123e134. Perfito, N., Kwong, J. M., Bentley, G. E., & Hau, M. (2008). Cue hierarchies and testicular development: is food a more potent stimulus than day length in an opportunistic breeder (Taeniopygia g. guttata)? Horm. Behav., 53, 567e572. Perrins, C. M. (1973). Some effects of temperature on breeding in the great tit and manx shearwater. J. Reprod. Fertil. Suppl., 19, 163e173. Proudman, J. A., & Opel, H. (1988). Stimulation of prolactin secretion from turkey anterior pituitary cells in culture. Proc. Soc. Exp. Biol. Med., 187, 448e454. Ralph, C. L., & Fraps, R. M. (1960). Induction of ovulation in the hen by injection of progesterone into the brain. Endocrinology, 66, 269e272. Reinert, B. D., & Wilson, F. E. (1996). Thyroid dysfunction and thyroxine-dependent programming of photoinduced ovarian growth in American tree sparrows (Spizella arborea). Gen. Comp. Endocrinol., 103, 71e81. Reppert, S. M., Weaver, D. R., Cassone, V. M., Godson, C., & Kolakowski, L. F., Jr. (1995). Melatonin receptors are for the birds: molecular analysis of two receptor subtypes differentially expressed in chick brain. Neuron., 15, 1003e1015. Ricklefs, R. E. (1970). Clutch size in birds: outcome of opposing predator and prey adaptations. Science, 168, 599e600. Riddle, O., Bates, R. W., & Lahr, E. L. (1935). Prolactin induces broodiness in fowl. Am. J. Zool., 111, 352e368.

Hormones and Reproduction of Vertebrates

Robinson, J. E., & Follett, B. K. (1982). Photoperiodism in Japanese quail: the termination of seasonal breeding by photorefractoriness. Proc. R. Soc. Lond., B, Biol. Sci., 215, 95e116. Romero, L. M., Soma, K. K., & Wingfield, J. C. (1998). Hypothalamicepituitaryeadrenal axis changes allow seasonal modulation of corticosterone in a bird. Am. J. Physiol., 274, 1338e1344. Rouille´, Y., Chauvet, M. T., Chauvet, J., & Acher, R. (1986). Phylogeny of neurohypophyseal hormones in birds: microidentification of mesotocin and vasotocin in the ostrich (Struthio camelus). C.R. Seances Soc. Biol. Fil., 180, 35e42. Rozenboim, I., Aharony, T., & Yahav, S. (2002). The effect of melatonin administration on circulating plasma luteinizing hormone concentration in castrated white leghorn roosters. Poult. Sci., 81, 1354e1359. Rzasa, J., & Ewy, Z. (1970). Effect of vasotocin and oxytocin on oviposition in the hen. J. Reprod. Fertil., 21, 549e550. Saito, N., & Koike, T. I. (1992). Alterations in uterine contractility during the oviposition cycle in domestic hens. Br. Poult. Sci., 33, 671e676. Sakai, H., & Ishii, S. (1980). Isolation and characterization of chicken follicle-stimulating hormone. Gen. Comp. Endocrinol., 42, 1e8. Sakamoto, H., Ubuka, T., Kohchi, C., Li, D., Ukena, K., & Tsutsui, K. (2000). Existence of galanin in lumbosacral sympathetic ganglionic neurons that project to the quail uterine oviduct. Endocrinology, 141, 4402e4412. Saldanha, C. J., Silverman, A. J., & Silver, R. (2001). Direct innervation of GnRH neurons by encephalic photoreceptors in birds. J. Biol. Rhythms, 16, 39e49. Sasaki, T., Shimada, K., & Saito, N. (1998). Changes of AVT levels in plasma, neurohypophysis and hypothalamus in relation to oviposition in the laying hen. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 121, 149e153. Satake, H., Hisada, M., Kawada, T., Minakata, H., Ukena, K., & Tsutsui, K. (2001). Characterization of a cDNA encoding a novel avian hypothalamic neuropeptide exerting an inhibitory effect on gonadotropin release. Biochem. J., 354, 379e385. Scanes, C. G. (1986). Pituitary gland. In P. D. Sturkie (Ed.), Avian Physiology (pp. 383e402). New York, NY: Springer-Verlag. Scanes, C. G., Chadwick, A., & Bolton, N. J. (1976). Radioimmunoassay of prolactin in the plasma of the domestic fowl. Gen. Comp. Endocrinol., 30, 12e20. Scanes, C. G., Godden, P. M., & Sharp, P. J. (1977). An homologous radioimmunoassay for chicken follicle-stimulating hormone: observations on the ovulatory cycle. J. Endocrinol., 73, 473e481. Schwanzel-Fukuda, M., & Pfaff, D. W. (1989). Origin of luteinizing hormone-releasing hormone neurons. Nature, 338, 161e164. Searcy, W. A. (1992). Measuring responses of female birds to male song. In P. K. McGregor (Ed.), Playback and Studies of Animal Communication (pp. 175e189). New York, NY: Plenum. Senior, B. E., & Cunningham, F. J. (1974). Oestradiol and luteinizing hormone during the ovulatory cycle of the hen. J. Endocrinol., 60, 201e202. Sharp, P. J. (1980). The endocrine control of ovulation in birds. Acta Cong. Int. Ornith., 17, 245e248. Sharp, P. J., & Klandorf, H. (1981). The interaction between day length and the gonads in the regulation of levels of plasma thyroxine and triiodothyronine in the Japanese quail. Gen. Comp. Endocrinol., 45, 504e512.

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

Sharp, P. J., & Sreekumar, K. P. (2001). Photoperiodic control of prolactin secretion. In A. Dawson, & C. M. Chaturvedi (Eds.), Avian Endocrinology (pp. 245e255). New Delhi, India: Narosa. Sharp, P. J., Macnamee, M. C., Sterling, R. J., Lea, R. W., & Pedersen, H. C. (1988). Relationships between prolactin, LH and broody behaviour in bantam hens. J. Endocrinol., 118, 279e286. Sharp, P. J., Sterling, R. J., Talbot, R. T., & Huskisson, N. S. (1989). The role of hypothalamic vasoactive intestinal polypeptide in the maintenance of prolactin secretion in incubating bantam hens: observations using passive immunization, radioimmunoassay and immunohistochemistry. J. Endocrinol., 122, 5e13. Sharp, P. J., Talbot, R. T., Main, G. M., Dunn, I. C., Fraser, H. M., & Huskisson, N. S. (1990). Physiological roles of chicken LHRH-I and -II in the control of gonadotrophin release in the domestic chicken. J. Endocrinol., 124, 291e299. Sherwood, N. M., Wingfield, J. C., Ball, G. F., & Dufty, A. M. (1988). Identity of gonadotropin-releasing hormone in passerine birds: comparison of GnRH in song sparrow (Melospiza melodia) and starling (Sturnus vulgaris) with five vertebrate GnRHs. Gen. Comp. Endocrinol., 69, 341e351. Shimada, K., Neldon, H. L., & Koike, T. I. (1986). Arginine vasotocin (AVT) release in relation to uterine contractility in the hen. Gen. Comp. Endocrinol., 64, 362e367. Shimizu, M., & Be´de´carrats, G. Y. (2006). Identification of a novel pituitary-specific chicken gonadotropin-releasing hormone receptor and its splice variants. Biol. Reprod., 75, 800e808. Shimizu, T., Cox, K., Karten, H. J., & Britto, L. R. (1994). Cholera toxin mapping of retinal projections in pigeons (Columbia livia), with emphasis on retinohypothalamic connections. Vis Neurosci., 11, 441e446. Sibley, C. G., & Monroe, B. L., Jr. (1990). Distribution and Taxonomy of Birds of the World. New Haven, CT: Yale University Press. Silver, R., Witkovsky, P., Horvath, P., Alones, V., Barnstable, C. J., & Lehman, M. N. (1988). Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res., 253, 189e198. Small, T. W., Sharp, P. J., Bentley, G. E., Millar, R. P., Tsutsui, K., Mura, E., et al. (2008). Photoperiod-independent hypothalamic regulation of luteinizing hormone secretion in a free-living Sonoran desert bird, the Rufous-winged Sparrow (Aimophila carpalis). Brain Behav. Evol., 71, 127e142. Solomon, S. E. (1983). Oviduct. In B. M. Freeman (Ed.), Physiology and Biochemistry of the Domestic Fowl (pp. 379e420). London, UK: Academic Press. Stevenson, T. J., Bentley, G. E., Ubuka, T., Arckens, L., Hampson, E., & MacDougall-Shackleton, S. A. (2008). Effects of social cues on GnRH-I, GnRH-II, and reproductive physiology in female house sparrows (Passer domesticus). Gen. Comp. Endocrinol., 156, 385e394. Stevenson, T. J., Lynch, K. S., Lamba, P., Ball, G. F., & Bernard, D. J. (2009). Cloning of gonadotropin-releasing hormone I complementary DNAs in songbirds facilitates dissection of mechanisms mediating seasonal changes in reproduction. Endocrinology. (In press). Stokes, T. M., Leonard, C. M., & Nottebohm, F. (1974). The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J. Comp. Neurol., 156, 337e374.

23

Storey, C. R., Nicholls, T. J., & Follett, B. K. (1980). Castration accelerates the rate of onset of photorefractoriness in the canary (Serinus canarius). Gen. Comp. Endocrinol., 42, 315e319. Sun, Y. M., Dunn, I. C., Baines, E., Talbot, R. T., Illing, N., Millar, R. P., et al. (2001a). Distribution and regulation by oestrogen of fully processed and variant transcripts of gonadotropin releasing hormone I and gonadotropin releasing hormone receptor mRNAs in the male chicken. J. Neuroendocrinol., 13, 37e49. Sun, Y. M., Flanagan, C. A., Illing, N., Ott, T. R., Sellar, R., Fromme, B. J., et al. (2001b). A chicken gonadotropin-releasing hormone receptor that confers agonist activity to mammalian antagonists. Identification of D-Lys(6) in the ligand and extracellular loop two of the receptor as determinants. J. Biol. Chem., 276, 7754e7761. Takahashi, T., Kawashima, M., Kamiyoshi, M., & Tanaka, K. (1992). Arginine vasotocin binding component in the uterus (shell gland) of the chicken. Acta Endocrinol. (Copenh.), 127, 179e184. Takahashi, J. S., & Menaker, M. (1984). Multiple redundant circadian oscillators within the isolated avian pineal gland. J. Comp. Physiol. A, 154, 435e440. Talbot, R. T., Dunn, I. C., Wilson, P. W., Sang, H. M., & Sharp, P. J. (1995). Evidence for alternative splicing of the chicken vasoactive intestinal polypeptide gene transcript. J. Mol. Endocrinol., 15, 81e91. Tanabe, Y. (1977). Differences in the endocrine mechanism of ovulation of the domestic fowl and the Japanese quail. In B. K. Follett (Ed.), Proceedings of the First International Symposium on Avian Endocrinology (pp. 68e70). Bangor: University College of North Wales. Tanaka, K., Goto, K., Yoshioka, T., Terao, T., & Koga, O. (1984). Changes in the plasma concentration of immunoreactive arginine vasotocin during oviposition in the domestic fowl. Br. Poult. Sci., 25, 589e595. Tobari, Y., Iijima, N., Tsunekawa, K., Osugi, T., Okanoya, K., Tsutsui, K., et al. (2010). Identification of gonadotropin-inhibitory hormone in the zebra finch (Taeniopygia guttata): peptide isolation, cDNA cloning and brain distribution. Peptides. In press. Toth, M., Olson, D. M., & Hertelendy, F. (1979). Binding of prostaglandin F2a to membranes of shell gland muscle of laying hens: correlations with contractile activity. Biol. Reprod., 20, 390e398. Tsutsui, K., & Ukena, K. (2006). Hypothalamic LPXRF-amide peptides in vertebrates: identification, localization and hypophysiotropic activity. Peptides, 27, 1121e1129. Tsutsui, K., Li, D., Azumaya, Y., Muneoka, Y., Minakata, H., & Nomoto, K. (1997). Demonstration, localization, and development of galanin receptors in the quail oviduct. J. Exp. Zool., 277, 57e65. Tsutsui, K., Li, D., Ukena, K., Kikuchi, M., & Ishii, S. (1998). Developmental changes in galanin receptors in the quail oviduct and the effect of ovarian sex steroids on galanin receptor induction. Endocrinology, 139, 4230e4236. Tsutsui, K., Saigoh, E., Ukena, K., Teranishi, H., Fujisawa, Y., Kikuchi, M., et al. (2000). A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem. Biophys. Res. Commun., 275, 661e667. Ubuka, T., & Bentley, G. E. (2009). Identification, localization and regulation of passerine gonadotropin-releasing hormone-I messenger RNA. J. Endocrinol. (In press). Ubuka, T., Bentley, G. E., Ukena, K., Wingfield, J. C., & Tsutsui, K. (2005). Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain. Proc. Natl. Acad. Sci. USA, 102, 3052e3057.

24

Ubuka, T., Cadigan, P. A., Wang, A., Liu, J., & Bentley, G. E. (2009). Identification of European starling GnRH-I precursor mRNA and its seasonal regulation. Gen. Comp. Endocrinol. Ubuka, T., Kim, S., Huang, Y. C., Reid, J., Jiang, J., Osugi, T., et al. (2008a). Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and -II neurons in European starling brain. Endocrinology, 149, 268e278, Erratum in: Endocrinology 149, 4229. Ubuka, T., McGuire, N. L., Calisi, R. M., Perfito, N., & Bentley, G. E. (2008b). The control of reproductive physiology and behavior by gonadotropin-inhibitory hormone. Integr. Comp. Biol., 48, 560e569. Ubuka, T., Sakamoto, H., Li, D., Ukena, K., & Tsutsui, K. (2001). Developmental changes in galanin in lumbosacral sympathetic ganglionic neurons innervating the avian uterine oviduct and galanin induction by sex steroids. J. Endocrinol., 170, 357e368. Ubuka, T., Ueno, M., Ukena, K., & Tsutsui, K. (2003). Developmental changes in gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica) hypothalamoehypophysial system. J. Endocrinol., 178, 311e318. Ubuka, T., Ukena, K., Sharp, P. J., Bentley, G. E., & Tsutsui, K. (2006). Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology, 147, 1187e1194. Ukena, K., Ubuka, T., & Tsutsui, K. (2003). Distribution of a novel avian gonadotropin-inhibitory hormone in the quail brain. Cell Tissue Res., 312, 73e79. Underwood, H., Barrett, R. K., & Siopes, T. (1990). The quail’s eye: a biological clock. J. Biol. Rhythms, 5, 257e265. Underwood, H., Binkley, S., Siopes, T., & Mosher, K. (1984). Melatonin rhythms in the eyes, pineal bodies, and blood of Japanese quail (Coturnix coturnix japonica). Gen. Comp. Endocrinol., 56, 70e81. Underwood, H., Steele, C. T., & Zivkovic, B. (2001). Circadian organization and the role of the pineal in birds. Microsc. Res. Tech., 53, 48e62. Van Gils, J., Absil, P., Grauwels, L., Moons, L., Vandesande, F., & Balthazart, J. (1993). Distribution of luteinizing hormone-releasing hormones I and II (LHRH-I and -II) in the quail and chicken brain as demonstrated with antibodies directed against synthetic peptides. J. Comp. Neurol., 334, 304e323. Van Tienhoven, A., & Schally, A. V. (1972). Mammalian luteinizing hormone-releasing hormone induces ovulation in the domestic fowl. Gen. Comp. Endocrinol., 19, 594e595. Wada, Y., Okano, T., & Fukada, Y. (2000). Phototransduction molecules in the pigeon deep brain. J. Comp. Neurol., 428, 138e144. Warren, D. C., & Scott, H. M. (1936). Influence of light on ovulation in the fowl. J. Exp. Zool., 74, 137e156. Wechsung, E., & Houvenaghel, A. (1976). A possible role of prostaglandins in the regulation of ovum transport and oviposition in the domestic hen? Prostaglandins, 12, 599e608. Wilson, F. E. (1991). Neither retinal nor pineal photoreceptors mediate photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea). J. Exp. Zool. 117e127. Wilson, F. E., & Follett, B. K. (1974). Plasma and pituitary luteinizing hormone in intact and castrated tree sparrows (Spizella arborea) during a photoinduced gonadal cycle. Gen. Comp. Endocrinol., 23, 82e93. Wilson, F. E., & Reinert, B. D. (1995). The photoperiodic control circuit in euthyroid American tree sparrows (Spizella arborea) is already

Hormones and Reproduction of Vertebrates

programmed for photorefractoriness by week 4 under long days. J. Reprod. Fertil., 103, 279e284. Wilson, F. E., & Reinert, B. D. (2000). Thyroid hormone acts centrally to programme photostimulated male American tree sparrows (Spizella arborea) for vernal and autumnal components of seasonality. J. Neuroendocrinol., 12, 87e95. Wilson, S. C., & Cunningham, F. J. (1981). Effect of photoperiod on the concentrations of corticosterone and luteinizing hormone in the plasma of the domestic hen. J. Endocrinol., 91, 135e143. Wilson, S. C., & Sharp, P. (1973). Variations in plasma LH levels during the ovulatory cycle of the hen, Gallus domesticus. J. Reprod. Fertil., 35, 561e564. Wingfield, J. C. (1983). Environmental and endocrine control of reproduction: an ecological approach. In S. I. Mikami, & M. Wada (Eds.), Avian Endocrinology: Environmental and Ecological Aspects (pp. 205e288). Berlin, Germany: Japanese Scientific Societies Press, Tokyo, and Springer-Verlag. Wingfield, J. C. (1993). Control of testicular cycles in the song sparrow, Melospiza melodia: interaction of photoperiod and an endogenous period? Gen. Comp. Endocrinol., 92, 388e401. Wingfield, J. C., & Farner, D. S. (1980). Control of seasonal reproduction in temperate-zone birds. In R. J. Reiter, & B. K. Follett (Eds.), Progress in Reproductive Biology, Vol. 5 (pp. 62e101). New York, NY: Karger. Wingfield, J. C., Follett, B. K., Matt, K. S., & Farner, D. S. (1980). Effect of day length on plasma FSH and LH in castrated and intact whitecrowned sparrows. Gen. Comp. Endocrinol., 42, 464e470. Wingfield, J. C., Jacobs, J. D., Tramontin, A. D., Perfito, N., Meddle, S., Maney, D. L., et al. (1999). In K. Wallen, & J. Schneider (Eds.), Reproduction in Context (pp. 85e128). Cambridge, MA: M.I.T. Press. Wingfield, J. C., Whaling, C. S., & Marler, P. R. (1994). Communication in vertebrate aggression and reproduction: the role of hormones. In E. Knobil, & J. D. Neil (Eds.), The Physiology of Reproduction (pp. 303e342). New York, NY: Raven Press. Wray, S., Grant, P., & Gainer, H. (1989). Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode. Proc. Natl. Acad. Sci. USA, 86, 8132e8136. Yamada, S., Mikami, S., & Yanaihara, N. (1982). Immunohistochemical localization of vasoactive intestinal polypeptide (VIP)-containing neurons in the hypothalamus of the Japanese quail, Coturnix coturnix. Cell Tissue Res., 226, 13e26. Yamamoto, K., Okano, T., & Fukada, Y. (2001). Chicken pineal Cry genes: light-dependent up-regulation of cCry1 and cCry2 transcripts. Neurosci, Lett., 313, 13e16. Yamamoto, N., Uchiyama, H., Ohki-Hamazaki, H., Tanaka, H., & Ito, H. (1996). Migration of GnRH-immunoreactive neurons from the olfactory placode to the brain: a study using avian embryonic chimeras. Brain. Res. Dev. Brain Res., 95, 234e244. Yamamura, T., Hirunagi, K., Ebihara, S., & Yoshimura, T. (2004). Seasonal morphological changes in the neuroeglial interaction between gonadotropin-releasing hormone nerve terminals and glial endfeet in Japanese quail. Endocrinology, 145, 4264e4267. Yamamura, T., Yasuo, S., Hirunagi, K., Ebihara, S., & Yoshimura, T. (2006). T(3) implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail. Cell Tissue Res., 324, 175e179.

Chapter | 1

Neuroendocrine Control of Reproduction in Birds

Yasuo, S., Watanabe, M., Nakao, N., Takagi, T., Follett, B. K., Ebihara, S., et al. (2005). The reciprocal switching of two thyroid hormoneactivating and -inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail. Endocrinology, 146, 2551e2554. Yasuo, S., Watanabe, M., Okabayashi, N., Ebihara, S., & Yoshimura, T. (2003). Circadian clock genes and photoperiodism: comprehensive analysis of clock gene expression in the mediobasal hypothalamus, the suprachiasmatic nucleus, and the pineal gland of Japanese quail under various light schedules. Endocrinology, 144, 3742e3748. Yin, H., Ukena, K., Ubuka, T., & Tsutsui, K. (2005). A novel G proteincoupled receptor for gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica): identification, expression and binding activity. J. Endocrinol., 184, 257e266. Yoshimura, T., Suzuki, Y., Makino, E., Suzuki, T., Kuroiwa, A., Matsuda, Y., et al. (2000). Molecular analysis of avian circadian clock genes. Brain Res. Mol. Brain Res., 78, 207e215. Yoshimura, T., Yasuo, S., Suzuki, Y., Makino, E., Yokota, Y., & Ebihara, S. (2001). Identification of the suprachiasmatic nucleus in birds. Am. J. Physiol. Regul. Integr. Comp. Physiol., 280, R1185eR1189. Yoshimura, T., Yasuo, S., Watanabe, M., Iigo, M., Yamamura, T., Hirunagi, K., & Ebihara, S. (2003). Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature, 426, 178e181.

25

You, S., Silsby, J. L., Farris, J., Foster, D. N., & El Halawani, M. E. (1995). Tissue-specific alternative splicing of turkey preprovasoactive intestinal peptide messenger ribonucleic acid, its regulation, and correlation with prolactin secretion. Endocrinology, 136, 2602e2610. Youngren, O. M., Chaiseha, Y., & El Halawani, M. E. (1998). Regulation of prolactin secretion by dopamine and vasoactive intestinal peptide at the level of the pituitary in the turkey. Neuroendocrinology, 68, 319e325. Youngren, O. M., Pitts, G. R., Phillips, R. E., & El Halawani, M. E. (1996). Dopaminergic control of prolactin secretion in the turkey. Gen. Comp. Endocrinol., 104, 225e230. Yuan, H., & Pang, S. F. (1990). [125I]Melatonin binding sites in membrane preparations of quail brain: characteristics and diurnal variations. Acta Endocrinol. (Copenh.), 122, 633e639. Yuan, H., & Pang, S. F. (1991). [125I]Iodomelatonin-binding sites in the pigeon brain: binding characteristics, regional distribution and diurnal variation. J. Endocrinol., 128, 475e482. Yuan, H., & Pang, S. F. (1992). [125I]Iodomelatonin binding sites in the chicken brain: diurnal variation and effect of melatonin injection or pinealectomy. Biol. Signals, 1, 208e218. Zann, R. A., Morton, S. R., Jones, K. R., & Burley, N. T. (1995). The timing of breeding by zebra finches in relation to rainfall in central Australia. Emu, 95, 208e222.

Chapter 2

Avian Testicular Structure, Function, and Regulation Pierre Deviche, Laura L. Hurley and H. Bobby Fokidis Arizona State University, Tempe, AZ, USA

SUMMARY In many birds, testes undergo dramatic annual changes in size and, as such, are among the most anatomically and physiologically plastic organs found in adult vertebrates. Adult testicular function is modulated by a myriad of external factors and orchestrated by numerous hormones that together enable birds to adapt to and breed in diverse habitats worldwide. These factors have generated a wide range of avian reproductive strategies, which has further shaped testicular structure and function. This chapter describes the mechanisms that control avian exocrine and endocrine testicular functions. It analyzes how these functions are regulated by ecological and behavioral factors and presents an overview of how environmental information is integrated and transduced into appropriate gonadal responses. It also discusses testicular dysfunction and the potential effects of anthropogenic disturbances on testis function. The chapter emphasizes areas where knowledge is lacking or incomplete, with the hope of fostering additional research on this exciting and fruitful area of avian biology.

1. CENTRAL MECHANISMS REGULATING TESTICULAR DEVELOPMENT Current studies of the hormonal regulation of testicular function focus on elucidating neuroendocrine pathways that integrate environmental information and convey it to the testes to initiate or terminate reproduction. This research is spurred by the development of novel molecular techniques and the identification of new neuropeptides that together enable researchers to uncover a multitude of neural processes regulating avian male reproduction. In vertebrates, the primary neural system responsible for regulating reproduction consists of hypothalamic neurons that secrete gonadotropin-releasing hormone (GnRH) into the median eminence. Of the three GnRH forms identified in birds thus far (King & Millar, 1982a; 1982b; Miyamoto et al., 1984; Berghman et al., 2000), Hormones and Reproduction of Vertebrates, Volume 4dBirds Copyright Ó 2011 Elsevier Inc. All rights reserved.

GnRH-I is considered the primary secretogogue of the gonadotropins (GTHs)dfollicle-stimulating hormone (FSH) and luteinizing hormone (LH)dfrom the pituitary gland (Kuenzel, 2000). The production and secretion of these hormones is presumably regulated also by the inhibitary neuropeptide, gonadotropin-inhibiting hormone (GnIH) (Tsutsui et al., 2000). The mechanisms of action of GnIH are not fully elucidated, but mounting evidence suggests that this neuropeptide acts at multiple levels: hypothalamus, anterior pituitary gland, and potentially the gonads (Bentley, Tsutsui, & Wingfield, 2007; see also Chapter 1, this volume). Several studies have also demonstrated an important role for thyroid hormones in regulating the seasonality of the male reproductive system (Dawson, Goldsmith, & Nicholls, 1984a, b; Goldsmith & Nicholls, 1984b; Lien & Siopes, 1991; Wilson & Reinert, 1993). Details of this regulatory action are not completely clear, but several lines of evidence support effects on GnRH production and secretion (Boulakoud & Goldsmith, 1991). Recent research has focused on how photic information is transduced into changes in GnRH cell function. One current model proposes that light-induced stimulation of neural thyrotropin (TSH) expression (Nakao et al., 2008) promotes the local conversion of thyroxine (T4) to triiodothyronine (T3) by the type 2 iodothyronine deiodinase (Dio2) (Yoshimura et al., 2003), which in turn stimulates GnRH release. The mechanism that controls this release is not fully understood and may involve a T3-mediated reduction of the encasement by glial cells of nerve terminals located in the median eminence (Yamamura, Yasuo, Hirunagi, Ebihara, & Yoshimura, 2006). The regulation of seasonal reproduction in birds may also involve a central role for brain-derived vasoactive intestinal peptide (VIP). Neurons producing VIP are thought to communicate directly with GnRH neurons and it has been proposed that they regulate the transduction of light signals to the reproductive system (Kiyoshi, Kondoh, 27

28

Hirunagi, & Korf, 1998; Teruyama & Beck, 2001). This mechanism remains poorly understood; some studies indicate an inverse relationship between VIP and GnRH expression (dark-eyed junco (Junco hyemalis) (Saldanha, Deviche, & Silver, 1994; Deviche, Saldanha, & Silver, 2000)) whereas other studies suggest that VIP stimulates the GnRH system (Li & Kuenzel, 2008).

2. ENDOCRINE INFLUENCE ON DEVELOPMENT OF THE AVIAN MALE PHENOTYPE Sex determination has been studied in more detail in mammals than in birds. Birds differ from mammals in that avian females are heterozygotic (ZW genotype) and males are homozygotic (ZZ genotype) (Kirby & Froman, 2000). In mammals, the sry gene on the Y chromosome codes for the expression of genes related to the development of the male phenotype. The absence of an sry gene homolog in birds results in the default formation of the male reproductive tract (Kirby & Froman, 2000). A survey of steroidogenic genes in developing chickens (Gallus gallus) demonstrated that embryos are capable of androgen synthesis by day two of incubation, but around day five only females express the aromatase enzyme (P450aro), which converts androgens to estrogens (Nomura, Nakabayashi, Nishimori, Yasue, & Mizuno, 1999). Sexual dimorphism in the expression of P450aro also has been observed in embryos of the Pekin duck (Anas platyrhynchos) (Koba et al., 2008b; 2008c), goose (Anser anser), and turkey (Meleagris gallopavo) (Koba et al., 2008b). A role for P450aro is further supported by studies utilizing P450aro inhibitors to convert genetic females to phenotypic males (Elbrecht & Smith, 1992) or individuals with mixed gender ovotestes (Koba et al., 2008a). In male embryos, P450aro may be inhibited by antiMu¨llerian hormone (AMH), named for its inhibitory effect on female Mu¨llerian duct development. Expression of AMH mRNA is greater in male than female chickens (Nishikimi et al., 2000; Yamamoto, Tsukada, Saito, & Shimada, 2003) and Japanese quail (Coturnix coturnix japonica) embryos (Nakamura et al., 2008). As demonstrated by studies in the chicken, the molecular control of AMH transcription remains poorly understood (Oreal, Mazaud, Picard, Magre, & Carre-Eusebe, 2002). Current research on sex determination in birds focuses on the specific roles of several ‘sex-determining’ genes (e.g., SF1, SOX9, DMRT1, and DAX1) (Oreal et al., 2002; Sechman, 2005) and on whether sex is controlled by ‘double dosing’ with Z chromosome (two in males, one in females) or the presence of the W chromosome in females.

Hormones and Reproduction of Vertebrates

3. AVIAN TESTICULAR ANATOMY Testes in birds are located deep in the abdominal cavity and are, therefore, visible only after removal of other organs, in particular the intestine. Testes are surrounded by a fibrous capsule that includes connective tissue and contractile fibers (Aire & Ozegbe, 2007). They contain interstitial tissue and seminiferous tubules, which are the site of spermatogenesis and, in developed testes, make up most of the testicular mass. Interstitial tissue includes Leydig or interstitial cells, the main source of testicular androgens (Dufty & Wingfield, 1986a; Galli, Irusta, & Wassermann, 1973; Halse, 1985; Madekurozwa, Chabvepi, Matema, & Teerds, 2002; Mauget, Jouventin, Lacroix, & Ishii, 1994; Nicholls & Graham, 1972; Rosenstrauch, Weil, Degen, & Friedlander, 1998; Woods & Domm, 1966) (see Section 3.1). Testes in some species are of identical sizes (e.g., tree swallow (Tachycineta bicolor) (Kempenaers, Peer, Vermeirssen, & Robertson, 2002); chicken (Hocking, 1992)), but many species show testicular size asymmetry, with one testis normally being larger in adulthood than the other (Yu, 1998; Gunn, Champion, Casey, Teal, & Casey, 2008). As in other vertebrates, the direction of testis size asymmetry within a species is generally consistent (Yu, 1998; Merila¨ & Sheldon, 1999). An extreme case of avian testicular asymmetry is found in coucals (Centropus sp.), which develop a single testis (Rand, 1933; Chapin, 1939; Ligon, 1997). The potential significance of avian testicular asymmetry is discussed below (Section 7.3).

3.1. Leydig Cells The ontogeny of Leydig cells has been described in the Japanese quail (Ottinger & Bakst, 1981). In this species, Leydig cells before and during hatching have a fibroblastlike appearance and are characterized by a smooth endoplasmic reticulum and lipid droplets, appearing two to three weeks posthatching, when plasma testosterone (T) increases. Consistent with this observation, steroidogenic activity of quail Leydig cells, as measured by 3b-hydroxysteroid dehydrogenase (3b-HSD), an enzyme that plays a key role in the conversion of cholesterol to androgens (Madekurozwa et al., 2002), is low during the first three weeks posthatching and then rapidly increases (Scheib, 1973). The ultrastructure of adult Leydig cells has been characterized in several species including the Mallard duck (A. platyrhynchos), chicken, budgerigar (Melopsittacus undulatus), white-crowned sparrow (Zonotrichia leucophrys), and Japanese quail (Connell, 1972; Humphreys, 1975; Lam & Farner, 1976; Aire, 1997; Rosenstrauch et al., 1998). Cells in these species show morphological changes that generally parallel their androgen secretion. For example, highly fertile, young adult chickens have

Chapter | 2

Avian Testicular Structure, Function, and Regulation

numerous tightly packed and functionally active Leydig cells and elevated plasma T. By contrast, older and less fertile chickens with low plasma T have fewer Leydig cells that show morphological signs of decreased androgen secretion (Rosenstrauch et al., 1998). Similar changes are observed when comparing Leydig cells during and outside the reproductive season in seasonal breeders (Humphreys, 1975; Lam & Farner, 1976; Rohss & Silverin, 1983; Tae et al., 2005). Photomanipulations of captive birds also support this conclusion. For example, in white-crowned sparrows, photostimulation increases plasma T and Leydig cell numbers (Lam & Farner, 1976). The morphology of these cells in photostimulated birdsdnumerous large mitochondria containing tubular cristae, a round nucleus, and a well-developed smooth endoplasmic reticulumd indicates elevated secretory activity. As sparrows become photorefractory, these effects are reversed. Similarly, gonadally quiescent budgerigars (Humphreys, 1975) and chickens (Aire, 1997) differ from reproductively active birds in having fewer Leydig cells, many showing signs of degeneration. The time course of differentiation and ultrastructural changes of Leydig cells during photostimulation have been described in detail in the Japanese quail (Nicholls & Graham, 1972).

3.2. Seminiferous Tubules Seminiferous tubules in birds are anastomosed and surrounded by a basal lamina consisting of fibroblasts, myoepithelial cells, and connective tissue. They contain Sertoli cells and the seminiferous epithelium, where germ cells divide and then differentiate while migrating from the basal lamina to the tubule lumen. Sertoli cells are elongated cells that extend from the basal lamina of seminiferous tubules to the lumen. Adjacent Sertoli cells are joined by tight junctions, thereby dividing the seminiferous epithelium into basal and distal (adluminal) regions, which form an effective bloodetestis barrier (Osman, Ekwall, & Ploen, 1980; Bergmann & Schindelmeiser, 1987). Sertoli cells play an essential role in the development and maturation of gametes and also serve an endocrine function, as they produce inhibin (Sedqyar et al., 2008). Some studies indicate that Sertoli cells multiply during a limited posthatching period and therefore do not proliferate in adulthood (De Reviers et al., 1980; Bozkurt, Aktas, Ulkay, & Firat, 2007). Other studies, however, describe extensive apoptosis of Sertoli cells at the end of the reproductive period in seasonally breeding birds (Section 4.4), suggesting the potential for these cells to regenerate in adulthood in preparation for the following breeding season. Sertoli cells express androgen receptors (Dornas, Oliveira, Dias, Mahecha, & Oliveira, 2008) and their adult size and function are hormonally regulated (Brown, Bayle, Scanes, & Follett, 1975; Ishii & Yamamoto, 1976). As demonstrated

29

in Japanese quail, FSH and T act synergistically to increase testicular weight by inducing Sertoli cell hypertrophy (Tsutsui & Ishii, 1978) (Section 5.2).

4. ENDOCRINE AND EXOCRINE FUNCTIONS OF AVIAN TESTES 4.1. Testicular Androgen Hormone Synthesis and Secretion Following Fevold and Eik-Nes’ (1962) initial work on house sparrows (Passer domesticus), several studies used in-vitro incubation of gonadal tissue in the presence of radioactive precursors to identify the biosynthetic pathways involved in T synthesis (chicken (Delrio, Lupo, & Chieffi, 1967; Nakamura & Tanabe, 1972b; Galli et al., 1973); Japanese quail (Nakamura & Tanabe, 1972b); Wilson’s phalarope (Phalaropus tricolor) (Fevold & Pfeiffer, 1968); red-winged blackbird (Agelaius phoeniceus) (Kerlan, Jaffe, & Payne, 1974)). Depending on the presence of cofactors (nicotinamide adenine dinucleotide (NADþ) or its reduced form (NADH)), testicular tissue of the chicken converts pregnenolone to T following the D4 or D5 pathway (Nakamura & Tanabe, 1972a). Even though the conversion of androstenedione (AND) to T by 17b-hydroxysteroid dehydrogenase (17b-HSD) is reversible, T is usually the quantitatively main end product in adults (Fevold & Pfeiffer, 1968; Nakamura & Tanabe, 1972a). The testes of immature birds, however, can produce more AND than T, presumably as a result of lower 17b-HSD activity than in adults (Fevold & Pfeiffer, 1968; Galli et al., 1973).

4.2. Spermatogenesis As in mammals, spermatogenesis in birds is defined as the formation of mature spermatozoa from spermatogonia and it includes three sequential steps: spermatocytogenesis, spermatidogenesis, and spermiogenesis. The anatomical characteristics and physiological control of avian spermatogenesis have been the object of extensive studies (Thurston & Korn, 2000; Aire, 2007; Jamieson, 2007). Early work identified one or two types of spermatogonia (e.g., Zlotnik, 1947; Kumaran & Turner, 1949; Lake, 1956), but subsequent work on Japanese quail found seminiferous tubules to contain four types of spermatogonia (Ad, Ap1, Ap2, and B) that differ with respect to their staining intensity and ultrastructural characteristics (Lin & Jones, 1992). More recently, Bakst, Akuffo, Trefil, and Brillard (2007) described three types of spermatogonia in the turkey. During spermatocytogenesis, a spermatogonium (Ad germ cell) undergoes mitosis to generate a new Ad cell and an Ap1 cell, which further divides into two daughter Ap2 cells. Each Ap2 cell divides into two B spermatogonia, which themselves each divide into two primary

30

Hormones and Reproduction of Vertebrates

spermatocytes. Primary spermatocytes undergo two meiotic divisions, thus giving birth to secondary spermatocytes, which each divide into spermatids (spermatidogenesis) (Aire, 2007). As a result of these cell divisions, each Ad spermatogonium can generate 32 spermatids. (To contrast this process in birds with that in mammals, see Volume 5, Chapter 5.) Spermatids transform into sperm cells during spermiogenesis, which has been best studied in Japanese quail (Lin & Jones, 1993) and chickens (Sprando & Russell, 1988). Spermiogenesis is characterized by a dramatic reduction of the amount of cytoplasm and a profound morphological transformation that results in mature sperm cells consisting of a head (acrosome, cylindrical nucleus, and mitochondria) and tail (flagellum), and spermiation is the release of sperm from Sertoli cells into the seminiferous tubule lumen. The structure of mature sperm in passerines is relatively conserved, but differs in several respects from that in nonpasserines (for details see Jamieson, 2007). The duration of spermatogenesis in mammals varies considerably from one species to another (e.g., prairie vole (Microtus ochrogaster): 29 days (Schuler & Gier, 1976); dog (Canis lupus familiaris): 42 days (Ghosal et al., 1983); chimpanzee (Pan troglodytes): 63 days (Smithwick, Young, & Gould, 1996)). Limited information in birds suggests a shorter and perhaps more consistent duration of spermatogenesis than in mammals (chicken: 12e13 days (De Reviers, 1975); Japanese quail: 13 days (Lin & Jones, 1992)).

1990), but, as they are transported along the excurrent ducts, chicken and quail sperm acquire the potential for motility due to the influence of factors, including presumably Ca2þ and glutamate, that are secreted into the accessory gland reproductive fluids (Ashizawa & Sano, 1990; Ashizawa, Wishart, Ranasinghe, Katayama, & Tsuzuki, 2004; Clulow & Jones, 1982; Froman & Feltmann, 2005). In the chicken, flagellar movement is temperature-dependent and actual sperm motility is thought to be acquired by a temperature decrease at the time of ejaculation and ejaculate transfer into the female cloaca (Ashizawa & Sano, 1990; Ashizawa et al., 2004). Sperm motility in the rock pigeon (Columba livia) is highest between 18 and 24 C and declines at 28 C (Cheng et al., 2002). Sperm motility in the chicken also depends on genetic factors that influence mitochondrial morphology and function (Froman & Kirby, 2005). In passerines, the distal end of the vas deferens forms the seminal glomus, a specialized sperm storage accessory structure (Gupta, Bhat, & Maiti, 1984; Samour, Spratt, Holt, & Smith, 1988). The glomus in passerines may have evolved as a result of these birds’ aerial lifestyle, which is incompatible with very large testes (Aire, 2007). The number of sperm in the seminal glomus of the house sparrow declines during the course of the day (Birkhead, Veiga, & Moller, 1994). Thus, the glomus may accumulate sperm during the night for use during the day in the course of multiple copulations. Nonpasserines have a limited capacity for extragonadal sperm storage (Clulow & Jones, 1982; Cecil, Bakst, & Monsi, 1988; Jones, 1999).

4.3. Sperm Maturation, Transport, and Storage

4.4. Seasonal Testicular Regression and Programmed Cell Death

Sperm released into the seminiferous tubules are suspended in seminiferous fluid and carried to the cloaca through excurrent ducts consisting of the rete testis, which comprises an intra- and an extratesticular region; the efferent duct; the connecting duct; the epididymis; and the deferent duct (Kirby & Froman, 2000). The ontogeny and adult cytological characteristics of excurrent ducts have been described in detail (Tingari, 1971; 1972; Aire, 1979; Aire, Ayeni, & Olowo-okorun, 1979; Aire, 1982). Sperm in birds are transported rapidly along the reproductive tract (Clulow & Jones, 1982; 1988). In Japanese quail, this transport requires approximately 24 hours (Clulow & Jones, 1988). During this time, sperm undergo final maturation (Esponda, 1991), most of the seminiferous fluid is reabsorbed by pinocytosis (Tingari & Lake, 1972; Nakai, Hashimoto, Kitagawa, Kon, & Kudo, 1989), and the composition of the fluid is altered to produce seminal plasma (Lake & Hatton, 1968; Stratil, 1970). Sperm in the seminiferous tubules, epididymis, and deferent duct in chickens lack motility (Ashizawa & Sano,

The testicular involution that takes place at the end of the reproductive season in seasonal breeders was originally attributed to tissue necrosis brought about by the failure of androgens to maintain the integrity of the seminiferous tubules (Thurston & Korn, 2000). Since then we have learned that seasonal testicular regression results from a precisely controlled process of programmed cell death (apoptosis) that is regulated by complex signaling mechanisms. Despite the large seasonal variation in testis size observed in many bird species, few studies have examined apoptosis in the avian testes. At the end of the breeding season, the American crow (Corvus brachyrhynchos) shows a 19-fold and 9-fold decrease in testis size and spermatogenetic activity, respectively (Jenkins, Ross, & Young, 2007). The decrease in size likely results primarily from Sertoli cell apoptosis (Rodriguez, Ody, Araki, Garcia, & Vassalli, 1997). In the European starling (Sturnus vulgaris), apoptosis associated with seasonal testicular regression was similarly limited to Sertoli and germ cells (Young, Ball, & Nelson, 2001).

Chapter | 2

Avian Testicular Structure, Function, and Regulation

5. ENDOCRINE AND PARACRINE CONTROL OF AVIAN TESTICULAR FUNCTION Two anterior pituitary hormones, LH and FSH, play a primary role in the control of testicular endocrine and exocrine functions. The importance of these hormones is underlined by the results of studies involving hypophysectomy. This surgery causes testicular involution in the chicken (Brown et al., 1975; Tanaka & Fujioka, 1981) and Japanese quail (Bayle, Kraus, & Van Tienhoven, 1970; Brown & Follett, 1977), whereas administration of chicken purified LH but especially chicken purified FSH to hypophysectomized Japanese quail stimulates testicular development and growth (Brown et al., 1975). Testes in Ttreated hypophysectomized immature quail remain undeveloped, but increase in size when birds also receive LH and especially FSH (Brown & Follett, 1977). This observation provides no evidence for a role for T in regulating testicular development. However, a role for T in adult testicular function is suggested by the finding in mature hypophysectomized quail that administration of large doses of T, while insufficient to maintain spermatogenesis, retards testicular regression resulting from the surgery (Brown & Follett, 1977). Avian testes synthesize various chemical mediators (Table 2.1) and their receptors (Table 2.2), suggesting direct, but as yet poorly understood, physiological regulation of testicular function by factors other than LH, FSH, and androgens. Receptors for these mediators in Sertoli cells and seminiferous tubules presumably influence aspects of spermatogenesis; those in Leydig cells may control steroid production and those in epididymal tissue may regulate sperm maturation and seminal fluid composition. The expression of various chemical messengers and their receptors by testes is not entirely surprising as testes are sites of extensive cell proliferation, differentiation, steroid synthesis, and apoptosis. These complex processes presumably require the participation of numerous regulatory hormones and growth factors, particularly as birds often exhibit large seasonal variation in testis size. The following sections summarize avian research on the direct regulation of steroidogenesis and spermatogenesis by LH, FSH, and some other mediators, and they outline potentially promising future avenues for research on this topic.

5.1. Luteinizing Hormone (LH) The primary action of LH on testes is to increase the secretion of androgens by Leydig cells (Kirby & Froman, 2000). The presence of 3b-HSD in Leydig cells and the generally hydrophobic nature of steroids suggest that LH stimulates androgen production and not just release.

31

Supporting this role, plasma LH, in response to photostimulation and ensuing photorefractoriness in captive white-crowned sparrows, changes in parallel with Leydig cell number and ultrastructure (Lam & Farner, 1976). In domestic ducks, plasma LH and T follow the same general time course of changes during constant light exposure starting at 60 days of age and lasting until puberty (160 days of age) (Yang, Medan, Watanabe, & Taya, 2005). In several species, seasonal changes in plasma LH parallel changes in plasma T (Magellanic penguin (Spheniscus magellanicus) (Fowler, Wingfield, Boersma, & Sosa, 1994); rufous-winged sparrow (Aimophila carpalis) (Deviche, Small, Sharp, & Tsutsui, 2006); emperor (Aptenodytes forsteri) and Adelie (Pygoscelis adeliae) penguins (Groscolas, Jallageas, Goldsmith, & Assenmacher, 1986); king penguin (Aptenodytes patagonicus) (Mauget et al., 1994)), although in other species seasonally maximal plasma LH precedes peak plasma T (great tit (Parus major) (Rohss & Silverin, 1983); ostrich (Struthio camelus) (Degen, Weil, Rosenstrauch, Kam, & Dawson, 1994); white-winged crossbill (Loxia leucoptera) (Deviche & Sharp, 2001)). A direct action of LH on Leydig cells is supported by the presence of putative LH receptors on these cells (ostrich (Madekurozwa et al., 2002); embryonic chicken (Akazome, Abe, & Mori, 2002)) and with the observation that LH rapidly increases the in-vitro testicular secretion of T (garden warbler (Sylvia borin) (Bluhm et al., 1991); ringnecked pheasant (Phasianus colchicus karpowi) (Tae et al., 2005)). The effects of in-vivo GTH treatment on testicular function were studied by Brown et al. (1975) in Japanese quail. Repeated injections of purified chicken LH to young males of this species induce differentiation of the interstitium and Leydig cell maturation. These injections also stimulate spermatogonial division and differentiation of Sertoli cells, but whether these effects are direct or result from increased androgen secretion has not been determined. The testicular effects of LH in Japanese quail are specific as they are not replicated by treatment with purified chicken FSH fractions. The specificity of LH action on androgen production in vivo and in vitro was confirmed by measuring the effects of purified chicken, turkey, and ostrich LH in several avian species (chicken, Japanese quail, mallard duck, and turkey (Chase, 1982)). In these species, LH generally induces a dose-related increase in androgen production, but FSH is inactive when given alone and does not alter the response to LH when both are administered together.

5.2. Follicle-stimulating Hormone (FSH) The production and maturation of sperm in mammals primarily depends on FSH acting on Sertoli cell receptors through cyclic adenosine 3’,5’-monophosphate (cAMP)

32

TABLE 2.1 Hormones reported within the testes of birds Hormone

Species

Stage

Growth hormone

Chicken

E, A

Whole testes

A

D

Leydig cells

Sertoli cells

Seminiferous tubules

Spermatogonia or spermatocytes

Epididymis or vas deferens

References

D

L

D

D

D

Luna et al. (2004)

D

D

D

Harvey et al. (2004)

Insulin-like growth factor-1

Chicken

A

D

Harvey et al. (2004); Tanaka et al. (1996)

Prepro-orexin

Chicken

A

D

Ohkubo et al. (2003)

Adiponectin

Chicken

A

Gonadotropin-releasing hormone-I

Chicken

A

D-aspartate

Mallard

A

D

D

D

Di Fiore et al. (2008)

Nitric oxide

Mallard

A

D

D

D

Di Fiore et al. (2008)

Inhibin

Chicken

A

D

Lovell et al. (2000); Bandivdekar et al. (1982)

J, A

D

Davis and Johnson (1998)

J

D

Onagbesan et al. (2004)

L

L

L

Ocon-Grove et al. (2008) Sun et al. (2001)

D

Quail

E, J, A

D

D

Duck

E, J

D

D

Chicken

A

D

Lovell et al. (2000)

J, A

D

Davis and Johnson (1998)

J

D

Onagbesan et al. (2004)

Quail Duck

E, J, A

Sedqyar et al. (2008) D

Yang et al. (2005)

D

D

Sedqyar et al. (2008)

D

D

Yang et al. (2005)

Hormones and Reproduction of Vertebrates

Activin

D

J, A

D

Davis and Johnson (1998)

Myostatin

Chicken

E

D

Kubota et al. (2007)

Agouti-related protein

Chicken

A

D

Takeuchi et al. (2000)

Anti-Mu¨llerian hormone

Chicken

E

D

E

D

Oreal et al. (2002)

Quail

E

D

Koba et al. (2008a)

Quail

J

D

Koba et al. (2008a); Nakamura et al. (2008)

Duck

E

D

Koba et al. (2008c)

Turkey; goose

J

D

Koba et al. (2008b)

Starling

A

D

Bentley et al. (2008)

Quail

A

D

D

House sparrow

A

D

D

Gonadotropin-inhibiting hormone

L

D

L

D

Eusebe et al. (1996)

L

D D

D

Bentley et al. (2008) McGuire and Bentley (2010)

Avian Testicular Structure, Function, and Regulation

Chicken

Chapter | 2

Follistatin

þ indicates the presence of hormone as determined by methods including radioligand binding assays, immunocytochemistry, and in-situ hybridization; indicates hormone presence was tested for but found absent. Abbreviations for life stages are as follows: E, embryo; J, juvenile; A, adult.

33

34

TABLE 2.2 Hormone receptors reported within the testes of birds Ligand

Species

Stage

Whole testes

Prolactin

Turkey

A, E

þ

Mao et al. (1999); Pitts et al. (2000)

Chicken

E

þ

Pitts et al. (2000)

A

þ

Mao et al. (1999); Tanaka et al. (2000)

Pigeon

A

þ

Mao et al. (1999)

Quail

A

þ

Mao et al. (1999)

Orexin

Chicken

A

þ

Ohkubo et al. (2003)

Progesterone

Chicken

J, A

þ

Gonza´lez-Mora´n et al. (2008)

Androgen

Chicken

A

þ

A

þ

þ

J, A

Estrogen

Leydig cells

Sertoli cells

Seminiferous tubules

Spermatogonia or spermatocytes

Epididymis or vas deferens

References

Shanbhag and Sharp (1996) þ

þ

Dornas et al. (2008) Gonza´lez-Mora´n et al. (2008)

Canary

A

þ

Duck

A

þ

þ

Nastiuk and Clayton (1994) þ

Dornas et al. (2008)

E

þ

Koba et al. (2008b)

Quail

J

þ

Nakamura et al. (2008)

Chicken

A

þ

Kwon et al. (1997)

þ

Gonza´lez-Mora´n et al. (2008)

Turkey

E

þ

Koba et al. (2008a)

Duck

E

þ

Koba et al. (2008a; 2008b)

Goose

E

þ

Koba et al. (2008a)

Quail

J

þ

Koba et al. (2008c); Nakamura et al. (2008) þ

Adiponectin

Chicken

Gonadotropin-releasing hormone

Chicken

þ

Growth hormone

Chicken

þ

þ

þ

þ

Ocon-Grove et al. (2008) Sun et al. (2001) þ

Harvey et al. (2004)

Hormones and Reproduction of Vertebrates

J, A

A

þ

Kwok et al. (2007)

Corticotropin-releasing hormone

Chicken

J

þ

De Groef et al. (2004)

Melatonin

Chicken

A

þ

Ayre et al. (1992)

Duck

A

þ

Ayre et al. (1994)

Quail

A

þ

Wang et al. (1992)

Quail

J, A

þ

Fu et al. (2001)

Retinoic acid

Gonadotropin-inhibiting Starling hormone Sparrow

A

þ

þ

Bentley et al. (2008)

A

þ

þ

Bentley et al. (2008)

House sparrow

A

D

Prostaglandin

Chicken

A

þ

Kwok et al. (2008)

Aryl hydrocarbon

Cormorant A

þ

Lee et al. (2007)

Motilin

Chicken

þ

Yamamoto et al. (2008)

J

D

D

McGuire and Bentley (2010)

þ indicates the presence of hormone receptor as determined by a variety of methods including radioligand binding assays of whole testes, immunocytochemistry, and in-situ hybridization. indicates receptor presence was tested for but found absent. Abbreviations for life stages are as follows: E, embryo; J, juvenile; A, adult.

Avian Testicular Structure, Function, and Regulation

Chicken

Chapter | 2

Glucocorticoid

35

36

activation of protein kinases (see Hadley, 2000). Several studies demonstrate that FSH likewise plays a major role in the control of avian Sertoli cell function and spermatogenesis. In captive mallard ducks exposed to natural photoperiod, plasma FSH is elevated during the vernal period of testicular growth, reaches a maximum when testes are fully developed during the breeding season, and then rapidly declines when birds become photorefractory and begin to molt (Haase, 1983; Haase, Sharp, & Paulke, 1985). Plasma FSH and testicular size undergo parallel changes during the annual cycle also in other species (great tit (Silverin, Kikuchi, & Ishii, 1997); European starling (Dawson & Goldsmith, 1983)). Photomanipulation experiments likewise show a correlation between plasma FSH and testicular development. Plasma FSH is low in white-crowned sparrows held on short days and with undeveloped testes (Wingfield, Follett, Matt, & Farner, 1980). Following photostimulation, plasma FSH increases gradually for approximately four weeks, concurrently with testicular development and the initiation of spermatogenesis. It should be noted that in these sparrows, as in the Japanese quail (Follett, 1976), photoinduced plasma FSH decreases despite testes remaining fully developed for several weeks, suggesting that early but not late stages of spermatogenesis require elevated plasma FSH. Further, plasma FSH is often higher than baseline in birds with regressed testes. For example, great tits in the fall, when these birds regain photosensitivity, show a small peak in plasma FSH (Silverin et al., 1997). Further research is needed to fully understand the significance of this observation. The most detailed work on the time course of photoinduced changes in plasma FSH and testicular development has been performed in Japanese quail (Follett & Maung, 1978). In this species, plasma FSH increases in parallel with testis development following photostimulation with photoperiods of various durations. For example, males exposed to 14 or more hours of light daily develop their testes fully and achieve peak plasma FSH after 10 long days. By contrast, quail exposed to 12 hours of light daily show reduced testicular development and lower plasma FSH than birds exposed to longer photoperiods. The role of FSH also has been studied through hormone-administration experiments (e.g., Purcell & Wilson, 1975; Balthazart, Massa, & Negri-Cesi, 1979). Administration of chicken purified FSH to hypophysectomized Japanese quail stimulates Sertoli cells and germ cell differentiation, resulting in enlarged seminiferous tubules and increased testicular weight, but the treatment does not lead to differentiation of Leydig cells (Brown et al., 1975). The hormonal specificity of these effects of exogenous FSH is revealed by the fact that they are not observed following treatment with chicken purified LH rather than FSH. Similarly, treatment of neonatal chickens with ovine FSH,

Hormones and Reproduction of Vertebrates

but not LH, dose-dependently increases their seminiferous tubule diameter (Ishii & Yamamoto, 1976). The effects of GTHs on testes depend on circulating concentrations of these hormones but also on their receptors. Beginning with Ishii and Yamamoto’s (1976) study of white-crowned sparrows, a number of studies used radioligand binding of mammalian FSH to avian testicular tissue preparations to characterize FSH receptors (Japanese quail (Ishii & Adachi, 1977); chicken (Tsutsui & Ishii, 1978); mallard duck (Bortolussi, Deviche, Colombo, & Marini, 1979); Indian weaver bird (Ploceus philippinus) (Tsutsui, Kawashima, Saxena, & Ishii, 1992; Tsutsui, Kawashima, V. Saxena, & A. Saxena, 1992; Kawashima, Tsutsui, Saxena, & Ishii, 1993)). It was found that testes contain specific, high affinity (nanomolar range) binding sites for FSH and these sites have a reduced binding affinity for LH (Ishii & Yamamoto, 1976; Ishii & Adachi, 1977; Tsutsui & Ishii, 1978; Kawashima et al., 1993). In white-crowned sparrows that are transferred from short to long days to stimulate gonadal development, FSH binding capacity (number of binding sites per testis) and plasma FSH increase (Ishii & Yamamoto, 1976). Similar observations have been made in Indian weaver birds (Tsutsui et al., 1992a; 1992b; Kawashima et al., 1993). Research on Japanese quail suggests that photoinduced increases in gonadal FSH binding capacity result from upregulation of binding sites by the hormone itself (self-potentiation), in addition to synergistic actions with T (Tsutsui & Ishii, 1978; but see Ottinger, Kubakawa, Kikuchi, Thompson, & Ishii, 2002). The mechanism mediating this putative synergism is unknown and its physiological importance remains in question, especially in view of the fact that T administration, alone or with FSH treatment, decreases the incorporation of 32P into testes of the chicken (Breneman & Zeller, 1982). The gene coding for avian testicular FSH receptors has been sequenced and cloned, and the putative amino-acid sequence of the receptor has been identified (chicken ovarian follicle (Wakabayashi, Suzuki, Hoshino, Nishimori, & Mizuno, 1997)), offering new opportunities to study the regulation of these receptors.

5.3. Gonadotropin-inhibiting Hormone (GnIH) The discovery of the hypothalamic inhibitory neuropeptide GnIH (Tsutsui et al., 2000) has stimulated considerable research into the physiological roles and mechanisms by which this neurohormone influences the hypothalamoe pituitary gland axis (Bentley et al, 2009; Tsutsui et al., 2010). As shown recently, avian testes also contain GnIH and its receptors (Bentley et al., 2008; McGuire & Bentley, 2010). Receptors are located in interstitial and germ cells, suggesting that GnIH controls testicular steroid production

Chapter | 2

Avian Testicular Structure, Function, and Regulation

and germ cell function through autocrine and/or paracrine actions. Supporting this proposition, GnIH decreases the gonadotropin-induced in-vitro stimulation of testosterone secretion by house sparrow testes (McGuire & Bentley, 2010). Stress in rodents (Kirby, Geraghty, Ubuka, Bentley, & Kaufer, 2009) and probably birds (Calisi, Rizzo, & Bentley, 2008) increases the brain expression of GnIH. A similar increase, if taking place in testes, may contribute to mediating the rapid in-vivo inhibition of T secretion that is observed in response to acute stress in the white-crowned (Wingfield, Smith & Farner, 1982) and rufous-winged (Deviche et al., 2010) (Section 5.7) sparrow.

5.4. Inhibin and Activin Gonadotropin-releasing hormone stimulates LH and FSH, but the secretion of the two GTHs is thought to be differentially regulated due to the negative feedback effects of inhibin on FSH secretion and to a lesser degree the stimulatory action of activin on FSH secretion (Davis & Johnson, 1998). Inhibin and activin are dimeric glycoproteins that share a common a subunit but differ with respect to their b subunit; inhibin has either a single bA or bB subunit, whereas activin has a homodimeric b subunit (Davis & Johnson, 1998). These structural similarities have made separating the biological effects and responses of the two hormones to FSH at the testis level challenging. Studies involving immunization against the inhibin a subunit have found immunized birds to have elevated testicular weights compared to control birds (chicken (Lovell, Knight, Groome, & Gladwell, 2000); Japanese quail (Satterlee, Castille, & Fioretti, 2006)). In the latter species, immunization also advances puberty and delays age-associated testicular involution. The mechanism that mediates inhibitory effects of inhibin on the reproductive system is unclear because, in the chicken, the increase in testicular weight resulting from immunization against inhibin a subunit is associated with decreased plasma LH but no change in plasma FSH or testicular morphology (Lovell et al., 2000). As these authors suggest, inhibin may act on testes to reduce their sensitivity to FSH, but this hypothesis warrants further research. A paracrine role of inhibin and activin on testes is indicated by studies suggesting that these hormones influence gamete growth and differentiation (Onagbesan, Safi, Decuypere, & Bruggeman, 2004; Sedqyar et al., 2008) and fetal steroidogenesis (Rombauts, Vanmontfort, Decuypere, & Verhoeven, 1996).

5.5. Melatonin (MEL) Melatonin (MEL) in birds is produced primarily by the pineal gland and the retina (Underwood, Binkley, Siopes, & Mosher, 1984) and exerts complex effects on the male

37

reproductive system (Gupta, Haldar-Misra, Ghosh, & Thapliyal, 1987; Ohta, Kadota, & Konishi, 1989; Sackman, 1977; Singh & Haldar, 2007). Studies have revealed an important modulatory role for MEL in the regulation of seasonal reproductive cycles, but much remains to be learned about the mechanisms involved (see also Chapter 8, this volume). Melatonin stimulates the reproductive axis under some conditions. For example, MEL pretreatment to red-headed buntings (Emberiza bruniceps) blocks the suppressive effect of prolactin (PRL) on testis growth (Trivedi, Rani, & Kumar, 2004). By contrast, other investigations found no evidence for an obligatory role of the pineal gland or its secretions in the regulation of seasonal reproduction (Wilson, 1991; Pant & Chandola-Saklani, 1992). In yet other studies, seasonal changes in pineal gland activity as measured cytologically (Indian weaver bird (Chakraborty, 1993)), enzymatically (house sparrow (Barfuss & Ellis, 1971)), or through plasma MEL (jungle bush-quail (Perdicula asiatica) (Singh & Haldar, 2007)) was inversely related to the activity of the reproductive system, suggesting inhibitory effects of pineal gland secretions on this activity. In the adult male Japanese quail, blinding results in elevated plasma LH (Konishi, Iida, Ohta, & Takahashi, 1988). This observation is consistent with an inhibitory effect of MEL on the reproductive system but does not rule out alternate mechanisms. More direct evidence for an inhibitory role for MEL comes from the demonstration that administration of this hormone inhibits testicular recrudescence in the rose-ringed parakeet (Psittacula krameri) (Sengupta & Kumar, 2006) and can delay reproductive maturation in the cockerel (Balemans, Van de Veerdonk, & Van de Kamer, 1977; Lewis, Middleton, & Gous, 2006; but see John, George, & Etches, 1986). Inhibitory effects of MEL may involve direct actions on the hypothalamus and/or pituitary gland (Gupta et al., 1987). Supporting this hypothesis, GnIH neurons express MEL receptors and MEL mediates the increase in GnIH expression seen in Japanese quail in response to short days (Ubuka, Bentley, Ukena, Wingfield, & Tsutsui, 2005). Melatonin may also affect gonadal tissue directly. Indeed, MEL decreases the in-vitro production of steroids from labeled precursors by testis homogenates (Mallard duck (Cardinali & Rosner, 1971)), and the testes of several avian species contain specific, high affinity binding sites for 125I-labeled MEL (Ayre, Yuan, & Pang, 1992; Wang, Cheng, Brown, Pang, & Pang, 1992; Ayre & Pang, 1994; Ayre, Wang, Brown, & Pang, 1994; Cheng et al., 1994). In the Japanese quail, the number of testicular MEL binding sites is photoperiodically regulated; birds have fewer such sites when exposed to short rather than long days (Pang et al., 1993). This difference may result from down- (short days) or up- (long days) regulation of MEL receptors.

38

5.6. Prolactin (PRL) Prolactin in birds often exerts an antigonadal influence (e.g., Bates et al., 1935; Nalbandov, 1945; Bailey, 1950; Bar, 2006) that is thought to play an important role in the control of seasonality (Dawson, King, Bentley, & Ball, 2001; Sharp & Blache, 2003). This influence presumably results in part from central effects of PRL. Indeed, in the ring dove (Streptopelia risoria), an intracerebroventricular PRL injection dose-dependently decreases plasma LH and induces testicular regression (Buntin, Lea, & Figge, 1988). Further, the preoptic region of the brain in this species (Fechner & Buntin, 1989; Buntin, Ruzycki, & Witebsky, 1993) and in Wilson’s phalarope (Buntin, El Halawani, Ottinger, Fan, & Fivizzani, 1998) contains specific, highaffinity PRL binding sites. It remains to be determined whether PRL reaches these sites after secretion from the pituitary gland into the blood or is produced within the brain itself (Buntin, Hnasko, & Zuzick, 1999; Ramesh, Kuenzel, Buntin, & Proudman, 2000). In most species examined, PRL secretion is photoinduced (Goldsmith & Nicholls, 1984a; Sharp, Klandorf, & McNeilly, 1986; Silverin & Goldsmith, 1997; Sharp, Dawson, & Lea, 1998; Sreekumar & Sharp, 1998). Maximal circulating PRL concentrations are reached toward the end of the reproductive season, coinciding with the onset of photorefractoriness, suggesting that PRL contributes to the gonadal regression taking place at this time (Dawson & Goldsmith, 1983; 1984; Haase et al., 1985; Stokkan, Sharp, Dunn, & Lea, 1988; Bluhm, Phillips, & Burke, 1989; Sharp et al., 1998). Experimental evidence, however, shows that PRL facilitates seasonal testicular involution but does not cause photorefractoriness. This evidence comes, in particular, from studies on the European starling, a species that responds to chronically long days by completely losing sensitivity to this stimulus (absolute photorefractoriness). Active immunization of starlings against VIP (see Section 1), the main PRL secretagogue in birds, slowed but did not prevent testicular regression associated with photorefractoriness (Dawson & Sharp, 1998). Further, plasma PRL in chronically refractory mallards increases but then returns to baseline values, indicating that it is not required for long-term maintenance of photorefractoriness (Sharp et al., 1986). Other species, including the Japanese quail (Robinson & Follett, 1982; Follett & Pearce-Kelly, 1990) and Aimophila sparrows (Deviche, Sabo, & Sharp, 2008; Small, Sharp, Bentley, & Deviche, 2008a; 2008b), respond to prolonged exposure to long days by losing sensitivity to these long days gradually, but incompletely (relative photorefractoriness). As in other species, PRL in the Japanese quail increases during photostimulation (Goldsmith & Hall, 1980). Contrary to the situation in the European starling, however, PRL may play a critical role in the

Hormones and Reproduction of Vertebrates

induction of photorefractoriness in relatively photorefractory species (Dawson et al., 2001). Mammalian testes contain GTH-dependent PRL receptors (Fishback, Arimura, & Turkelson, 1982) and, in humans, PRL is thought to decrease T secretion through an LH-independent mechanism, suggesting direct testicular effects in this species (Suescun et al., 1985). Prolactin receptors (PRL-Rs) are expressed in avian testes as well (Zhou, Zadworny, Guemene, & Kuhnlein, 1996; Leclerc, Zadworny, Bedecarrats, & Kuhnlein, 2007; see Table 2.2). Research in chickens has identified testis-specific PRL-R truncated transcripts that are expressed in an age-related fashion (Mao et al., 1999). These data suggest direct actions of PRL on avian testicular tissue. In one of the few studies on this subject, Stetson and Erickson (1970) found in cockerels that treatment with large doses of mammalian PRL alone has no effect on testicular incorporation of 32P, but acts synergistically with exogenous LH to increase this incorporation. Additional research is necessary to clarify whether PRL exerts a direct physiological influence on avian testicular function and to elucidate potential interactions between this hormone and LH at the testicular level.

5.7. Glucocorticoids and Metabolic Hormones Research on the effects of stress on the male reproductive system has demonstrated a generally negative relation between plasma corticosterone (CORT), the primary avian glucocorticoid, and T (reviewed by Wingfield & Sapolsky, 2003). During a prolonged stressful situation, plasma T and LH levels are thought to decline as a result of elevated plasma CORT. Supporting this hypothesis, CORT administration blocks photoperiod-induced testicular development in the male Japanese quail (Deviche, Massa, Bottoni, & Hendrick, 1982), and, in the red-headed bunting, pharmacological blockade of CORT secretion delays seasonal testicular regression (Bhatt, Patel, & Chaturvedi, 2001). The mechanism that mediates these effects remains speculative. Testes express glucocorticoid receptors (Table 2.2) and CORT may, therefore, act directly on testes to inhibit their function, but the decline in plasma LH that follows CORT treatment (Deviche et al., 1982) suggests actions also on the hypothalamus and/or pituitary gland. Inhibitory effects of stress may also involve GnIH because stress can in some circumstances increase the number of hypothalamic GnIH-expressing neurons (house sparrow (Calisi et al., 2008) (Section 5.3)). Acute stress can also have inhibitory effects on reproductive hormones. In the white-crowned (Wingfield et al., 1982) and rufous-winged (Deviche et al., 2010) sparrows, plasma T decreases within one hour and fifteen minutes, respectively, of capture and handling. In neither study was

Chapter | 2

Avian Testicular Structure, Function, and Regulation

this decrease associated with a decrease in plasma LH, suggesting a stress-mediated inhibition of testicular endocrine function. In contrast to these studies, other research has found a positive relation between plasma T and shortterm stress. This increase in roosters is not seen in castrated birds, indicating that T is presumably secreted by testes and not adrenal glands (Heiblum, Arnon, Gvaryahu, Robinzon, & Snapir, 2000). Several hypotheses have been proposed to explain the stimulatory effects of stress on plasma T: changes in adrenal androgen biosynthesis (Robinzon & Cutolo, 1999), natural temporal variation of T resulting from GnRH pulsatility (Wilson, Rogler, & Erb, 1979), and a direct stimulation of Leydig cells by catecholamines (Landsberg & Young, 1992). More research is warranted to clarify the effects of stress on the hypothalamoepituitarye testicular axis and in particular the specific role in this respect of glucocorticoids, the reasons for stress having either stimulatory or inhibitory actions on reproductive hormones, and the peripheral and central sites involved. Interesting opportunities to investigate relations between stress and reproduction come from genetic lines selected for divergence in adrenocortical activity. Selection of Japanese quail for reduced adrenocortical response to restraint stress (Satterlee, Truax, Jacobsperry, & Johnson, 1982; Satterlee, Johnson, & Jacobsperry, 1983; Satterlee & Johnson, 1988; Satterlee & Jones, 1997) has resulted in individuals that show accelerated development of the cloacal gland (Marin & Satterlee, 2004; Satterlee & Marin, 2004; Satterlee, Cole, & Castille, 2006; Satterlee, Tong, Castille, & Marin, 2007), larger testis weight relative to body mass (Marin & Satterlee, 2004; Satterlee & Marin, 2004; Satterlee et al., 2006b), and increased frequencies of male androgen-dependent sexual behaviors (Marin & Satterlee, 2003). An important consideration is that stress effects on testicular function may be difficult to identify when stress results from metabolic challenges (Wingfield & Sapolsky, 2003). Studies in laboratory rodents found that anabolic hormones (growth hormone (GH) and insulin-like growth factor (IGF)) associated with energy balance and growth exert local effects on testicular steroidogenesis. In mammals, GH is thought to influence gametogenesis through IGF-1 and stimulates T synthesis by inducing the production of steroidogenic enzymes such as 3b-HSD (reviewed in Hull & Harvey, 2000a; 2000b; Chandrashekar, Zaczek, & Bartke, 2004). Indeed, evidence from mammals supports the hypothesis that both GH and IGF-1 are synthesized de novo in testes and act independently or in concert via receptors on both Sertoli and Leydig cells (Hull & Harvey, 2000b). Avian testes contain immunoreactive GH and IGF-1, and receptors for these peptides (Harvey et al., 2004). Similar mechanisms as in mammals may, therefore, operate in birds. The recent characterization of the GH gene sequence in the chicken (Kansaku, Hiyama, Sasanami, &

39

Zadworny, 2008) and pied flycatcher (Ficedula hypoleuca) (Buggiotti, Hellstrom, & Primmer, 2006) will hopefully lead to the development of probes that can be used to address the specific role of GH on avian testicular function.

5.8. Nitric Oxide (NO) and D-aspartate (D-Asp) It has been proposed in mammals that nitric oxide (NO) serves as a paracrine inhibitor of Leydig cell T synthesis (Adams, Nock, Truong, & Cicero, 1992; Lamanna, Assisi, Vittoria, Botte, & Di Fiore, 2007). This inhibition is opposed by the amino acid D-aspartate (D-Asp), which in mammals stimulates steroidogenesis (D’Aniello et al., 1998; Lamanna, Assisi, Botte, & Di Fiore, 2006; 2007a; Lamanna et al., 2007b). A potential role for NO in avian reproduction has been investigated in two species, the Japanese quail (regulation of GTH release (Chaturvedi & Kumar, 2007; Kumar & Chaturvedi, 2008)) and the mallard duck (regulation of T production by NO and D-Asp (Di Fiore, Lamanna, Assisi, & Botte, 2008)). In the latter study, D-Asp and NO were localized in Leydig cells, with D-Asp more prevalent during the reproductive period and NO more prevalent outside this period. This observation supports a stimulatory and inhibitory role, respectively, of these chemical mediators in testicular function (Di Fiore et al., 2008).

5.9. An Avian Androgen-binding Protein? Testosterone in vertebrates is thought to regulate spermatogenesis by binding to a testicular androgen-binding glycoprotein (ABP) that concentrates T within the seminiferous tubules, resulting in the elevated luminal T levels necessary to promote sperm maturation in the epididymis (Norris, 2007). Although evidence supports an important role for T in sperm maturation in birds, it is unknown whether avian seminiferous tubules contain ABP. Human ABP and sex hormone-binding globulin (SHBG) (Gershagen, Lundwall, & Fernlund, 1989) are products of the same gene, have identical amino-acid sequences, and differ only with respect to the oligosaccharides attached to them (Hammond & Bocchinfuso, 1996). Early studies concluded that SHBG is absent in birds (Murphy, 1968; Corvol & Bardin, 1973) but more recent work suggests that 90e95% of plasma androgens circulate bound to a CORT-binding globulin (CBG), raising the possibility that avian CBG acts as the primary SHBG in circulation (Deviche, Breuner, & Orchinik, 2001; Breuner & Orchinik, 2002). The aminoacid sequence of avian CBG has not been identified (but see Noel, Ramsey, Crews, & Breuner, 2004) and whether testes produce this protein is unknown. Corticosterone-binding globulin is, however, the most likely candidate for an ABP in the avian male reproductive system.

40

6. EXOGENOUS REGULATION OF TESTICULAR FUNCTION In many avian species, testes are maximally developed during the breeding season, which is preceded and followed by a period of reproductive quiescence during which testes are regressed and do not produce gametes (Figure 2.1) (Dawson et al., 2001; Meddle, Wingfield, Millar, & Deviche, 2006; Dawson & Sharp, 2007; Leska & Dusza, 2007). As a result, testicular size can change several-hundred-fold during the year (Table 2.3) as compared to the less-than-fivefold change often seen in seasonally breeding mammals (e.g., Lincoln & Short, 1980; Nicholls, Goldsmith, & Dawson, 1988; Urbanski, Fahy, & Collins, 1993; Dawson, 2002). The dramatic morphological and physiological changes associated with seasonal (in-)activation of the avian reproductive system require time. Males must, therefore, be able to anticipate the start and end of the optimal time for breeding to maximize their chances of successful reproduction. The specific cues used to predict seasonal environmental changes vary among species. This section discusses abiotic cues used to determine the annual cycle of testicular development, with particular emphasis on birds exhibiting different breeding schedules and life histories.

6.1. Abiotic Factors 6.1.1. Photophase The annual change in daylength (photophase) is the primary initial predictive cue that many birds use to time reproduction. Changes in testicular size/weight stimulated by a change in photoperiod are species-specific and often associated with differences in breeding phenology and mating system (Section 6.2) (Garamszegi, Eens, HurtrezBousses, & Moller, 2005; Pitcher, Dunn, & Whittingham, 2005). To our knowledge, no avian species has been identified that relies exclusively on nonphotic cues to time

Hormones and Reproduction of Vertebrates

reproduction. Thus, photoperiod exerts at least a permissive effect on the reproductive system (see Section 6.1.4 for discussion of reduced reliance on photic cues). In many species, increasing photoperiod from short winter days stimulates testicular recrudescence (Hamner, 1968; Dawson et al., 2001; Sharp, 2005; Dawson & Sharp, 2007). However, the short-day-breeding emu (Dromaius novaehollandiae) shows a similar increase in testicular development, but in response to decreasing photoperiod (Malecki et al., 1998). Little work has been done on the effect of photoperiod on the reproductive system of nocturnal species (Guchhait & Haldar, 1999) and the mechanisms that regulate seasonal gonadal cycles in these species are largely unknown. Birds can respond to even small photoperiodic changes around the critical day length, defined as the shortest photoperiod that stimulates testicular development. The duration of the critical day length varies intra- and interspecifically. For example, the critical day length in starlings is 12 hours light (L) and birds kept under a 12L : 12 dark (D) light schedule show normal testicular cycling (Dawson, 2006). However, a 30-minute shift in photoperiod (increasing to 12.5L and then decreasing to 11.5L) results in a permanently photorefractory or photosensitive state, respectively. Thus, the directionality, rather than only the magnitude of a change in photoperiod, is important for photoperiodic regulation of testicular development (Dawson, 2006). The same applies to equatorial species, in which small changes in both photoperiod (i.e., 17 minutes) and light intensity can suffice to induce testicular development (spotted antbird (Hylophylax naevioides) (Hau, Wikelski, & Wingfield, 1998; Wikelski, Hau, & Wingfield, 2000)).

6.1.2. Precipitation The average amount of precipitation in most temperate regions varies seasonally. In these regions, a seasonal increase in photophase, and rising temperatures, are often

FIGURE 2.1 Photomicrographs of (a) nonbreeding and (b) breeding variegated fairy-wren (Malurus lamberti assimilis) testis sections. I, interstitium; L, lumen; S, seminiferous tubule; o, spermatogonium; *, secondary spermatocytes; -, spermatids; /, elongating spermatids. Pictures taken at 20 magnification. From M. Rowe, unpublished data.

Chapter | 2

41

Avian Testicular Structure, Function, and Regulation

TABLE 2.3 Breeding to non-breeding testis mass and volume ratios in birds and mammals as reported in or estimated from cited publications Common name

Scientific name

Mass ratio

Emu

Dromaius novaehollandiae

1.9

Malecki et al. (1998)

Korean ring-necked pheasant Phasianus colchicus karpowi

15.8

Kim and Yang (2001)

Chicken

Gallus gallus domesticus

40

Gonza´lez-Mora´n et al. (2008)

Japanese quail

Coturnix coturnix japonica

5e11

Artoni et al. (1999); Sudhakumari et al. (2001)

Turkey

Meleagris gallopavo

22.2

Noirault et al. (2006)

Mallard duck

Anas Platyrhynchos

100.4

Johnson (1961)

Indian rose-ringed parakeet

Psittacula krameri

50

Krishnaprasadan et al. (1988)

Spotted antbird

Hylophylax n. naevioides

American crow

Corvus brachyrhynchos

Brahminy myna

Sturnus pagodarum

Starling

Sturnus vulgaris

Canary

Serinus canaria

House sparrow

Passer domesticus

Redheaded bunting

Emberiza bruniceps

Song sparrow

Melospiza melodia

White-crowned sparrow

Volume ratio

11 19

Citation

Hau (2001) Jenkins et al. (2007)

60e90

Kumar and Kumar (1993)

190.5e250

Dawson et al. (2002); Dawson (2003; 2005)

50

Bentley et al. (2003); Hurley et al. (2008)

46.4

Hegner and Wingfield (1986); Trivedi et al. (2006)

45

Kumar et al. (2002); Rani et al. (2005)

50e125

Wingfield (1984); Perfito et al. (2004)

Zonotrichia leucophrys pugetensis

38e80

Wingfield et al. (1997)

Rufous-collared sparrow

Zonotrichia capensis

11.9

Moore et al. (2004; 2005)

Syrian/golden hamster

Mesocricetus auratus

3.0e5.0

Donham et al. (1996); Kawazu et al. (2003)

Siberian hamster

Phodopus sungorus

5.3e5.8

Gorman and Zucker (1995); Prendergast et al. (2000)

Vole

Microtus agrestis

Ram

Ovis musimon

Deer

Axis axis

160

166.7

12.5

5

Kro´l et al. (2005)

1.9 1.4 1.6

Cervus elaphus

associated with increased rainfall, and these factors combine to increase plant and insect food resources. Increased food availability in turn provides energetic resources that birds can use to develop testes and for other aspects of reproduction. Indeed, unusually heavy winter rains that cause early greening of vegetation can advance the timing of breeding even in strictly seasonal breeders (canary (Serinus canaria) (Leitner, Van’t Hof, & Gahr, 2003; Voigt, Goymann, & Leitner, 2007); zebra finch (Taeniopygia guttata) (Perfito, Zann, Bentley, & Hau,

Lincoln (1998) Willard and Randel (2002)

1.8

Suttie et al. (1992)

2007)). By contrast, in regions such as the Sonoran Desert, the vernal increase in photophase and temperature is not typically associated with increased precipitation (Small, Sharp, & Deviche, 2007) and, in other areas (e.g., central Australia), rains are unpredictable and do not follow a consistent seasonal pattern (Immelmann, 1963; Zann, Morton, Jones, & Burley, 1995). In such situations, male birds are often flexible breeders and their reproductive physiology can rapidly respond to stimuli associated with irregular rainfall.

42

For example, zebra finches breed seasonally along the southeast Australian coast, where rains are relatively predictable. Birds in this region have moderately developed testes in preparation for the breeding season and regressed testes outside this season (Perfito et al., 2007). By contrast, in the arid center of the continent, where rains are unpredictable, zebra finches breed opportunistically, maintaining semideveloped, yet functional, testes year-round, even when their body condition deteriorates as a result of poor environmental conditions (Perfito et al., 2007). In droughtsimulated captive conditions, zebra finches reduce their testis size but testes retain the capacity to produce sperm (Vleck & Priedkalns, 1985; Perfito, Bentley, & Hau, 2006). More predictably, in the Sonoran Desert, male rufouswinged sparrows start developing their testes in the spring in response to increasing photoperiod, but do not normally breed until the onset of the summer monsoon (Deviche & Small, 2006; Deviche et al., 2006; Small et al., 2007). In both zebra finches and Aimophila sparrows, it remains unclear whether reproductive responses to precipitation are mediated directly by rainfall (e.g., increased humidity, sound of rain, physical contact with water) or indirectly and through an increase in food resources. Suggesting direct effects, testicular regression in captive rufous-winged sparrows is delayed in birds that receive food and water ad libitum and are exposed to artificial rain under fall-like photoperiod, compared to control sparrows that are not exposed to artificial rain (Deviche, unpublished observation). By contrast, other research suggests that rain influences testicular function indirectly, by acting as a predictive cue for future increase in biomass availability (Zann et al., 1995). These authors found a lag (four months showing the most profound effect) between when the first rains fell and breeding, suggesting that birds use rain to time reproduction so that young hatch when grass seeds are first ripening (Zann et al., 1995). Research on the zebra finch also shows that increased humidity and water availability lead to an increase in testicular size (Priedkalns, Oksche, Vleck, & Bennett, 1984; Vleck & Priedkalns, 1985).

6.1.3. Temperature In seasonal environments, changes in ambient temperature provide a secondary cue that birds can use to predict future breeding conditions. We have little information on whether temperature influences testicular development directly or indirectly. Further, as average temperature in many regions changes seasonally in parallel with the photophase (e.g., Deviche & Sharp, 2001), separating the influence of these two factors on reproductive functions in natural conditions can be difficult. Temperature exerts complex effects on testicular function and development. For example, in chickens, high ambient temperatures impair testicular function and

Hormones and Reproduction of Vertebrates

decrease semen output (Wilson, Siopes, & Itho, 1972), and cold temperatures suppress testicular growth and fertility (Huston, 1975). By contrast, comparative studies using several subspecies of white-crowned sparrows that breed at different latitudes found that temperature does not influence testicular development in high-latitude breeders with short, predictable breeding seasons. However, lower-latitude breeders with more flexible breeding seasons than arctic breeders show a positive association between temperature and testicular development (Wingfield, Hahn, Wada, Astheimer, & Schoech, 1996; Wingfield et al., 2003). Captive studies examining the effects of temperature on testicular development found that cold temperatures can delay reproductive readiness and the onset of photorefractoriness in male black-billed magpies (Pica pica) (Jones, 1986), song sparrows (Melospiza melodia morphna) (Perfito et al., 2004), and tits (Parus spp.) (Silverin & Viebke, 1994; Silverin et al., 2008). Conversely, warmer temperatures can advance testicular development in southern-breeding great tits (Silverin et al., 2008) and seasonal testicular regression in European starlings (Dawson, 2005). Research comparing species inhabiting environments differing in seasonal temperature patterns, combined with captive studies manipulating ambient temperatures and photoperiod, should help untangle the role and mechanism of action of temperature on testicular function.

6.1.4. Food The type, amount, quality, and predictability of food resources can exert complex effects on the reproductive system (Hahn, Pereyra, Katti, & Ward, 2005). In environments where food availability is relatively predictable and breeding flexible, food supplementation can advance or enhance testicular development (Newton, 1998; Hau, Wikelski, & Wingfield, 2000; Hahn et al., 2005). For example, in free-ranging song sparrows inhabiting coastal and mountain habitats that differ with respect to seasonal food availability, testicular growth rates and maximal testicular size differ between years and as a function of altitude and presumably food availability (Perfito et al., 2004). Similarly, food restriction at the onset of the breeding season can delay seasonal testicular regression (Dawson, 1986), and restriction during reproduction can cause a decrease in testicular weight (Kobayashi & Ishii, 2002; Kobayashi, Cockrem, & Ishii, 2002). These observations indicate that food availability may serve as a secondary cue for reproduction. For most of the year, crossbills (Loxia spp.) consume primarily conifer seeds, the availability of which often varies unpredictably in time and space. As a result, reproduction in these birds is not thought to be tightly regulated by photoperiod (Hahn, 1995). Instead, access to sufficient

Chapter | 2

Avian Testicular Structure, Function, and Regulation

food resources can lead to testicular development even when birds are exposed to short winter days (Hahn, 1995; Hahn, Wingfield, Mullen, & Deviche, 1995; Hahn, 1998; Deviche & Sharp, 2001). Despite this, food alone does not act as the primary cue (Hahn et al., 2005) because testicular development occurs only in the presence of a mate (Hahn et al., 1995). The only time of year that crossbills have small testes and appear limited in their ability to breed, even if food is available, is during autumnal molt. This limitation may be photoperiod-mediated (Deviche & Sharp, 2001; MacDougall-Shackleton, Deviche, Crain, Ball, & Hahn, 2001). Uniquely, zebra finches may use food as a primary cue, as males exposed to short or long days do not develop their testes when food-restricted (Perfito, Kwong, Bentley, & Hau, 2008). However, exposure to long photoperiod and adlibitum food availability induce maximal testicular development (Perfito et al., 2008). More research is needed in order to understand the importance of food and interactions between food availability and photoperiod in this species.

6.2. Life History 6.2.1. Breeding strategy Seasonal breeders are often categorized based on the development of a refractory state at the end of their breeding period rather than by the cues used to stimulate reproductive development. These categories, although often presented as discrete units, exist on a continuum that sometimes makes it difficult to clearly categorize a species’ breeding strategy. A combination of studies on free-ranging (e.g., Silverin, Massa, & Stokkan, 1993; Deviche & Sharp, 2001; Leitner et al., 2003; Silverin et al., 2008) and captive birds (e.g., Macdougall-Schackleton et al., 2001; Bentley, Audage, Hanspal, Ball, & Hahn, 2003; Hahn, Pereyra, Sharbaugh, & Bentley, 2004; Voigt et al., 2007; Hurley, Wallace, Sartor, & Ball, 2008) is often required to do so. The seasonal breeders that are most easily defined are the absolutely photorefractory species. In these species, transfer from short to long (i.e., longer than the critical day length) photoperiod induces testicular growth, but testes then spontaneously regress even during exposure to increasing or previously stimulatory day lengths (Hamner, 1968; Nicholls et al., 1988). Termination of absolute photorefractoriness requires exposure to short days and coincides with an increase in hypothalamic GnRH-I expression, but not testicular size (Dawson & Goldsmith, 1997). Less clearly categorized are species the testicular cycle of which does not obligatorily include spontaneous regression in response to prolonged exposure to long days. These species, such as the Japanese quail (Robinson & Follett, 1982) and sparrows of the genus Aimophila (Deviche et al., 2008; Small et al., 2008a), are said to be

43

relatively photorefractory. Their testicular growth is stimulated by long days, but testicular regression does not begin until day length decreases. In these species, exposure to artificial long days can increase testicular size even during natural testicular involution (rufous-winged sparrow (Small et al., 2008c)). Testicular regression in the Japanese quail is not associated with decreased hypothalamic GnRH-I (Foster, Plowman, Goldsmith, & Follett, 1987). A third category consists of species that exhibit considerable reproductive flexibility or breed opportunistically, some of which may be relatively photorefractory. Flexible breeders tend to breed seasonally and use day length to time gonadal functioning, but the exact timing of reproduction is largely dependent on nonphotic secondary cues such as rainfall or temperature (Leitner et al., 2003; Wingfield et al., 2003). Opportunistic breeders breed less seasonally, respond minimally to day length, and primarily rely on nonphotic cues, such as food or mates, as signals to stimulate testicular function (Deviche & Sharp, 2001; Perfito et al., 2008). These birds typically inhabit environments where the cues used to time reproduction are largely unpredictable. They must be capable of rapidly developing their gonads when conditions become favorable (Perfito et al., 2007; Hahn et al., 2008). The degree to which a given species exhibits absolute or relative photorefractoriness varies within and between species. For example, within cardueline finches, common redpolls (Carduelis flammea) breed seasonally, pine siskins (Carduelis pinus) breed flexibly but show spontaneous testicular regression, and white-winged crossbills breed almost opportunistically (Hahn et al., 2004) (see Section 6.1.4). Another study on cardueline finches found that red crossbills (Loxia curvirostra), pine siskins, and graycrowned rosy-finches (Leucosticte tephrocotis), but not Cassin’s finches (Carpodacus cassinii), develop testes and have elevated plasma LH when exposed to constant light in autumn (MacDougall-Shackleton, Katti, & Hahn, 2006). The closely related canary (Serinus canaria), breeds flexibly in the wild (Leitner et al., 2003), but artificial selection has generated genetic lines with characteristics of absolute photorefractoriness (Hurley et al., 2008) and breeders with a variable photorefractory response (Bentley, Wingfield, Morton, & Ball, 2000; Bentley et al., 2003). Studies on cardueline finches illustrate the diversity and complexity that need to be considered in order to understand mechanisms that regulate avian reproductive cycles.

6.2.2. Migratory vs. sedentary species Many species migrate before and after their breeding season. Preparation for migration limits the duration of the reproductive period (Lofts & Murton, 1973). Other birds do not migrate, which may extend their breeding season and allow maintenance of territories year-round (Silverin et al.,

44

1993; Hau et al., 2000; Hau, 2001). Still other species exhibit nomadic behavior with large home ranges and unpredictable annual movements (Hahn 1995; Hahn et al., 1995; Hahn, 1998; Perfito et al., 2007). Migration is energetically demanding and thus may constrain the energy available for testicular growth (Drent, Both, Green, Madsen, & Piersma, 2003; Battley & Piersma, 2005). Therefore, migrants must balance the energetic constraints associated with migration with the need to develop their reproductive system so as to minimize the impact on reproductive success and body condition (Bauchinger, Van’t Hof, & Biebach, 2007; 2008). Testicular development in migratory species appears closely tied to changes in photoperiod, particularly on wintering grounds (e.g., Gwinner, 1987; 1989; Silverin, 1995; Ro¨dl, Goymann, Schwabl, & Gwinner, 2004), and short- and longdistance migrants may differ with respect to their responsiveness to small changes in day length. This difference may in turn enable long-distance migrants to initiate migration earlier than short-distance migrants (e.g., stonechats (Saxicola torquata) (Helm & Gwinner, 2005; Raess & Gwinner, 2005)). In many migratory species, males reach breeding grounds before females, which provides time to complete testicular recrudescence and establish territories before females arrive (Kokko, Gunnarsson, Morrell, & Gill, 2006). In these species, particularly long-distance migrants with brief breeding seasons, testicular growth often begins during migration and, as a result, testes can become fully developed shortly after arrival on breeding grounds (Bauchinger et al., 2007). Some species even produce sperm and mate during migration, but it is unclear whether sperm produced at this time are viable enough to ensure fertilization (Quay, 1985; 1989). Ample food supplies at ‘stopover’ sites may contribute to partial or advanced testicular development (Bauchinger et al., 2008). Sedentary species show a diversity of testicular cycles and greater variation than migratory species in their onset of reproduction, depending on whether they are paired and maintain year-round territories or defend territories only during the breeding period (Small et al., 2007; Hahn et al., 2008; Jawor & MacDougall-Shackleton, 2008; Wingfield, 2008). The latter species in temperate regions typically exhibit an annual testicular cycle that parallels changes in day length, but with greater flexibility than seen in migratory species (Phillmore, Hoshooley, Sherry, & MacDougall-Shackleton, 2006; Jawor & MacDougall-Shackleton, 2008; Wingfield, 2008). In species such as the rufouswinged sparrow that maintain pair bonds and territories year-round (Ohmart, 1969; Lowther, Groschupf, & Russell, 1999), males develop testes in spring but generally do not breed until the summer monsoon, when day length is decreasing (Small et al., 2007). The timing of final testicular maturation is flexible, which is advantageous as the

Hormones and Reproduction of Vertebrates

onset and intensity of the monsoon varies considerably from one year to another. Similarly to the rufous-winged sparrow, in sedentary tropical species, factors such as spatial and temporal shifts in food availability play important roles in the control of testicular cycles (Kumar, Singh, Misra, Malik, & Rani, 2002; Wikelski, Hau, Robinson, & Wingfield, 2003; Ro¨dl et al., 2004; O’Brien & Hau, 2005; Hahn et al., 2008). However, in these species there appears to be an annual cycle of testicular recrudescence and involution that is minimally influenced by photoperiod (Hau et al., 1998; Wikelski et al., 2000). Nomadic species such as crossbills and zebra finches, which travel widely in search of food resources, rely heavily on nonphotic factors to time reproductive development (Hahn, 1995; Hahn et al., 1995; Zann et al., 1995; Hahn, 1998; Perfito et al., 2007). Species exhibiting this breeding strategy constitute particularly interesting models to investigate the role of secondary cues in the timing of reproduction. Our understanding of the role of life strategies in testicular cycles is constrained by the paucity of data on this subject for free-ranging birds. Replicating the energetic demands of migration in captive birds is difficult and limits our ability to study how migration impacts testicular functions. More studies are needed that sample birds prior to migration, during stopovers, and shortly after arrival on breeding grounds (Bauchinger et al., 2007; 2008). Identifying factors that influence the flexibility of the annual testicular cycle should enable us to better predict how environmental perturbations such as global climate change (Section 9.2) may impact avian reproduction.

6.2.3. Brood parasitism Brood parasites lay their eggs in the nests of other birds and rarely build nests or rear their own young. In the few studies on this subject, testicular development in brood parasites apparently matched that of their primary host species, suggesting control by similar factors (Payne, 1967; Scott & Middleton, 1968; Payne, 1973a; 1973b; 1977). In the brown-headed cowbird (Molothrus ater), an increase in photophase stimulates testicular development (Dufty & Wingfield, 1986a). In this study, captive and free-ranging males developed larger testes when mated than when unpaired, demonstrating a role for social cues in testicular development (Dufty & Wingfield, 1986b).

6.2.4. Social cues Numerous studies have investigated the role of social factors in avian reproduction. Many investigations on this topic have emphasized effects of auditory and pairing cues (reviewed in Helm, Piersma, & Van der Jeugd, 2006). Studies on the role of auditory cues have primarily focused

Chapter | 2

Avian Testicular Structure, Function, and Regulation

on how male song production in passerines enhances the reproductive system development of conspecific females (Kroodsma, 1976; Leboucher, Depraz, Kreutzer, & Nagle, 1998; Bentley et al., 2000; Maney, Goode, Lake, Lange, & O’Brien, 2007). By contrast, little work has been done on the effects of song on testicular function of other males. In one of the few studies on this subject, exposure of rufouswinged sparrows to conspecific song increased the effects of long-day exposure on testicular growth (Small et al., 2008c). No such effect has, however, been observed in the canary (Boseret, Carere, Ball, & Balthazart, 2006). Testicular function, particularly in monogamous species, is influenced by the presence of a mate. Captive male European starlings, Japanese quail, and brown-headed cowbirds that are kept without or with only limited exposure to a female exhibit a decreased capacity to develop their testes, and/or regress them sooner than males held with a female (Dawson & Goldsmith, 1984; Delville, Sulon, Hendrick, & Balthazart, 1984; Dufty & Wingfield, 1986b; Gwinner, Van’t Hof, & Zeman, 2002). The importance of the pair bond is also demonstrated in crossbills, which can develop their testes and breed in winter provided that they receive proper food and are exposed to mates (Hahn et al., 2005). Similarly, captive male ptarmigans (Lagopus sp.) show a truncated breeding season relative to free-ranging conspecifics (Stokkan et al., 1988) and this difference may result from lack of exposure to social factors. The role of such factors should be considered during studies, particularly those using captive birds from wild populations, on the environmental control of reproduction.

7. ECOLOGY OF TESTICULAR FUNCTIONS Birds have become model organisms for addressing questions related to the evolution of breeding systems, costs of reproduction, and sexual selection of ornamental traits. Work on this subject largely stems from three basic characteristics of birds: (1) The dependence of measurable behaviors on numerous physiology-based processes such as territoriality and courtship displays; (2) Breeding structures and behaviors that are easily quantifiable as potential costs of reproduction; (3) Highly variable and flexible breeding strategies resulting from numerous physiological adaptations (Section 6). The two main functions of testesdandrogen synthesis and sperm productiondare under intensive natural and sexual selection pressures and are considered to be energetically costly. Detailed understanding of these functions has led researchers to examine broad-scale patterns related to testicular size, plasma T, and androgen-dependent

45

behaviors, leading to free-ranging birds becoming one of the best-studied taxa for investigating this topic.

7.1. Linking Testosterone (T) and Sperm Quality Testosterone in vertebrates is essential for spermatogenesis, but the negative feedback effect of T on the hypothalamus and pituitary gland can also lead to suppressed testicular functions. The degree to which plasma T levels reflects spermatogenetic activity or sperm quality is controversial, but a few studies have attempted to clarify this link. An early study on turkeys found no relationship between serum T and ejaculate volume (Cecil & Bakst, 1986). Similarly, T administration either does not alter or in some cases decreases the ejaculate volume of free-ranging male darkeyed juncos, but this effect depends on the breeding stage (Kast, Ketterson, & Nolan, 1998). An inverse relation between plasma T and ejaculate volume in T-treated birds may reflect a treatment-mediated increase in copulation rate that in turn results in reduced residual ejaculate volumes (Kast et al., 1998). Alternately or in addition, the negative action of T on the hypothalamoepituitary gland axis may decrease testicular function, resulting in smaller ejaculate volume. In contrast to the above studies, Penfold et al. (2000) reported that circulating T levels in breeding northern pintail (Anas acuta) are correlated to both the total number of sperm and the percentage of sperm exhibiting normal morphological characteristics, and T administration in some circumstances stimulates testicular functions (e.g., Deviche et al., 2006). Future studies should aim at elucidating the mechanisms mediating this increase and address the relation between T and sperm quality and/or production, particularly by comparing taxa with varying seasonal T profiles and male fertility rates.

7.2. Correlates of Testicular Size 7.2.1. Body size and age Most testicular tissue is devoted to spermatogenesis and testis size is, therefore, often used to estimate sperm production (Section 3) (Moller, 1988). Large testes produce more sperm than small testes in the house sparrow (Birkhead et al., 1994) and the zebra finch (Birkhead, Pellatt, & Fletcher, 1993). However, little empirical information concerning sperm production in wild birds is available with which to assess whether these data can be generalized, especially as sperm production estimates can be highly variable (Briskie & Montgomerie, 2007). Inter- and intraspecific comparisons suggest allometric associations between testis and body sizes, but the strength of this association varies (Rising, 1987a; Moller & Erritzoe, 1988; Moller, 1988; 1991; Olsen, 1991; Moller, 1994; Moller &

46

Briskie, 1995; Rising, 1996; Merila¨ & Sheldon, 1999; Coker, McKinney, Hays, Briggs, & Cheng, 2002; Pochron & Wright, 2002; Garamszegi et al., 2005; Pitcher et al., 2005; Calhim & Birkhead, 2007; Gunn et al., 2008). These observations have prompted researchers to correct testis sizes for variations in body mass, most often by using regression residual methods. Several studies have documented age-related variation in testis size, with older adults generally having larger testes than younger adults (Selander & Hauser, 1965; Morton, Peterson, Burns, & Allan, 1990; Hill, 1994; Deviche, Wingfield, & Sharp, 2000b; Graves, 2004; Laskemoen, Fossoy, Rudolfsen, & Lifjeld, 2008). These studies have primarily compared after-hatch-year males with older males (two or more years of age), as it is often difficult to age birds, especially passerines, that are older than two years. Age-related differences in testis size may result from younger birds secreting less GTHs than older birds (Ketterson & Nolan, 1992; Silverin et al., 1997; but see Morton et al., 1990), but whether testicular sensitivity to these hormones is also age-dependent has not been investigated. Age-dependent differences in mean and maximal testis size may account for lower plasma T in younger adult males compared with older males (Sorenson, Nolan, Brown, Derrickson, & Monfort, 1997; Deviche et al., 2000b; Deviche & Sharp, 2001). Age-related variation in other sexual characteristics, such as the size of the seminal glomerula and cloacal protuberance, has been documented in the bluethroat (Luscinia svecica) (Laskemoen et al., 2008). Superb fairy-wrens (Malurus cyaneus) are thought to endure intensive sexual selection. In adult males of this species, the size of the cloacal tip, which likely serves as an intromittent organ (Rowe, Bakst, & Pruett-Jones, 2008), also increases with age (Mulder & Cockburn, 1993). Collectively, these results are consistent with evidence for age-related variation in male reproductive success, particularly in reference to the number of extrapair matings (Richardson & Burke, 1999; GonzalezSolis & Becker, 2002; Westneat & Stewart, 2003; Laskemoen et al., 2008). However, specific associations between age-related variation in testicular functions and fitness are few, and this topic warrants further investigation.

7.2.2. Testosterone (T), mating systems, and geography Testosterone in male birds influences the expression of various behaviors, particularly in relation to the establishment of territories, the pursuit of extrapair mating opportunities, the defense of females against their extrapair forays, and the allocation of energy towards paternal care of offspring (Ketterson et al., 1991; De Ridder, Pinxten, & Eens, 2000; Van Roo, 2004; Garamszegi et al., 2005; Schwabl, Flinks, & Gwinner, 2005; Soma, 2006).

Hormones and Reproduction of Vertebrates

Reviewing the effects of T on male bird behavior is beyond the scope of this chapter (see Chapters 7 and 8, this volume), but collectively these studies suggest a link between testis size and T profiles, particularly through comparative studies in avian taxa whose life-history traits differ. Seasonally maximal plasma T levels are thought to be higher in birds exhibiting polygynous mating systems than in monogamous species, which is considered to reflect the intensity of sexual selection (Wingfield, Hegner, Dufty, & Ball, 1990). Further, polygynous species tend to have larger testicular volumes than size-matched monogamous birds (Garamszegi et al., 2005). Interspecific studies on this subject have provided largely consistent results, but intraspecific comparisons attempting to relate plasma T to testicular size have generated mixed results. For example, a positive relation between these variables was reported for mallards (Denk & Kempenaers, 2006) but not red-winged blackbirds (Weatherhead, Metz, Bennett, & Irwin, 1993). A further complication is illustrated by a study comparing 116 bird species in which positive associations between testicular size and circulating T concentrations were confounded by strong latitudinal variation, with tropical species having lower plasma T and smaller testes than temperate or high-latitude breeders (Section 6.2.2) (Garamszegi et al., 2005). Similar latitudinal trends of increasing testicular size have been reported in other comparative studies (Merila¨ & Sheldon, 1999; Moore, Perfito, Wada, Sperry, & Wingfield, 2002; Pitcher et al., 2005). The length of the breeding season and, therefore, potentially the period during which plasma T is elevated, often decrease as latitude increases (Wingfield & Hunt, 2002; Hau, Gill, & Goymann, 2008). At high latitudes, reproduction within a species often is more synchronous than at low latitudes, where relatively constant environmental conditions may enable longer reproductive periods (Wingfield & Hunt, 2002; Goymann et al., 2004; Moore, Wingfield, & Brenowitz, 2004; Hau et al., 2008). As a result, extrapair paternity is thought to be less frequent in tropical than temperate or high-latitude-region species (Stutchbury, Morton, & Piper, 1998; Spottiswoode & Moller, 2004). This hypothesis is supported by intraspecific observations showing that testicular size increases with latitude (house finch (Carpodacus mexicanus), red-eyed vireo (Vireo olivaceus), and greenfinch (Carduelis chloris) (Merila¨ & Sheldon, 1999)). However, no such increase was found in black-throated blue warblers (Dendroica caerulescens) (Graves, 2004) and the opposite situation was described in savannah sparrows (Passerculus sandwichensis) (Rising, 1987b; Pitcher & Stutchbury, 1998). It is currently unclear whether positive correlations between testicular size and latitude reflect genetic differences between populations or species, or are induced by environmental effects on the phenotype. In support of the latter, Silverin et al. (2008) compared the testicular development

Chapter | 2

Avian Testicular Structure, Function, and Regulation

of photostimulated great tits obtained from different latitudes (45 to 70 N) and held in identical captive conditions. It was found in this species that the time course of photoinduced changes in testicular size depends on the latitude of origin, but populations do not differ with respect to their maximal testicular size.

47

experimental work investigating testicular asymmetry in species belonging to various phylogenetic groups and exhibiting diverse lifestyles (e.g., aerial vs. terrestrial) is needed to address these issues. Age and reproductive condition (Dang & Guraya, 1978) are also thought to influence avian testicular asymmetry and studies would benefit from incorporating these factors into the data analysis and interpretation.

7.3. Evolutionary Explanations for Testicular Size Asymmetry

7.4. Theories of Sperm Competition

Variation in size between the left and right testes has also drawn the attention of researchers. Moller (1994) proposed that, in some species with asymmetric testes, such as the house sparrow and the barn swallow (Hirundo rustica), the normally smaller testis develops only when the other testis fails to grow normally (‘compensation hypothesis’). This hypothesis is supported by studies showing that hemicastration causes compensatory growth of the remaining testis, regardless of which testis is removed (Farner, Morton, & Follett, 1968; Driot, De Reviers, & Williams, 1979), and increased FSH secretion (Wilson & Follett, 1978). Thus, the normally less developed testis in a species with asymmetric testicular sizes presumably is sensitive to gonadostimulatory factors, such as GTHs. Within an individual, however, the two testes may be differentially sensitive to GTHs, but the cellular basis of this potential difference has not been researched. The compensation hypothesis predicts that males in poor body condition have a lower capacity to engage in this compensatory growth. Accordingly, within a population the degree of testicular asymmetry should reflect overall male quality, with lower quality males having less symmetric testes. This was the case in some studies (house sparrow and barn swallow (Moller, 1994)) but not others (tree swallow (Kempenaers et al., 2002); blackthroated blue warbler (Graves, 2004)) and the generality of the compensation hypothesis remains to be established. The degree of adult testicular size asymmetry is also thought to be associated with survival (Birkhead et al., 1997). The observation in black-throated blue warblers that adult testicular size asymmetry increases with age is consistent with this view (Graves, 2004). However, there is no identified mechanism linking the degree of testicular size asymmetry to adult survival, and a causal relation between these variables remains speculative. Finally, testicular asymmetry may be advantageous in increasing flight efficiency by reducing paired testicular mass and, therefore, wing loading. However, why the same increase in flight efficiency could not be attained by developing symmetric testes of same paired mass as that of asymmetric testes is unclear. Further, some predominantly terrestrial birds (chicken (Hocking, 1992)), but also highly aerial species (e.g., tree swallows (Kempenaers et al., 2002)), show no testicular size asymmetry. New descriptive and

Two seminal papers (Parker, 1970a, b; no pun intended) introduced the concept of ‘sperm competition.’ Accordingly, in situations where females mate with multiple males during a given reproductive cycle, fertilization and thus paternity of offspring would be determined by the outcome of competition between the sperm of the mated males. This hypothesis, initially developed based on insect studies, has become a predominant theme in avian research. Sperm competition may be especially prominent in birds. Females of many species can store sperm for several days or weeks in specialized sperm storage tubules (SSTs), which may result in competition between several males with which they mated (Briskie & Montgomerie, 1993). In situations of sperm competition, males can gain more fertilizations by (1) producing greater quantities of sperm per ejaculate (often inferred from studies of testicular sizedsee Section 7.2) or (2) altering sperm morphology to increase sperm mobility or longevity in the female reproductive tract. Few data exist on whether an increase in testicular size is associated with increased sperm production. Further, this relation does not need to be linear because large increases in testicular size may be associated with a proportionally small increase in sperm production (Calhim & Birkhead, 2007). Sperm morphology varies considerably among species (for reviews see Briskie & Montgomerie, 2007; Jamieson, 2007). Sperm length, in particular, may be an important determinant of mobility, but the limited experimental data available on this subject do not support this assertion (Denk, Holzmann, Peters, Vermeirssen, & Kempenaers, 2005). Sperm length is highly consistent within individuals but varies among individuals (Laskemoen, Kleven, Fossoy, & Lifjeld, 2007), and a study on zebra finches suggests that individual variation in sperm size is heritable (Birkhead, Pellatt, Brekke, Yeates, & Castillo-Juarez, 2005). A comparative study of 16 shorebird species revealed that longer sperm are produced in polyandrous and polygynous than in monogamous species (Johnson & Briskie, 1999). However, an earlier study on passerines found no relation between sperm length and mating system, but rather a positive and a negative correlation between sperm length and the length of female SSTs and the number of SSTs, respectively (Briskie & Montgomerie, 1992). These

48

authors reasoned that longer sperm may swim faster, which would be advantageous when there is little opportunity for sperm storage (i.e., fewer SSTs). Testes may also be sites of a physiological tradeoff between energetic investment into individual sperm size and the number of sperm produced or the volume of the ejaculate, as suggested by studies in other diverse taxa (mammals (Gomendio & Roldan, 1991); snails (Oppliger, Hosken, & Ribi, 1998)). In birds, intense sperm competition appears to be more closely associated with variation in sperm size than ejaculate volume, but few direct comparisons of these parameters are available (Briskie, Montgomerie, & Birkhead, 1997). Evolutionary theory suggests that, for a given trait under intense stabilizing or directional selection, additive genetic variance in a heritable trait should decrease. A recent study (Kleven, Laskemoen, Fossoy, Robertson, & Lifjeld, 2008) demonstrates decreased variance in sperm length with increasing frequency of extrapair paternity for 22 passerine species, suggesting that sperm length is under strong selection pressure via sperm competition (Figure 2.2). Postcopulatory sexual selection may account for the evolution of sperm morphology, but little empirical research exists in birds concerning how variation in sperm morphological characteristics relates to increased fertilization success. A current topic of research on sperm competition is sperm precedence, where copulation may result in

Hormones and Reproduction of Vertebrates

disproportionate fertilization success simply due to the sequence by which mating occurred. Several models have been proposed to explain situations of sperm precedence, but one in particulardthe passive sperm loss modeldhas received the most attention (Lessells & Birkhead, 1990; Birkhead & Biggins, 1998). Accordingly, sperm are lost from a female at a constant rate and, thus, the longer the time between two matings, all else being equal, the greater the proportion of offspring fathered by the second mating (Birkhead & Biggins, 1998). This model is supported by studies in chickens, turkeys (Birkhead & Biggins, 1998), and zebra finches (Birkhead & Fletcher, 1998). The study of sperm competition in birds is a fruitful area of research that has contributed substantially to our understanding of the flexibility of avian reproductive systems. However, much of this work has focused on describing large-scale patterns in free-living birds and includes relatively little experimental research. We have few empirical data regarding how sperm characteristics influence their mobility and have largely relied on the assumption that greater sperm length translates to increased speed (although see Humphries, Evans, & Simmons, 2008).

7.5. Negative Consequences of Large Testes Large testes may impart benefits but also physiological costs. One such cost is the increased energetic investment

FIGURE 2.2 Relationship between extrapair paternity (proportion of young sired by extrapair males) and (a) intraspecific (22 species) and (b) individual (20 species) variation (coefficient of variation (CV)) in total sperm length in passerines. Each point represents the mean value per species. Data are presented as untransformed values and are not corrected for phylogeny. Labels refer to the following species: 1, Acrocephalus schoenobaenus; 2, Agelaius phoeniceus; 3, Carduelis tristis; 4, Dendroica petechia; 5, Emberiza schoeniclus; 6, Fringilla coelebs; 7, Geothlypis trichas; 8, Hirundo rustica; 9, Luscinia svecica; 10, Malurus splendens; 11, Melospiza georgiana; 12, Melospiza melodia; 13, Passerculus sandwichensis; 14, Passerina cyanea; 15, Phoenicurus phoenicurus; 16, Phylloscopus trochilus; 17, Poecile atricapilla; 18, Riparia riparia; 19, Setophaga ruticilla; 20, Sialia sialis; 21, Tachycineta bicolor; 22, Vermivora chrysoptera. Adapted from Kleven, Laskemoen, Fossoy, Robertson, and Lifjeld (2008), with permission.

Chapter | 2

Avian Testicular Structure, Function, and Regulation

involved in maintaining testicular tissue. This may be the case particularly in seasonally breeding birds in which testicular mass fluctuates dramatically throughout the year. The added mass of larger testes during breeding may also increase wing loading, thus increasing flight cost. Little empirical data on this topic exists, but, in one study on European starlings, addition of weights comparable to fully developed testes decreased the nest visitation rate, possibly as a result of decreased flight efficiency (Wright & Cuthill, 1989). Increased sperm production by larger testes may be associated with greater androgen production (Garamszegi et al., 2005; Denk & Kempenaers, 2006). As with many steroids, chronically high T levels can be immunosuppressive (Muehlenbein & Bribiescas, 2005; Singh & Haldar, 2005; Deviche & Parris, 2006; Mougeot, Redpath, & Piertney, 2006; Boonekamp, Ros, & Verhulst, 2008). Females may asses the quality of males on the basis of characteristics that are androgen-dependent, and it is suggested that better-quality males are in a better condition to cope with the immunosuppressive effects of higher androgen levels (Moller, 1990; Folstad & Karter, 1992; Day, McBroom, & Schlinger, 2006; Fusani, 2008; Mcglothlin et al., 2008). The suppressive action of T remains paradoxical, but an interesting hypothesis suggests that this hormone, which concentrates in the seminiferous tubules during spermatogenesis, may act locally to deter autoimmune responses (i.e., antibody production) to antigenic sperm (Folstad & Skarstein, 1997; Hillgarth, Ramenofsky, & Wingfield, 1997). Reproductive ‘lower-quality’ males that are combating infectious organisms may have difficulty regulating this localized immunosuppression, which may interfere with sperm production (Folstad & Skarstein, 1997; Hillgarth et al., 1997). Thus, increased T production by larger testes may increase susceptibility to infection and ultimately interfere with sperm production. Future studies aimed at testing this hypothesis may lead to further insights into the costs of maintaining large testes.

8. TESTICULAR DYSFUNCTION The exocrine and endocrine functions of avian testes normally are carefully regulated at multiple levels ranging from the brain to locally produced chemicals. A myriad of conditions may, however, interfere with normal testicular function. This topic is of great interest to reproductive biologists, conservationists, evolutionists, veterinarians, and those interested in the artificial propagation of game and poultry species. A complete analysis of avian testicular dysfunction and its ultimate causes is beyond the scope of this chapter. Instead, we will discuss some findings on naturally occurring and anthropogenically induced conditions in birds, particularly with reference to the endocrine function of the testes (see also Chapter 9, this volume).

49

8.1. Phytoestrogens One proposed form of testicular dysfunction results from effects of natural plant compounds termed endocrine-active phytochemicals (Vajda & Norris, 2006) ingested by birds. Some plants produce phytoestrogenic compounds (substances with natural chemical properties similar to estrogens) that can act as endocrine disruptors in insects (Lafont, 1997), mammals (Shackell, Kelly, & Johnstone, 1993; Saloniemi, Wahala, Nykanenkurki, Kallela, & Saastamoinen, 1995; Santti, Makela, Strauss, Korkman, & Kostian, 1998; Odum et al., 2001; Dixon, 2004; see Volume 5, Chapter 14), fishes (Ishibashi et al., 2004; see Volume 1, Chapter 13), and birds (Berry, Zhang, & MacDaniel, 1999; Millam et al., 2002; Corbitt, Satre, Adamson, Cobbs, & Bentley, 2007; Rochester et al., 2008b; see Chapter 9, this volume). These phytoestrogenic compounds are thought to have evolved as a defense against herbivory (Labov, 1977; Hughes, 1988; Wynne-Edwards, 2001) and can vary in potency depending on factors such as the part and age of the plant and whether the plant is under stress (e.g., drought or constant herbivory) (Leopold, Erwin, Oh, & Browning, 1976; McMurray, Laidlaw, & McElroy, 1986; Tsao, Papadopoulos, Yang, Young, & McRae, 2006; Rochester et al., 2008b). Exposure to phytoestrogens decreases testicular weight relative to body size in developing Japanese quail (Rochester et al., 2008b) and can inhibit T production in cultured avian Leydig cells from chickens and geese (Opalka, Kaminska, Ciereszko, & Dusza, 2004; Opalka, Kaminska, Puchajda-Skowronska, & Dusza, 2006), but the mechanism involved is unclear. These effects may explain the decrease in fertility and reproductive success as well as differential breeding responses observed in birds that consume phytoestrogenic plants or plant-based diets (Leopold et al., 1976; Beck, Unterrieder, Krenn, Kubelka, & Jungbauer, 2003; Corbitt et al., 2007). Effects of phytoestrogens are not always pronounced (Opalka et al., 2008) but, when apparent, seem to affect male more than female reproductive functions (Wilhelms, Scanes, & Anderson, 2006; Rochester et al., 2008b). As the suppressive actions of phytoestrogens on the reproductive system are being unraveled, it will be important to research interactions between these effects and those of endocrine disruptors (Section 9.3).

8.2. Hybridization and Infertility Hybridization between closely related taxa has long fascinated biologists due to the nature of the outcome, implications for the biological species concept, and the possibility of a rapid mechanism for genetic evolution via introgression. Hybridization has been recorded in wild birds more commonly than in other vertebrate taxa and incidences of hybrids have been reported in numerous

50

orders (P. Grant & B. Grant, 1992). We have long known that hybrid offspring often exhibit lower fertility and in some cases complete sterility, and studies of free-ranging avian populations have documented declines in the reproductive success of hybrids relative to parental species (Bell, 1997; Baker & Boylan, 1999; Solberg, Jensen, Ringsby, & Saether, 2006; Svedin, Wiley, Veen, Gustafsson, & Qvarnstrom, 2008). However, little research has been conducted to investigate physiological consequences of hybridization, particularly in male birds. Crossbreeding of Muscovy duck drakes (Cairina moschata) and Pekin duck females produces hybrids with testes of intermediate size relative to those of the parents (Snapir et al., 1998). Hybrids produce normal quantities of T, at levels intermediate to those of males of the two parent species, and they exhibit normal testicular growth and organization of the seminiferous tubules. However, they do not produce mature spermatids, indicating an inability to successfully complete spermatogenesis (Snapir et al., 1998). This deficiency likely results from genetic incompatibility at the chromosomal level (Snapir et al., 1998). Hybrids between hermit warblers (Dendroica occidentalis) and Townsend’s warblers (Dendroica townsendi) likewise have plasma T levels intermediate relative to those of males of the parent species (Owen-Ashley & Butler, 2004). These levels are positively associated with the degree of backcrossing (hybrid score) to the parent phenotypes and possibly reflect genetic divergence in aggressiveness between males of the species (Owen-Ashley & Butler, 2004). Although most hybridizations result in sterile offspring, they can in some cases increase fitness by increasing heterozygosity (i.e., hybrid vigor (P. Grant & B. Grant, 1992)). This outcome is of particular interest to researchers concerned with adaptations at the microgeographic level. In particular, hybrid zones where the ranges of two species overlap, thus resulting in higher frequencies of hybridization, are thought to be especially prominent in ‘edge’ habitats (Hayes, 2001; Adamik & Bures, 2007). Anthropogenic disturbance increases these types of transitional habitats, which in turn may influence the frequency of hybridization. This may become especially important for vulnerable or threatened species, in which hybridization with a more common species can influence population status. The degree to which hybridization may impact free-ranging avian populations is poorly explored. Understanding the reproductive consequences of hybridization requires an appreciation of its effects on steroidogenesis and spermatogenesis.

8.3. Testicular Pathology Several conditions, many of which are associated with epididymal abnormalities, can negatively affect fertility in domestic poultry. In turkeys, yellow semen syndrome (YSS), which results from overaccumulation of lipid

Hormones and Reproduction of Vertebrates

droplets in the efferent duct epithelia, is associated with an increase in seminal proteins (Thurston, 1979; Thurston, Hess, Froman, & Biellier, 1982) and cholesterol (Hess & Thurston, 1982), as well as with increased frequency of abnormal sperm and spermatids (Thurston & Korn, 1997). Turkeys exhibiting YSS also show elevated plasma levels of the androgen 5a-dihydrotestosterone (DHT) and increased capacity to bind DHT in semen, but the mechanism that accounts for this increased binding capacity remains unresolved (Hess, Birrenkott, & Thurston, 1984). In one study androgen treatment of turkeys failed to induce YSS (Froman & Thurston, 1983), suggesting that androgen dysfunction was not responsible for the condition. The cause of YSS in turkeys is unknown, but most of the existing evidence points to a viral origin (Boltz et al., 2006; C. Boltz, D. Boltz, Bunick, Scherba, & Bahr, 2007; Villarreal et al., 2007). Another condition affecting the epididymis of male birds is the formation of calcium stones, known as epididymal lithiasis, which can impair T and sperm production primarily by limiting testicular size (Janssen et al., 2000). These stones are thought to block the passage of sperm, leading to increased pressure in dilated seminiferous tubules and impaired spermatogenesis. The factors that cause calcium stones have not been identified. Birds with such stones exhibit reduced fertility even after artificial insemination using equal amounts of sperm from birds with and without stones. Thus, epididymal stones may impair specifically sperm maturation (Janssen et al., 2000). The formation of stones has been linked to the avian infectious bronchitis virus (Boltz et al., 2006; 2007; Villarreal et al., 2007). In a couple of captive species, testicular tumors have been reported as neoplasms of the Sertoli cells (Gorham & Ottinger, 1986; Rossi, Ceccherelli, Piersigilli, & Tarantino, 2003), which likely impairs male fertility. The occurrence of Sertoli cell tumors in birds is thought to be rare, but has been documented in Passeriformes (Rossi et al., 2003), Galliformes (Gorham & Ottinger, 1986), Psittaciformes (Beach, 1962), and Columbiformes (Turk, Kim, & Gallina, 1981). In the Gouldian finch (Erythrura gouldiae), testicular neoplastic tissue was associated with a polyomavirus (Rossi et al., 2003), but in most cases the cause was unknown. Little research has been done that addresses how specific diseases impact testicular function in captive or wild species, even though this topic is of considerable importance to the poultry industry and to investigators interested in the captive breeding of rare species.

9. ANTHROPOGENIC EFFECTS ON TESTICULAR FUNCTION 9.1. Introduced Species Some successful invasive/introduced species, such as the European starling (Dawson & Goldsmith, 1982; Dawson,

51

Avian Testicular Structure, Function, and Regulation

9.2. Climate Change Global climate change has the potential to profoundly affect factors that birds utilize to time their reproductive development. However, to our knowledge, no research on the direct effects of climate change on testicular function has been conducted. In the recent past, the average breeding dates of many bird species have advanced by a few days to over a week from historic breeding dates (generally established by long-term studies of species populations), presumably as a result of ambient temperature increases (Jarvinen, 1989; Crick, Dudley, Glue, & Thomson, 1997; Both, Bijlsma, & Visser, 2005; PearceHiggins, Yalden, & Whittingham, 2005; Torti & Dunn, 2005) and the subsequent earlier availability of insect

food sources (e.g., Visser, Holleman, & Gienapp, 2006). As global climate changes continue, the degree to which birds will be able to adapt the phenology of their annual cycle to new environmental conditions is not known. The long-term effects of changes in ambient conditions also are hypothetical. Intraspecific variation in the timing of testicular development in captive-bred (Bentley et al., 2003; Hurley et al., 2008) and free-ranging birds originating from different areas of their range have been observed (Figure 2.3). These findings suggest that within species some flexibility exists with respect to the cues used to regulate reproduction. However, the evolutionary time course for these adaptations is unclear and may be insufficient to cope with the drastic pace of current and

(a) 8

Milano (45º25') Goteborg (57º42') Tromso (69º40') Control Birds

Testis Length (mm)

7 6 5 4 3 2 1 0

7

0 8

10

weeks 12

14 14

16

Day Length (Hours)

(b) 45

9

40 8 35 30

7

25 6 5 4

3 4/24/08

20 Colorado Testis Arizona Testis Colorado CP Arizona CP Summer Solstice 2008 AZ Monsoon 2008 AZ Daily Rainfall

5/24/08

15 10 5

6/23/08

7/23/08

8/22/08

Daily Rain fall Amount (mm)

1983; Young et al., 2001; Dawson & Sharp, 2007) and house sparrow (Hegner & Wingfield, 1986; Anderson, 2006; Trivedi, Rani, & Kumar, 2006), are also among the best-studied species in avian physiology. Other species, such as the rock pigeon, have been less studied, but have been noted to breed year-round, despite some evidence for photoperiodic influence on testicular function (Johnston, 1992; Ramachandran, Patel, & Patel, 1996). Overall, little research has been done on differences in testicular cycles that may exist between the invasive, introduced, and native ranges of any species. Indirectly, based on captive studies on birds from both native and introduced populations, there is little evidence for drastic differences in annual testicular development (Dawson & Goldsmith, 1982; Dawson, 1983; Young et al., 2001). Whether introduced species alter their testicular cycle to adapt to local environmental conditions or whether only species with cycles similar to those of local native species adapt successfully is not known and warrants new studies. A major question of interest to wildlife managers is why some species are more successful colonizers than others. For example, house sparrows have spread throughout the world following multiple introductions, whereas congeneric Eurasian tree sparrows (Passer montanus) have not spread far beyond their North American initial release area (St. Louis & Barlow, 1988; Lang & Barlow, 1997). Factors other than the flexibility of the testicular cycle, the number of birds released, the number of releases, and the ability to exploit urban resources (see Section 9.3) may contribute to determining the success of introduced species. New studies are warranted to compare species that differ with regard to their capacity for invasiveness and their ability to breed in human-modified environments. Research on this subject may provide valuable information on how to manage the potentially damaging effects of invasive species on native wildlife and may improve our understanding of how reproductive flexibility influences adaption to novel environmental conditions.

Testis Length / CP Width (mm)

Chapter | 2

0 9/21/08

Date FIGURE 2.3 Intraspecific variation in photoinduced testicular development. (a) Testicular development in captive great tits (Parus major) from three sedentary populations at varying latitudes as a function of photophase. Birds were photostimulated by increasing day length 30 minutes weekly for 16 weeks, starting at 8L : 16D. Control birds remained exposed to 8L : 16D and all birds were maintained at 20 C. Adapted with permission from Silverin et al., 1993. (b) Development of testes and cloacal protuberance (CP) (mm) in two geographically separate populations of free-ranging Cassin’s sparrows (Aimophila cassinii) during the 2008 breeding season. From L.L. Hurley, unpublished observations. Values are means standard error (SE).

52

projected climate change (Dawson, 2008; Gienapp, Teplitsky, Alho, Mills, & Merila¨, 2008). Research on the impact of climate change on reproductive physiology is urgently needed to answer these questions.

9.3. Direct Human ImpactdEndocrine Disruption and Urbanization In many regions of the earth, the natural landscape has been heavily impacted by humans in terms of land use (e.g., farming and urbanization) and as a result of the release of pollutants (e.g., chemicals or light) into the environment. A plethora of studies have investigated how these impacts influence avian reproduction. One major area of this research is the influence of xenobiotic (manmade) substances introduced into the environment through agriculture and industry and that mimic the actions of phytoestrogens or endogenous hormones (endocrine-disrupting chemicals). Most work on this topic has involved administering these chemicals in ovo or after hatching and then determining the effects of the treatments on reproductive development, behavior, fertility, and nesting success (Adkins, 1975, 1978; Adkins-Regan & Ascenzi, 1987; Millam et al., 2001). In male zebra finches, early post-hatch treatment with estradiol benzoate can reduce fertility due to lowered sperm aggregation, decreased sperm density, and alterations in seminiferous tubule organization (Figure 2.4). This treatment can also lead to oviduct formation in males during development (Wade, Gong, & Arnold, 1997). Males exposed to low doses of xenobiotic compounds still display stereotypical courting and mating behaviors, but those given higher doses exhibit female parental behavior and hatch fewer young than control birds (Millam et al., 2001; Rochester, Heiblum, Rozenboim, & Millam, 2008). These findings suggest that xenobiotic chemicals mimic endogenous hormones and are capable of disrupting normal endocrine function, resulting in decreased male fertility (Millam, 2005). If the same applies to free-ranging avian populations, these populations could be affected negatively. A broader discussion of endocrine-disrupting chemicals in birds is found in Chapter 9 of this volume. Urbanization also has the potential to have a major impact on avian populations. As urban landscapes expand and encroach on native habitats, they alter many components of the environment, resulting, in a decrease in native vegetation, an increase in exotic plant and animal species, an alteration of food types and their availability, exposure to a great variety of anthropogenic chemicals, and exposure to artificial lights and increased ambient temperatures (Schoech, Bowman, Bridge, & Boughton, 2007; Schoech & Hahn, 2007; Robb, McDonald, Chamberlain, & Bearhop, 2008; Fokidis, Orchinik, & Deviche, 2009). Changes

Hormones and Reproduction of Vertebrates

in native landscapes also impact parasite and disease risks (Ruiz, Rosenmann, Novoa, & Sabat, 2002; Fokidis, Greiner, & Deviche, 2008) and physiological responses to acute stress (Ruiz et al., 2002; Schoech et al., 2007; Fokidis et al., 2009; see also Chapter 5, this volume). Several studies have demonstrated that urbanization is associated with a seasonal shift of breeding dates (European blackbirds (Turdus merula) (Partecke, Van’t Hof, & Gwinner, 2004; 2005); Florida scrub jays (Aphelocoma coerulescens) (Schoech et al., 2007); curve-billed thrasher (Toxostoma curvirostre) (Fokidis, unpublished data)) and gonadal development (Figure 2.5). The drastic environmental changes outlined above have great potential to alter the specific cues that birds use to time their testicular development. Research on this topic may help us understand how birds adapt to urbanization by changing their use of environmental factors that control reproductive cycles.

10. CONCLUSIONS AND FUTURE DIRECTIONS Investigations conducted in the past half-century have informed us about many aspects of avian testicular functions. As a result, considerable information is available on the environmental control of testicular function, including the influence of day length and other abiotic factors such as temperature and food availability; the mechanisms by which photic information, in particular, is integrated by the brain and used to regulate seasonal testicular cycles; the regulation of sperm formation and testicular steroidogenesis; and the mode of action of a wide and ever-expanding variety of paracrine and other chemical mediators on testes. In addition, birds have become choice experimental models for research related to sperm competition, effects of acute and chronic stress on the male reproductive system, and the influence of intraspecific social interactions on the secretion of testicular androgens. Despite this progress, large gaps remain in our understanding of avian testicular function and its regulation. This is partly due to the fact that most work on this topic has used either captive or domesticated species. Thus, large groups of birds, in particular those inhabiting tropical and equatorial regions, where most of the global diversity in avian species is present, remain essentially unstudied. This situation may, however, improve in the near future as an increasing number of physiologists focus their attention on the control of reproduction in birds inhabiting these regions. A particularly promising area for future research concerns the effects of global climate changes and urbanization on testicular function. Global climate changes are already impacting avian populations, and the rapid

Chapter | 2

Avian Testicular Structure, Function, and Regulation

53

FIGURE 2.4 Testicular disruption resulting from postnatal estradiol benzoate treatment in the zebra finch. The figure shows representative photomicrographs of testicular sections from adult male zebra finches treated from post-hatch days 5 to 11 with 10 (EB10) or 100 (EB100) nmol/g body weight estradiol benzoate or control canola oil. (a and b) Testicular morphology in a control male. Note the orderly progression of spermatogenesis development through the germinal epithelium (GE), from spermatogonia (sg) near the basal lamina (BL) to primary spermatocytes (sc); the spermatids (est, elongated spermatids; rst, rounded spermatids) near the lumen (L); and the normal thickness of the germinal epithelium (dotted line). (c and d) Testicular morphology in an EB100 male. Note the thinner germinal epithelium and lumen containing a large matrix of developing sperm cells. Black arrows denote vacuoles. (e and f) Testicular morphology in an EB10 male. Note the absence of laminarity and lumen. Reprinted from Rochester, Forstmeier, and Millam (2010), with permission.

urbanization that is taking place in many regions of the world is having severe detrimental effects on natural ecosystems. These effects are thought to result from many factors including direct habitat alterations; the release into the environment of endocrine disruptors and pollutants; and, in some cases, the development of urban microclimates It is likely that at least some of these factorsdin particular endocrine disruptors, pollutants, and locally altered enviromentsdinfluence testicular function directly or indirectly, but whether and the extent to which this is the case is not well known. We also have a poor understanding of the specific mechanisms involved and the relative

sensitivity of various avian species to these factors. Shortand long-term studies that address these questions are consequential because they may shed light on the resiliency of bird communities to anthropogenic disturbances and, thus, also on the extent to which these communities will be affected by future climate change and urbanization. Research on the above and related topics will likely be most beneficial if it combines work on some already wellstudied domesticated and free-ranging species with new studies, using a primarily comparative perspective. Along with our already vast knowledge on the subject, this research has the potential to serve as a focus point for work

54

Hormones and Reproduction of Vertebrates

CBG CORT D-Asp DHT FSH GH GnIH GnRH GTH IGF LH MEL NADD NADH NO P450aro PRL PRL-R SHBG SST T T3 T4 TSH VIP YSS

Corticosteroid-binding globulin Corticosterone D-aspartate 5a-dihydrotestosterone Follicle-stimulating hormone Growth hormone Gonadotropin-inhibiting hormone Gonadotropin-releasing hormone Gonadotropin Insulin-like growth factor Luteinizing hormone Melatonin Nicotinamide adenine dinucleotide Reduced nicotinamide dinucleotide Nitric oxide Aromatase enzyme Prolactin Prolactin receptor Sex hormone-binding globulin Sperm storage tubule Testosterone Triiodothyronine Thyroxine Thyrotropin Vasoactive intestinal peptide Yellow semen syndrome

REFERENCES FIGURE 2.5 (upper panel) Seasonal change in testicular width of freeranging European blackbirds (Turdus merula) sampled in an urban (open circles) and forest (filled squares) environment in Germany. Adapted from Partecke, Van’t Hof, and Gwinner (2005), with permission. (lower panel) Seasonal change in testicular length of free-ranging curve-billed thrashers (Toxostoma curvirostre) sampled in Phoenix, Arizona (urban, open circles) and in the surrounding Sonoran Desert (rural, filled squares). From H.B. Fokidis, unpublished data. Each panel shows linear regression lines for each sampled population and each point represents one individual.

at multiple levels of organizationdfrom molecular to the whole organism in its environmentdand that integrates concepts drawn, among others, from population biology, ecology, ethology, physiology, genetics, immunology, and neuroscience.

ABBREVIATIONS 17b-HSD 3b-HSD ABP AMH AND cAMP

17b-hydroxysteroid dehydrogenase 3b-hydroxysteroid dehydrogenase Androgen-binding glycoprotein Anti-Mu¨llerian hormone Androstenedione Cyclic adenosine 3’,5’-monophosphate

Adamik, P., & Bures, S. (2007). Experimental evidence for speciesspecific habitat preferences in two flycatcher species in their hybrid zone. Naturwissenschaften., 94, 859e863. Adams, M. L., Nock, B., Truong, R., & Cicero, T. J. (1992). Nitric oxide control of steroidogenesis: endocrine effects of NG-nitro-L-arginine and comparisons to alcohol. Life. Sci., 50, 35e40. Adkins, E. K. (1975). Hormonal basis of sexual differentiation in the Japanese quail. J. Comp. Physiol. Psychol., 89, 61e71. Adkins, E. K. (1978). Sex steroids and differentiation of avian reproductive behavior. Amer. Zool., 18, 501e509. Adkins-Regan, E., & Ascenzi, M. (1987). Social and sexual behavior of male and female zebra finches treated with estradiol during the nestling period. Anim. Behav., 35, 1100e1112. Aire, T. A. (1979). The epididymal region of the Japanese quail (Coturnix coturnix japonica). Acta. Anat. (Basel), 103, 305e312. Aire, T. A. (1982). Surface morphology of the ducts of the epididymal region of the drake (Anas platyrhynchos) as revealed by scanning and transmission electron microscopy. J. Anat., 135, 513e520. Aire, T. A. (1997). The structure of the interstitial tissue of the active and resting avian testis. Onderstepoort. J. Vet. Res., 64, 291e299. Aire, T. A. (2007). Spermatogenesis and testicular cycles. In B. G. M. Jamieson (Ed.), Reproductive Biology and Phylogeny of Birds, Vol. 6 (pp. 279e347). Enfield, NH: Science Publishers. Aire, T. A., & Ozegbe, P. C. (2007). The testicular capsule and peritubular tissue of birds: morphometry, histology, ultrastructure and immunohistochemistry. J. Anat., 210, 731e740. Aire, T. A., Ayeni, J. S., & Olowo-okorun, M. O. (1979). The structure of the excurrent ducts of the testis of the Guinea fowl (Numida meleagris). J. Anat., 129, 633e643.

Chapter | 2

Avian Testicular Structure, Function, and Regulation

Akazome, Y., Abe, T., & Mori, T. (2002). Differentiation of chicken gonad as an endocrine organ: expression of LH receptor, FSH receptor, cytochrome P450c17 and aromatase genes. Reproduction, 123, 721e728. Anderson, T. R. (2006). Biology of the Ubiquitous House Sparrow: From Genes to Populations. Oxford University Press. Artoni, S. M. B., Orsi, A. M., Carvalho, T. L. L., Vicentini, C. A., & Stefanini, M. A. (1999). Seasonal morphology of the domestic quail (Coturnix coturnix japonica). Testis. Anat. Histol. Embryol., 28, 217e220. Ashizawa, K., & Sano, R. (1990). Effects of temperature on the immobilization and the initiation of motility of spermatozoa in the male reproductive tract of the domestic fowl, Gallus domesticus. Comp. Biochem. Physiol. A: Comp. Physiol., 96, 297e301. Ashizawa, K., Wishart, G. J., Ranasinghe, A. R., Katayama, S., & Tsuzuki, Y. (2004). Protein phosphatase type 2B is involved in the regulation of the acrosome reaction but not in the temperaturedependent flagellar movement of fowl spermatozoa. Reproduction, 128, 783e787. Ayre, E. A., & Pang, S. F. (1994). 2-[125I]iodomelatonin binding sites in the testis and ovary: putative melatonin receptors in the gonads. Biol. Signals, 3, 71e84. Ayre, E. A., Yuan, H., & Pang, S. F. (1992). The identification of 125 I-labelled iodomelatonin binding sites in the testes and ovaries of the chicken (Gallus domesticus). J. Endocrinol., 133, 5e11. Ayre, E. A., Wang, Z. P., Brown, G. M., & Pang, S. F. (1994). Localization and characterization of [125I]iodomelatonin binding sites in duck gonads. J. Pineal. Res., 17, 39e47. Bailey, R. E. (1950). Inhibition of light-induced gonad increase in Whitecrowned Sparrows. Condor., 52, 247e251. Baker, M. C., & Boylan, J. T. (1999). Singing behavior, mating associations and reproductive success in a population of hybridizing Lazuli and indigo buntings. Condor., 101, 493e504. Bakst, M. R., Akuffo, V., Trefil, P., & Brillard, J. P. (2007). Morphological and histochemical characterization of the seminiferous epithelial and Leydig cells of the turkey. Anim. Reprod. Sci., 97, 303e313. Balemans, M. G., Van de Veerdonk, F. C. G., & Van de Kamer, J. C. (1977). Effect of injecting 5-methoxy indoles, pineal compounds, on testicular weight of white leghorn cockerels (Gallus domesticus L.). J. Neural. Transm., 41, 47e57. Balthazart, J., Massa, R., & Negri-Cesi, P. (1979). Photoperiodic control of testosterone metabolism, plasma gonadotrophins, cloacal gland growth, and reproductive behavior in the Japanese quail. Gen. Comp. Endocrinol., 39, 222e235. Bandivdekar, A. H., Vijayalakshmi, S., Moodbidri, S. B., & Sheth, A. R. (1982). Low molecular weight inhibin from sheep, human, rat, and chicken testes. J. Androl., 3, 140e143. Bar, M. S. (2006). Role of thyroxine and prolactin in the testicular status of spotted munia (Lonchura punctulata). J. Environ. Biol., 27, 141e145. Barfuss, D. W., & Ellis, L. C. (1971). Seasonal cycles in melatonin synthesis by the pineal gland as related to testicular function in the house sparrow (Passer domesticus). Gen. Comp. Endocrinol., 17, 183e193. Bates, R. W., Lahr, E. L., & Riddle, O. (1935). The gross action of prolactin and follicle-stimulating hormone on mature ovary and sex accessories of fowl. Amer. J. Physiol., 111, 368.

55

Battley, P. F., & Piersma, T. (2005). Body composition and flight ranges of bar-tailed godwits (Limosa lapponica baueri) from New Zealand. Auk., 122, 922e937. Bauchinger, U., Van’t Hof, T., & Biebach, H. (2007). Testicular development during long-distance spring migration. Horm. Behav., 51, 295e305. Bauchinger, U., Van’t Hof, T., & Biebach, H. (2008). Migratory stopover conditions affect the developmental state of male gonads in garden warblers (Sylvia borin). Horm. Behav., 54, 312e318. Bayle, J. D., Kraus, M., & Van Tienhoven, A. (1970). The effects of hypophysectomy and testosterone propionate on the testes of Japanese quail, Coturnix coturnix japonica. J. Endocrinol., 46, 403e404. Beach, J. E. (1962). Diseases of budgerigars and other cage birds. A survey of post-mortem findings. Vet. Rec., 74, 63e68. Beck, V., Unterrieder, E., Krenn, L., Kubelka, W., & Jungbauer, A. (2003). Comparison of hormonal activity (estrogen, androgen and progestin) of standardized plant extracts for large scale use in hormone replacement therapy. J. Steroid. Biochem. Mol. Biol., 84, 259e268. Bell, D. A. (1997). Hybridization and reproductive performance in gulls of the Larus glaucescens occidentalis complex. Condor, 99, 585e594. Bentley, G. E., Audage, N. C., Hanspal, E. K., Ball, G. F., & Hahn, T. P. (2003). Photoperiodic response of the hypothalamoepituitaryegonad axis in male and female canaries, Serinus canaria. J. Exper. Zool. A: Comp. Exper. Biol., 296, 143e151. Bentley, G. E., Tsutsui, K., & Wingfield, J. C. (2007). Endocrinology of Reproduction. In B. G. M. Jamieson (Ed.), Reproductive Biology and Phylogeny of Birds, Vol. 6 (pp. 181e242). Enfield, NH: Science Publishers. Bentley, G. E., Wingfield, J. C., Morton, M. L., & Ball, G. F. (2000). Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song. Horm. Behav., 37, 179e189. Bentley, G. E., Ubuka, T., McGuire, N. L., Calisi, R., Perfito, N., Kriegsfeld, L. J., et al. (2009). Gonadotrophin-inhibitory hormone: a multifunctional neuropeptide. J. Neuroendocrinol., 21, 276e281. Bentley, G. E., Ubuka, T., McGuire, N. L., Chowdhury, V. S., Morita, Y., Yano, T., et al. (2008). Gonadotropin-inhibitory hormone and its receptor in the avian reproductive system. Gen. Comp. Endocrinol., 156, 34e43. Bergmann, M., & Schindelmeiser, J. (1987). Development of the bloodetestis barrier in the domestic fowl (Gallus domesticus). Int. J. Androl., 10, 481e488. Berghman, L. R., D’Hondt, E., Puebla, N., Dees, L., Hiney, J., & Vandesande, F. (2000). Immunocytochemical evidence for the existence of lamprey LHRH-III-like peptide in the chicken hypothalamus. Br. Poult. Sci., 41, 56e57. Berry, W., Zhang, X. F., & MacDaniel, G. (1999). Growth of chick oviduct in response to genistein. Biol. Reprod., 60. 262. Bhatt, R., Patel, S., & Chaturvedi, C. M. (2001). Involvement of adrenal and thyroid activity in the annual testicular regression of red headed bunting (Emberiza bruniceps). J. Environ. Biol., 22, 171e175. Birkhead, T. R., & Biggins, J. D. (1998). Sperm competition mechanisms in birds: models and data. Behav. Ecol., 9, 253e260. Birkhead, T. R., & Fletcher, F. (1998). Sperm transport in the reproductive tract of female zebra finches (Taeniopygia guttata). J. Reprod. Fertil., 114, 141e145.

56

Birkhead, T. R., Buchanan, K. L., DeVoogd, T. J., Pellatt, E. J., Szekely, T., & Catchpole, C. K. (1997). Song, sperm quality and testes asymmetry in the sedge warbler. Anim. Behav., 53, 965e971. Birkhead, T. R., Pellatt, E. J., & Fletcher, F. (1993). Selection and utilization of spermatozoa in the reproductive tract of the female zebra Finch Taeniopygia guttata. J. Reprod. Fertil., 99, 593e600. Birkhead, T. R., Veiga, J. P., & Moller, A. P. (1994). Male sperm reserves and copulation behavior in the house sparrow, Passer domesticus. Proc. R. Soc. Lond. B: Biol. Sci., 256, 247e251. Birkhead, T. R., Pellatt, E. J., Brekke, P., Yeates, R., & Castillo-Juarez, H. (2005). Genetic effects on sperm design in the Zebra Finch. Nature., 434, 383e387. Bluhm, C. K., Phillips, R. E., & Burke, W. H. (1989). Vernal increases in prolactin levels of nonbreeding male and female canvasbacks (Aythya valisineria). Gen. Comp. Endocrinol., 76, 286e291. Bluhm, C. K., Schwabl, H., Schwabl, I., Perera, A., Follett, B. K., Goldsmith, A. R., et al. (1991). Variation in hypothalamic gonadotrophin-releasing hormone content, plasma and pituitary LH, and invitro testosterone release in a long-distance migratory bird, the garden warbler (Sylvia borin), under constant photoperiods. J. Endocrinol., 128, 339e345. Boltz, C. R., Boltz, D. A., Bunick, D., Scherba, G., & Bahr, J. M. (2007). Vaccination against the avian infectious bronchitis virus affects sperm concentration, sperm quality and blood testosterone concentrations in cockerels. Br. Poult. Sci., 48, 617e624. Boltz, D. A., Zimmerman, C. R., Nakai, M., Bunick, D., Scherba, G., & Bahr, J. M. (2006). Epididymal stone formation and decreased sperm production in roosters vaccinated with a killed strain of avian infectious bronchitis virus. Avian. Dis., 50, 594e598. Boonekamp, J. J., Ros, A. H. F., & Verhulst, S. (2008). Immune activation suppresses plasma testosterone level: a meta-analysis. Biol. Lett., 4, 741e744. Bortolussi, M., Deviche, P., Colombo, L., & Marini, G. (1979). In-vitro binding of radioiodinated rat follicle-stimulating hormone to the testis of the mallard duck, Anas platyrhynchos L. Basic. Appl. Histochem., 23, 279e284. Boseret, G., Carere, C., Ball, G. F., & Balthazart, J. (2006). Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria). J. Neurobiol., 66, 1044e1060. Both, C., Bijlsma, R. G., & Visser, M. E. (2005). Climatic effects on timing of spring migration and breeding in a long-distance migrant, the pied flycatcher, Ficedula hypoleuca. J. Avian. Biol., 36, 368e373. Boulakoud, M. S., & Goldsmith, A. R. (1991). Thyroxine treatment induces changes in hypothalamic gonadotrophin-releasing hormone characteristic of photorefractoriness in starlings (Sturnus vulgaris). Gen. Comp. Endocrinol., 82, 78e85. Bozkurt, H. H., Aktas, A., Ulkay, M. B., & Firat, U. B. (2007). Sertoli cell proliferation during the post hatching period in domestic fowl. J. Vet. Sci., 8, 219e222. Breneman, W. R., & Zeller, F. J. (1982). Testosterone inhibition of FSH action on testicular 32P uptake in white leghorn cockerels. Gen. Comp. Endocrinol., 46, 225e235. Breuner, C. W., & Orchinik, M. (2002). Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol., 175, 99e112. Briskie, J. V., & Montgomerie, R. (1992). Sperm size and sperm competition in birds. Proc. R. Soc. Lond. Ser. B: Biol. Sci., 247, 89e95.

Hormones and Reproduction of Vertebrates

Briskie, J. V., & Montgomerie, R. (1993). Patterns of sperm storage in relation to sperm competition in passerine birds. Condor, 95, 442e454. Briskie, J. V., & Montgomerie, R. (2007). Testis size, sperm size and sperm competition. In B. G. M. Jamieson (Ed.), Reproductive Biology and Phylogeny of Birds, Vol. 6 (pp. 513e551). Enfield, NH: Science Publishers. Briskie, J. V., Montgomerie, R., & Birkhead, T. R. (1997). The evolution of sperm size in birds. Evolution, 51, 937e945. Brown, N. L., & Follett, B. K. (1977). Effects of androgens on the testes of intact and hypophysectomized Japanese quail. Gen. Comp. Endocrinol., 33, 267e277. Brown, N. L., Bayle, J. D., Scanes, C. G., & Follett, B. K. (1975). Chicken gonadotrophins: their effects on the testes of immature and hypophysectomized Japanese quail. Cell. Tissue. Res., 156, 499e520. Buggiotti, L., Hellstrom, M. A., & Primmer, C. R. (2006). Characterization of the first growth hormone gene sequence for a passerine birddthe pied flycatcher (Ficedula hypoleuca). DNA Seq., 17, 401e406. Buntin, J. D., Lea, R. W., & Figge, G. R. (1988). Reductions in plasma LH concentration and testicular weight in ring doves following intracranial injection of prolactin or growth hormone. J. Endocrinol., 118, 33e40. Buntin, J. D., El Halawani, M. E., Ottinger, M. A., Fan, Y., & Fivizzani, A. J. (1998). An analysis of sex and breeding stage differences in prolactin binding activity in brain and hypothalamic GnRH concentration in Wilson’s phalarope, a sex role-reversed species. Gen. Comp. Endocrinol., 109, 119e132. Buntin, J. D., Hnasko, R. M., & Zuzick, P. H. (1999). Role of the ventromedial hypothalamus in prolactin-induced hyperphagia in ring doves. Physiol. Behav., 66, 255e261. Buntin, J. D., Ruzycki, E., & Witebsky, J. (1993). Prolactin receptors in dove brain: autoradiographic analysis of binding characteristics in discrete brain regions and accessibility to blood-borne prolactin. Neuroendocrinology, 57, 738e750. Calhim, S., & Birkhead, T. R. (2007). Testis size in birds: quality versus quantitydassumptions, errors, and estimates. Behav. Ecol., 18, 271e275. Calisi, R. M., Rizzo, N. O., & Bentley, G. E. (2008). Seasonal differences in hypothalamic EGR-1 and GnIH expression following capturehandling stress in house sparrows (Passer domesticus). Gen. Comp. Endocrinol., 157, 283e287. Cardinali, D. P., & Rosner, J. M. (1971). Effects of melatonin, serotonin and N-acetylserotonin on the production of steroids by duck testicular homogenates. Steroids, 18, 25e37. Cecil, H. C., & Bakst, M. R. (1986). Serum testosterone concentration during two breeding cycles of turkeys with low and high ejaculate volumes. Domest. Anim. Endocrinol., 3, 27e32. Cecil, H. C., Bakst, M. R., & Monsi, A. (1988). Daily output of spermatozoa and extragonadal spermatozoal reserves in turkeys. Poult. Sci., 67, 327e332. Chakraborty, S. (1993). A comparative study of annual changes in the pineal gland morphology with reference to the influence of melatonin on testicular activity in tropical birds, Psittacula cyanocephala and Ploceus philippinus. Gen. Comp. Endocrinol., 92, 71e79. Chandrashekar, V., Zaczek, D., & Bartke, A. (2004). The consequences of altered somatotropic system on reproduction. Biol. Reprod., 71, 17e27.

Chapter | 2

Avian Testicular Structure, Function, and Regulation

Chapin, J. P. (1939). The birds of the Belgian Congo. Part II. Bull. Amer. Museum Nat. History, 75, 1e632. Chase, D. J. (1982). Gonadotropin specificity of acute testicular androgen secretion in birds. Gen. Comp. Endocrinol., 46, 486e499. Chaturvedi, C. M., & Kumar, P. (2007). Nitric oxide modulates gonadal and adrenal function in Japanese quail, Coturnix coturnix japonica. Gen. Comp. Endocrinol., 151, 285e299. Cheng, F. P., Guo, T. J., Wu, J. T., Lin, T. E., Ursem, P. J., Colenbrander, B., et al. (2002). Annual variation in semen characteristics of pigeons (Columba livia). Poult. Sci., 81, 1050e1056. Cheng, K. M., Pang, C. S., Wang, Z. P., Yuan, H., Nichols, C. R., Brown, G. M., et al. (1994). A comparison of [125I]iodomelatonin binding sites in testes and brains of heavy meat-type Japanese quail with a randombred strain. J. Hered., 85, 136e139. Clulow, J., & Jones, R. C. (1982). Production, transport, maturation, storage and survival of spermatozoa in the male Japanese quail, Coturnix coturnix. J. Reprod. Fertil., 64, 259e266. Clulow, J., & Jones, R. C. (1988). Studies of fluid and spermatozoal transport in the extratesticular genital ducts of the Japanese quail. J. Anat., 157, 1e11. Coker, C. R., McKinney, F., Hays, H., Briggs, S. V., & Cheng, K. M. (2002). Intromittent organ morphology and testis size in relation to mating system in waterfowl. Auk, 119, 403e413. Connell, C. J. (1972). The effect of luteinizing hormone on the ultrastructure of the Leydig cell of the chick. Z. Zellforsch. Mikrosk. Anat., 128, 139e151. Corvol, P., & Bardin, C. W. (1973). Species distribution of testosteronebinding globulin. Biol. Reprod., 8, 277e282. Corbitt, C., Satre, D., Adamson, L. A., Cobbs, G. A., & Bentley, G. E. (2007). Dietary phytoestrogens and photoperiodic response in a male songbird, the dark-eyed junco (Junco hyemalis). Gen. Comp. Endocrinol., 154, 16e21. Crick, H. Q. P., Dudley, C., Glue, D. E., & Thomson, D. L. (1997). UK birds are laying eggs earlier. Nature, 388. 526. Dang, H. R., & Guraya, S. S. (1978). Seasonal fluctuations in the testicular asymmetry of birds. Acta. Morphol. Acad. Sci. Hung., 26, 1e2. D’Aniello, A., Di Fiore, M. M., D’Aniello, G., Colin, F. E., Lewis, G., & Setchell, B. P. (1998). Secretion of D-aspartic acid by the rat testis and its role in endocrinology of the testis and spermatogenesis. FEBS. Lett., 436, 23e27. Davis, A. J., & Johnson, P. A. (1998). Expression pattern of messenger ribonucleic acid for follistatin and the inhibin. Biol. Reprod., 59, 271e277. Dawson, A. (1983). Plasma gonadal steroid levels in wild starlings (Sturnus vulgaris) during the annual cycle and in relation to the stages of breeding. Gen. Comp. Endocrinol., 49, 286e294. Dawson, A. (1986). The effect of restricting the daily period of food availability on testicular growth of Starlings, Sturnus vulgaris. Ibis, 128, 572e575. Dawson, A. (2002). Photoperiodic control of the annual cycle in birds and comparison with mammals. Ardea, 90, 355e367. Dawson, A. (2003). A comparison of the annual cycles in testicular size and moult in captive European starlings (Sturnus vulgaris) during their first and second years. J. Avian. Biol., 34, 119e123. Dawson, A. (2005). The effect of temperature on photoperiodically regulated gonadal maturation, regression and moult in Starlingsdpotential consequences of climate change. Funct. Ecol., 19, 995e1000.

57

Dawson, A. (2006). Control of molt in birds: association with prolactin and gonadal regression in starlings. Gen. Comp. Endocrinol., 147, 314e322. Dawson, A. (2008). Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Phil. Trans. Royal. Soc. B: Biol. Sci., 363, 1621e1633. Dawson, A., & Goldsmith, A. R. (1982). Prolactin and gonadotropin secretion in wild starlings (Sturnus vulgaris) during the annual cycle and in relation to nesting, incubation, and rearing young. Gen. Comp. Endocrinol., 48, 213e221. Dawson, A., & Goldsmith, A. R. (1983). Plasma prolactin and gonadotrophins during gonadal development and the onset of photorefractoriness in male and female starlings (Sturnus vulgaris) on artificial photoperiods. J. Endocrinol., 97, 253e260. Dawson, A., & Goldsmith, A. R. (1984). Effects of gonadectomy on seasonal changes in plasma LH and prolactin concentrations in male and female starlings (Sturnus vulgaris). J. Endocrinol., 100, 213e218. Dawson, A., & Goldsmith, A. R. (1997). Changes in gonadotrophinreleasing hormone (GnRH-I) in the pre-optic area and median eminence of starlings (Sturnus vulgaris) during the recovery of photosensitivity and during photostimulation. J. Reprod. Fertil., 111, 1e6. Dawson, A., & Sharp, P. J. (1998). The role of prolactin in the development of reproductive photorefractoriness and postnuptial molt in the European starling (Sturnus vulgaris). Endocrinology, 139, 485e490. Dawson, A., & Sharp, P. J. (2007). Photorefractoriness in birdsdphotoperiodic and non-photoperiodic control. Gen. Comp. Endocrinol., 153, 378e384. Dawson, A., Goldsmith, A. R., & Nicholls, T. J. (1985). Thyroidectomy results in termination of photorefractoriness in starlings (Sturnus vulgaris) kept in long daylengths. J. Reprod. Fertil., 74, 527e533. Dawson, A., King, V. M., Bentley, G. E., & Ball, G. F. (2001). Photoperiodic control of seasonality in birds. J. Biol. Rhythms, 16, 365e380. Dawson, A., Talbot, R. T., Dunn, I. C., & Sharp, P. J. (2002). Changes in basal hypothalamic chicken gonadotropin-releasing hormone-I and vasoactive intestinal polypeptide associated with a photoinduced cycle in gonadal maturation and prolactin secretion in intact and thyroidectomized starlings (Sturnus vulgaris). J. Neuroendocrinol., 14, 533e539. Day, L. B., McBroom, J. T., & Schlinger, B. A. (2006). Testosterone increases display behaviors but does not stimulate growth of adult plumage in male golden-collared manakins (Manacus vitellinus). Horm. Behav., 49, 223e232. De Groef, B., Grommen, S. V. H., Mertens, I., Schoofs, L., Kuhn, E. R., & Darras, V. M. (2004). Cloning and tissue distribution of the chicken type 2 corticotropin-releasing hormone receptor. Gen. Comp. Endocrinol., 138, 89e95. De Reviers, M. (1975). Sperm transport and survival in male birds. In E. S. E. Hafez, & C. G. Thibault (Eds.), The Biology of Spermatozoa (pp. 10e16). Basel, Switzerland: INSERM International Symposium, Nouzilly. S. Karger. De Reviers, M., Hochereau-De Reviers, M. T., Blanc, M. R., Brillard, J. P., Courot, M., & Pelletier, J. (1980). Control of Sertoli and germ cell populations in the cock and sheep testes. Reprod. Nutr. Dev., 20, 241e249.

58

De Ridder, E., Pinxten, R., & Eens, M. (2000). Experimental evidence of a testosterone-induced shift from paternal to mating behaviour in a facultatively polygynous songbird. Behav. Ecol. Sociobiol., 49, 24e30. Degen, A. A., Weil, S., Rosenstrauch, A., Kam, M., & Dawson, A. (1994). Seasonal plasma levels of luteinizing and steroid hormones in male and female domestic ostriches (Struthio camelus). Gen. Comp. Endocrinol., 93, 21e27. Delrio, G., Lupo Di, P. C., & Chieffi, G. (1967). Steroid hormones in the testicular tissue of Gallus domesticus. Experientia, 23, 594. Delville, Y., Sulon, J., Hendrick, J. C., & Balthazart, J. (1984). Effect of the presence of females on the pituitary testicular activity in male Japanese quail (Coturnix coturnix japonica). Gen. Comp. Endocrinol., 55, 295e305. Denk, A. G., & Kempenaers, B. (2006). Testosterone and testis size in mallards (Anas platyrhynchos). J. Ornithol., 147, 436e440. Denk, A. G., Holzmann, A., Peters, A., Vermeirssen, E. L. M., & Kempenaers, B. (2005). Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behav. Ecol., 16, 825e833. Deviche, P., & Parris, J. (2006). Testosterone treatment to free-ranging male dark-eyed juncos (Junco hyemalis) exacerbates hemoparasitic infection. Auk, 123, 548e562. Deviche, P., & Sharp, P. J. (2001). Reproductive endocrinology of a freeliving, opportunistically breeding passerine (white-winged crossbill, Loxia leucoptera). Gen. Comp. Endocrinol., 123, 268e279. Deviche, P., & Small, T. (2006). Non-photic environmental control of post-breeding reproductive regression and molt in a Sonoran Desert passerine, the rufous-winged sparrow. J. Ornithol., 147, 55. Deviche, P., Breuner, C., & Orchinik, M. (2001). Testosterone, corticosterone, and photoperiod interact to regulate plasma levels of binding globulin and free steroid hormone in dark-eyed juncos, Junco hyemalis. Gen. Comp. Endocrinol., 122, 67e77. Deviche, P., Saldanha, C. J., & Silver, R. (2000a). Changes in brain gonadotropin-releasing hormone and vasoactive intestinal polypeptide-like immunoreactivity accompanying reestablishment of photosensitivity in male dark-eyed juncos (Junco hyemalis). Gen. Comp. Endocrinol., 117, 8e19. Deviche, P., Massa, R., Bottoni, L., & Hendrick, J. C. (1982). Effect of corticosterone on the hypothalamicepituitaryegonadal system of male Japanese quail exposed to either short or long photoperiods. J. Endocrinol., 95, 165e173. Deviche, P., Sabo, J., & Sharp, P. J. (2008). Glutamatergic stimulation of luteinising hormone secretion in relatively refractory male songbirds. J. Neuroendocrinol., 20, 1191e1202. Deviche, P., Small, T., Sharp, P., & Tsutsui, K. (2006). Control of luteinizing hormone and testosterone secretion in a flexibly breeding male passerine, the rufous-winged sparrow, Aimophila carpalis. Gen. Comp. Endocrinol., 149, 226e235. Deviche, P., Wingfield, J. C., & Sharp, P. J. (2000b). Year-class differences in the reproductive system, plasma prolactin and corticosterone concentrations, and onset of prebasic molt in male dark-eyed juncos (Junco hyemalis) during the breeding period. Gen. Comp. Endocrinol., 118, 425e435. Deviche, P. J., Hurley, L. L., Fokidis, H. B., Lerbour, B., Silverin, B., Silverin, B., et al. (2010). Acute stress rapidly decreases plasma testosterone but not luteinizing hormone in a free-ranging male songbird: potential site of action and mechanism. Submitted for publication.

Hormones and Reproduction of Vertebrates

Di Fiore, M. M., Lamanna, C., Assisi, L., & Botte, V. (2008). Opposing effects of D-aspartic acid and nitric oxide on tuning of testosterone production in mallard testis during the reproductive cycle. Reprod. Biol. Endocrinol., 6, 28. Dixon, R. A. (2004). Phytoestrogens. Annual. Rev. Plant. Biol., 55, 225e261. Donham, R. S., Goodear, G., & Stetson, M. H. (1996). Dissociation of spontaneous testicular recrudescence and photorefractoriness in the Syrian hamster. J. Reprod. Fertil., 108, 205e209. Dornas, R. A., Oliveira, A. G., Dias, M. O., Mahecha, G. A., & Oliveira, C. A. (2008). Comparative expression of androgen receptor in the testis and epididymal region of roosters (Gallus domesticus) and drakes (Anas platyrhynchos). Gen. Comp. Endocrinol., 155, 773e779. Drent, R., Both, C., Green, M., Madsen, J., & Piersma, T. (2003). Pay-offs and penalties of competing migratory schedules. Oikos., 103, 274e292. Driot, F. J., De Reviers, M., & Williams, J. (1979). Plasma testosterone levels in intact and hemicastrated growing cockerels. J. Endocrinol., 81, 169e174. Dufty, A. M., & Wingfield, J. C. (1986a). Temporal patterns of circulating LH and steroid hormones in a brood parasite, the brown-headed cowbird, Molothrus ater. 1. Males. J. Zool., 208, 191e203. Dufty, A. M., & Wingfield, J. C. (1986b). The influence of social cues on the reproductive endocrinology of male brown-headed cowbirdsd field and laboratory studies. Horm. Behav., 20, 222e234. Elbrecht, A., & Smith, R. G. (1992). Aromatase enzyme activity and sex determination in chickens. Science, 255, 467e470. Esponda, P. (1991). Spermatozoon maturation in vertebrates with internal fertilization. Microsc. Electron. Biol. Celular., 15, 1e23. Eusebe, D. C., diClemente, N., Rey, R., Pieau, C., Vigier, B., Josso, N., et al. (1996). Cloning and expression of the chick anti-Mu¨llerian hormone gene. J. Biol. Chem., 271, 4798e4804. Farner, D. S., Morton, M. L., & Follett, B. K. (1968). The limitation of rate of photoperiodically induced testicular growth in the whitecrowned sparrow Zonotrichia leucophyrys gambelii: the effect of hemicastration. Arch. Anat. Histol. Embryol., 51, 189e196. Fechner, J. H., Jr., & Buntin, J. D. (1989). Localization of prolactin binding sites in ring dove brain by quantitative autoradiography. Brain. Res., 487, 245e254. Fevold, H. R., & Eik-Nes, K. B. (1962). Progesterone metabolism by testicular tissue of the English sparrow (Passer domesticus) during the annual reproductive cycle. Gen. Comp. Endocrinol., 2, 506e515. Fevold, H. R., & Pfeiffer, E. W. (1968). Androgen production in vitro by phalarope gonadal tissue homogenates. Gen. Comp. Endocrinol., 10, 26e33. Fishback, J. B., Arimura, A., & Turkelson, C. M. (1982). Effects of an LHRH agonist and gonadotropins on testicular prolactin receptors. Peptides, 3, 845e850. Fokidis, H. B., Greiner, E. C., & Deviche, P. (2008). Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. J. Avian. Biol., 39, 300e310. Fokidis, H. B., Orchinik, M. O., & Deviche, P. (2009). Corticosterone and corticosteroid binding globulin in birds: relation to urbanization in a desert city. Gen. Comp. Endocrinol., 160, 259e270. Follett, B. K. (1976). Plasma follicle-stimulating hormone during photoperiodically induced sexual maturation in male Japanese quail. J. Endocrinol., 69, 117e126.

Chapter | 2

Avian Testicular Structure, Function, and Regulation

Follett, B. K., & Maung, S. L. (1978). Rate of testicular maturation, in relation to gonadotrophin and testosterone levels, in quail exposed to various artificial photoperiods and to natural daylengths. J. Endocrinol., 78, 267e280. Follett, B. K., & Pearce-Kelly, A. (1990). Photoperiodic control of the termination of reproduction in Japanese quail (Coturnix coturnix japonica). Proc. R. Soc. Lond. B: Biol. Sci., 242, 225e230. Folstad, I., & Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. Amer. Nat., 139, 603e622. Folstad, I., & Skarstein, F. (1997). Is male germ line control creating avenues for female choice? Behav. Ecol., 8, 109e112. Foster, R. G., Plowman, G., Goldsmith, A. R., & Follett, B. K. (1987). Immunohistochemical demonstration of marked changes in the LHRH system of photosensitive and photorefractory European starlings (Sturnus vulgaris). J. Endocrinol., 115, 211e220. Fowler, G. S., Wingfield, J. C., Boersma, P. D., & Sosa, R. A. (1994). Reproductive endocrinology and weight change in relation to reproductive success in the magellanic penguin (Spheniscus magellanicus). Gen. Comp. Endocrinol., 94, 305e315. Froman, D. P., & Feltmann, A. J. (2005). Fowl (Gallus domesticus) sperm motility depends upon mitochondrial calcium cycling driven by extracellular sodium. Biol. Reprod., 72, 97e101. Froman, D. P., & Kirby, J. D. (2005). Sperm mobility: phenotype in roosters (Gallus domesticus) determined by mitochondrial function. Biol. Reprod., 72, 562e567. Froman, D. P., & Thurston, R. J. (1983). The influence of testosterone propionate on semen quality and testis morphology in the domestic turkey, Meleagris gallopavo. Poult. Sci., 62, 169e174. Fu, Z. W., Kubo, T., Sugahara, K., Noguchi, T., & Kato, H. (2001). Cloning of complementary deoxyribonucleic acids encoding quail (Coturnix coturnix japonica) retinoic acid receptor beta isoforms and changes in their gene expression during gonadotropic growth. Biol. Reprod., 64, 231e241. Fusani, L. (2008). Testosterone control of male courtship in birds. Horm. Behav., 54, 227e233. Galli, F. E., Irusta, O., & Wassermann, G. F. (1973). Androgen production by testes of Gallus domesticus during postembryonic development. Gen. Comp. Endocrinol., 21, 262e266. Garamszegi, L. Z., Eens, M., Hurtrez-Bousses, S., & Moller, A. P. (2005). Testosterone, testis size, and mating success in birds: a comparative study. Horm. Behav., 47, 389e409. Gershagen, S., Lundwall, A., & Fernlund, P. (1989). Characterization of the human sex hormone binding globulin (SHBG) gene and demonstration of two transcripts in both liver and testis. Nucleic. Acids. Res., 17, 9245e9258. Ghosal, S. K., LaMarche, P. H., Bhanja, P., Joardar, S., Sengupta, A., & Midya, T. (1983). Duration of meiosis and spermiogenesis in the dog. Can. J. Genet. Cytol., 25, 678e681. Gienapp, P., Teplitsky, C., Alho, J. S., Mills, J. A., & Merila¨, J. (2008). Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol., 17, 167e178. Goldsmith, A. R., & Hall, M. (1980). Prolactin concentrations in the pituitary gland and plasma of Japanese quail in relation to photoperiodically induced sexual maturation and egg laying. Gen. Comp. Endocrinol., 42, 449e454. Goldsmith, A. R., & Nicholls, T. J. (1984a). Thyroidectomy prevents the development of photorefractoriness and the associated rise in plasma prolactin in starlings. Gen. Comp. Endocrinol., 54, 256e263.

59

Goldsmith, A. R., & Nicholls, T. J. (1984b). Thyroxine induces photorefractoriness and stimulates prolactin secretion in European starlings (Sturnus vulgaris). J. Endocrinol., 101, R1eR3. Gomendio, M., & Roldan, E. R. S. (1991). Sperm competition influences sperm size in mammals. Proc. R. Soc. Lond. B: Biol. Sci., 243, 181e185. Gonza´lez-Mora´n, M. G., Guerra-Araiza, C., Campos, M. G., & CamachoArroyo, I. (2008). Histological and sex steroid hormone receptor changes in testes of immature, mature, and aged chickens. Domest. Anim. Endocrinol., 35, 371e379. Gonzalez-Solis, J., & Becker, P. H. (2002). Mounting frequency and number of cloacal contacts increase with age in common terns Sterna hirundo. J. Avian. Biol., 33, 306e310. Gorham, S. L., & Ottinger, M. A. (1986). Sertoli cell tumors in Japanese quail. Avian Dis., 30, 337e339. Gorman, M. R., & Zucker, I. (1995). Seasonal adaptations of Siberian hamsters. 2. Pattern of change in day length controls annual testicular and body weight rhythms. Biol. Reprod., 53, 116e125. Goymann, W., Moore, I. T., Scheuerlein, A., Hirschenhauser, K., Grafen, A., & Wingfield, J. C. (2004). Testosterone in tropical birds: effects of environmental and social factors. Amer. Nat., 164, 327e334. Grant, P. R., & Grant, B. R. (1992). Hybridization of bird species. Science, 256, 193e197. Graves, G. R. (2004). Testicular volume and asymmetry are age-dependent in black-throated blue warblers (Dendroica caerulescens). Auk, 121, 473e485. Groscolas, R., Jallageas, M., Goldsmith, A., & Assenmacher, I. (1986). The endocrine control of reproduction and molt in male and female emperor (Aptenodytes forsteri) and adelie (Pygoscelis adeliae) penguins. I. Annual changes in plasma levels of gonadal steroids and LH. Gen. Comp. Endocrinol., 62, 43e53. Guchhait, P., & Haldar, C. (1999). Regulation of pineal gland and gonadal functions of a tropical nocturnal bird, Indian spotted owlet, Athene brama, following different 5-methoxyindoles treatments. Biogenic. Amines, 15, 263e273. Gunn, M. R., Champion, Z., Casey, M. E., Teal, P., & Casey, P. J. (2008). Testicular and spermatozoan parameters in the pukeko (Porphyrio porphyrio melanotus). Anim. Reprod. Sci., 109, 330e342. Gupta, b. B., Haldar-Misra, C., Ghosh, M., & Thapliyal, J. P. (1987). Effect of melatonin on gonads, body weight, and luteinizing hormone (LH) dependent coloration of the Indian finch, Lal munia (Estrilda amandava). Gen. Comp. Endocrinol., 65, 451e456. Gupta, S. K., Bhat, G., & Maiti, B. R. (1984). Gonadal hormonedependent changes in the concentrations of sialic acid and fructose in the seminal glomus and of glycogen in the oviduct of the Indian pied myna. Gen. Comp. Endocrinol., 54, 389e391. Gwinner, E. (1987). Annual rhythms of gonadal size, migratory disposition and molt in garden warblers, Sylvia borin, exposed in winter to an equatorial or a southern hemisphere photoperiod. Ornis. Scandinav., 18, 251e256. Gwinner, E. (1989). Photoperiod as a modifying and limiting factor in the expression of avian circannual rhythms. J. Biol. Rhythms, 4, 237e250. Gwinner, H., Van’t Hof, T., & Zeman, M. (2002). Hormonal and behavioral responses of starlings during a confrontation with males or females at nest boxes during the reproductive season. Horm. Behav., 42, 21e31.

60

Haase, E. (1983). The annual reproductive cycle in mallards. J. Steroid Biochem., 19, 731e737. Haase, E., Sharp, P. J., & Paulke, E. (1985). Seasonal changes in the concentrations of plasma gonadotropins and prolactin in wild mallard drakes. J. Exp. Zool., 234, 301e305. Hadley, M. E. (2000). Endocrinology. Englewood Cliffs, NJ: Prentice Hall. Hahn, T. P. (1995). Integration of photoperiodic and food cues to time changes in reproductive physiology by an opportunistic breeder, the red crossbill, Loxia curvirostra (Aves, Carduelinae). J. Exp. Zool., 272, 213e226. Hahn, T. P. (1998). Reproductive seasonality in an opportunistic breeder, the red crossbill, Loxia curvirostra. Ecology, 79, 2365e2375. Hahn, T. P., Cornelius, J. M., Sewall, K. B., Kelsey, T. R., Hau, M., & Perfito, N. (2008). Environmental regulation of annual schedules in opportunistically breeding songbirds: adaptive specializations or variations on a theme of white-crowned sparrow? Gen. Comp. Endocrinol., 157, 217e226. Hahn, T. P., Pereyra, M. E., Sharbaugh, S. M., & Bentley, G. E. (2004). Physiological responses to photoperiod in three cardueline finch species. Gen. Comp. Endocrinol., 137, 99e108. Hahn, T. P., Pereyra, M. E., Katti, M., & Ward, G. M. (2005). Effects of food availability on the reproductive system. In A. Dawson, & P. J. Sharp (Eds.), Avian Endocrinology (pp. 167e180). Alpha Science International, Ltd. Hahn, T. P., Wingfield, J. C., Mullen, R., & Deviche, P. J. (1995). Endocrine bases of spatial and temporal opportunism in arcticbreeding birds. Amer. Zool., 35, 259e273. Halse, S. A. (1985). Gonadal cycles and levels of luteinizing hormone in wild spur-winged geese, Plectropterus gambensis. J. Zool., 205, 335e355. Hammond, G. L., & Bocchinfuso, W. P. (1996). Sex hormone-binding globulin: gene organization and structure function analyses. Horm. Res., 45, 197e201. Hamner, W. M. (1968). Photorefractory period house finch. Ecology, 49, 211e227. Harvey, S., Baudet, M. L., Murphy, A., Luna, M., Hull, K. L., & Aramburo, C. (2004). Testicular growth hormone (GH): GH expression in spermatogonia and primary spermatocytes. Gen. Comp. Endocrinol., 139, 158e167. Hau, M. (2001). Timing of breeding in variable environments: tropical birds as model systems. Horm. Behav., 40, 281e290. Hau, M., Gill, S. A., & Goymann, W. (2008). Tropical field endocrinology: ecology and evolution of testosterone concentrations in male birds. Gen. Comp. Endocrinol., 157, 241e248. Hau, M., Wikelski, M., & Wingfield, J. C. (1998). A neotropical forest bird can measure the slight changes in tropical photoperiod. Proc. R. Soc. Lond. B: Biol. Sci., 265, 89e95. Hau, M., Wikelski, M., & Wingfield, J. C. (2000). Visual and nutritional food cues fine-tune timing of reproduction in a neotropical rainforest bird. J. Exp. Zool., 286, 494e504. Hayes, F. E. (2001). Geographic variation, hybridization, and the leapfrog pattern of evolution in the suiriri flycatcher (Suiriri suiriri) complex. Auk, 118, 457e471. Hegner, R. E., & Wingfield, J. C. (1986). Gonadal development during autumn and winter in house sparrows. Condor, 88, 269e278. Heiblum, R., Arnon, E., Gvaryahu, G., Robinzon, B., & Snapir, N. (2000). Short-term stress increases testosterone secretion from testes in male domestic fowl. Gen. Comp. Endocrinol., 120, 55e66.

Hormones and Reproduction of Vertebrates

Helm, B., & Gwinner, E. (2005). Carry-over effects of day length during spring migration. J. Ornithol., 146, 348e354. Helm, B., Piersma, T., & Van der Jeugd, H. (2006). Sociable schedules: interplay between avian seasonal and social behaviour. Anim. Behav., 72, 245e262. Hess, R. A., & Thurston, R. J. (1982). Incidence and biochemistry of yellow turkey semen. Poult. Sci., 61. 1381-1381. Hess, R. A., Birrenkott, G. P., & Thurston, R. J. (1984). Seminal plasma androgen-binding protein activity in turkeys with normal white or abnormal yellow semen. J. Reprod. Fertil., 71, 403e409. Hill, G. E. (1994). Testis mass and subadult plumage in black-headed grossbeaks. Condor, 96, 626e630. Hillgarth, N., Ramenofsky, M., & Wingfield, J. (1997). Testosterone and sexual selection. Behav. Ecol., 8, 108e109. Hocking, P. M. (1992). Bilateral testicular asymmetry and supernumerary testes in the domestic fowl (Gallus domesticus). Br. Poult. Sci., 33, 455e460. Hughes, C. L. (1988). Phytochemical mimicry of reproductive hormones and modulation of herbivore fertility by phytoestrogens. Environ. Health Perspect., 78, 171e175. Hull, K. L., & Harvey, S. (2000a). Growth hormonedroles in male reproduction. Endocrine, 13, 243e250. Hull, K. L., & Harvey, S. (2000b). Growth hormone: a reproductive endocrineeparacrine regulator? Rev. Reprod., 5, 175e182. Humphreys, P. N. (1975). Ultrastructure of the budgerigar testis during a photoperiodically induced cycle. Cell. Tissue. Res., 159, 541e550. Humphries, S., Evans, J. P., & Simmons, L. W. (2008). Sperm competition: linking form to function. BMC. Evol. Biol., 8, 319. Hurley, L. L., Wallace, A. M., Sartor, J. J., & Ball, G. F. (2008). Photoperiodic induced changes in reproductive state of border canaries (Serinus canaria) are associated with marked variation in hypothalamic gonadotropin-releasing hormone immunoreactivity and the volume of song control regions. Gen. Comp. Endocrinol., 158, 10e19. Huston, T. M. (1975). The effects of environmental temperature on fertility of the domestic fowl. Poultry Sci., 54, 1180e1183. Immelmann, K. (1963). Drought adaptations in Australian desert birds. In C. G. Sibley (Ed.). Washington, DC: AOU. Ishibashi, H., Tachibana, K., Tsuchimoto, M., Soyano, K., Tatarazako, N., Matsumura, N., et al. (2004). Effects of nonylphenol and phytoestrogen-enriched diet on plasma vitellogenin, steroid hormone, hepatic cytochrome P450 1A, and glutathione-s-transferase values in goldfish (Carassius auratus). Comp. Med., 54, 54e62. Ishii, S., & Adachi, T. (1977). Binding of avian testicular homogenate with rat follicle stimulating hormone and inhibition of the binding by hypophyseal extracts of lower vertebrates. Gen. Comp. Endocrinol., 31, 287e294. Ishii, S., & Yamamoto, K. (1976). Demonstration of follicle stimulating hormone (FSH) activity in hypophyseal extracts of various vertebrates by the response of the Sertoli cells of the chick. Gen. Comp. Endocrinol., 29, 506e510. Jamieson, B. G. M. (2007). Avian spermatozoa: structure and phylogeny. In B. G. M. Jamieson (Ed.), Reproductive Biology and Phylogeny of Birds (pp. 349e511). Enfield, NH: Science Publishers. Janssen, S. J., Kirby, J. D., Hess, R. A., Rhoads, M., Bunick, D., Bailey, K. L., et al. (2000). Identification of epididymal stones in diverse rooster populations. Poult. Sci., 79, 568e574.

Chapter | 2

Avian Testicular Structure, Function, and Regulation

Jarvinen, A. (1989). Geographical variation in temperature variability and predictability and their implications for the breeding strategy of the pied flycatcher, Ficedula hypoleuca. Oikos, 54, 331e336. Jawor, J. M., & MacDougall-Shackleton, S. A. (2008). Seasonal and sexrelated variation in song control nuclei in a species with nearmonomorphic song, the Northern Cardinal. Neurosci. Lett., 443, 169e173. Jenkins, L. K., Ross, W. L., & Young, K. A. (2007). Increases in apoptosis and declines in Bcl-X-L protein characterise testicular regression in American crows (Corvus brachyrhynchos). Reprod. Fertil. Devel., 19, 461e469. John, T. M., George, J. C., & Etches, R. J. (1986). Influence of subcutaneous melatonin implantation on gonadal development and on plasma levels of luteinizing hormone, testosterone, estradiol, and corticosterone in the pigeon. J. Pineal. Res., 3, 169e179. Johnson, D. D. P., & Briskie, J. V. (1999). Sperm competition and sperm length in shorebirds. Condor, 101, 848e854. Johnson, O. W. (1961). Reproductive cycle of the mallard duck. Condor, 63, 351e364. Johnston, R. F. (1992). Rock pigeon (Columba Livia). In A. Poole (Ed.), The Birds of North America Online. Ithaca, NY: Cornell Lab of Ornithology. http://bna.birds.cornell.edu.ezproxy1.lib.asu.edu/bna/ species/013 Retrieved from the Birds of North America Online. Jones, L. R. (1986). The effect of photoperiod and temperature on testicular growth in captive black-billed magpies. Condor, 88, 91e93. Jones, R. C. (1999). To store or mature spermatozoa? The primary role of the epididymis. Int. J. Androl., 22, 57e67. Kansaku, N., Hiyama, G., Sasanami, T., & Zadworny, D. (2008). Prolactin and growth hormone in birds: protein structure, gene structure and genetic variation. J. Poult. Sci., 45, 1e6. Kast, T. L., Ketterson, E. D., & Nolan, V. (1998). Variation in ejaculate quality in dark-eyed juncos according to season, stage of reproduction, and testosterone treatment. Auk, 115, 684e693. Kawashima, S., Tsutsui, K., Saxena, R. N., & Ishii, S. (1993). Photoperiodic regulation of follicle-stimulating hormone binding to gonads and of plasma gonadotropin concentrations in Indian weaver birds. Gen. Comp. Endocrinol., 92, 250e259. Kawazu, S., Kishi, H., Saita, E., Jin, W. Z., Suzuki, A. K., Watanabe, G., et al. (2003). Inhibin secretion in the golden hamster (Mesocricetus auratus) testis during active and inactive states of spermatogenesis induced by the restriction of photoperiod. J. Reprod. Devel., 49, 87e97. Kempenaers, B., Peer, K., Vermeirssen, E. L. M., & Robertson, R. J. (2002). Testis size and asymmetry in the tree swallow Tachycineta bicolor: a test of the compensation hypothesis. Avian Sci., 2, 115e122. Kerlan, J. T., Jaffe, R. B., & Payne, A. H. (1974). Sex steroid formation in gonadal tissue homogenates during the testicular cycle of the redwinged blackbird (Agelaius phoeniceus). Gen. Comp. Endocrinol., 24, 352e363. Ketterson, E. D., & Nolan, V., Jr. (1992). Hormones and life histories: an integrative approach. Amer. Nat., 140, S33eS62. Ketterson, E. D., Nolan, V., Wolf, L., Ziegenfus, C., Dufty, A. M., Ball, G. F., et al. (1991). Testosterone and avian life historiesdthe effect of experimentally elevated testosterone on corticosterone and body mass in dark-eyed juncos. Horm. Behav., 25, 489e503. Kim, I. S., & Yang, H. H. (2001). Seasonal changes of testicular weight, sperm production, serum testosterone, and in-vitro testosterone

61

release in Korean ring-necked pheasants (Phasianus colchicus karpowi). J. Vet. Med. Sci., 63, 151e156. King, J. A., & Millar, R. P. (1982a). Structure of chicken hypothalamic luteinizing hormone-releasing hormone. 1. Structural determination on partially purified material. J. Biol. Chem., 257, 722e728. King, J. A., & Millar, R. P. (1982b). Structure of chicken hypothalamic luteinizing hormone-releasing hormone. 2. Isolation and characterization. J. Biol. Chem., 257, 729e732. Kirby, J. D., & Froman, D. P. (2000). Reproduction in male birds. In G. C. Whittow (Ed.), Sturkie’s Avian Physiology (pp. 597e615). San Diego, CA: Academic Press. Kirby, E. D., Geraghty, A. C., Ubuka, T., Bentley, G. E., & Kaufer, D. (2009). Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats. Proc. Natl. Acad. Sci. USA, 106, 11324e11329. Kleven, O., Laskemoen, T., Fossoy, F., Robertson, R. J., & Lifjeld, J. T. (2008). Intraspecific variation in sperm length is negatively related to sperm competition in passerine birds. Evolution, 62, 494e499. Koba, N., Mori, M., Ha, Y., Mizushima, S., Tsukada, A., Saito, N., et al. (2008a). Effects of aromatase inhibitor (Fadrozole)-induced sex reversal on gonadal differentiation and mRNA expression of p450arom, AMH and ER alpha in embryos and growth in posthatching quail. J. Poult. Sci., 45, 116e124. Koba, N., Ohfuji, T., Ha, Y., Mizushima, S., Tsukada, A., Saito, N., et al. (2008b). Expression of P450arom, AMH and ER alpha mRNA in gonads of turkey, duck and goose within one week of age. J. Poult. Sci., 45, 220e226. Koba, N., Ohfuji, T., Ha, Y., Mizushima, S., Tsukada, A., Saito, N., et al. (2008c). Profiles of mRNA expression of FOXL2, P450arom, DMRT 1, AMH, P450(c17), SF1, ER alpha and AR, in relation to gonadal sex differentiation in duck embryo. J. Poult. Sci., 45, 132e138. Kobayashi, M., & Ishii, S. (2002). Effects of starvation on gonadotropin and thyrotropin subunit mRNA levels and plasma hormone levels in the male Japanese quail (Coturnix coturnix japonica). Zool. Sci., 19, 331e342. Kobayashi, M., Cockrem, J. F., & Ishii, S. (2002). Effects of starvation and refeeding on gonadotropin and thyrotropin subunit mRNAs in male Japanese quail. Zool. Sci., 19, 449e461. Kokko, H., Gunnarsson, T. G., Morrell, L. J., & Gill, J. A. (2006). Why do female migratory birds arrive later than males? J. Anim. Ecol., 75, 1293e1303. Konishi, H., Iida, K., Ohta, M., & Takahashi, M. (1988). A possible role for the eyes in the photoperiodic response of quail. Gen. Comp. Endocrinol., 72, 461e466. Krishnaprasadan, T. N., Kotak, V. C., Sharp, P. J., Schmedemann, R., & Haase, E. (1988). Environmenal and hormonal factors in seasonal breeding in free-living male Indian rose-ringed parakeets (Psittacula krameri). Horm. Behav., 22, 488e496. Kro´l, E., Redman, P., Thomson, P. J., Williams, R., Mayer, C., Mercer, J. G., et al. (2005). Effect of photoperiod on body mass, food intake and body composition in the field vole, Microtus agrestis. J. Exp. Biol., 208, 571e584. Kroodsma, D. E. (1976). Reproductive development in a female songbirdddifferential stimulation by quality of male song. Science, 192, 574e575. Kubota, K., Sato, F., Aramaki, S., Soh, T., Yamauchi, N., & Hattori, M. (2007). Ubiquitous expression of myostatin in chicken embryonic tissues: its high expression in testis and ovary. Comp. Biochem. Physiol. A: Molec. Integr. Physiol., 148, 550e555.

62

Kuenzel, W. J. (2000). Central nervous system regulation of gonadal development in the avian male. Poult. Sci., 79, 1679e1688. Kumar, B. S., & Kumar, V. (1993). Photoperiodic control of annual reproductive cycle in subtropical brahminy myna (Sturnus pagodarum). Gen. Comp. Endocrinol., 89, 149e160. Kumar, P., & Chaturvedi, C. M. (2008). Correlation of nitric oxide (NO) activity and gonadal function in Japanese quail, Coturnix coturnix japonica following temporal phase relation of serotonergic and dopaminergic oscillations. Anim. Reprod. Sci., 106, 48e64. Kumar, V., Singh, S., Misra, M., Malik, S., & Rani, S. (2002). Role of melatonin in photoperiodic time measurement in the migratory redheaded bunting (Emberiza bruniceps) and the nonmigratory Indian weaver bird (Ploceus philippinus). J. Exp. Zool., 292, 277e286. Kumaran, J. D. S., & Turner, C. W. (1949). The normal development of the testis in the white plymouth rock. Poult. Sci., 28, 511e520. Kwok, A. H. Y., Wang, Y., Wang, C. Y., & Leung, F. C. (2007). Cloning of chicken glucocorticoid receptor (GR) and characterization of its expression in pituitary and extrapituitary tissues. Poult. Sci., 86, 423e430. Kwok, A. H. Y., Wang, Y., Wang, C. Y., & Leung, F. C. (2008). Molecular cloning and characterization of chicken prostaglandin E receptor subtypes 2 and 4 (EP2 and EP4). Gen. Comp. Endocrinol., 157, 99e106. Kwon, S., Hess, R. A., Bunick, D., Kirby, J. D., & Bahr, J. M. (1997). Estrogen receptors are present in the epididymis of the rooster. J. Androl., 18, 378e384. Kiyoshi, K., Kondoh, M., Hirunagi, K., & Korf, H. (1998). Confocal laser scanning and electron microscopic analyses of the relationship between VIP-like and GnRH-like-immunoreactive neurons in the lateral septal-preoptic area of the pigeon. Cell. Tissue. Res., 293, 39e46. Labov, J. B. (1977). Phytoestrogens and mammalian reproduction. Comp. Biochem. Physiol. A: Physiol., 57, 3e9. Lafont, R. (1997). Ecdysteroids and related molecules in animals and plants. Arch. Insect. Biochem. Physiol., 35, 3e20. Lake, P. E. (1956). The structure of the germinal epithelium of the fowl testis with special reference to the presence of multinuclear cells. Quat. J. Morphol. Sci., 97, 487e497. Lake, P. E., & Hatton, M. (1968). Free amino acids in the vas deferens, semen, transparent fluid and blood plasma of the domestic rooster, Gallus domesticus. J. Reprod. Fertil., 15, 139e143. Lam, F., & Farner, D. S. (1976). The ultrastructure of the cells of Leydig in the white-crowned sparrow (Zonotrichia leucophrys gambelii) in relation to plasma levels of luteinizing hormone and testosterone. Cell. Tissue. Res., 169, 93e109. Lamanna, C., Assisi, L., Botte, V., & Di Fiore, M. M. (2006). Endogenous testicular D-aspartic acid regulates gonadal aromatase activity in boar. J. Endocrinol. Invest., 29, 141e146. Lamanna, C., Assisi, L., Botte, V., & Di Fiore, M. M. (2007a). Involvement of D-Asp in P450 aromatase activity and estrogen receptors in boar testis. Amino Acids, 32, 45e51. Lamanna, C., Assisi, L., Vittoria, A., Botte, V., & Di Fiore, M. M. (2007b). D-Aspartic acid and nitric oxide as regulators of androgen production in boar testis. Theriogenol., 67, 249e254. Landsberg, L., & Young, J. B. (1992). Catecholamines and the adrenal medulla. In J. D. Wilson, & D. W. Foster (Eds.), Williams Textbook of Endocrinology (pp. 621e705). Philadelphia, PA: W.B. Saunders Co.

Hormones and Reproduction of Vertebrates

Lang, A. L., & Barlow, J. C. (1997). Cultural evolution in the Eurasian tree sparrow: divergence between introduced and ancestral populations. Condor, 99, 413e423. Laskemoen, T., Fossoy, F., Rudolfsen, G., & Lifjeld, J. T. (2008). Agerelated variation in primary sexual characters in a passerine with male age-related fertilization success, the bluethroat, Luscinia svecica. J. Avian. Biol., 39, 322e328. Laskemoen, T., Kleven, O., Fossoy, F., & Lifjeld, J. T. (2007). Intraspecific variation in sperm length in two passerine species, the bluethroat, Luscinia svecica, and the willow warbler, Phylloscopus trochilus. Ornis. Fenn., 84, 131e139. Leboucher, G., Depraz, V., Kreutzer, M., & Nagle, L. (1998). Male song stimulation of female reproduction in canaries: features relevant to sexual displays are not relevant to nest-building or egg-laying. Ethology, 104, 613e624. Leclerc, B., Zadworny, D., Bedecarrats, G., & Kuhnlein, U. (2007). Ontogenesis of the expression of prolactin receptor messenger ribonucleic acid during late embryogenesis in turkeys and chickens. Poult. Sci., 86, 1174e1179. Lee, J., Kim, E., Iwata, H., & Tanabe, S. (2007). Molecular characterization and tissue distribution of aryl hydrocarbon receptor nuclear translocator isoforms, ARNT1 and ARNT2, and identification of novel splice variants in common cormorant (Phalacrocorax carbo). Comp. Biochem. Physiol. C: Toxicol. Pharmacol., 145, 379e393. Leitner, S., Van’t Hof, T. J., & Gahr, M. (2003). Flexible reproduction in mild canaries is independent of photoperiod. Gen. Comp. Endocrinol., 130, 102e108. Leopold, A. S., Erwin, M., Oh, J., & Browning, B. (1976). Phytoestrogensdadverse effects on reproduction in California quail. Science, 191, 98e100. Leska, A., & Dusza, L. (2007). Seasonal changes in the hypothalamoepituitaryegonadal axis in birds. Reprod. Biol., 7, 99e126. Lessells, C. M., & Birkhead, T. R. (1990). Mechanisms of sperm competition in birdsdmathematical models. Behav. Ecol. Sociobiol., 27, 325e337. Lewis, P. D., Middleton, B. A., & Gous, R. M. (2006). Exogenous melatonin modifies rate of sexual maturation in domestic pullets. Poult. Sci., 85, 117e122. Li, H., & Kuenzel, W. J. (2008). A possible neural cascade involving the photoneuroendocrine system (PNES) responsible for regulating gonadal development in an avian species, Gallus gallus. Brain Res. Bull., 76, 586e596. Lien, R. J., & Siopes, T. D. (1991). Influence of thyroidectomy on reproductive responses of male domestic turkeys (Meleagris gallopavo). Br. Poult. Sci., 32, 405e415. Ligon, J. D. (1997). A single functional testis as a unique proximate mechanism promoting sex role reversal in coucals. Auk, 114, 800e801. Lin, M., & Jones, R. C. (1992). Renewal and proliferation of spermatogonia during spermatogenesis in the Japanese quail, Coturnix coturnix japonica. Cell. Tissue. Res., 267, 591e601. Lin, M., & Jones, R. C. (1993). Spermiogenesis and spermiation in the Japanese quail (Coturnix coturnix japonica). J. Anat., 183, 525e535. Lincoln, G. A. (1998). Reproductive seasonality and maturation throughout the complete life cycle in the mouflon ram (Ovis Musimon). Anim. Reprod. Sci., 53, 87e105. Lincoln, G. A., & Short, R. V. (1980). Seasonal breeding: nature’s contraceptive. Rec. Prog. Horm. Res., 36, 1e52.

Chapter | 2

Avian Testicular Structure, Function, and Regulation

Lofts, B., & Murton, R. K. (1973). Reproduction in birds. In D. S. Farner, & J. R. King (Eds.), Avian Biology, vol. 3 (pp. 1e107). New York, NY: Academic Press. Lovell, T. M., Knight, P. G., Groome, N. P., & Gladwell, R. T. (2000). Measurement of dimeric inhibins and effects of active immunization against inhibin alpha-subunit on plasma hormones and testis morphology in the developing cockerel. Biol. Reprod., 63, 213e221. Lowther, P. E., Groschupf, K. D., & Russell, S. M. (1999). Rufous-winged sparrow (Aimophila carpalis). In A. Poole, & F. Gill (Eds.), The Birds of North America, No. 422. Philadelphia, PA: The Birds of North America, Inc. Luna, M., Huerta, L., Berumen, L., Martinez-Coria, H., Harvey, S., & Aramburo, C. (2004). Growth hormone in the male reproductive tract of the chicken: heterogeneity and changes during ontogeny and maturation. Gen. Comp. Endocrinol., 137, 37e49. MacDougall-Shackleton, S. A., Deviche, P. J., Crain, R. D., Ball, G. F., & Hahn, T. P. (2001). Seasonal changes in brain GnRH immunoreactivity and song-control nuclei volumes in an opportunistically breeding songbird. Brain. Behav. Evol., 58, 38e48. Macdougal-Shackleton, S. A., Katti, M., & Hahn, T. P. (2006). Tests of absolute photorefractoriness in four species of cardueline finch that differ in reproductive schedule. J. Exper. Biol., 209, 3786e3794. Madekurozwa, M. C., Chabvepi, T. S., Matema, S., & Teerds, K. J. (2002). Relationship between seasonal changes in spermatogenesis in the juvenile ostrich (Stuthio camelus) and the presence of the LH receptor and 3b-hydroxysteroid dehydrogenase. Reproduction, 123, 735e742. Malecki, I. A., Martin, G. B., O’Malley, P. J., Meyer, G. T., Talbot, R. T., & Sharp, P. J. (1998). Endocrine and testicular changes in a short-day seasonally breeding bird, the emu (Dromaius novaehollandiae), in southwestern Australia. Anim. Reprod. Sci., 53, 143e155. Maney, D. L., Goode, C. T., Lake, J. I., Lange, H. S., & O’Brien, S. (2007). Rapid neuroendocrine responses to auditory courtship signals. Endocrinology, 148, 5614e5623. Mao, J. N. C., Burnside, J., Li, L. J., Tang, J. S., Davolos, C., & Cogburn, L. A. (1999). Characterization of unique truncated prolactin receptor transcripts, corresponding to the intracellular domain, in the testis of the sexually mature chicken. Endocrinology., 140, 1165e1174. Marin, R. H., & Satterlee, D. G. (2003). Selection for contrasting adrenocortical responsiveness in Japanese quail (Coturnix japonica) influences sexual behaviour in males. Appl. Anim. Behav. Sci., 83, 187e199. Marin, R. H., & Satterlee, D. G. (2004). Cloacal gland and testis development in male Japanese quail selected for divergent adrenocortical responsiveness. Poult. Sci., 83, 1028e1034. Mauget, R., Jouventin, P., Lacroix, A., & Ishii, S. (1994). Plasma LH and steroid hormones in king penguin (Aptenodytes patagonicus) during the onset of the breeding cycle. Gen. Comp. Endocrinol., 93, 36e43. McGlothlin, J. W., Jawor, J. M., Greives, T. J., Casto, J. M., Phillips, J. L., & Ketterson, E. D. (2008). Hormones and honest signals: males with larger ornaments elevate testosterone more when challenged. J. Evol. Biol., 21, 39e48. McGuire, N. L., & Bentley, G. E. (2010). A functional neuropeptide system in vertebrate gonads: gonadotropin-inhibitory hormone and its receptor in testes of field-caught house sparrow (Passer domesticus). Gen. Comp. Endocrinol., 166, 565e572.

63

McMurray, C. H., Laidlaw, A. S., & McElroy, M. (1986). The effect of plant development and environment on formononetin concentration in red clover (Trifolium pratense L.). J. Sci. Food Agric., 37, 333e340. Meddle, S. L., Wingfield, J. C., Millar, R. P., & Deviche, P. J. (2006). Hypothalamic GnRH-I and its precursor during photorefractoriness onset in free-living male dark-eyed juncos (Junco hyemalis) of different year classes. Gen. Comp. Endocrinol., 145, 148e156. Merila¨, J., & Sheldon, B. C. (1999). Testis size variation in the greenfinch, Carduelis chloris: relevance for some recent models of sexual selection. Behav. Ecol. Sociobiol., 45, 115e123. Millam, J. R. (2005). Endocrine disruption in a songbird, the zebra finch. In A. Dawson, & P. J. Sharp (Eds.), Functional Avian Endocrinology (pp. 285e297). New Delhi, India: Narosa Publishing House. Millam, J. R., Craig-Veit, C. B., Quaglino, A. E., Erichsen, A. L., Famula, T. R., & Fry, D. M. (2001). Posthatch oral estrogen exposure impairs adult reproductive performance of zebra finch in a sexspecific manner. Horm. Behav., 40, 542e549. Millam, J. R., Craig-Veit, C. B., Batchelder, M. E., Viant, M. R., Herbeck, T. M., & Woods, L. W. (2002). An avian bioassay for environmental estrogens: the growth response of zebra finch (Taeniopygia guttata) chick oviduct to oral estrogens. Environ. Toxicol. Chem., 21, 2663e2668. Miyamoto, K., Hasegawa, Y., Nomura, M., Igarashi, M., Kangawa, K., & Matsuo, H. (1984). Identification of the second gonadotropinreleasing hormone in chicken hypothalamusdevidence that gonadotropin secretion is probably controlled by two distinct gonadotropin-releasing hormones in avian species. Proc. Nat. Acad. Sci. USA Biol. Sci., 81, 3874e3878. Moller, A. P. (1988). Testis size, ejaculate quality and sperm competition in birds. Biol. J. Linnean. Soc., 33, 273e283. Moller, A. P. (1990). Parasites and sexual selectiondcurrent status of the Hamilton and Zuk hypothesis. J. Evol. Biol., 3, 319e328. Moller, A. P. (1991). Sperm competition, sperm depletion, paternal care, and relative testis size in birds. Amer. Nat., 137, 882e906. Moller, A. P. (1994). Directional selection on directional asymmetry: testis size and secondary sexual characters in birds. Proc. R. Soc. London. B: Biol. Sci., 258, 147e151. Moller, A. P., & Briskie, J. V. (1995). Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behav. Ecol. Sociobiol., 36, 357e365. Moller, A. P., & Erritzoe, J. (1988). Badge, body and testis size in house sparrows, Passer domesticus. Ornis. Scandinav., 19, 72e73. Moore, I. T., Bonier, F., & Wingfield, J. C. (2005). Reproductive asynchrony and population divergence between two tropical bird populations. Behav. Ecol., 16, 755e762. Moore, I. T., Perfito, N., Wada, H., Sperry, T. S., & Wingfield, J. C. (2002). Latitudinal variation in plasma testosterone levels in birds of the genus Zonotrichia. Gen. Comp. Endocrinol., 129, 13e19. Moore, I. T., Wingfield, J. C., & Brenowitz, E. A. (2004). Plasticity of the avian song control system in response to localized environmental cues in an equatorial songbird. J. Neurosci., 24, 10182e10185. Morton, M. L., Peterson, L. E., Burns, D. M., & Allan, N. (1990). Seasonal and age-related changes in plasma testosterone levels in mountain white-crowned sparrows. Condor, 92, 166e173. Mougeot, F., Redpath, S. M., & Piertney, S. B. (2006). Elevated spring testosterone increases parasite intensity in male red grouse. Behav. Ecol., 17, 117e125.

64

Muehlenbein, M. P., & Bribiescas, R. G. (2005). Testosterone-mediated immune functions and male life histories. Am. J. Hum. Biol., 17, 527e558. Mulder, R. A., & Cockburn, A. (1993). Sperm competition and the reproductive anatomy of male superb fairy-wrens. Auk, 110, 588e593. Murphy, B. E. P. (1968). Binding of testosterone and estradiol in plasma. Can. J. Biochem., 46, 299e302. Nakai, M., Hashimoto, Y., Kitagawa, H., Kon, Y., & Kudo, N. (1989). Histological study on seminal plasma absorption and spermiophagy in the epididymal region of domestic fowl. Poult. Sci., 68, 582e589. Nakamura, K., Shibuya, K., Saito, N., Shimada, K., Ohshima, A., Hirai, T., et al. (2008). mRNA expression of cytochrome P450 17 alpha hydroxylase, cytochrome P450 aromatase, anti-Mu¨llerian hormone, estrogen receptor alpha, and androgen receptor in developing gonads of Japanese quail. J. Poult. Sci., 45, 298e302. Nakamura, T., & Tanabe, Y. (1972a). In-vitro steroidogenesis by testes of the chicken (Gallus domesticus). Gen. Comp. Endocrinol., 19, 432e440. Nakamura, T., & Tanabe, Y. (1972b). Pathways for androgen synthesis in vitro by the testes of Japanese quail (Coturnix coturnix japonica). J. Endocrinol., 55, 499e506. Nakao, N., Ono, H., Yamamura, T., Anraku, T., Takagi, T., Higashi, K., et al. (2008). Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature, 452, 317e322. Nalbandov, A. V. (1945). A study of the effect of prolactin on broodiness and on cock testes. Endocrinology, 36, 258. Nastiuk, K. L., & Clayton, D. F. (1994). Seasonal and tissue-specific regulation of canary androgen receptor messenger ribonucleic acid. Endocrinology, 134, 640e649. Newton, I. (1998). Finches. Englewood Cliffs, NJ: Taplinger. Nicholls, T. J., & Graham, G. P. (1972). Observations on the ultrastructure and differentiation of Leydig cells in the testis of the Japanese quail (Coturnix coturnix japonica). Biol. Reprod., 6, 179e192. Nicholls, T. J., Goldsmith, A. R., & Dawson, A. (1988). Photorefractoriness in birds and comparison with mammals. Physiol. Rev., 68, 133e176. Nishikimi, H., Kansaku, N., Saito, N., Usami, M., Ohno, Y., & Shimada, K. (2000). Sex differentiation and mRNA expression of P450c17, P450arom and AMH in gonads of the chicken. Mol. Reprod. Dev., 55, 20e30. Noel, M., Ramsey, M., Crews, D., & Breuner, C. (2004). Cloning and characterization of corticosteroid binding globulin (CBG) in an avian species, Passer domesticus. Integr. Comp. Biol., 44. 731-731. Noirault, K., Brillard, J. P., & Bakst, M. R. (2006). Spermatogenesis in the turkey (Meleagris gallopavo): Quantitative approach in immature and adult males subjected to various photoperiods. Theriogenol., 65, 845e859. Nomura, O., Nakabayashi, O., Nishimori, K., Yasue, H., & Mizuno, S. (1999). Expression of five steroidogenic genes including aromatase gene at early developmental stages of chicken male and female embryos. J. Steroid. Biochem. Mol. Biol., 71, 103e109. Norris, D. O. (2007). Vertebrate Endocrinology. San Diego, CA: Academic Press. O’Brien, S., & Hau, M. (2005). Food cues and gonadal development in neotropical spotted antbirds (Hylophylax naevioides). J. Ornithol., 146, 332e337.

Hormones and Reproduction of Vertebrates

Ocon-Grove, O. M., Krzysik-Walker, S. M., Maddineni, S. R., Hendricks, Gilbert L., III, & Ramachandran, R. (2008). Adiponectin and its receptors are expressed in the chicken testis: influence of sexual maturation on testicular ADIPOR1 and ADIPOR2 mRNA abundance. Reproduction, 136, 627e638. Odum, J., Tinwell, H., Jones, K., Van Miller, J. P., Joiner, R. L., Tobin, G., et al. (2001). Effect of rodent diets on the sexual development of the rat. Toxicol. Sci., 61, 115e127. Ohkubo, T., Tsukada, A., & Shamoto, K. (2003). cDNA cloning of chicken orexin receptor and tissue distribution: sexually dirnorphic expression in chicken gonads. J. Mol. Endocrinol., 31, 499e508. Ohmart, R. D. (1969). Physiological and Ethological Adaptations of the Rufous-winged Sparrow (Aimophila carpalis) to a Desert Environment. Ph.D. dissertation. University of Arizona. Ohta, M., Kadota, C., & Konishi, H. (1989). A role of melatonin in the initial stage of photoperiodism in the Japanese quail. Biol. Reprod., 40, 935e941. Olsen, P. D. (1991). Do large males have small testesda note on allometric variation and sexual size dimorphism in raptors. Oikos, 60, 134e136. Onagbesan, O. M., Safi, M., Decuypere, E., & Bruggeman, V. (2004). Developmental changes in inhibin alpha and inhibin/activin betaA and betaB mRNA levels in the gonads during post-hatch prepubertal development of male and female chickens. Mol. Reprod. Dev., 68, 319e326. Opalka, M., Kaminska, b., Ciereszko, R., & Dusza, L. (2004). Genistein affects testosterone secretion by Leydig cells in roosters (Gallus gallus domesticus). Reprod. Biol., 4, 185e193. Opalka, M., Kaminska, b., Puchajda-Skowronska, H., & Dusza, L. (2006). Phytoestrogen action in Leydig cells of bilgoraj ganders (Anser anser). Reprod. Biol. 6, Suppl., 2, 47e54. Opalka, M., Kugla-Owczarska, J., Kaminska, b., Puchajda-Skowronska, H., Hryniewicka, W., & Dusza, L. (2008). Effects of dietary meals containing different levels of phytoestrogens on reproductive function in bilgoraj ganders. Acta. Vet. Hung., 56, 379e391. Oppliger, A., Hosken, D. J., & Ribi, G. (1998). Snail sperm production characteristics vary with sperm competition risk. Proc. R. Soc. Lond. B: Biol. Sci., 265, 1527e1534. Oreal, E., Mazaud, S., Picard, J. Y., Magre, S., & Carre-Eusebe, D. (2002). Different patterns of anti-Mu¨llerian hormone expression, as related to DMRT1, SF-1, WT1, GATA-4, Wnt-4, and Lhx9 expression, in the chick differentiating gonads. Dev. Dyn., 225, 221e232. Osman, D. I., Ekwall, H., & Ploen, L. (1980). Specialized cell contacts and the bloodetestis barrier in the seminiferous tubules of the domestic fowl (Gallus domesticus). Int. J. Androl., 3, 553e562. Ottinger, M. A., & Bakst, M. R. (1981). Peripheral androgen concentrations and testicular morphology in embryonic and young male Japanese quail. Gen. Comp. Endocrinol., 43, 170e177. Ottinger, M. A., Kubakawa, K., Kikuchi, M., Thompson, N., & Ishii, S. (2002). Effects of exogenous testosterone on testicular luteinizing hormone and follicle-stimulating hormone receptors during aging. Exp. Biol. Med., 227, 830e836. Owen-Ashley, N. T., & Butler, L. K. (2004). Androgens, interspecific competition and species replacement in hybridizing warblers. Proc. R. Soc. Lond. B: Biol. Sci., 271, S498eS500. Pang, S. F., Cheng, K. M., Pang, C. S., Wang, Z. P., Yuan, H., & Brown, G. M. (1993). Differential effects of short photoperiod on 2-

Chapter | 2

Avian Testicular Structure, Function, and Regulation

[125I]iodomelatonin binding in the testis and brain of quail. Biol. Signals, 2, 146e154. Pant, K., & Chandola-Saklani, A. (1992). Pinealectomy and LL abolished circadian perching rhythms but did not alter circannual reproductive or fattening rhythms in finches. Chronobiol. Int., 9, 413e420. Parker, G. A. (1970a). Sperm competition and its evolutionary consequences in insects. Biol. Rev. Camb. Philos. Soc., 45, 525e567. Parker, G. A. (1970b). Sperm competition and its evolutionary effect on copula duration in fly, Scatophaga stercoraria. J. Insect. Physiol., 16, 1301e1328. Partecke, J., Van’t Hof, T., & Gwinner, E. (2004). Differences in the timing of reproduction between urban and forest European blackbirds (Turdus merula): result of phenotypic flexibility or genetic differences? Proc. R. Soc. Lond. B: Biol. Sci., 271, 1995e2001. Partecke, J., Van’t Hof, T. J., & Gwinner, E. (2005). Underlying physiological control of reproduction in urban and forest-dwelling European blackbirds, Turdus merula. J. Avian. Biol., 36, 295e305. Payne, R. B. (1967). Interspecific communication signals in parasitic birds. Amer. Nat., 101, 363e375. Payne, R. B. (1973a). Breeding season of a parasitic birddbrown-headed cowbird, in central California. Condor, 75, 80e99. Payne, R. B. (1973b). Individual laying histories and clutch size and numbers of eggs of parasitic cuckoos. Condor, 75, 414e438. Payne, R. B. (1977). Ecology of brood parasitism in birds. Ann. Rev. Ecol. Syst., 8, 1e28. Pearce-Higgins, J. W., Yalden, D. W., & Whittingham, M. J. (2005). Warmer springs advance the breeding phenology of golden plovers, Pluvialis apricaria, and their prey (Tipulidae). Oecologia, 143, 470e476. Penfold, L. M., Wildt, D. E., Herzog, T. L., Lynch, W., Ware, L., Derrickson, S. E., et al. (2000). Seasonal patterns of LH, testosterone and semen quality in the Northern pintail duck (Anas acuta). Reprod. Fertil. Devel., 12, 229e235. Perfito, N., Bentley, G., & Hau, M. (2006). Tonic activation of brain GnRH immunoreactivity despite reduction of peripheral reproductive parameters in opportunistically breeding zebra finches. Brain Behav. Evol., 67, 123e134. Perfito, N., Kwong, J. M., Bentley, G. E., & Hau, M. (2008). Cue hierarchies and testicular development: is food a more potent stimulus than day length in an opportunistic breeder (Taeniopygia g. guttata)? Horm. Behav., 53, 567e572. Perfito, N., Tramontin, A. D., Meddle, S., Sharp, P., Afik, D., Gee, J., et al. (2004). Reproductive development according to elevation in a seasonally breeding male songbird. Oecologia, 140, 201e210. Perfito, N., Zann, R. A., Bentley, G. E., & Hau, M. (2007). Opportunism at work: habitat predictability affects reproductive readiness in freeliving zebra finches. Funct. Ecol., 21, 291e301. Phillmore, L. S., Hoshooley, J. S., Sherry, D. F., & MacDougallShackleton, S. A. (2006). Annual cycle of the black-capped chickadee: seasonality of singing rates and vocal control brain regions. J. Neurobiol., 66, 1002e1010. Pitcher, T. E., & Stutchbury, B. J. M. (1998). Latitudinal variation in testis size in six species of North American songbirds. Can. J. Zool., 76, 618e622. Pitcher, T. E., Dunn, P. O., & Whittingham, L. A. (2005). Sperm competition and the evolution of testis size in birds. J. Evol. Biol., 18, 557e567.

65

Pitts, G. R., You, S., Foster, D. N., & El Halawani, M. E. (2000). Evidence for multiple prolactin receptor transcripts in the turkey. Poult. Sci., 79, 355e362. Pochron, S. T., & Wright, P. C. (2002). Dynamics of testis size compensates for variation in male body size. Evol. Ecol. Res., 4, 577e585. Prendergast, B. J., Flynn, A. K., & Zucker, I. (2000). Triggering of neuroendocrine refractoriness to short-day patterns of melatonin in Siberian hamsters. J. Neuroendocrinol., 12, 303e310. Priedkalns, J., Oksche, A., Vleck, C., & Bennett, R. K. (1984). The response of the hypothalamoegonadal system to environmental factors in the zebra finch, Poephila guttata castanotisdstructural and functional studies. Cell. Tissue. Res., 238, 23e35. Purcell, S. M., & Wilson, W. O. (1975). Growth and maturation of testes in young coturnix and modification by exogenous FSH, LH, and testosterone - a stereologic evaluation. Poult. Sci., 54, 1115e1122. Quay, W. B. (1985). Sperm release in migrating wood warblers (Parulinae) nesting at higher latitudes. Wilson. Bull., 97, 283e295. Quay, W. B. (1989). Timing of sperm releases and inseminations in resident emberizidsda comparative study. Condor, 91, 941e961. Raess, M., & Gwinner, E. (2005). Gonadal status upon spring arrival in long-distance and short-distance migrating stonechats (Saxicola torquata). J. Ornithol., 146, 325e331. Ramachandran, A. V., Patel, M. M., & Patel, C. S. (1996). Effects of pineal indoles and parachlorophenylalanine on seasonal reproduction in the pigeon. J. Exp. Biol., 199, 793e800. Ramesh, R., Kuenzel, W. J., Buntin, J. D., & Proudman, J. A. (2000). Identification of growth hormone- and prolactin-containing neurons within the avian brain. Cell. Tissue. Res., 299, 371e383. Rand, A. L. (1933). Testicular asymmetry in the Madagascar coucal. Auk, 50, 219e220. Rani, S., Singh, S., Misra, M., Malik, S., Singh, B. P., & Kumar, V. (2005). Daily light regulates seasonal responses in the migratory male redheaded bunting (Emberiza bruniceps). J. Exp. Zool. A: Comp. Exp. Biol., 303, 541e550. Richardson, D. S., & Burke, T. (1999). Extra-pair paternity in relation to male age in Bullock’s orioles. Mol. Ecol., 8, 2115e2126. Rising, J. D. (1987a). Geographic variation in testis size in savannah sparrows (Passerculus sandwichensis). Wilson. Bull., 99, 63e72. Rising, J. D. (1987b). Geographic variation of sexual dimorphism in size of savannah sparrows (Passerculus sandwichensis) - a test of hypotheses. Evolution, 41, 514e524. Rising, J. D. (1996). Relationship between testis size and mating systems in American sparrows (Emberizinae). Auk, 113, 224e228. Robb, G. N., McDonald, R. A., Chamberlain, D. E., & Bearhop, S. (2008). Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front. Ecol. Environ., 6, 476e484. Robinson, J. E., & Follett, B. K. (1982). Photoperiodism in Japanese quail: the termination of seasonal breeding by photorefractoriness. Proc. R. Soc. Lond. B: Biol. Sci., 215, 95e116. Robinzon, B., & Cutolo, M. (1999). Should dehydroepiandrosterone replacement therapy be provided with glucocorticoids? Rheumatology, 38, 488e495. Rochester, J. R., Heiblum, R., Rozenboim, I., & Millam, J. R. (2008a). Post-hatch oral estrogen exposure reduces oviduct and egg mass and alters nest-building behavior in adult zebra finches (Taeniopygia guttata). Physiol. Behav., 95, 370e380.

66

Rochester, J. R., Forstmeier, W., & Millam, J. R. (2010). Post-hatch oral estrogen in zebra finches (Taeniopygia guttata): is infertility due to disrupted testes morphology or reduced copulatory behavior? Physiol. and Behav. In Press. Rochester, J. R., Klasing, K. C., Stevenson, L., Denison, M. S., Berry, W., & Millam, J. R. (2008b). Dietary red clover (Trifolium pratense) induces oviduct growth and decreases ovary and testes growth in Japanese quail chicks. Reprod. Toxicol., 27, 63e71. Ro¨dl, T., Goymann, W., Schwabl, I., & Gwinner, E. (2004). Excremental androgen metabolite concentrations and gonad sizes in temperate zone vs. tropical stonechats (Saxicola torquata ssp.). Gen. Comp. Endocrinol., 139, 124e130. Rodriguez, I., Ody, C., Araki, K., Garcia, I., & Vassalli, P. (1997). An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO. J., 16, 2262e2270. Rohss, M., & Silverin, B. (1983). Seasonal variations in the ultrastructure of the Leydig cells and plasma levels of luteinizing hormone and steroid hormones in juvenile and adult male great tits, Parus major. Ornis. Scandinav., 14, 202e212. Rombauts, L., Vanmontfort, D., Decuypere, E., & Verhoeven, G. (1996). Inhibin and activin have antagonistic paracrine effects on gonadal steroidogenesis during the development of the chicken embryo. Biol. Reprod., 54, 1229e1237. Rosenstrauch, A., Weil, S., Degen, A. A., & Friedlander, M. (1998). Leydig cell functional structure and plasma androgen level during the decline in fertility in aging roosters. Gen. Comp. Endocrinol., 109, 251e258. Rossi, G., Ceccherelli, R., Piersigilli, A., & Tarantino, C. (2003). Sertoli cell tumor associated with polyomavirus infection in a gouldian finch (Erythrura gouldiae). Avian. Dis., 47, 240e243. Rowe, M., Bakst, M. R., & Pruett-Jones, S. (2008). Good vibrations? Structure and function of the cloacal tip of male Australian Maluridae. J. Avian. Biol., 39, 348e354. Ruiz, G., Rosenmann, M., Novoa, F. F., & Sabat, P. (2002). Hematological parameters and stress index in rufous-collared sparrows dwelling in urban environments. Condor, 104, 162e166. Sackman, J. W. (1977). The effect of melatonin on LH-RH induced changes in pituitary and gonadal function of immature domestic fowl. Biol. Reprod., 17, 718e722. Saldanha, C. J., Deviche, P. J., & Silver, R. (1994). Increased VIP and decreased GnRH expression in photorefractory dark-eyed juncos (Junco hyemalis). Gen. Comp. Endocrinol., 93, 128e136. Saloniemi, H., Wahala, K., Nykanenkurki, P., Kallela, K., & Saastamoinen, I. (1995). Phytoestrogen content and estrogenic effect of legume fodder. Proc. Soc. Exper. Biol. Med., 208, 13e17. Samour, J. H., Spratt, D. M., Holt, W. V., & Smith, C. A. (1988). Ultrastructure and secretory nature of the seminal glomus in budgerigars (Melopsittacus undulatus). Res. Vet. Sci., 45, 194e197. Santti, R., Makela, S., Strauss, L., Korkman, J., & Kostian, M. L. (1998). Phytoestrogens: potential endocrine disruptors in males. Toxicol. Ind. Health, 14, 223e237. Satterlee, D. G., & Johnson, W. A. (1988). Selection of Japanese quail for contrasting blood corticosterone response to immobilization. Poult. Sci., 67, 25e32. Satterlee, D. G., & Jones, R. B. (1997). Ease of capture in Japanese quail of two lines divergently selected for adrenocortical response to immobilization. Poult. Sci., 76, 469e471.

Hormones and Reproduction of Vertebrates

Satterlee, D. G., & Marin, R. H. (2004). Photoperiod-induced changes in cloacal gland physiology and testis weight in male Japanese quail selected for divergent adrenocortical responsiveness. Poult. Sci., 83, 1003e1010. Satterlee, D. G., Castille, S. A., & Fioretti, W. C. (2006a). Active immunization of broiler breeder cockerels against chicken inhibin accelerates puberty and prevents age-induced testicular involution. Poult. Sci., 85, 1087e1094. Satterlee, D. G., Cole, C. A., & Castille, S. A. (2006b). Cloacal gland and gonadal photoresponsiveness in male Japanese quail selected for divergent plasma corticosterone response to brief restraint. Poult. Sci., 85, 1072e1080. Satterlee, D. G., Johnson, W. A., & Jacobsperry, L. A. (1983). Genetic selection for high and low corticosterone response lines in Japanese quaildan updated report. Poult. Sci., 62, 1496e1497. Satterlee, D. G., Tong, M., Castille, S. A., & Marin, R. H. (2007). Cloacal gland growth differences in high and low plasma corticosterone stress response line male quail reared under short daylengths. Poult. Sci., 86, 1213e1217. Satterlee, D. G., Truax, R. E., Jacobsperry, L. A., & Johnson, W. A. (1982). Genetic selection of wild-type Japanese quail for high and low plasma corticosterone response to albino quail intrusion. Poult. Sci., 61, 1394e1395. Scheib, D. (1973). Cytologic study of the postnatal differentiation of interstitial testis cells of the Japanese quail. C.R. Acad. Sci. Hebd. Seances. Acad. Sci. D., 276, 999e1002. Schoech, S. J., & Hahn, T. P. (2007). Food supplementation and timing of reproduction: does the responsiveness to supplementary information vary with latitude? J. Ornithol., 148, S625eS632. Schoech, S. J., Bowman, R., Bridge, E. S., & Boughton, R. K. (2007). Baseline and acute levels of corticosterone in Florida scrub-jays (Aphelocoma coerulescens): effects of food supplementation, suburban habitat, and year. Gen. Comp. Endocrinol., 154, 150e160. Schuler, H. M., & Gier, H. T. (1976). Duration of the cycle of the seminiferous epithelium in the prairie vole (Microtus ochrogaster ochrogaster). J. Exp. Zool., 197, 1e11. Schwabl, H., Flinks, H., & Gwinner, E. (2005). Testosterone, reproductive stage, and territorial behavior of male and female European stonechats Saxicola torquata. Horm. Behav., 47, 503e512. Scott, D. M., & Middleton, A. (1968). Annual testicular cycle of brown-headed cowbird (Molothrus ater). Can. J. Zool., 46, 77e87. Sechman, A. (2005). Molecular mechanisms of sex determination in birds. Med. Weter., 61, 19e23. Sedqyar, M., Weng, Q., Watanabe, G., Kandiel, M. M., Takahashi, S., Suzuki, A. K., et al. (2008). Secretion of inhibin in male Japanese quail (Coturnix japonica) from one week of age to sexual maturity. J. Reprod. Dev., 54, 100e106. Selander, R. K., & Hauser, R. J. (1965). Gonadal and behavioral cycles in the great-tailed grackle. Condor, 67, 157e182. Sengupta, A., & Kumar, M. S. (2006). The pineal gland, but not melatonin, is associated with the termination of seasonal testicular activity in an annual reproductive cycle in roseringed parakeet, Psittacula krameri. Chronobiol. Int., 23, 915e933. Shackell, G. H., Kelly, R. W., & Johnstone, P. D. (1993). Effects of prolonged exposure of ewes to estrogenic pasture.1. Permanent flock infertility following long-term grazing of red clover (Grasslands Pawera) dominant pasture. NZ. J. Agric. Res., 36, 451e457.

Chapter | 2

Avian Testicular Structure, Function, and Regulation

Shanbhag, B. A., & Sharp, P. J. (1996). Immunocytochemical localization of androgen receptor in the comb, uropygial gland, testis, and epididymis in the domestic chicken. Gen. Comp. Endocrinol., 101, 76e82. Sharp, P. J. (2005). Photoperiodic regulation of seasonal breeding in birds. Tr. Comp. Endocrinol. Neurobiol., 1040, 189e199. Sharp, P. J., & Blache, D. (2003). A neuroendocrine model for prolactin as the key mediator of seasonal breeding in birds under long- and short-day photoperiods. Can. J. Physiol. Pharmacol., 81, 350e358. Sharp, P. J., Dawson, A., & Lea, R. W. (1998). Control of luteinizing hormone and prolactin secretion in birds. Comp. Biochem. Physiol. C.: Pharmacol. Toxicol. Endocrinol., 119, 275e282. Sharp, P. J., Klandorf, H., & McNeilly, A. S. (1986). Plasma prolactin, thyroxine, triiodothyronine, testosterone, and luteinizing hormone during a photoinduced reproductive cycle in mallard drakes. J. Exp. Zool., 238, 409e413. Silverin, B. (1995). Reproductive adaptations to breeding in the North. Amer. Zool., 35, 191e202. Silverin, B., & Goldsmith, A. (1997). Natural and photoperiodically induced changes in plasma prolactin levels in male great tits. Gen. Comp. Endocrinol., 105, 145e154. Silverin, B., & Viebke, P. A. (1994). Low temperatures affect the photoperiodically induced LH and testicular cycles differently in closely related species of tits (Parus spp). Horm. Behav., 28, 199e206. Silverin, B., Kikuchi, M., & Ishii, S. (1997). Seasonal changes in folliclestimulating hormone in free-living great tits. Gen. Comp. Endocrinol., 108, 366e373. Silverin, B., Massa, R., & Stokkan, K. A. (1993). Photoperiodic adaptation to breeding at different latitudes in great tits. Gen. Comp. Endocrinol., 90, 14e22. Silverin, B., Wingfield, J., Stokkan, K., Massa, R., Jarvinen, A., Andersson, N., et al. (2008). Ambient temperature effects on photo induced gonadal cycles and hormonal secretion patterns in great tits from three different breeding latitudes. Horm. Behav., 54, 60e68. Singh, S. S., & Haldar, C. (2005). Melatonin prevents testosteroneinduced suppression of immune parameters and splenocyte proliferation in Indian tropical jungle bush quail, Perdicula asiatica. Gen. Comp. Endocrinol., 141, 226e232. Singh, S. S., & Haldar, C. (2007). Peripheral melatonin modulates seasonal immunity and reproduction of Indian tropical male bird Perdicula asiatica. Comp. Biochem. Physiol. A: Mol. Integr. Physiol., 146, 446e450. Small, T. W., Sharp, P. J., Bentley, G. E., & Deviche, P. (2008a). Relative photorefractoriness, prolactin, and reproductive regression in a flexibly breeding sonoran desert passerine, the rufous-winged sparrow, Aimophila carpalis. J. Biol. Rhythms., 23, 69e80. Small, T. W., Sharp, P. J., & Deviche, P. (2007). Environmental regulation of the reproductive system in a flexibly breeding Sonoran Desert bird, the rufous-winged sparrow, Aimophila carpalis. Horm. Behav., 51, 483e495. Small, T. W., Sharp, P. J., Bentley, G. E., Millar, R. P., Tsutsui, K., Mura, E., et al. (2008b). Photoperiod-independent hypothalamic regulation of luteinizing hormone secretion in a free-living Sonoran Desert bird, the rufous-winged sparrow (Aimophila carpalis). Brain Behav. Evol., 71, 127e142. Small, T. W., Sharp, P. J., Bentley, G. E., Millar, R. P., Tsutsui, K., Strand, C., et al. (2008c). Auditory stimulation of reproductive

67

function in male rufous-winged sparrows, Aimophila carpalis. Horm. Behav., 53, 28e39. Smithwick, E. B., Young, L. G., & Gould, K. G. (1996). Duration of spermatogenesis and relative frequency of each stage in the seminiferous epithelial cycle of the chimpanzee. Tissue. Cell., 28, 357e366. Snapir, N., Rulf, J., Meltzer, A., Gvaryahu, G., Rozenboim, I., & Robinzon, B. (1998). Testosterone concentrations, testis weight and morphology of mule drakes (Muscovy drake x Khaki Campbell). Br. Poult. Sci., 39, 572e574. Solberg, E. J., Jensen, H., Ringsby, T. H., & Saether, B. E. (2006). Fitness consequences of hybridization between house sparrows (Passer domesticus) and tree sparrows (P. montanus). J. Ornithol., 147, 504e506. Soma, K. K. (2006). Testosterone and aggression: Berthold, birds and beyond. J. Neuroendocrinol., 18, 543e551. Sorenson, L. G., Nolan, P. M., Brown, A. M., Derrickson, A. M., & Monfort, S. L. (1997). Hormonal dynamics during mate choice in the northern pintail: a test of the challenge hypothesis. Anim. Behav., 57, 1117e1133. Spottiswoode, C., & Moller, A. P. (2004). Extrapair paternity, migration, and breeding synchrony in birds. Behav. Ecol., 15, 41e57. Sprando, R. L., & Russell, L. D. (1988). Spermiogenesis in the red-ear turtle (Pseudemys scripta) and the domestic fowl (Gallus domesticus): a study of cytoplasmic events including cell volume changes and cytoplasmic elimination. J. Morphol., 198, 95e118. Sreekumar, K. P., & Sharp, P. J. (1998). Effect of photostimulation on concentrations of plasma prolactin in castrated bantams (Gallus domesticus). J. Neuroendocrinol., 10, 147e154. Stetson, M. H., & Erickson, J. E. (1970). The antigonadal properties of prolactin in birds: failure of prolactin to inhibit the uptake of 32 P by testes of cockerels in vivo. Gen. Comp. Endocrinol., 15, 484e487. St. Louis, V. L., & Barlow, J. C. (1988). Genetic differentiation among ancestral and introduced populations of the Eurasian tree sparrow (Passer montanus). Evolution, 42, 266e276. Stokkan, K. A., Sharp, P. J., Dunn, I. C., & Lea, R. W. (1988). Endocrine changes in photostimulated willow ptarmigan (Lagopus lagopus lagopus) and Svalbard ptarmigan (Lagopus mutus hyperboreus). Gen. Comp. Endocrinol., 70, 169e177. Stratil, K. A. (1970). Studies on proteins of seminal fluid from the vasa deferentia in the cock. Int. J. Biochem., 1, 728e734. Stutchbury, B. J. M., Morton, E. S., & Piper, W. H. (1998). Extra-pair mating system of a synchronously breeding tropical songbird. J. Avian. Biol., 29, 72e78. Sudhakumari, C. C., Haldar, C., & Senthilkumaran, B. (2001). Seasonal changes in adrenal and gonadal activity in the quail, Perdicula asiatica: involvement of the pineal gland. Comp. Biochem. Physiol. B: Biochem. Mol. Biol., 128, 793e804. Suescun, M. O., Scorticati, C., Chiauzzi, V. A., Chemes, H. E., Rivarola, M. A., & Calandra, R. S. (1985). Induced hypoprolactinemia and testicular steroidogenesis in man. J. Androl., 6, 10e14. Sun, Y. M., Dunn, I. C., Baines, E., Talbot, R. T., Illing, N., Millar, R. P., et al. (2001). Distribution and regulation by oestrogen of fully processed and variant transcripts of gonadotropin releasing hormone I and gonadotropin releasing hormone receptor mRNAs in the male chicken. J. Neuroendocrinol., 13, 37e49.

68

Suttie, J. M., Fennessy, P. F., Corson, I. D., Veenvliet, B. A., Littlejohn, R. P., & Lapwood, K. R. (1992). Seasonal pattern of luteinizing hormone and testosterone pulsatile secretion in young adult red deer stags (Cervus elaphus) and its association with the antler cycle. J. Reprod. Fertil., 95, 925e933. Svedin, N., Wiley, C., Veen, T., Gustafsson, L., & Qvarnstrom, A. (2008). Natural and sexual selection against hybrid flycatchers. Proc. R. Soc. Lond. B: Biol. Sci., 275, 735e744. Tae, H. J., Jang, B. G., Ahn, D. C., Choi, E. Y., Kang, H. S., Kim, N. S., et al. (2005). Morphometric studies on the testis of Korean ringnecked pheasant (Phasianus colchicus karpowi) during the breeding and non-breeding seasons. Vet. Res. Commun., 29, 629e643. Takeuchi, S., Teshigawara, K., & Takahashi, S. (2000). Widespread expression of agouti-related protein (AGRP) in the chicken: a possible involvement of AGRP in regulating peripheral melanocortin systems in the chicken. Biochim. Biophys. Acta. Mol. Cell. Res., 1496, 261e269. Tanaka, M., Hayashida, Y., Sakaguchi, K., Ohkubo, T., Wakita, M., Hoshino, S., et al. (1996). Growth hormone-independent expression of insulin-like growth factor I messenger ribonucleic acid in extrahepatic tissues of the chicken. Endocrinology, 137, 30e34. Tanaka, M., Yamamoto, I., Hayashida, Y., Nakao, N., Ohkubo, T., Wakita, M., et al. (2000). Two novel first exons in the prolactin receptor gene are transcribed in a tissue-specific and sexual maturation-dependent manner to encode multiple 5 ’-truncated transcripts in the testis of the chicken. Biochim. Biophys. Acta Gene Struct Expression, 1491, 279e284. Tanaka, S., & Fujioka, T. (1981). Histological changes in the testis of the domestic fowl after partial adenohypophysectomy. Poult. Sci., 60, 444e452. Teruyama, R., & Beck, M. M. (2001). Double immunocytochemistry of vasoactive intestinal peptide and cGnRH-I in male quail: photoperiodic effects. Cell. Tissue. Res., 303, 403e414. Thurston, R. J. (1979). Seminal plasma proteins in white and yellow turkey semen. Poult. Sci., 58. 1026. Thurston, R. J., & Korn, N. (1997). Semen quality in the domestic turkey: the yellow semen syndrome. Poult. Avian. Biol. Rev., 8, 109e121. Thurston, R. J., & Korn, N. (2000). Spermiogenesis in commercial poultry species: anatomy and control. Poult. Sci., 79, 1650e1668. Thurston, R. J., Hess, R. A., Froman, D. P., & Biellier, H. V. (1982). Elevated seminal plasma protein - a characteristic of yellow turkey semen. Poult. Sci., 61, 1905e1911. Tingari, M. D. (1971). On the structure of the epididymal region and ductus deferens of the domestic fowl (Gallus domesticus). J. Anat., 109, 423e435. Tingari, M. D. (1972). The fine structure of the epithelial lining of the excurrent duct system of the testis of the domestic fowl (Gallus domesticus). Quat. J. Exp. Physiol. Cogn. Med. Sci., 57, 271e295. Tingari, M. D., & Lake, P. E. (1972). Ultrastructural evidence for resorption of spermatozoa and testicular fluid in the excurrent ducts of the testis of the domestic fowl, Gallus domesticus. J. Reprod. Fertil., 31, 373e381. Torti, V. M., & Dunn, P. O. (2005). Variable effects of climate change on six species of North American birds. Oecologia, 145, 486e495. Trivedi, A. K., Rani, S., & Kumar, V. (2004). Melatonin blocks inhibitory effects of prolactin on photoperiodic induction of gain in body mass, testicular growth and feather regeneration in the migratory male

Hormones and Reproduction of Vertebrates

redheaded bunting (Emberiza bruniceps). Reprod. Biol. Endocrinol., 2, 79. Trivedi, A. K., Rani, S., & Kumar, V. (2006). Control of annual reproductive cycle in the subtropical house sparrow (Passer domesticus): evidence for conservation of photoperiodic control mechanisms in birds. Front. Zool., 3, 12. Tsao, R., Papadopoulos, Y., Yang, R., Young, J. C., & McRae, K. (2006). Isoflavone profiles of red clovers and their distribution in different parts harvested at different growing stages. J. Agric. Food. Chem., 54, 5797e5805. Tsutsui, K., & Ishii, S. (1978). Effects of follicle-stimulating hormone and testosterone on receptors of follicle-stimulating hormone in the testis of the immature Japanese quail. Gen. Comp. Endocrinol., 36, 297e305. Tsutsui, K., Bentley, G. E., Bedecarrats, G., Osugi, T., Ubuka, T., & Kriegsfeld, L. J. (2010). Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Front. Neuroendocrinol., 2010. Tsutsui, K., Kawashima, S., Saxena, R. N., & Ishii, S. (1992a). Annual changes in the binding of follicle-stimulating hormone to gonads and plasma gonadotropin concentrations in Indian weaver birds inhabiting the subtropical zone. Gen. Comp. Endocrinol., 88, 444e453. Tsutsui, K., Kawashima, S., Saxena, V. L., & Saxena, A. K. (1992b). Binding properties and photoperiodic influence of follicle-stimulating hormone receptors in the subtropical wild quail. Zool. Sci., 9, 649e657. Tsutsui, K., Saigoh, E., Ukena, K., Teranishi, H., Fujisawa, Y., Kikuchi, M., et al. (2000). A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem. Biophys. Res. Commun., 275, 661e667. Turk, J. R., Kim, J., & Gallina, A. M. (1981). Seminoma in a pigeon. Avian. Dis., 25, 752e755. Ubuka, T., Bentley, G. E., Ukena, K., Wingfield, J. C., & Tsutsui, K. (2005). Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain. Proc. Natl. Acad. Sci. USA, 102, 3052e3057. Underwood, H., Binkley, S., Siopes, T., & Mosher, K. (1984). Melatonin rhythms in the eyes, pineal bodies, and blood of Japanese quail (Coturnix coturnix japonica). Gen. Comp. Endocrinol., 56, 70e81. Urbanski, H. F., Fahy, M. M., & Collins, P. M. (1993). Influence of Nmethyl-D-aspartate on the reproductive axis of male Syrian hamsters. J. Endocrinol., 137, 247e252. Vajda, A. M., & Norris, D. O. (2006). In D. O. Norris, & J. A. Carr (Eds.), Endocrine Disruption: Biological Bases for Health Effects in Wildlife and Humans (pp. 390e423). New York, NY: Oxford University Press. Van Roo, B. L. (2004). Exogenous testosterone inhibits several forms of male parental behavior and stimulates song in a monogamous songbird: the blue-headed vireo (Vireo solitarius). Horm. Behav., 46, 678e683. Villarreal, L. Y. B., Brandao, P. E., Chacon, J. L., Assayag, M. S., Maiorka, P. C., Raffi, P., et al. (2007). Orchitis in roosters with reduced fertility associated with avian infectious bronchitis virus and avian metapneumovirus infections. Avian. Dis., 51, 900e904. Visser, M. E., Holleman, L. J. M., & Gienapp, P. (2006). Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia, 147, 164e172.

Chapter | 2

Avian Testicular Structure, Function, and Regulation

Vleck, C. M., & Priedkalns, J. (1985). Reproduction in zebra finchesdhormone levels and effect of dehydration. Condor, 87, 37e46. Voigt, C., Goymann, W., & Leitner, S. (2007). Green matters! Growing vegetation stimulates breeding under short-day conditions in wild canaries (Serinus canaria). J. Biol. Rhythms., 22, 554e557. Wade, J., Gong, A., & Arnold, A. P. (1997). Effects of embryonic estrogen on differentiation of the gonads and secondary sexual characteristics of male zebra finches. J. Exp. Zool., 278, 405e411. Wakabayashi, N., Suzuki, A., Hoshino, H., Nishimori, K., & Mizuno, S. (1997). The cDNA cloning and transient expression of a chicken gene encoding a follicle-stimulating hormone receptor. Gene, 197, 121e127. Wang, Z. P., Cheng, K. M., Brown, G. M., Pang, C. S., & Pang, S. F. (1992). Characterization of 2-[125I]iodomelatonin binding sites in quail testes at mid-light and mid-dark. Neurosci. Lett., 146, 195e198. Weatherhead, P. J., Metz, K. J., Bennett, G. F., & Irwin, R. E. (1993). Parasite faunas, testosterone and secondary sexual traits in male redwinged blackbirds. Behav. Ecol. Sociobiol., 33, 13e23. Westneat, D. F., & Stewart, I. R. K. (2003). Extra-pair paternity in birds: causes, correlates, and conflict. Annu. Rev. Ecol. Evol. Syst., 34, 365e396. Wikelski, M., Hau, M., Robinson, W. D., & Wingfield, J. C. (2003). Reproductive seasonality of seven neotropical passerine species. Condor, 105, 683e695. Wikelski, M., Hau, M., & Wingfield, J. C. (2000). Seasonality of reproduction in a neotropical rain forest bird. Ecology, 81, 2458e2472. Wilhelms, K. W., Scanes, C. G., & Anderson, L. L. (2006). Lack of estrogenic or antiestrogenic actions of soy isoflavones in an avian model: the Japanese quail. Poult. Sci., 85, 1885e1889. Willard, S. T., & Randel, R. D. (2002). Testicular morphology and sperm content relative to age, antler status and season in axis deer stags (Axis axis). Small. Ruminant. Res., 45, 51e60. Wilson, E. K., Rogler, J. C., & Erb, R. E. (1979). Effect of sexual experience, location, malnutrition, and repeated sampling on concentrations of testosterone in blood plasma of Gallus domesticus roosters. Poult. Sci., 58, 178e186. Wilson, F. E. (1991). Neither retinal nor pineal photoreceptors mediate photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea). J. Exper. Zool., 259, 117e127. Wilson, F. E., & Follett, B. K. (1978). Dissimilar effects of hemicastration on plasma LH and FSH in photostimulated tree sparrows (Spizella arborea). Gen. Comp. Endocrinol., 34, 251e255. Wilson, F. E., & Reinert, B. D. (1993). The thyroid and photoperiodic control of seasonal reproduction in American tree sparrows (Spizella arborea). J. Comp. Physiol. B: Biochem. Syst. Environ. Physiol., 163, 563e573. Wilson, W. O., Siopes, T. D., & Itho, S. (1972). Production of traits of leghorn pullets in controlled temperatures. Poult. Sci., 51, 1014. Wingfield, J. C. (1984). Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia. I. Temporal organization of the breeding cycle. Gen. Comp. Endocrinol., 56, 406e416. Wingfield, J. C. (2008). Comparative endocrinology, environment and global change. Gen. Comp. Endocrinol., 157, 207e216. Wingfield, J. C., & Hunt, K. E. (2002). Arctic spring: hormone-behavior interactions in a severe environment. Comp. Biochem. Physiol. B: Biochem. Molec. Biol., 132, 275e286. Wingfield, J. C., & Sapolsky, R. M. (2003). Reproduction and resistance to stress: when and how. J. Neuroendocrinol., 15, 711e724.

69

Wingfield, J. C., Smith, M. J., & Farner, D. S. (1982). Endocrine responses of white-crowned sparrows to environmental stress. Condor, 84, 399e409. Wingfield, J. C., Follett, B. K., Matt, K. S., & Farner, D. S. (1980). Effect of day length on plasma FSH and LH in castrated and intact whitecrowned sparrows. Gen. Comp. Endocrinol., 42, 464e470. Wingfield, J. C., Hegner, R. E., Dufty, A. M., & Ball, G. F. (1990). The challenge hypothesisdtheoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Amer. Nat., 136, 829e846. Wingfield, J. C., Hahn, T. P., Maney, D. L., Schoech, S. J., Wada, M., & Morton, M. L. (2003). Effects of temperature on photoperiodically induced reproductive development, circulating plasma luteinizing hormone and thyroid hormones, body mass, fat deposition and molt in mountain white-crowned sparrows, Zonotrichia leucophrys oriantha. Gen. Comp. Endocrinol., 131, 143e158. Wingfield, J. C., Hahn, T. P., Wada, M., Astheimer, L. B., & Schoech, S. (1996). Interrelationship of day length and temperature on the control of gonadal development, body mass, and fat score in white-crowned sparrows, Zonotrichia leucophrys gambelii. Gen. Comp. Endocrinol., 101, 242e255. Wingfield, J. C., Hahn, T. P., Wada, M., & Schoech, S. J. (1997). Effects of day length and temperature on gonadal development, body mass, and fat depots in white-crowned sparrows, Zonotrichia leucophrys pugetensis. Gen. Comp. Endocrinol., 107, 44e62. Woods, J. E., & Domm, L. V. (1966). A histochemical identification of androgen-producing cells in gonads of domestic fowl and albino rat. Gen. Comp. Endocrinol., 7, 559e570. Wright, J., & Cuthill, I. (1989). Manipulation of sex differences in parental care. Behav. Ecol. Sociobiol., 25, 171e181. Wynne-Edwards, K. E. (2001). Evolutionary biology of plant defenses against herbivory and their predictive implications for endocrine disruptor susceptibility in vertebrates. Environ. Health Perspect., 109, 443e448. Yamamoto, I., Kaiya, H., Tsutsui, C., Sakai, T., Tsukada, A., Miyazato, M., et al. (2008). Primary structure, tissue distribution, and biological activity of chicken motilin receptor. Gen. Comp. Endocrinol., 156, 509e514. Yamamoto, I., Tsukada, A., Saito, N., & Shimada, K. (2003). Profiles of mRNA expression of genes related to sex differentiation of the gonads in the chicken embryo. Poult. Sci., 82, 1462e1467. Yamamura, T., Yasuo, S., Hirunagi, K., Ebihara, S., & Yoshimura, T. (2006). T-3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail. Cell. Tissue. Res., 324, 175e179. Yang, P., Medan, M. S., Watanabe, G., & Taya, K. (2005). Developmental changes of plasma inhibin, gonadotropins, steroid hormones, and thyroid hormones in male and female shao ducks. Gen. Comp. Endocrinol., 143, 161e167. Yoshimura, T., Yasuo, S., Watanabe, M., Iigo, M., Yamamura, T., Hirunagi, K., & Ebihara, S. (2003). Light-induced hormone conversion of T-4 to T-3 regulates photoperiodic response of gonads in birds. Nature, 426, 178e181. Young, K. A., Ball, G. F., & Nelson, R. J. (2001). Photoperiod-induced testicular apoptosis in European starlings (Sturnus vulgaris). Biol. Reprod., 64, 706e713. Yu, Z. H. (1998). Asymmetrical testicular weights in mammals, birds, reptiles and amphibian. Int. J. Androl, 21, 53e55.

70

Zann, R. A., Morton, S. R., Jones, K. R., & Burley, N. T. (1995). The timing of breeding by zebra finches in relation to rainfall in central Australia. Emu, 95, 208e222. Zhou, J. F., Zadworny, D., Guemene, D., & Kuhnlein, U. (1996). Molecular cloning, tissue distribution, and expression of the prolactin

Hormones and Reproduction of Vertebrates

receptor during various reproductive states in Meleagris gallopavo. Biol. Reprod., 55, 1081e1090. Zlotnik, I. (1947). The cytoplasmic components of germ cells during spermatogenesis in the domestic fowl. Quat. J. Morphol. Sci., 88, 353e365.

Chapter 3

Organization and Functional Dynamics of the Avian Ovary A.L. Johnson The Pennsylvania State University, University Park, PA, USA

SUMMARY The development of avian ovarian follicles at the beginning of the reproductive season is followed by atresia and reabsorption of all growing follicles at the termination of breeding. This seasonal cyclicity is postulated to be an adaptation to minimize the metabolic cost of flight and reduce the risk of predation. A distinct hierarchy of growing and, in particular, preovulatory follicles enables multiple yolk-filled ova to be sequentially ovulated and fertilized over a series of days prior to the initiation of egg incubation. The species-specific number of eggs laid (the clutch size) ideally represents an attribute that, given adequate resources, enables the female and/or male parent to adequately nurture each offspring with an optimal investment of energy. This chapter provides an updated integration of endocrine, paracrine, and autocrine factors (including associated cell-signaling mechanisms) regulating the organization and adaptive functions of the avian ovary. Moreover, several evolved features are considered in context with the avian ovary’s origin from the reptilian lineage of vertebrates, and are compared to those described within the extant synapsid (therian mammal) lineage.

1. THE AVIAN OVARY The avian ovary evolved from that of an ancestral sauropsid (reptilian) lineage, and its derived features reflect characteristics adaptive for seasonal breeding and flight. As would be expected for an animal group numbering approximately 10 000 species, there is considerable variability in reproductive strategies and behaviors. Nevertheless, the fundamental organization and function of the ovary among avian species studied in any detail is largely conserved, and Aves represents the only vertebrate class in which viviparity does not exist in some form. A comparison of avian hormone actions and cell signaling processes that regulate avian ovarian function and follicle differentiation with those from extant sauropsids (e.g., turtles, lizards, and crocodilians) and synapsids (e.g., prototherian and therian mammals) enables informed assumptions regarding evolutionarily Hormones and Reproduction of Vertebrates, Volume 4dBirds Copyright Ó 2011 Elsevier Inc. All rights reserved.

conserved, convergent, or divergent characteristics. Two initial comparisons at the organismal level serve to illustrate this point. First, it is now well accepted that the avian lineage is derived from the archosaur clade, which includes crocodiles and nonavian dinosaurs. Although we know virtually nothing about nonavian dinosaur endocrinology or ovarian dynamics, we do know that at least some dinosaurs produced a clutch of eggs, much like a bird. Moreover, since there is evidence of medullary bone formation in dinosaurs but not in crocodiles (Schweitzer, Elsey, Dacke, Horner, & Lamm, 2006), it can be surmised that estrogenmediated medullary bone formation first evolved within the archosaur lineage, after the divergence of crocodilians. Second, based upon fundamental differences in ovarian morphology and the ovulatory cycle between birds and almost all mammals, it could be assumed that endocrine and cell-signaling mechanisms mediating follicular growth, selection, and development in extant species from the two lineages have divergently evolved. Notably, however, prototherians (e.g., the platypus and echidnas) represent a synapsid lineage separated from sauropsids some 315 million years ago, yet they maintain a combination of sauropsid plus mammalian reproductive characteristics. Among these is an avian-like ovary that produces one to three (depending upon the species) amniotic eggs per season. Given that the platypus genome encodes an eclectic combination of proteins found exclusively in birds (e.g., the egg envelope protein, ZPAX) or therian mammals (e.g., human zona pellucida proteins) (Warren, Hillier, & Graves, 2008), it is not untenable to predict that a number of plesiomorphic characteristics of ovarian function are well conserved between the sauropsid and synapsid lineages. An exhaustive comparison of ovarian physiological processes between avian species and the remaining vertebrate lineages is beyond the scope of the present chapter, and unfortunately there is little information derived from free-ranging wild birds and nonavian/nonmammalian amniotes. Nevertheless, there are several stages during 71

72

follicular development, specifically in birds vs. mammals, where sufficient published data exist to warrant speculation about conserved mechanisms regulating ovarian development and the expression of genes critical for follicular growth and maturation. Such comparisons also raise some unresolved questions regarding follicular development, and highlight key processes for which the avian ovary serves as an exceptional model system to extend our understanding of vertebrate ovarian function.

2. DEVELOPMENTAL DYNAMICS AND ORGANIZATION OF THE AVIAN OVARY The embryonic ovary begins morphological differentiation during the first third of incubation, and establishes the capacity to produce steroids prior to the functional maturation of the hypothalamicepituitaryegonadal axis. Estrogen synthesis mediated by aromatase (P450aro¼ CYP19) enzyme activity plays a key role in the differentiation of the female gonad, and differences between left vs. right ovarian development depend upon the selective expression of the estrogen receptor (ER) by the left ovary. The left ovary develops within the abdominal region immediately ventral to the caudal vena cava and adjacent to the kidney and adrenal gland. The growing ovary becomes suspended from the body wall by the mesovarium plus connective tissue (the hilus). This structure serves as a channel for vasculature, nervous tissues, and smooth muscle, each of which serves to integrate ovarian function with environmental and central nervous system input.

2.1. Organization of the Embryonic Ovary In the domestic hen, primordial germ cells (PGCs) can first be identified using the germline-specific marker, vasa homolog (cvh), following the first cleavage of fertilized eggs (Tsunekawa, Naito, Sakai, Nishida, & Noce, 2000). Primordial germ cells originate from within a central area of the blastoderm overlying the subgerminal cavity (the area pellucida), and subsequently migrate to the anterior border of the area pellucida (germinal crescent) after the first 18 hours of incubation. Maximal numbers of PGCs accumulated within this area prior to migration are estimated at 439 94 (Nakamura et al., 2007). A unique characteristic of both reptiles and birds is the use of the vascular system, compared to extravascular migration in most vertebrates, as a conduit to populating the germinal ridge of the presumptive gonad. In a fashion resembling the transendothelial migration of lymphocytes and macrophages, PGCs enter the blood vessels by diapedesis and migrate to the gonad after 50e55 hours of development. Primordial germ cells presumably exit the vasculature at the germinal ridge in response to chemotactic signals, including stromal cell-derived factor-1 (SDF-1) (Stebler

Hormones and Reproduction of Vertebrates

et al., 2004). In cultured mammalian PGCs, a variety of growth factors has been demonstrated to promote PGC proliferation and survival, including stem cell factor (SCF/c-kit ligand), leukemia-inhibitory factor (LIF), basic fibroblast growth factor (bFGF), pituitary adenylate cyclase-activating peptide (PACAP) and interleukin-4 (IL-4) (Kawase, Hashimoto, & Pedersen, 2004, and references therein). Both SCF and ciliary neurotrophic factor (CNTF) promote the proliferation of avian PGCs in vitro (Karagenc & Petitte, 2000). Although both follicle-stimulating hormone (FSH) treatment and estradiol (E2) treatment, in ovo or of embryonic day 18 ovarian explant cultures, is also reported to increase the total number of PGCs in the developing chick (Xie, Zhang, Zeng, & Mi, 2004), it is likely that FSH actions are mediated via paracrine factors and/or steroids produced by ovarian medullary cells, rather than by a direct effect on the germ cells. The total number of primary oocytes within the domestic chick (Gallus domesticus) ovary increases from an estimated 28 000 on the ninth day of incubation to 680 000 on the seventeenth day, then decreases to 480 000 by the time of hatching or shortly thereafter. Only a small fraction of these oocytes (200e500) subsequently develops to the preovulatory stage within the lifespan of most domesticated species, and considerably fewer mature to this stage in wild species. Recently, methods to isolate and culture avian PGCs in vitro have been described (Van de Lavoir et al., 2006). Such technology provides the first opportunity to genetically modify avian PGCs to enable the generation of transgenic birds, much like is currently available in mice. This advancement promises to have agricultural and biomedical implications, as well as to re-establish the avian embryo as a premier animal model system for the study of developmental biology. Sex in birds is genetically determined at the time of fertilization, with the female characterized by sex chromosome heterogamety (ZW) and the male by homogamety (ZZ). Although the SRY gene located on the Y chromosome of mammals represents a primary ‘switch’ for testis determination, a likely candidate for sex determination in nonmammalian vertebrates is the dmrt1 gene. In birds, dmrt1 maps to the Z chromosome and DMRT1 protein is expressed in the testes of ZZ males at higher levels during the critical period of morphologic sex determination (Ferguson-Smith, 2007). To date, however, the mechanisms by which either syr or dmrt1 gene products direct sex determination remain unclear. Significantly, in-ovo knockdown of dmrt1 mRNA during early development using RNA interference selectively reduced DMRT1 protein expression and resulted in the feminization of genetically male gonads (Smith et al., 2009). Among the downstream effects attributed to a reduction in Dmrt1 expression are enhanced foxl2 (implicated in ovarian development) and cyp19 expression, plus downregulation

Chapter | 3

Organization and Functional Dynamics of the Avian Ovary

of sox9 (a conserved and important gene mediating testis formation in vertebrates) expression. Collectively, these findings provide strong support for Dmrt1 as a key sex-determination gene in birds, but do not necessarily eliminate the possible influence by additional W-chromosome-linked genes. Despite the prediction that genetic sex determination should produce an approximately equal ratio of female : male offspring, it is well-documented that adjustments in the sex ratio occur under a range of developmental and ecological conditions. Prior to ovulation and fertilization, epigenetic modifications of sex chromosomes may, in part, account for such sex bias (Rutkowska & Badyaev, 2008). Such epigenetic modifications may effect a direct influence on the segregation of sex chromosomes after the completion of the first meiotic division. Although temperaturedependent sex determination is common in reptiles, there is currently no information available to indicate that incubation temperature directly influences the primary sex ratio of birds. Nevertheless, some species of megapodes (order Galliformes, family Megapodiidae) that deposit their eggs within mounds of dirt or rotting vegetation (similar to crocodilians) produce a greater proportion of females at hatch when incubation occurs at higher than normal temperatures. This temperature-dependent sex bias, however, is proposed to occur as a result of increased male mortality (Goth & Booth, 2004). During embryogenesis, the avian ovary begins development as paired organs, but in most species it is only the left ovary that develops and is functional by the time of hatch. Prior to sexual differentiation (initiated during the first third of embryonic development), both presumptive ovaries contain cortical and medullary tissues. Embryonic ovarian medullary tissue contains both steroidogenic interstitial cells and adrenergic innervation, yet the adulttype distribution of extrinsic and intrinsic nervous tissue is not fully established until after hatch. The left ovary develops mostly from the cortex, whereas bilateral development of Sertoli and Leydig cells in testes occurs from the medulla. Several studies have demonstrated an early requirement for estrogen synthesis within medullary tissue for normal ovarian development, and that phenotypic sex reversal of genetic males can be affected by E2 administration prior to sexual differentiation. Although estrogen receptor-a (ERa) is initially expressed in cortical tissue of both ovaries, regression of the right ovary subsequent to the initiation of sexual differentiation ultimately results from the loss of ERa expression, and, thus, from the lack of estrogen responsiveness (Smith & Sinclair, 2004). Recent results attribute ERa loss to a selective expression of a homeobox gene, pitx2, within the left presumptive ovary (Ishimaru et al., 2008). Such expression drives the asymmetric expression of a retinoic acidsynthesizing enzyme, raldh2, in the right presumptive

73

ovary, which in turn terminates local expression of the nuclear receptors, era and ad4bp/sf-1. Significantly, the continued expression of ad4bp/sf-1 in the left ovary is required to promote cortical cell proliferation. The presence of two functional ovaries is maintained in approximately 5% of bird species (e.g., kiwi, some falcons, eagles, and vultures), yet even in such species some size asymmetry and difference in ovulation frequency often exists between the two ovaries. The presence of two functional ovaries presumably represents a primitive sauropsid characteristic that is found in most extant reptiles, including crocodilians. Much critical information about molecular components regulating the development of the avian ovary can be derived from a comparison of species exhibiting one vs. two functional gonads, yet such studies have yet to be reported.

2.2. Postembryonic Development of the Ovary Females in many reptilian species maintain mitotically active oogonial stem cells throughout their reproductive lifespan, and these cells are maintained within discrete germinal beds derived from the ovarian epithelium. The total number of germinal beds established may be positively correlated with clutch size among different reptilian species (Radder, Pizzatto, & Shine, 2008). By comparison, it is traditionally accepted that all oogonia in birds and mammals are arrested in meiotic prophase I by the end of embryogenesis and a proportion of these subsequently become organized into primordial follicles. The adaptive features of a finite (compared to a renewable) germ pool in female birds and mammals are not clear, although it is possible that this trait is associated with a general reduction in the number of offspring produced and increased parental care per reproductive cycle. Interestingly, the concept that adult female mammals are born with a fixed pool of oocytes has recently been challenged (Johnson, Canning, Kaneko, Pru, & Tilly, 2004). Results of these dogma-challenging studies in mice led to the hypothesis that new oocytes can be generated from an intraovarian site following chemotherapeutic depletion of existing germ cells. Such oocytes may be derived from residual germ stem cells residing within the ovary, or may be transformed from circulating stem cells and nurtured by germ cell niches (e.g., resident follicles) (Lee et al., 2007). Nevertheless, these studies remain to be confirmed, and, although there are significant conservation and economical implications of the potential for postnatal oocyte renewal in avian species, comparable studies have not been reported. The arrangement of developing follicles within the ovary differs significantly between birds and placental

74

mammals such that, in the former, growing follicles protrude from ovarian stromal tissue and are suspended by a pedicle, whereas in the latter all follicles remain within the cortical tissue and encased within a common surface epithelium. During the first weeks following hatch, oocytes are primarily embedded within the well-vascularized cortical tissue, but a limited number remain within the ovarian medulla. As a developing follicle grows out from the cortex, blood vessels reach the thecal layer via the pedicle. The stigma (site of ovulation) represents a region of reduced stromal tissue containing a limited microcapillary system within the innermost portion of the follicular wall. The avian ovary also contains both efferent and afferent nerve fibers. Although small follicles initially contain no extrinsic nerve fibers, innervation by adrenergic and cholinergic fibers is initiated as development progresses. These fibers enter the follicle via the pedicle, and ultrastructural studies in mature follicles demonstrate that the majority of thecal cells are eventually contacted by nerve fibers. It has been established that such innervation provides a variety of neurochemicals (e.g., catecholamines, dopamine, serotonin) and neurohumoral factors (e.g., neurotropins, vasoactive intestinal peptide, substance P) to the developing follicles. These neurosecretions have been implicated in diverse roles such as regulation of steroidogenesis in the embryonic ovary, the organization and initial recruitment of primordial follicles, the differentiation of growing follicles, and, eventually, the process of ovulation (Bahr, Ritzhaupt, McCullough, Arbogast, & Ben-Jonathan, 1986; Jensen & Johnson, 2001). The length of time required to reach sexual maturation depends upon the species, and is determined by both physiology and environmental cues. Domesticated female Japanese quail (Coturnix japonica) are hatched in a precocial state and may begin breeding within weeks after hatch. However, most wild species attain sexual maturity only during the following breeding season. The inability of juvenile European starlings (Sturnis vulgaris), partridges (Alectoris spp.), and white-crowned sparrows (Zonatrichia leucophrys) to develop reproductive responsiveness during the season in which they are hatched is presumably due to a photorefractory state, much like in the photorefractory adult (Section 3). Larger birds, such as penguins, condors, and albatrosses, may take five to ten years to reach sexual maturity, and even then some species may not breed every year. Although the reasons for a late onset to sexual maturity are not entirely understood, there is a strong correlation to longevity of adult survival and increased body size. Accordingly, large birds are predicted to require a longer time for somatic and physiological maturation, whereas the frequency of breeding may be limited by habitat, food availability, and energetic constraints (Jouventin & Dobson, 2002).

Hormones and Reproduction of Vertebrates

2.3. Endocrine, Paracrine, and Autocrine Factors Regulating Ovarian Function There is considerable information from a variety of avian species regarding the various hormones that influence the initial development or seasonal recrudescence of the ovary together with the growth and differentiation of follicles. The predominance of information from wild (often freeranging) species consists of circulating levels of hormones or hormones sequestered within egg yolk, but most data describing ovarian production of paracrine and autocrine factors plus the cell-signaling and molecular mechanisms mediating follicular growth and differentiation have been generated from domesticated species (e.g., Japanese quail (C. japonica), chickens, and domesticated ducks and geese). Some of these endocrine and neuroendocrine factors are synthesized at a site other than the ovary and are transported to the ovary via the circulatory or nervous systems, whereas others are produced by ovarian tissues and act in a paracrine or autocrine fashion.

2.3.1. Protein hormones Among the most important anterior pituitary hormones that act at the level of the ovary are the gonadotropins (GTHs): FSH and luteinizing hormone (LH). Although circulating concentrations of FSH and LH remain low during the nonbreeding season, levels of FSH gradually rise with an increase in photoperiod associated with the onset of the breeding season. The threshold for the length of photoperiod required to promote increasing FSH secretion is less than that for LH. Thus, photoperiod-induced LH secretion is delayed relative to FSH but the eventual increase in LH occurs more rapidly (Sharp, Dawson, & Lea, 1998). Initial increasing concentrations of circulating FSH are required to support early follicular growth and to maintain the viability of slow-growing follicles. Circulating levels of LH during the breeding season are capable of promoting steroidogenesis by the thecal layer throughout follicular development. By contrast, cells within the granulosa layer are responsive to LH only in the most mature (preovulatory) follicles, and this responsiveness is associated with the initial expression of a functional LH receptor (LHR). The hormones and associated cell-signaling pathways responsible for regulating FSH receptor (FSHR) and LHR expression in granulosa cells during follicular development are discussed in Section 4. Circulating concentrations of prolactin (PRL) in adult females gradually increase during the breeding season, and reach maximal levels at the termination of breeding even as the daylength continues to increase (Sharp & Blache, 2003). Prolactin receptor mRNA and specific binding occur within both the hypothalamus and the ovarian tissues, and prolonged elevated blood levels of PRL promote

Chapter | 3

Organization and Functional Dynamics of the Avian Ovary

photorefractoriness, initiate incubation behavior (broodiness), and attenuate ovarian steroidogenesis. Prolactin’s inhibitory effects on steroidogenesis occur both indirectly via its ability to decrease pituitary LH secretion and directly by inhibiting ovarian steroid enzyme gene expression (Tabibzadeh et al., 1995). A gene encoding the precursor protein for gonadotropininhibiting hormone (GnIH) has been isolated from the hypothalamus of several avian species (Bentley, Perfito, Ukena, Tsutsui, & Wingfield, 2003; Ikemoto & Park, 2005). Although a primary role ascribed to gonadotropin-releasing hormone (GnRH) is the seasonal inhibition of pituitary LH secretion, the GnIH receptor is also expressed in both the thecal and granulosa layers of the hen ovary (Maddineni, Ocon-Grove, Krzysik-Walker, Hendricks, & Ramachandran, 2008). This receptor has been characterized as a Gaicoupled receptor that is reported to inhibit adenylyl cyclase activity. Given that the GnIH receptor is expressed at highest levels in the ovary of sexually immature (vs. reproductively active) chickens and in prehierarchical (vs. preovulatory) follicles, it will be of significance to evaluate the potential role of GnIH in follicular development and, in particular, granulosa cell differentiation. Similarly, there are several reports of GnRH expression and potential function within the mammalian ovary; however, related studies have yet to be reported for the avian ovary. Neurons containing vasoactive intestinal peptide (VIP) permeate the theca interna and externa layers, and may play an active role in maintaining steroid secretion and viability of the follicle (Johnson, Li, Gibney, & Malamed, 1994). Granulosa and thecal tissues from the avian ovary also contain measurable levels of immunoreactive oxytocin and mesotocin, yet it is not clear whether these are of neurohypophysial origin or are synthesized locally. The actions of these factors have been associated with both ovulation and oviposition. There is an ever-increasing number of growth factors and cytokines plus their associated receptors expressed in ovarian somatic cells and the oocyte. Generalizations about their actions according to major growth factor families are outlined here, whereas more specific actions are detailed later (Section 4). Members of the epidermal growth factor (EGF) family include EGF, transforming growth factor-a (TGFa), betacellulin, epiregulin, amphiregulins, and neuregulins. All of these growth factors, together with their receptors (ErbB1, Erb2, and ErbB4), are expressed within various tissues of the hen ovary. The primary cell-signaling pathways activated following ligand-receptor binding include mitogen-activated protein kinases (MAPK) and protein kinase B (Akt). Important actions of these factors within the avian ovary include their ability to promote proliferation, prevent apoptotic death, and block differentiation in somatic cells. Additional factors associated with the inhibition of granulosa

75

cell differentiation early in follicular development include bone morphogenetic proteins (BMPs). Bone morphogenetic proteins comprise a subfamily from the larger TGFb superfamily of growth factors that act by promoting the dimerization of BMP type II receptor (BMPRII) with BMP type I receptor (BMPRI), and cell signaling via the nuclear transcription factors (TFs) Smad1, Smad5, and Smad8. Each of these signaling components is expressed in the hen ovary and is activated by the receptor-mediated phosphorylation of Smad proteins (Onagbesan, Bruggeman, & Decuypere, 2008). Generally opposing the actions of EGF-family and BMP-family ligands in the hen ovary are members of the TGFb subfamily (the prototype being TGFb1) and the activin/inhibin subfamily members. These paracrine/autocrine factors help promote a differentiated granulosa cell phenotype by initiating the dimerization of type I (e.g., Alk4, Alk5) with type II serine/threonine kinase receptors, which results in the phosphorylation of Smad2 and Smad3 TFs (Johnson & Woods, 2008). Inhibins A and B are produced and secreted by both differentiated preovulatory follicles and undifferentiated prehierarchical follicles (Johnson, Brooks, & Davis, 2005). A primary action for the inhibins is to provide negative feedback on hypophysial FSH secretion. Anti-Mu¨llerian hormone (AMH) (also known as Mu¨llerian-inhibiting substance) represents yet another member of the TGFb superfamily that was originally identified in the embryonic gonad. Anti-Mu¨llerian hormone mRNA is expressed in the embryonic gonad by day five of incubation, with male embryos expressing higher levels than females. A function for AMH during sexual differentiation is to promote the selective regression of the right Mu¨llerian duct in females, plus the regression of both Mu¨llerian ducts in male birds. Following sexual maturation, AMH is selectively expressed by the granulosa layer of small growing follicles and is proposed to regulate early follicular development (Johnson, Kent, Urick, & Giles, 2008). Finally, both BMP15 and growth and differentiating factor-9 (GDF9) are selectively expressed by the oocyte, and each has been implicated in negatively regulating granulosa cell steroidogenesis at various stages of follicular development (Johnson, Dickens, Kent, & Giles, 2005; Elis et al., 2007). Insulin-like growth factor (IGF)-1 and IGF2, together with the type 1 IGF receptor (IGFR), are expressed in both the granulosa and thecal layers throughout follicular development. The thecal layer from preovulatory follicles represents a major source of IGFs, whereas the IGFR is most abundant in the granulosa layer from preovulatory follicles. Insulin-like growth factor signaling occurs predominantly via the intracellular Akt/phosphatidylinositol 3-kinase (PI3K) signaling pathway, and has been implicated in promoting granulosa cell survival, proliferation, and differentiation (Onagbesan et al., 1999).

76

There are several cytokines belonging to the tumor necrosis factor superfamily (TNFSF) expressed in the hen ovary, together with the associated family of TNFSF receptors (TNFSFRs). Among the related ligands and receptors characterized thus far are tumor necrosis factor-a (TNFa, or TNFSF1), which signals via its receptor (TNFRSF1A); TNF-related apoptosis-inducing ligand (TRAIL, or TNFSF10), signaling via TNFRSF10A; and Fas ligand (FasL, or TNFSF6) via TNFSFR6 (Bridgham, Wilder, Hollocher, & Johnson, 2003; Johnson & Woods, 2007). Actions of these cytokines are often associated with mediating follicle atresia, in part, by inducing apoptosis in granulosa cells (Section 4). Finally, no fewer than six interleukins plus interferon-g are expressed within the granulosa and thecal layers of the most mature (F1) follicle and in postovulatory follicles. Their reported actions have been associated with regression of the postovulatory follicle and involution of the ovary during molt (Sundaresan et al., 2007; 2008).

2.3.2. Steroids and steroidogenesis The developing chick embryo begins to express the key enzymes responsible for steroidogenesis and to synthesize measurable amounts of steroids within the first week of incubation (Bruggemn, Van As, & Decuypere, 2002). Studies conducted in vitro demonstrate that the type of steroids and quantities produced by day six of incubation are dependent upon the sex of the embryo. For instance, genetic males produce higher levels of testosterone (T) than females, whereas genetic females selectively express P450aro and synthesize estradiol-17b (E2). Following hatch, the production of ovarian steroids remains relatively low and nonresponsive to gonadotropin treatment up to the beginning of sexual maturation. Circulating concentrations of E2 increase two to three weeks before the onset of lay (at approximately 21 weeks of age), whereas levels of progesterone (P4) begin to increase about one week prior to lay. At sexual maturation, growing primary follicles attain competence to produce the quantity and diversity of steroids required for initiating the development of the reproductive tract. In the reproductively active hen, slow-growing, nonvitellogenic follicles produce no measurable P4, but represent a major source of androgens and E2 (Robinson & Etches, 1986). In free-range white-crowned sparrows, circulating levels of estrogens increase shortly after the female arrives at the breeding area (Jacobs & Wingfield, 2000). Enhanced circulating levels of estrogens at the start of the reproductive season are responsible for stimulating the synthesis of vitellogenin and very-low-density lipoprotein by the liver. The increase in plasma E2 preceding egg production in the starling is associated with increasing levels of plasma vitellogenin (Williams, Kitaysky, &

Hormones and Reproduction of Vertebrates

Vezina, 2004). An avian-unique function for estrogens is the development of medullary bone, which serves as a labile source of calcium during eggshell formation (Whitehead, 2004). Unlike other vertebrates, which reabsorb calcium from cortical or endochondral bone, birds mobilize large amounts of calcium for eggshell formation directly from endosteal cavities within the long bones. In preovulatory follicles, the granulosa layer is the primary source of P4 production whereas the inner thecal layer (theca interna) produces androgens but limited amounts of P4. The outer thecal layer (theca externa) produces predominantly androgens and is the sole site of P450aro enzyme expression for the production of estrogens (Nitta, Osawa, & Bahr, 1991). Steroidogenesis in the ovary is stimulated primarily by circulating GTHs (LH, and to a lesser extent FSH) that promote cell signaling via cyclic adenosine monophosphate (cAMP). In turn, ovarian steroids serve to negatively feed back on the secretion of GnRH from the median eminence and/or LH secretion from the pituitary. The classical mechanism for steroid signaling involves intracellular receptors that act as ligand-dependent transcription factors that promote changes in gene expression. In addition to genomic mechanisms, steroids also act through nongenomic (nonclassical) mechanisms. Nongenomic effects are generally more rapid, occur at membrane and cytoplasmic levels, and are not sensitive to transcription and protein synthesis inhibitors. Nonclassical signaling mechanisms include interactions of steroids with ion channels, g-aminobutyric acid (GABA) receptors, and a variety of growth factor and neurotransmitter receptors coupled to G-proteins. Unfortunately, unlike the classical steroid receptors, little work has been conducted in birds to describe the identity or actions of nongenomic steroid receptors. In growing follicles prior to selection, the thecal layer expresses significantly higher levels of LH receptor (mRNA and binding capacity) and functional FSH receptor compared to thecal tissue from preovulatory follicles. By comparison, granulosa cells from prehierarchical follicles express significantly higher levels of FSH receptor mRNA (vs. granulosa from preovulatory follicles) but are largely incapable of synthesizing the P4 precursor, pregnenolone. The latter is related to low levels of cAMP formation, cytochrome P450 side-chain cleavage (P450scc ¼ CYP11A1) activity and steroidogenic acute regulatory (StAR) protein expression (Johnson & Bridgham, 2001; Tilly, Kowalski, & Johnson, 1991). It is noteworthy that StAR protein, which is prerequisite for cholesterol transport to the site of P450scc within the inner mitochondrial membrane, is highly conserved among vertebrate species (Bauer, Bridgham, Langenau, Johnson, & Goetz, 2000). The induction of both P450scc and StAR protein in granulosa cells is dependent upon cAMP signaling. The process

Chapter | 3

Organization and Functional Dynamics of the Avian Ovary

of follicular selection and final differentiation initiates the transition of FSHR dominance to LHR dominance and the capacity for significant amounts of LH-induced P4 production by the granulosa layer (Section 4). Steroids also represent potent mediators of pre- and postnatal maternal effects. Exposure to these hormones during early development can influence the behavior of offspring long after hatch. Among the maternal-derived steroids deposited in the egg yolk of preovulatory follicles are corticosterone (CORT), androstenedione, T, and E2. There are a number of consequences attributed to varied levels of yolk steroids both during and after incubation, and only a few examples are provided here (see also Chapter 4, this volume). In the European starling, yolk concentrations of maternal-derived CORT are reported to increase with each successive egg laid within a clutch. Higher concentrations of this ‘stress hormone’ in eggs laid late in the clutch are predicted to result in a smaller body size at hatch, and such hatchlings are more likely to be outcompeted by larger offspring when resources are limited. This hormonal mechanism for brood reduction serves to ensure the quality of surviving offspring (Love, Wynne-Edwards, Bond, & Williams, 2008). Similarly, differences in the quantity of yolk androgens have been associated with levels of aggression, competitiveness, increased early growth, and survival (see Groothuis, Muller, Von Engelhardt, Carere, & Eising, 2005). In the zebra finch (Taeniopygia guttata), greater amounts of yolk T are found in female (compared to male) eggs produced under suboptimal conditions (e.g., poor physical condition of the mother or eggs laid late in the clutch). These findings suggest that the mother may utilize yolk androgens to enhance the fitness of these developing female embryos (Gilbert, Rutstein, Hazon, & Graves, 2005). Although some investigators have proposed that differences in the ratio of androgen : estrogen within the yolk represent a nongenetic mechanism to influence the secondary sex ratio, results from a more recent study in Japanese quail fail to support this (Pitz, Adkins-Regan, & Schwabl, 2005).

2.3.3. Prostaglandins and thyroid hormones Several prostaglandins (e.g., PGE1, PGE2, PGF2a), plus their synthetic enzymes (e.g., phospholipase A2, cyclooxygenase, lipoxygenase) have been found in various ovarian tissues. Prostaglandins of ovarian origin have been implicated in a variety of functions, including the modulation of steroidogenesis and cell viability, granulosa cell mitosis, plus the process of oviposition. Circulating thyroid hormones have long been implicated in female seasonal reproduction, as thyroidectomy is known to inhibit ovarian growth in response to long days (Wilson & Reinert, 1999). In general, levels of thyroxine (T4) and triiodothyronine (T3) in free-ranging birds

77

increase during the breeding season and reach peak levels at its termination (Wingfield & Farner, 1993). Although the localized synthesis and actions of T3 within the medial basal hypothalamus have been directly linked to the photoperiodic response of the gonads (Section 3), direct actions within the avian ovary have been less studied. Both T4 and T3 are transferred from the maternal system to the yolk of preovulatory follicles, and these may influence selected growth parameters (including early brain development) prior to the maturation of the embryonic hypothalamic/hypophysial/thyroid axis (Darras, Van Herck, Geysens, & Reyns, 2008).

2.3.4. Innate and adaptive immunity in ovarian tissues Recent studies provide evidence for both a functional innate (nonspecific) and an adaptive (cell-mediated) immune response in the avian ovary, and in particular within developing ovarian follicles. A rapid activation of the innate immune system occurs within follicular tissues when exposed to pathogens (e.g., Salmonella) that express pathogen-associated molecular patterns (PAMPs) (e.g., lipopolysaccharides or mannose) on their outer cell wall. Among the cellular endpoints for this ancient and evolutionarily conserved form of immunity are initiation of the complement cascade, induction of an inflammatory response by cytokines, and activation of the adaptive immune system. An innate response is mediated via constitutively expressed pattern-recognition receptors (PRRs), such as toll-like receptors (TLRs) and mannose receptors. Components of the innate immune system identified within the hen ovary include five different TLRs (TLR-2, TLR-4, TLR-5, TLR-7, and TLR-15), together with their intracellular adaptor molecules (e.g., MyD88, TOLLIP, IRAK4, TRAF6) (Subdei, Isobe, Nishibori, & Yoshimuri, 2007a; Woods, Schorey, & Johnson, 2009) and associated cell-signaling pathways (nuclear factor-kB (NFkB) and MAPK). Notably, TLR activation of NFkB and MAPK signaling leads to enhanced transcription of proinflammatory cytokines (e.g., interleukins, interferon-g, TNFa) and anti-microbial b-defensins (e.g., gallinacin-1, -2, -7, -8, -10, -12) (Subedi, Isobe, Nishibori, & Yoshimuri, 2007b). Included among the functional endpoints attributed to activation of the innate immune system are induction of granulosa cell apoptosis, modulation of steroidogenesis, and protection of follicular tissues from invasive pathogens. Cell-mediated immunity represents a complementary element for neutralizing pathogenic agents within the ovary. In contrast to innate immunity, the adaptive immune response entails antigen-specific activation and clonal expansion of B and T lymphocytes, yet initial activation of adaptive immunity requires several days or longer. Initiation of this response occurs via activation of T helper (CD4

78

antigen-positive) cells and T cytotoxic (CD8 antigenpositive) cells, which reside within ovarian stromal tissue and the thecal layer of ovarian follicles (Yoshimura, 2004). As in mammals, the presentation of major histocompatibility complex (MHC) class I and class II molecules by antigen-presenting cells (APCs) activates T helper cells and T cytotoxic cells, respectively. In turn, T helper cells promote the maturation of B (immunoglobulin-producing) cells, whereas activated T cytotoxic cells directly promote pathogen cytolysis. Studies of the domestic hen ovary have found that numbers of MHC class IIþ APC, T helper cells, T cytotoxic cells, and B cells in stroma and thecal tissues increase with sexual maturation then decline with advancing age. These findings provide an association between a functional cell-mediated immune system and adult fertility. By contrast, autoimmune responses to ovarian tissues may be associated with declining fertility. To date, the ability of ovarian paracrine and autocrine factors to modulate a local immune response has not been extensively investigated. Sequestration of maternal-derived IgY within the egg yolk during follicular development results in the passive transmission of immunity to the developing embryo. Levels of IgY deposited in the yolk have been reported to decline with increasing age of the female (Yoshimura, 2004). Significantly, the quantity of immunoglobulin deposited in eggs of free-ranging barn swallows (Hirundo rustica) has been associated with the reproductive value of the offspring (Saino et al., 2002), as enhanced levels of antibody transfer presumably provide such offspring with a selective advantage to posthatch survival. In summary, studies to date provide convincing evidence that both the innate and adaptive immune systems serve roles in regulating ovarian function and follicular development, as well as providing protection to adults and their offspring against microbial infection.

3. REPRODUCTIVE SEASONALITY Relatively few avian species are capable of exhibiting breeding activity outside of some defined period within the year. Even within this period, the time of breeding may be very predictable or remain quite flexible and dependent upon adequate resources (e.g., opportunistic breeders). Most, if not all, birds are considered to be photoperiodic to at least some extent, and to possess an endogenous circannual rhythm of reproduction that is synchronized and modified by external environmental cues. Although seasonal growth of the ovary is stimulated in almost all species by increasing photoperiod, there are only a few species known to initiate reproductive activity during a season of deceasing or short (less than 12 hours L) photoperiod (e.g., emperor penguin (Aptenodytes forsteri); crossbills (Loxia spp.). No doubt this is largely a reflection

Hormones and Reproduction of Vertebrates

of the seasonal availability of food resources required for raising offspring. It is now widely accepted that a central pacemaker clock serves as an underlying mechanism mediating the photoperiodic response of the ovary and testes in both birds and mammals (Yoshimura, 2006; see also Chapter 1, this volume). Whereas in mammals the retina is the sole site of photoreception, birds are capable of perceiving light via both ocular and extraocular photoreceptors. Accumulating evidence in several avian species points to the medial basal hypothalamus (MBH) as the critical site where photoperiodic input intersects with a central circadian clock. Specifically, a circadian clock consists of positive and negative transcriptional feedback loops that drive transcription of clock genes (e.g., clock, per2, per3, bmal1, cry1, cry2). In male Japanese quail, clock genes within the MBH (but not the suprachiasmatic nucleus or pineal gland) maintain approximately 24-hour rhythms of expression under both stimulatory (16 hours light (L) : 8 hours dark (D) and nonstimulatory (8L : 16D) photoperiods (Yasou, Watanabe, Okabayashi, Ebihara, & Yoshimura, 2003). Based upon such data, it is proposed that a clock located within the MBH serves to maintain a steady-state photoinducible phase by which photoperiod is measured. Among the possible target genes upregulated by the photoperiodic MBH clock is that encoding type 2 iodothyronine deiodinase (dio2), which converts the prohormone T4 to its active form, T3 (Yoshimura et al., 2003). The photoperiodinduced increase in T3 localized within the MBH of male Japanese quail is hypothesized to rapidly (within hours) enhance GnRH secretion. This proposed model is supported by the observations that the T3 content in the MBH is 10-fold greater under long vs. short days, and that intracerebroventricular injection of T3 mimics the photoperiodic-induced growth of the gonads (Yasou et al., 2005). Evidence for an MBH-localized clock in male Japanese quail can explain the photoinducible phase associated with the initiation of seasonal breeding, yet this remains to be tested in females.

3.1. Environmental Cues Mediating Ovarian Growth Considering avian species studied to date, photoperiod is no doubt the ultimate factor that is most widely utilized to reinitiate the slow growth phase of follicular development at the beginning of each breeding season. Seasonal breeders from temperate environments typically demonstrate annual phases of photosensitivity (responsive but not yet stimulated by an appropriate photoperiod), photostimulation (reproductively active), followed by photorefractoriness (unable to respond to changes in photoperiod). Such species initially respond to increasing day length with

Chapter | 3

Organization and Functional Dynamics of the Avian Ovary

increased hypothalamic secretion of GnRH followed by increased circulating levels of FSH and eventually LH. In Japanese quail, the increase in GnRH secretion occurs within the first day of photostimulation. The initial development of the ovary culminates after approximately six weeks, when ovarian mass becomes enlarged and follicles typically reach a size of 1 to 5 mm in diameter (depending upon species) but do not synthesize appreciable amounts of steroids. Subsequently, proximal factors (e.g., quality and abundance of food or nesting sites, temperature, or interactions with a male) are required to initiate follicular selection and the establishment of the preovulatory hierarchy (Jacobs & Wingfield, 2000). For example, exposure to male song alone augments the rate of follicular differentiation in white-crowned sparrows. By comparison, birds that breed under tropical (low latitude) conditions often demonstrate less rigidity in regards to a photoperiodic response. Although seasonal breeding is initially cued by a minimal (often less than one hour) change in photoperiod, it is more strongly influenced by supplementary information for the exact timing of ovarian growth and follicular maturation (Hau, 2001). In contrast to the eloquent model offered to explain photoperiodic sensitivity via the hypothalamus (Yoshimura, 2006), mechanisms describing how nonphotoperiodic cues stimulate gonadal development are poorly understood. Species that live in regions where environmental changes are much less predictable or entirely unpredictable lack appropriate proximal factors to cue ovarian recrudescence in a timely fashion. Accordingly, such species must opportunistically respond to environmental cues in a fashion that ensures the coincidence of fertility with optimal breeding and rearing conditions. The classical definition of an opportunistic breeder is one that shows no predictable changes in gonadal function relative to time of year and maintains a continuous capacity for reproduction. Recent studies, however, have questioned this strict definition for some avian (?) species. For instance, an example of an archetypal opportunistic breeder is the zebra finch, which has adapted to arid regions of Australia. Female finches inhabiting arid areas where rainfall is unpredictable are reported to undergo ovarian growth beginning shortly after hatch and continuing throughout the first 100 days. Thereafter, the developing ovarian follicles enter an indefinite resting stage where, following an appropriate cue (e.g., rainfall), selected follicles enter the rapid growth phase and ovulation occurs within one to two weeks. The precocious ovarian development observed in the zebra finch following hatch is attributed to the absence of any detectable photorefractory period. However, female finches inhabiting a semiarid area where seasonal changes are more predictable demonstrate seasonal cycles of development and regression. These findings are interpreted as reflecting considerable plasticity in the responsiveness to

79

environmental conditions among finch populations (Hahn et al., 2008). Similarly, crossbills inhabit extreme northern latitudes where local availability of their primary food source, conifer seeds, widely varies from year to year. Crossbills are responsive to both ultimate (e.g., increasing photoperiod) and proximate (e.g., food availability and social) cues. Ovarian development can occur during the winter months given adequate food or a mating stimulus. Nevertheless, ovarian regression does occur in response to the stimulatory effects of long days, presumably in response to elevated PRL levels in late summer (Deviche & Sharp, 2001; Hahn et al., 2008). Gonadal growth is subsequently reinitiated under conditions of short photoperiod during the fall months.

3.2. OvulationeOviposition Cycles In contrast to the estrous or menstrual cycles of mammals, the avian ovulationeoviposition cycle recurs on an approximately daily basis until a species-specific clutch size is produced. This pattern of a single ovulation closely followed by oviposition also differs from turtles, many oviparous lizards, and crocodilians. In these latter groups, multiple follicles are simultaneously ovulated, then subsequently oviposited as a single event. Among avian species, oviposition typically follows ovulation by some 24 hours (most species) to 48 hours (e.g., ostrich), and always occurs prior to the next ovulation. A notable exception to this interval length is the kiwi (Apteryx mantelli), with an ovulation to oviposition period of seven to ten days (Jensen & Durrant, 2006). The Indonesian maleo (Macrocephalon maleo), which buries its eggs in geothermally or solar-heated soil for incubation, displays the longest observed interval between laying successive eggs (10 to 12 days). Differing clutch sizes among various species of bird, or within a species populating areas with differing amounts and qualities of resources, are postulated to reflect the maximal number of offspring that they can successfully nurture. This optimal number ideally reflects both the potential within a clutch plus for lifetime reproductive success (Lack’s hypothesis). Larger birds generally lay fewer eggs per clutch compared to smaller birds. Subarctic and arctic nesting species tend to have larger clutch sizes than tropical-breeding species because the availability of food in northern latitudes is short-lived and there is sufficient time for only a single nesting. In lesser snow geese (Anser caerulescens) which breed in the arctic, it has been proposed that the clutch size can be adjusted to the female’s nutrient reserve plane at a time just before or at the onset of laying. This adjustment occurs by the reabsorption (atresia) of one or more less mature preovulatory follicles, and assures adequate development of the remaining follicles

80

plus a favorable nutrient plane for the mother during nesting. It is predicted that the loss of potential offspring is offset by a higher probability of successful fledging. By comparison, clutch size is typically smaller in tropical and subtropical birds compared to those in temperate northern climates, despite the prediction that abundant food availability in tropical regions should provide for optimal egg laying. It has been proposed that higher rates of nest predation in subtropical regions limit the rate at which parent birds can provide food to the nestlings; thus, clutch size tends to be smaller. Alternative, and not necessarily mutually exclusive, hypotheses implicate physiological constraints (e.g., large clutches place more physiological strain on females than small clutches) plus seasonal and habitat constraints as factors regulating clutch size in subtropical species. Clutch size can also differ relative to the age of the female and the time within the breeding season when eggs are laid. For example, both the size and number of eggs laid is observed to increase with age, and the largest improvement occurs between the first and second breeding seasons. In starlings, this increase in performance subsequent to the first year is associated with a greater number of hypothalamic GnRH fibers, a greater amount of vitellogenin production, and consequent increased ovarian follicular diameter in females that have experienced a prior period of photostimulation (Sockman, Williams, Daeson, & Ball, 2004). In species that lay a single clutch per season, females that initiate reproduction early in the season produce more eggs compared to those laying eggs late in the season. It is reasoned that the seasonal decline in clutch size may reflect a reduction in late-season habitat resources, which are required for the successful rearing of offspring. A potential endocrine mechanism that may, at least in part, mediate this reduction in the number of eggs occurs via the inhibitory effects of PRL on follicular development (Sockman, Sharp, & Schwabl, 2006). Many species produce a single clutch per season (determinant layers; e.g., white pelican (Pelecanus erythrorrhynchos); blue-winged teal (Anas discors); barn swallow (H. rustica)). Others, including many tropical species, produce more than one clutch or extend laying within a clutch, particularly if the clutch is destroyed or the first eggs of the clutch are removed (indeterminate layers; e.g., European starling; song sparrow (Melospiza melodia); common flicker (Colaptes auratus); barn owl (Tyto alba)). There is evidence that the extension of a clutch in indeterminate breeders can be accomplished by the rescue of small preovulatory follicles from atresia, rather than the selection of additional follicles into the preovulatory hierarchy. Following hatch there may occur further modifications in the number of offspring reared. For instance, the common coot (Fulica atra) can hatch up to 10 eggs per clutch but in the absence of adequate food resources will

Hormones and Reproduction of Vertebrates

aggressively attack one or more young that beg for food until they eventually starve to death.

3.3. Regression of the Ovary During the Photorefractory Period and Molt The final stage of the annual reproductive cycle consists of photorefractoriness, a state where the reproductive system no longer responds to changes in photoperiodic or supplemental cues. Absolute photorefractoriness is analogous to the prepubertal state, and both states are associated with a very low synthesis and content of hypothalamic GnRH. The consequence of this is the absence of ovarian support by circulating GTHs. In starlings, a transition towards photorefractoriness begins when the photoperiod exceeds 12L : 12D and corresponds to a time when circulating concentrations of PRL are increasing. Peak concentrations of circulating PRL in starlings coincide with the onset of ovarian regression. This photorefractory state is terminated by a short photoperiod (less than 12L : 12D) for some critical interval of time, after which GnRH production and eventually secretion can be renewed. By comparison, relative photorefractoriness, such as occurs in quail, entails the regression of the ovary, but there is no marked decline in hypothalamic GnRH. Thus, recrudescence can occur during continued exposure to this photoperiod (Dawson, 2008). There is some evidence that nonphotoperiodic cues (temperature, social cues, and food availability) can affect the timing of the onset of photorefractoriness, but no evidence that such cues can influence the termination of photorefractoriness. Associated with photorefractoriness and regression of the ovary is the process of molt. This represents the replacement of old feathers with new, and is an important but energetically costly endeavor. Accordingly, the timing of molt is such that it does not overlap with reproduction or migration. The increased circulating concentrations of both PRL and thyroid hormones associated with the termination of ovarian function are also implicated in the induction of molt.

4. FOLLICULAR DEVELOPMENT Following the onset of puberty, the reproductively active avian ovary contains follicles at all stages of development. These include resting primordial follicles, slow-growing primary follicles, a smaller cohort of fully organized prehierarchical follicles, plus a hierarchy of preovulatory follicles with increasing amounts of yellow yolk. The preovulatory hierarchy enables a single ovulation on successive days for the length of a clutch. The avian follicular hierarchy is a reflection of its archosaur lineage, which includes some dinosaurs (Sato, Cheng, Wu, Zelenitsky, & Hsiao, 2005). This pattern of ovulation

Chapter | 3

Organization and Functional Dynamics of the Avian Ovary

differentiates the avian ovary from its mammalian counterpart in that viviparity necessitates the simultaneous ovulation of multiple mature follicles. As previously noted, the seasonal reproductive process is energetically expensive and is associated with an increase in the female’s resting metabolic rate. Much of this energy is invested in the vitellogenic (preovulatory) stage of egg production. Total metabolic expenditures involved in egg production are dependent upon the rate and duration of preovulatory follicular growth and clutch size.

4.1. Primordial Follicular Reserve and Initial Recruitment Within a few days of hatch, PGCs become organized into primordial follicles via the recruitment of a single somatic (presumptive granulosa) cell layer. Any remaining PGCs that fail to become enclosed die via apoptosis. Prior to hatch, the primary oocyte becomes arrested in prophase of the first meiotic division and remains in arrest until shortly before ovulation. Primordial follicles have the potential to survive in an arrested state of development for years, and remain embedded within the vascularized cortex of the ovary. Although the molecular mechanisms by which avian primordial follicles are maintained in this arrested state have apparently not been studied, a recent study in mice provides evidence for direct inhibition of initial recruitment via the PI3K signaling pathway. This signaling pathway is activated specifically within the oocyte (Reddy et al., 2008). The transition from primordial to primary follicle represents the initial recruitment stage, when follicles initiate slow growth and begin to emerge from the ovarian cortex. In the near-continuously laying hen, this earliest growth phase can progress over months to several years, and generally represents an increase in follicle size to up to 1 mm in diameter. This early growth is primarily attributed to the increased size of the oocyte as it accumulates increasing amounts of cytoplasm. Cells of mesenchymal origin (presumptive theca) are recruited by one or more factors secreted by the follicle to initiate the formation of a peripheral thecal layer. The granulosa and thecal layers are anatomically separated by a basement membrane (the basal lamina) that precludes the granulosa from receiving either a direct blood supply or contacting nervous tissue. The basal lamina consists of fibronectin, collagen, and laminin, and expresses integrins that may actively mediate signaling to the granulosa layer (Asem, Qin, & Rane, 2002). In mammals, factors implicated in the organization of the thecal layer include SCF, BMPs, LIF, and TGFb synthesized by the granulosa layer, plus GDF9 and basic FGF produced by the oocyte (Knight & Glister, 2006). As noted earlier, these factors are expressed in avian granulosa

81

cells or the oocyte during early follicular development, and are predicted to have homologous actions in the avian ovary. Similarly, AMH is highly expressed specifically within the granulosa layer from hen primary follicles, and its expression decreases at a time coincident with follicular selection (Johnson, P.A. et al., 2008). Accordingly, the production of AMH from primary follicles may serve to negatively regulate the selection of prehierarchical follicles into the preovulatory hierarchy. Although the growth of primary follicles is thought to occur largely independently of GTHs, the viability of follicles remains dependent upon the support of both GTH and growth factors. During early organization of the follicle, the single-cellthick layer of granulosa expands to accommodate follicular growth and cells become interconnected by desmosomes, tight junctions, and gap junctions. A perivitelline membrane, produced by the granulosa, largely separates this cell layer from the oocyte; however, granulosa cells project macrovilli through the perivitelline membrane to make contact with the surrounded oocyte. The initial layer of thecal cells subsequently differentiates into morphologically and functionally distinct theca interna and externa layers. Beginning with this phase of development, the oocyte begins to accumulate aggregated spheres of white yolk. Continued support for the viability of most slowgrowing and prehierarchical follicles during the reproductive season is important particularly for indeterminate and opportunistic breeders in which undifferentiated follicles must be maintained for periods lasting for weeks to months. Eventually, the slow growth of primary follicles terminates in the formation of a relatively small cohort of prehierarchical follicles. In the domestic hen, follicles within this cohort measure approximately 6 to 8 mm in diameter and generally number 8 to 20. It is from this cohort that a single follicle becomes recruited into a rapid growth phase on an approximately daily basis for final differentiation prior to ovulation. The development of cryopreservation techniques for the long-term storage of avian ova has been largely unsuccessful, primarily as a result of the characteristic accumulation of yolk within the avian germ cell plus its intimate association with the granulosa layer. Unlike the demonstrated success of cryopreservation in a variety of mammals, this shortcoming in birds limits the ability to preserve valuable genetic resources. As a possible alternative to frozen ova, recent studies demonstrated that ovarian cortical tissues orthotopically transplanted from donor to recipient within 24 hours of hatch resulted in the production of fertile eggs and viable offspring derived from the donor tissue (Song & Silversides, 2007). Success of this technique at this early stage of development is attributed to the absence of a competent immune response plus the ability of transplanted cortical tissues to develop the requisite ovarian vasculature from the recipient.

82

4.2. Follicular Selection The process of follicular selection (also referred to as cyclic recruitment) represents the rate-limiting stage for the development of mature ovulable oocytes. Thus, this process ultimately determines the reproductive capacity for vertebrate species the strategy of which emphasizes a limited number of offspring combined with significant parental investment (as compared to most bony fish and amphibians). The proximate factors and cell-signaling pathways responsible for the selection of a follicle destined for ovulation have yet to be fully defined in any vertebrate species. In monovular mammals (e.g., women, cows, and mares), the earliest markers of a recently selected follicle are increased follicular diameter and elevated FSHR mRNA levels within the granulosa layer. In such species the selective ability to maintain FSH-induced signaling in the face of declining concentrations of circulating FSH subsequently promotes a shift from FSHR to LHR dominance within the granulosa layer, followed by final differentiation. By contrast, the fate of all subordinate (nonselected) follicles is atresia (Milm & Evans, 2008). Yet, it is abundantly clear that elevated FSHR expression in the selected follicle represents the result, and not the proximal cause, of selection. In the domestic hen, the ability of a single prehierarchical follicle to be selected into the preovulatory hierarchy is similarly associated with elevated expression of FSHR within the granulosa layer. Recent work has focused on developing working models to describe (1) inhibitory signals and transcriptional mechanisms that normally preclude premature selection of more than one prehierarchical follicle per day and (2) transcriptional mechanisms that selectively promote FSHR and LHR expression in the selected follicle (reviewed in Johnson & Woods, 2008). Only a brief synopsis of these evolving concepts is presented here. Although the granulosa layer from all prehierarchical follicles expresses some level of FSHR, the comparatively low levels of receptor-activated cAMP generated (compared to the most recently selected follicle) are apparently not sufficient to initiate granulosa-cell differentiation (e.g., induced expression of LHR or StAR proteins). Nevertheless, treatment with TGFb1 or activin A in vitro induces a small increase in levels of FSHR mRNA expression, yet this stimulatory effect is effectively blocked by epidermal growth factor ligands (EGFLs) via MAPK/ extracellular regulated kinase (Erk) signaling. Moreover, granulosa cells from prehierarchical follicles, in situ, demonstrate elevated MAPK signaling compared to granulosa from differentiated follicles (Woods, Haugen, & Johnson, 2007). More recent data show that BMP2 and GDF9 (signaling via Smad1/5/8) can also block granulosa cell differentiation via a MAPK-dependent pathway.

Hormones and Reproduction of Vertebrates

Collectively, these findings provide evidence that the increase in FSHR mRNA levels within the single selected follicle can occur only following the alleviation of inhibitory signaling (Figure 3.1). As a consequence of a selective reduction in MAPK signaling, enhanced FSHR-induced cAMP signaling is sufficient to initiate the transition to a differentiated preovulatory follicle. Notably, this concept that follicular selection is enabled by the release from inhibitory mechanisms is similar to that proposed for the process of initial recruitment in mice (Reddy et al., 2008). Recent studies in mammals have described binding of the TFs upstream stimulatory factor-1 (USF1) and USF2 to the FSHR promoter region as a prerequisite for maximal FSHR mRNA transcription (Hermann, Hornbaker, Rice, Sawadogo, & Heckert, 2008). These TFs represent members of the basic helix-loop-helix (bHLH) family, which bind to an E-box promoter site characterized by the canonical nucleic acid sequence CANNTG. Importantly, the formation of bHLH hetero- or homodimers is required to enable proteineDNA promoter binding. Included within the bHLH family of TFs are the inhibitor of differentiation/ DNA binding (Id) proteins (Id isoforms 1e4), which lack a DNA-binding domain. Consequently, Id proteins can serve as dominant-negative inhibitors of transcription by heterodimerizing with bHLH family transcription-activating factors and preventing their binding to E-box sites. Significantly, analysis of the Gallus FSHR promoter sequence has identified a number of putative E-box sites plus several putative Smad binding elements (SBEs)

FIGURE 3.1 Working model for cell-signaling mechanisms proposed to prevent premature differentiation of granulosa cells from prehierarchical follicles. Epidermal growth factor family ligands (EGFRLs) and bone morphogenetic proteins (BMPs) (including BMP2 and growth and differentiation factor-9 (GDF9)) bind to their cognate receptors to activate mitogen-activated protein kinase (MAPK) and phosphorylate extracellular regulated kinase (Erk-P) or phosphorylate Smad (Smad-P; specifically, Smad-1, -5, or -8), respectively. These inhibitory signals mediate the active suppression of follicle-stimulating hormone receptor (FSHR) transcription. cAMP, cyclic adenosine monophosphate. Adapted from Johnson and Woods (2008). See color plate section.

Chapter | 3

Organization and Functional Dynamics of the Avian Ovary

(capable of mediating the stimulatory actions of TGFb1 and activin) within the first several hundred bases of the predicted start codon. Levels of Id1, Id3, and Id4 mRNA expression are highest in undifferentiated granulosa cells from prehierarchical follicles compared to actively differentiating granulosa from recently selected (9e12 mm) follicles and differentiated granulosa from preovulatory follicles. In addition, the expression of Id1, Id3, and Id4 mRNA is rapidly upregulated by MAPK/Erk signaling, whereas levels of each Id protein are rapidly decreased following inhibition of MAPK/Erk signaling. These data provide initial evidence that EGFLs negatively regulate FSHR mRNA expression in prehierarchical follicles by enhancing Id1, Id3, and/or Id4 dimerization with, and inhibiting the transcriptional activity of, one or more bHLH TFs (Johnson et al., 2008). As noted above, BMP2 and GDF9 also block granulosa cell differentiation, and this is attributed to their ability to induce Id1, Id3, and Id4 expression plus expression of the EGFLs: EGF and BTC. Finally, BMP15 derived from the oocyte, plus BMP4, -6, -7, and AMH from the granulosa and/or thecal layer, have also been reported to block granulosa cell differentiation (reviewed by Onagbesan et al., 2008). It is predicted that the inhibitory actions of these factors are also mediated via induced expression of EGFLs and/or Id1, Id3, and Id4 proteins. A model depicting transcriptional mechanisms that inhibit FSHR mRNA expression in prehierarchical follicles is presented in Figure 3.2. Although the proximal mechanism(s) responsible for the release from inhibitory signaling at the time of follicular selection have yet to be identified, it is predicted that the cue signaling follicular selection will involve a local ovarian clock (see Section 4.6).

4.3. Preovulatory Follicular Growth and Final Differentiation Immediately subsequent to follicular selection, enhanced FSHR-mediated cAMP signaling within the granulosa layer provides for the initial upregulation of LHR expression (Johnson & Bridgham, 2001). The transition from FSHR to LHR dominance represents the stage at which granulosa cells begin to produce increasing large amounts of P4. Results from a series of in-vitro studies provide evidence that increased transcription of FSHR and LHR mRNA during this period is dependent upon enhanced expression of the bHLH protein Id2. In contrast to Id1, Id3, and Id4 (discussed above), Id2 expression is inhibited by both MAPK/Erk and Smad1, -5, and -8 signaling, but is upregulated by enhanced cAMP signaling. This implies that during the initial stages of differentiation (e.g., following the suppression of inhibitory signaling) there exists a stimulatory feedback loop consisting of gradually

83

FIGURE 3.2 Epidermal growth factor family ligand (EGFL)-, bone morphogenetic protein-2 (BMP2)-, and growth and differentiation factor-9 (GDF9)-induced expression of Id1, Id3, and/or Id4 proteins (Id) prevents the binding of basic helix-loop-helix (bHLH) transcription factors (TFs) to an E-box site (canonical sequence, CANNTG) within the folliclestimulating hormone receptor (FSHR) promoter region. In the absence of transcriptional activator binding to the E-box site, transforming growth factor-b (TGFb)- and activin-induced Smad2 binding to Smad binding elements (SBEs) fails to fully potentiate FSHR mRNA transcription. As a consequence, FSHR-mediated cyclic adenosine monophosphate (cAMP) formation and signaling is maintained at relatively low levels. See text for additional details. See color plate section.

increasing Id2 expression, enhanced FSHR expression, and consequent cAMP signaling. At the same time, cAMP signaling decreases expression of Id1, Id3, and Id4 (Johnson & Woods, 2008). The transition from expression of Id1, Id3, and Id4 to predominant Id2 expression coincident with follicular selection enables fully potentiated FHSR transcription. The increased capacity for FSHRmediated cAMP formation initiates LHR expression shortly thereafter. Although the regulatory factor targeted by Id2 binding has not yet been identified, it is proposed that Id2 may heterodimerize with a corepressor of FSHR (and possibly LHR) transcription. Proposed mechanisms promoting FSHR transcription in recently selected follicles are presented in Figure 3.3. The preovulatory phase represents the terminal stage of follicular development, when the most rapid and dramatic growth occurs. The number of follicles recruited into the preovulatory hierarchy of any given species is often associated with the female’s size and the number of eggs produced within a clutch. Of particular note is the kiwi, which has perhaps the largest egg-to-body ratio and the most yolk as a percentage of total egg weight (61%) among birds. In this species, the rapid growth phase of a single follicle is estimated to occur over some 15 to 17 days and results in an egg size of some 80þ mm. Combined with

84

FIGURE 3.3 Following an alleviation of inhibitory signaling via epidermal growth factor family ligands (EGFLs) and bone morphogenetic proteins (BMPs), levels of Id1, Id3, and Id4 rapidly decrease due to the loss of supportive signaling (not depicted). The decrease in Id1, Id3, and Id4 levels enables one or more basic helix-loop-helix (bHLH) transcription factors (TFs) to bind the follicle-stimulating hormone receptor (FSHR) promoter to enable enhanced FSHR expression (Johnson, Haugen, & Woods, 2008). As a result, increasing cyclic adenosine monophosphate (cAMP) formation stimulates upregulation of Id2 protein. It is proposed that Id2 indirectly promotes FSHR mRNA transcription by preventing a corepressor (CoR) from attenuating promoter activity. Collectively, these actions enable transforming growth factor-b (TGFb) and activin (acting via Smad2 binding to a Smad binding element (SBE)) to fully potentiate FSHR transcription. Enhanced levels of FSHR generate the increasing amounts of cAMP required to initiate luteinizing hormone receptor (LHR) expression (not depicted). GDF9, growth and differentiation factor-9. See color plate section.

a 70- to 90-day incubation period, these adaptive characteristics enable the kiwi embryo to hatch at a precocial state of development (Jensen & Durrant, 2006). In a variety of species studied, the number of preovulatory follicles initiating yolk deposition commonly exceeds the number of eggs laid within the clutch, and the fate of these nonovulated follicles is atresia. The volume of a recently selected preovulatory follicle rapidly increases due to yolk incorporation. To accommodate this growth, granulosa cells proliferate from the site of the germinal disc. The oocyte nucleus, together with 99% of the oocyte organelles, resides within the germinal disc region, and it is here that one or more paracrine factors produced by the oocyte (including BMP15 and GDF9) are secreted to promote a localized proliferation of granulosa cells. Consequently, granulosa within the germinal disc region remain proliferative but undifferentiated, whereas granulosa distal to the germinal disc undergo differentiation (e.g., are LHR-dominant) but are largely nonproliferative (Yao & Bahr, 2001). With the expansion of the

Hormones and Reproduction of Vertebrates

granulosa layer, cells distal to the germinal disc undergo remodeling to become flattened and less densely packed due to a reduction of cell-to-cell connections (tight junctions) (Schuster, Schmierer, Shkumatava, & Kuchler, 2004). This reduction of tight junctions facilitates the paracellular transport of some 2 g of yolk per day into domestic hen preovulatory oocytes. The incorporation of lipid-rich yellow yolk by the oocyte is accomplished by receptor-mediated endocytosis of vitellogenin (Vtg) and very-low-density lipoprotein (VLDL). The receptor responsible is a 95 kDa transmembrane protein designated as LR8 (gene designated as Gallus gallus VLDLR). Interestingly, a point mutation of this gene in a strain of chickens (known as ‘restricted ovulator’) results in the laying of only a very limited number of small, yolk-deficient eggs. Further, an alternatively spliced VLDLR variant encoding a 28-amino-acid Olinked sugar domain (LR8þ) and a 515 kDa low-density lipoprotein receptor (LRP1) are expressed by follicle somatic cells, and are responsible for supplying lowdensity lipoprotein (LDL)-derived cholesterol as a precursor for steroid production (Schneider, 2009). Increased production of the yolk precursors Vtg and VLDL by the liver occurs in response to increasing concentrations of estrogen produced by the thecal layer from developing follicles. The rate and consistency of yolk incorporation into the oocyte varies according to a diurnal rhythm, as evidenced by the presence of concentric rings of deposition. This banding corresponds to daily patterns of feeding and yolk synthesis by the liver, as wide yellow bands are laid down during the day and narrower white bands during the night. The total energetic costs of yolk formation can account for 40 to 50% of the bird’s daily energy budget, and the extra energy required results in a 13 to 41% increase in basal metabolic rate in passerines, and more than a 200% increase in some waterfowl (Meijer & Drent, 1999). Preovulatory follicles also accumulate maternal mRNA, primarily within the germinal disc region. A variety of translated products derived from these mRNAs are associated with promoting fertilization plus early zygote viability and development prior to activation of the embryonic genome (Muscarella, Rachlinski, & Bloom, 1998; Malewska & Olszanska, 1999).

4.4. Ovulation The preovulatory surge of LH is a primary stimulus for the initiation of both meiotic maturation within the oocyte and the process of ovulation. In avian species studied to date, peak circulating levels of LH typically precede ovulation by four to six hours. In contrast to mammals, there is no apparent increase in circulating FSH coincident with the preovulatory LH surge (Krishnan, Proudman, Bolt, & Bahr,

Chapter | 3

Organization and Functional Dynamics of the Avian Ovary

1993). The preovulatory LH surge does, however, occur coincidently with increased secretion of P4, particularly from the largest (F1) preovulatory follicle. Studies conducted in vivo have demonstrated a stimulatory interaction between LH and P4 such that in the absence of P4 secretion a fully potentiated LH surge fails to occur (Johnson & Van Tienhoven, 1984). Comparable studies of circulating GTHs and gonadal steroids during the hours immediately prior to ovulation have apparently not been reported in free-ranging birds. Nevertheless, there is no obvious reason to propose marked deviations from the patterns observed in domesticated birds, other than perhaps in the timing or magnitude of hormone concentrations. Mechanisms responsible for timing the LH surge and ovulation in birds have been the topic of study for decades, and conventional models predict that the primary signals involve interactions between a central circadian clock (likely located within the MBH; Section 3) and hormonal events regulating follicle development. Mating-induced GTH release and ovulation (reflex ovulation) occur in a select few mammals, lizards, snakes, and turtles, yet this characteristic has apparently not been reported for any avian species. The necessity for precise synchrony between ovulation and fertilization is largely obviated by the presence of sperm storage glands within the avian reproductive tract. Initiation of germinal vesicle breakdown (e.g., condensation of chromatin, extrusion of the first polar body, and formation of the second maturation spindle) selectively occurs in the largest (F1) preovulatory follicle and precedes ovulation by one to two hours (Yoshimura, Okamoto, & Tamura, 1993). A recent study identified an oocyte-localized mRNA transcript (chkmos) encoding the chicken homolog of mammalian mos. The protein product of this gene is required for meiotic maturation in other vertebrates (Elis et al., 2008). Nevertheless, the complex interactions of mechanisms described to reinitiate meiosis in birds have not been studied to the same extent as in selected fishes, amphibians, and mammals. Hormonal factors directly implicated in these latter groups include GTHs, growth factors (e.g., amphiregulin, epiregulin), and ovarian steroids. Significantly, P4 is a primary steroid implicated in initiating meiotic maturation in a variety of nonavian vertebrates, and the F1 follicle produces significantly higher levels of P4 during the LH surge compared to lessmature follicles. This enhanced capacity for P4 production is related to particularly high levels of StAR expression specifically within the F1 follicle granulosa layer (Johnson & Bridgham, 2001). Rupture of the F1 follicle and the release of the oocyte at ovulation are facilitated by coordinated events localized within the stigma region. These include enzyme activation, physical forces brought about by smooth muscle contraction, and localized apoptosis. Unlike the mammalian corpus luteum, the avian postovulatory follicle (POF)

85

begins the process of reabsorption within the initial 24 hours following ovulation and rapidly becomes steroidogenically inactive. Regression of the POF may be aided by an infiltration of immune cells. Such cells may serve to enhance the rate of apoptotic cell death via the secretion of cytokines (Sundaresan et al., 2008). Factors secreted by the most recent POF exert a direct or indirect influence on oviduct contractility, as removal of the most recent POF results in delayed oviposition.

4.5. Follicular Atresia The loss of primary oocytes during late embryogenesis and of growing follicles at various stages of development is considered a normal physiological process that presumably ensures the greatest chance for producing fertilizable oocytes from surviving follicles. In the laying hen, it is estimated that greater than 90% of all primordial and growing follicles will eventually succumb to atresia, and that atresia occurs almost exclusively in follicles that have yet to reach the rapid growth (preovulatory) phase. In seasonally breeding birds, the incidence of atresia increases as the breeding season advances, with peak rates of atresia occurring at the time of nesting. Atresia in follicles already selected into the preovulatory hierarchy represents a mechanism with which to adjust the clutch size to the female’s nutrient reserve. Accordingly, the loss of a potential offspring would be balanced by a higher probability for the survival of remaining offspring (Hamann, Andrews, & Cooke, 1986). The loss of all growing follicles by atresia, together with the dramatic regression of the ovary at the termination of each breeding season, re-establishes more efficient flight and conserves metabolic resources required for incubation and rearing of offspring. The death and degeneration of yolk-filled preovulatory follicles is sometimes referred to as ‘bursting atresia.’ The large quantities of yolk are rapidly reabsorbed via lacunae within the thecal layer (aided by macrophages) following a breakdown of the basal lamina (Nili & Kelly, 1996). In all vertebrate species studied to date, the death of follicular tissues associated with atresia occurs via the process of apoptosis. The natural death of follicles associated with the termination of reproduction and with molt occurs following decreased secretion of supportive hormones and the consequent loss of antiapoptotic cell signaling. In avian follicles, granulosa and germ cell viability is attributed to GTHs, EGFLs, GDF9, BMP15, and IGFs signaling via protein kinase A/cAMP, MAPK/Erk, and/or protein kinase B/Akt. Apoptosis can also be actively induced from within the oocyte or follicular somatic cells (via intrinsic apoptotic pathways), or in response to other extracellular factors, such as cytokines, signaling through extracellular receptors (e.g., TNFRSF members that initiate extrinsic pathways). Once initiated, the connecting

86

gap junctions in granulosa cells are capable of rapidly disseminating apoptotic signals throughout the granulosa layer (Krysko, Mussche, Leybaert, & D’Herde, 2004). The cellular mechanisms mediating apoptosis comprise a complex cascade of intracellular signaling pathways that eventually leads to the activation of one or more caspase. In viable cells, these cell-death pathways are normally opposed by the expression of various antiapoptotic proteins, including members of the Bcl-2-related and inhibitor of apoptosis (IAP) protein families. For a comprehensive review of cell survival pathways plus extrinsic and intrinsic mechanisms mediating apoptosis in the avian ovary, see Johnson and Woods (2007).

4.6. Evidence for, and Proposed Functions of, a Local Ovarian Clock Ultimately, it is predicted that the ovulationeoviposition cycle in birds is regulated by interactions among a central circadian pacemaker within the MBH (Section 3), physiological systems controlling the rate of follicular maturation (e.g., endocrine, paracrine, and autocrine factors plus associated cell-signaling mechanisms), and a local ovarian clock. It has recently been demonstrated that the clockrelated genes per2, per3, clock, and bmal1 are each expressed in preovulatory follicles from Japanese quail (Nakao et al., 2007). In particular, Clock and Bmal proteins represent members of the bHLH family of transcription factors that bind to E-box enhancer binding sites within the promoter region. It was also determined that star gene transcription in granulosa cells is enhanced by Clock/Bmal binding to an E-box element within the StAR promoter region. Levels of per2 and per3 expression vary according to a 16L : 8D photoperiod in both the granulosa and thecal layers from preovulatory (but not prehierarchal) follicles. Moreover, the 24-hour profile of star mRNA expression in granulosa cells from the F1 follicle is in phase with that of per2. Collectively, these data provide initial evidence not only for a functional clock within the avian ovary but also for the role of this local clock in timing the enhanced production of P4 by the F1 follicle, which initiates meiotic maturation and is a prerequisite for ovulation.

5. SUMMARY The data summarized herein, together with phylogenetic comparisons presented and unresolved questions raised, emphasize the prominent role birds play in our understanding of vertebrate reproductive biology. Several of the most recent working models discussed (e.g., molecular clocks within the MBH and the ovary; proximal mechanisms mediating follicular selection) are based upon

Hormones and Reproduction of Vertebrates

information not currently available from other vertebrate species. Continued study of reproductive strategies and mechanisms regulating ovarian function over a broad range of species and encompassing different breeding strategies will enable avian biologists to better understand how biological rhythms, proximal and ultimate environmental cues, and endocrine/neuroendocrine factors intersect with local ovarian physiology to regulate annual breeding cycles. For instance, it is predicted that gene expression regulated by an ovarian clock (e.g., via clockregulated genes) serves to precisely ‘phase’ not only the centrally located ‘open period’ for ovulation but also the initial and cyclic recruitment phases of follicular development. Finally, studies of avian model systems contribute significantly to our general understanding of the vertebrate ovary, in that the avian ovary provides unique information about follicular growth and maturation in a vertebrate group that produces a limited number of offspring. Such information will inevitably contribute to the further development of methods that enhance fecundity in threatened and endangered species, and will help with identifying targets for addressing causes of subfertility or infertility in domesticated animals and in women.

ACKNOWLEDGEMENTS The author thanks Drs. D.C. Woods, J.T. Bridgham, and T. Jensen, and Ms. M.J. Haugen for their invaluable contributions to portions of the primary research discussed herein. These efforts were supported by funding from the National Science Foundation (IBN-0131185, IOB-0445949, and IOS-0968784), the National Institutes of Health (NIH HD-36095) and the United States Department of Agriculture (NRI 99-35203-7736).

ABBREVIATIONS Akt AMH APC bFGF bHLH BMP BMPRI BMPRII cAMP CNTF CORT CYP11A1 CYP19 E2 EGF EGFL ER ERa Erk

Protein kinase B Anti-Mu¨llerian hormone Antigen-presenting cells Basic fibroblast growth factor Basic helix-loop-helix Bone morphogenetic protein Bone morphogenetic protein type I receptor Bone morphogenetic protein type II receptor Cyclic adenosine monophosphate Ciliary neurotrophic factor Corticosterone See P450scc See P450aro Estradiol Epidermal growth factor Epidermal growth factor ligand Estrogen receptor Estrogen receptor-a Extracellular regulated kinase

Chapter | 3

FasL FGF FSH FSHR GABA GDF-9 GnIH GTH IAP Id IGF1 IGF2 IGFR IL-4 LDL LH LHR LIF MAPK MBH MHC NFkB P4 P450aro P450scc PACAP PAMP PG PGC PI3K POF PRL PRR SBE SCF SDF-1 StAR T T3 T4 TF TGF TLR TNFa TNFRSF1A TNFSF TNFSF1 TNFSF10 TNFSF6 TNFSFR TRAIL USF1 USF2 VIP VLDL Vtg ZPAX

Organization and Functional Dynamics of the Avian Ovary

Fas ligand Fibroblast growth factor Follicle-stimulating hormone Follicle-stimulating hormone receptor g-aminobutyric acid Growth differentiation factor-9 Gonadotropin-inhibiting hormone Gonadotropin Inhibitor of apoptosis Inhibitor of differentiation/DNA binding Insulin-like growth factor-1 Insulin-like growth factor-2 Type 1 insulin-like growth factor receptor Interleukin-4 Low-density lipoprotein Luteinizing hormone Luteinizing hormone receptor Leukemia-inhibitory factor Mitogen-activated protein kinase Medial basal hypothalamus Major histocompatibility complex Nuclear factor-kB Progesterone Aromatase P450 cholesterol side-chain cleavage Pituitary adenylate cyclase-activating polypeptide Pathogen-associated molecular pattern Prostaglandin Primordial germ cell Phosphatidylinositol 3-kinase Postovulatory follicle Prolactin Pattern-recognition receptor Smad binding element Stem cell factor Stromal cell-derived factor-1 Steroidogenic acute regulatory Testosterone Triiodothyronine Thyroxine Transcription factor Transforming growth factor Toll-like receptor Tumor necrosis factor-a Tumor necrosis factor-a receptor Tumor necrosis factor superfamily See TNFa See TRAIL See FasL Tumor necrosis factor superfamily receptor Tumor necrosis factor-related apoptosis-inducing ligand Upstream stimulatory factor-1 Upstream stimulatory factor-2 Vasoactive intestinal peptide Very-low-density lipoprotein Vitellogenin The egg envelope protein

87

REFERENCES Asem, E. K., Qin, W., & Rane, S. G. (2002). Effect of basal lamina of ovarian follicle on T- and L-type Ca2þ currents in differentiated granulosa cells. Am. J. Physiol. Endocrinol. Metab., 282, E184eE196. Bahr, J. M., Ritzhaupt, L. K., McCullough, S., Arbogast, L. A., & Ben-Jonathan, N. (1986). Catecholamine content of the preovulatory follicles of the domestic hen. Biol. Reprod., 34, 502e506. Bauer, M. J., Bridgham, J. T., Langenau, D. M., Johnson, A. L., & Goetz, F. W. (2000). Conservation of steroidogenic acute regulatory (StAR) protein structure and expression in vertebrates. Mol. Cell. Endocrinol., 168, 119e125. Bentley, G. E., Perfito, N., Ukena, K., Tsutsui, K., & Wingfield, J. C. (2003). Gonadotropin-inhibitory peptide in song sparrows (Melospiza melodia) in different reproductive conditions, and in house sparrows (Passer domesticus) relative to chicken-gonadoatropin-releasing hormone. J. Neuroendocrinol., 15, 794e802. Bridgham, J. T., Wilder, J. A., Hollocher, H., & Johnson, A. L. (2003). All in the family: evolutionary relationships among vertebrate death receptors. Cell Death Differ., 10, 19e25. Bruggeman, V., Van As, P., & Decuypere, E. (2002). Developmental endocrinology of the reproductive axis in the chicken embryo. Comp. Biochem. Physiol., 131, 839e846, Part A. Darras, V. M., Van Herck, S. L. J., Geysens, S., & Reyns, G. E. (2008). Involvement of thyroid hormones in chicken embryonic brain development. Gen. Comp. Endocrinol. doi: 10.1016/j.ygcen.2008.11.014. Dawson, A. (2008). Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability. Phil. Trans. R. Soc. B, 363, 1621e1633. Deviche, P., & Sharp, P. J. (2001). Reproductive endocrinology of a freeliving, opportunistically breeding passerine (white-winged crossbill, Loxia leucoptera). Gen. Comp. Endocrinol., 123, 268e279. Elis, S., Batellier, F., Couty, I., Balzergue, S., Martin-Magniette, M.-L., Monget, P., et al. (2008). Search for the genes involved in oocyte maturation and early embryo development in the hen. BMC Genomics, 9, 110e129. Elis, S., Dupont, J., Couty, I., Persani, L., Govoroun, M., Blebois, E., et al. (2007). Expression and biological effects of bone morphogenetic protein-15 in the hen ovary. J. Endocrinol., 194, 485e497. Ferguson-Smith, M. (2007). The evolution of sex chromosomes and sex determination in vertebrates and the key role of DMRT1. Sex. Dev., 1, 2e11. Gilbert, L., Rutstein, A. N., Hazon, N., & Graves, J. A. (2005). Sex-biased investment in yolk androgens depends on female quality and laying order in zebra finches (Taeniopygia guttata). Naturwissenschaften, 92, 178e181. Goth, A., & Booth, D. T. (2004). Temperature-dependent sex ratio in a bird. Biol. Lett. doi: 10.1098/rsbl.2004.0247. Groothuis, T. G. G., Muller, W., Von Engelhardt, N., Carere, C., & Eising, C. (2005). Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev., 29, 329e352. Hahn, T. P., Cornelius, J. M., Sewall, K. B., Kelsey, T. R., Hau, M., & Perfito, N. (2008). Environmental regulation of annual schedules in opportunistically-breeding songbirds: adaptive specializations or variations on a theme of white-crowned sparrow? Gen. Comp. Endocrinol., 157, 217e226.

88

Hamann, J., Andrews, B., & Cooke, F. (1986). The role of follicular atresia in inter- and intra-seasonal clutch size variation in lesser snow geese (Anser caerulescens caerulescens). J. Anim. Ecol., 55, 481e489. Hau, M. (2001). Timing of breeding in variable environments: tropical birds as model systems. Horm. Behav., 40, 281e290. Hermann, B. P., Hornbaker, K., Rice, D. A., Sawadogo, M., & Heckert, L. L. (2008). In-vivo regulation of FSH-receptor (Fshr) by the transcription factors USF1 and USF2 is cell specific. Endocrinology, 149, 5297e5306. Ikemoto, T., & Park, M. K. (2005). Chicken RFamide-related peptide (GnIH) and two distinct receptor subtypes: identification, molecular characterization, and evolutionary considerations. J. Reprod. Develop., 51, 359e377. Ishimaru, Y., Komatsu, T., Kasahara, M., Katoh-Fukui, Y., Ogawa, H., Toyama, Y., et al. (2008). Mechanism of asymmetric ovarian development in chick embryos. Development, 135, 677e685. Jacobs, J. D., & Wingfield, J. C. (2000). Endocrine control of life-cycle stages: a constraint on response to the environment. Condor, 102, 35e51. Jensen, T., & Durrant, B. (2006). Assessment of reproductive status and ovulation in female brown kiwi (Apteryx mantelli) using fecal steroids and ovarian follicle size. Zoo Biology, 25, 25e34. Jensen, T., & Johnson, A. L. (2001). Expression and function of brainderived neurotrophin factor and its receptor TrkB in hen ovarian follicles. J. Exp. Biol., 204, 2087e2095. Johnson, A. L., & Bridgham, J. T. (2001). Regulation of steroidogenic acute regulatory protein and luteinizing hormone receptor messenger ribonucleic acid in hen granulosa cells. Endocrinology, 142, 3116e3124. Johnson, A. L., Bridgham, J. T., Witty, J., & Tilly, J. L. (1996). Susceptibility of avian granulosa cells to apoptosis is dependent upon stage of follicle development and is related to endogenous levels of bclxlong gene expression. Endocrinology, 137, 2059e2066. Johnson, A. L., Li, Z., Gibney, J. A., & Malamed, S. (1994). Vasoactive intestinal peptide-induced expression of cytochrome P450 cholesterol side chain cleavage and 17a-hydroxylase enzyme activity in hen granulosa cells. Biol. Reprod., 51, 327e333. Johnson, A. L., Haugen, M. J., & Woods, D. C. (2008). Role for inhibitor of differentiation/deoxyribonucleic acid-binding (Id) proteins in granulosa cell differentiation. Endocrinology, 149, 3187e3195. Johnson, A. L., & Woods, D. C. (2007). Ovarian dynamics and follicle development. In B. G. M. Jamieson (Ed.), Reproductive Biology and Phylogeny of Birds, Vol. 6A (pp. 243e277). Enfield, NH: Science Publishers. Johnson, A. L., & Woods, D. C. (2008). Dynamics of avian follicle development: mechanisms of granulosa cell differentiation. Gen. Comp. Endocrinol. doi:10.1016/j.ygcen.2008.11.012. Johnson, A. L., & Van Tienhoven, A. (1984). Effects of aminoglutethimide on LH and steroid secretion, and ovulation in the hen, Gallus domesticus. Endocrinology, 114, 2276e2283. Johnson, J., Canning, J., Kaneko, T., Pru, J., & Tilly, J. L. (2004). Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature, 428, 145e150. Johnson, P. A., Brooks, C. F., & Davis, A. J. (2005a). Pattern of secretion of immunoreactive inhibin/activin subunits by avian granulosa cells. Gen Comp. Endocrinol., 141, 233e239.

Hormones and Reproduction of Vertebrates

Johnson, P. A., Dickens, M. J., Kent, T. R., & Giles, J. R. (2005b). Expression and function of growth and differentiation factor-9 in an oviparous species, Gallus domesticus. Biol. Reprod., 72, 1095e1100. Johnson, P. A., Kent, T. R., Urick, M. E., & Giles, J. R. (2008). Expression and regulation of anti-Mu¨llerian hormone in an oviparous species. Biol. Reprod., 78, 13e19. Jouventin, P., & Dobson, S. (2002). Why breed every other year? The case of albatrosses. Proc. R. Soc. Lond., 269, 1955e1961. Karagenc, L., & Petitte, J. N. (2000). Soluble factors and the emergence of chick primordial germs cells in vitro. Poult. Sci., 79, 80e85. Kawase, E., Hashimoto, K., & Pedersen, R. A. (2004). Autocrine and paracrine mechanisms regulating primordial germ cell proliferation. Mol. Reprod. Dev., 68, 5e16. Knight, P. G., & Glister, C. (2006). TGF-b superfamily members and ovarian follicle development. Reproduction, 132, 191e206. Krishnan, K. A., Proudman, J. A., Bolt, D. J., & Bahr, J. M. (1993). Development of an homologous radioimmunoassay for chicken follicle-stimulating hormone and measurement of plasma FSH during the ovulatory cycle. Comp. Biochem. Physiol. Comp. Physiol., 105, 729e734. Krysko, D. V., Mussche, S., Leybaert, L., & D’Herde, K. (2004). Gap junctional communication and connexin43 expression in relation to apoptotic cell death and survival of granulosa cells. J. Histochem., 52, 1199e1207. Lee, H. J., Selesniemi, K., Niikura, Y., Niikura, T., Dombkowski, D. M., & Tilly, J. L. (2007). Bone marrow transplantation generates immature oocytes and rescues long-term fertility in a preclinical mouse model of chemotherapy-induced premature ovarian failure. J. Clin Oncol., 25, 3198e3204. Love, O. P., Wynne-Edwards, K. E., Bond, L., & Williams, T. D. (2008). Determinants of within- and among-clutch variation in yolk corticosterone in the European starling. Horm. Behav., 53, 104e111. Maddineni, S. R., Ocon-Grove, O. M., Krzysik-Walker, S. M., Hendricks, G. L., & Ramachandran, R. (2008). Gonadotropininhibitory hormone (GnIH) receptor gene is expressed in the chicken ovary: potential role of GnIH in follicular maturation. Reproduction, 135, 267e274. Malewska, A., & Olszanska, B. (1999). Accumulation and localisation of maternal RNA in oocytes of Japanese quail. Zygote, 7, 51e59. Meijer, T., & Drent, R. (1999). Re-examination of the capital and income dichotomy in breeding birds. Ibis, 141, 399e414. Milm, M., & Evans, A. C. O. (2008). Mechanisms for dominant follicle selection in monovulatory species: a comparison of morphological, endocrine and intraovarian events in cows, mares and women. Reprod. Dom. Anim., 43(suppl. 2), 48e56. Muscarella, D. E., Rachlinski, M. K., & Bloom, S. E. (1998). Expression of cell death regulatory genes and limited apoptosis induction in avian blastodermal cells. Mol. Reprod. Dev., 51, 130e142. Nakamura, Y., Yamamoto, Y., Usui, F., Mushika, T., Ono, T., Setioko, A. R., et al. (2007). Migration and proliferation of primordial germ cells in the early chicken embryo. Poult. Sci., 86, 2182e2193. Nakao, N., Yasuo, S., Nishimura, A., Yamamura, T., Wantanabe, T., Anraku, T., et al. (2007). Circadian clock gene regulation of steroidogenic acute regulatory protein gene expression in preovulatory ovarian follicles. Endocrinology, 148, 3031e3038. Nili, H., & Kelly, W. R. (1996). Form and function of lacunae in the ovary of the laying hen. Anat. Rec., 244, 165e174.

Chapter | 3

Organization and Functional Dynamics of the Avian Ovary

Nitta, H., Osawa, Y., & Bahr, J. M. (1991). Multiple steroidogenic cell populations in the thecal layer of preovulatory follicles of the chicken ovary. Endocrinology, 129, 2033e2040. Onagbesan, O. M., Bruggeman, V., & Decuypere, E. (2008). Intra-ovarian growth factors regulating ovarian function in avian species: a review. Anim. Reprod. Sci., doi: 10.1016/j.anirprosci.2008.09.017. Onagbesan, O. M., Vieugels, B., Buys, N., Bruggeman, V., Safi, M., & Decuypere, E. (1999). Insulin-like growth factors in the regulation of ovarian functions. Dom. Anim. Reprod., 17, 299e313. Pitz, K. M., Adkins-Regan, E., & Schwabl, H. (2005). No sex steroid differences in yolk steroid concentrations of avian eggs at laying. Biol. Lett., 1, 318e321. Radder, R. S., Pizzatto, L., & Shine, R. (2008). Morphological correlates of life-history variation: is lizard clutch size related to the number of germinal beds in the ovary? Biol. J. Linnean Soc, 94, 81e88. Reddy, P., Liu, L., Adhikari, D., Jagarlamudi, K., Rajareddy, S., Shen, Y., et al. (2008). Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science, 319, 611e613. Robinson, F. E., & Etches, R. J. (1986). Ovarian steroidogenesis during follicular maturation in the domestic fowl (Gallus domesticus). Biol. Reprod., 35, 1096e1105. Rutkowska, J., & Badyaev, A. V. (2008). Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds. Phil. Trans. R. Soc. B, 363, 1675e1686. Saino, N., Ferrari, R. P., Martinelli, R., Romano, M., Rubolini, D., & Moller, A. P. (2002). Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proc. R. Soc.Lond. B., 269, 1005e1009. Sato, T., Cheng, Y. N., Wu, X. C., Zelenitsky, D. K., & Hsiao, Y. F. (2005). A pair of shelled eggs inside a female dinosaur. Science, 308, 375. Schneider, W. J. (2009). Receptor-mediated mechanisms in ovarian follicle and oocyte development. Gen. Comp. Endocrinol., 163, 18e23. Schuster, M. K., Schmierer, B., Shkumatava, A., & Kuchler, K. (2004). Activin A and follicle-stimulating hormone control tight junctions in avian granulosa cells by regulating occluding expression. Biol. Reprod., 70, 1493e1499. Schweitzer, M. H., Elsey, R. M., Dacke, C. G., Horner, J. R., & Lamm, E.T. (2006). Do egg-laying crocodilian (Alligator mississippiensis) archosaurs form medullary bone? Bone, 40, 1152e1158. Sharp, P. J., & Blache, D. (2003). A neuroendocrine model for prolactin as the key mediator of seasonal breeding in birds under long- and short-day photoperiods. Can. J. Physiol. Pharmacol., 81, 350e358. Sharp, P. J., Dawson, A., & Lea, R. W. (1998). Control of luteinizing hormone and prolactin release in birds. Comp. Biochem. Physiol., 119, 275e282. Smith, C. A., & Sinclair, A. H. (2004). Sex determination: insights from the chicken. BioEssays, 26, 120e132. Smith, C. A., Roeszler, K. N., Ohnesorg, T., Cummins, D. M., Farlie, P. G., Doran, T. J., et al. (2009). The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature, 461, 267e271. Sockman, K. W., Sharp, P. J., & Schwabl, H. (2006). Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases of flexibility in clutch size, incubation behavior, and yolk androgen deposition. Biol. Rev., 81, 629e666.

89

Sockman, K. W., Williams, T. D., Daeson, A., & Ball, G. F. (2004). Prior experience with photostimulation enhances photo-induced reproductive development in female European starlings: a possible basis for the age-related increase in avian reproductive performance. Biol. Reprod., 71, 979e986. Song, Y., & Silversides, F. G. (2007). Offspring produced from orthotopic transplantation of chicken ovaries. Poult. Sci., 86, 107e111. Stebler, J., Spieler, D., Slanchev, K., Molyneaux, K. A., Richter, U., Cojocaru, V., et al. (2004). Primordial germ cell migration in the chick and mouse embryo: the role of the chemokine SDF-1/CXCL12. Dev. Biol., 272, 351e361. Subedi, K., Isobe, N., Nishibori, M., & Yoshimuri, Y. (2007a). Changes in the expression of toll-like receptor mRNAs during follicular growth and in response to lipopolysaccharide in the ovarian follicles of laying hens. J. Reprod. Dev., 53, 1227e1235. Subedi, K., Isobe, N., Nishibori, M., & Yoshimuri, Y. (2007b). Changes in the expression of gallinacins, antimicrobial peptides, in ovarian follicles during follicular growth and in response to lipopolysaccharide in laying hens (Gallus domesticus). Reproduction, 133, 127e133. Sundaresan, N. R., Anish, D., Sastry, K. V., Saxena, V. K., Mohan, J., & Ahmed, K. A. (2007). Cytokines in reproductive remodeling of molting white leghorn hens. J. Reprod. Immunol., 73, 39e50. Sundaresan, N. R., Saxena, V. K., Sastry, K. V., Nagarajan, K., Jain, P., Singh, R., et al. (2008). Cytokines and chemokines in postovulatory follicle regression of domestic chicken (Gallus gallus domesticus). Dev. Comp. Immunol., 32, 253e264. Tabibzadeh, C., Rozenboim, I., Silsby, J. L., Pitts, G. R., Foster, D. N., & El Halawani, M. (1995). Modulation of ovarian cytochrome P450 17a-hydroxylase and cytochrome aromatase messenger ribonucleic acid by prolactin in the domestic turkey. Biol. Reprod., 52, 600e608. Tilly, J. L., Kowalski, K. I., & Johnson, A. L. (1991). Stage of ovarian follicular development associated with the initiation of steroidogenic competence in avian granulosa cells. Biol. Reprod., 44, 305e314. Tsunekawa, N., Naito, M., Sakai, Y., Nishida, T., & Noce, T. (2000). Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells. Development, 127, 2741e2750. Van de Lavoir, M.-C., Diamond, J. H., Leighton, P. A., Mather-Love, C., Heyer, B. S., Bradshaw, R., et al. (2006). Germline transmission of genetically modified primordial germ cells. Nature, 441, 766e769. Warren, W. C., Hillier, L. W., Graves, J. A., et al. (2008). Genome analysis of the platypus reveals unique signatures of evolution. Nature, 453, 175e183. Whitehead, C. C. (2004). Overview of bone biology in the egg-laying hen. Poult. Sci., 83, 193e199. Williams, T. D., Kitaysky, & Vezina, F. (2004). Individual variation in plasma estradiol-17 b and androgen levels during egg formation in the European starling Sturnis vulgaris: implications for regulation of yolk steroids. Gen. Comp. Endocrinol., 136, 346e352. Wilson, F. E., & Reinert, B. D. (1999). Time of thyroidectomy variably affects seasonality in female American tree sparrows (Spizella arborea). Gen. Comp. Endocrinol., 114, 425e430. Wingfield, J. C., & Farner, D. S. (1993). Endocrinology of reproduction in wild species. In D. S. Farner, J. R. King, & K. C. Parkes (Eds.), Avian Biology, Vol. 9 (pp. 163e327). London, UK: Academic Press. Woods, D. C., Haugen, M. J., & Johnson, A. L. (2007). Actions of epidermal growth factor receptor/mitogen-activated protein kinase and protein kinase C signaling in granulosa cells from Gallus gallus are dependent upon stage of differentiation. Biol. Reprod., 77, 61e70.

90

Woods, D. C., Schorey, J. S., & Johnson, A. L. (2009). Toll-like receptor signaling in hen ovarian granulosa cells is dependent on stage of follicle maturation. Reproduction, 137, 987e996. Xie, M., Zhang, C., Zeng, W., & Mi, Y. (2004). Effects of folliclestimulating hormone and 17b-estradiol on proliferation of chick embryonic germ cells in culture. Comp. Biochem. Physiol., 139, 521e527, Part A. Yao, H. H., & Bahr, J. M. (2001). Chicken granulosa cells show differential expression of epidermal growth factor (EGF) and luteinizing hormone (LH) receptor messenger RNA and differential responsiveness to EGF and LH dependent upon location of granulosa cells to the germinal disc. Biol. Reprod., 64, 1790e1796. Yasou, S., Watanabe, M., Nakao, N., Takagi, T., Follett, B. K., Ebihara, S., et al. (2005). The reciprocal switching of two thyroid hormone activating and inactivating enzyme genes is involved in the photoperiodic gonadal response of Japanese quail. Endocrinology, 146, 2551e2554.

Hormones and Reproduction of Vertebrates

Yasou, S., Watanabe, M., Okabayashi, N., Ebihara, S., & Yoshimura, T. (2003). Circadian clock genes and photoperiodism: comprehensive analysis of clock gene expression in the mediobasal hypothalamus, the suprachiasmatic nucleus, and the pineal gland of Japanese quail under various light schedules. Endocrinology, 144, 3742e3748. Yoshimura, T. (2006). Molecular mechanism of the photoperiodic response of gonads in birds and mammals. Comp. Biochem. Physiol., 144, 345e350, Part A. Yoshimura, T., Yasuo, S., Wantanabe, M., Iigo, M., Yamamura, T., Hirunagi, K., et al. (2003). Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature, 426, 178e181. Yoshimura, Y. (2004). Significance of local immunity in hen reproductive organs. Anim. Sci. J., 75, 183e191. Yoshimura, Y., Okamoto, T., & Tamura, T. (1993). Electron microscope observations on LH-induced oocyte maturation in Japanese quail (Coturnix coturnix japonica). J. Reprod. Fert., 98, 401e407.

Chapter 4

Maternal Hormones in Avian Eggs Nikolaus von Engelhardt* and Ton G.G. Groothuisy *

University of Bielefeld, Bielefeld, Germany, y University of Groningen, Haren, The Netherlands

SUMMARY Avian eggs contain substantial levels of maternal hormones. Their levels vary in relation to a range of factors such as laying order, food availability, breeding density, and male quality. Yolk hormones subsequently influence offspring growth, behavior, physiology, immune system, and ultimately survival and reproduction. Some studies support the idea that maternal hormones may signal and prepare offspring for prevailing conditions. Adaptive effects require flexible mechanisms of hormone deposition and response. Separate control over hormone levels in circulation and yolk allows independent effects on offspring and mothers, while regulation of the response to maternal hormones allows offspring to fine-tune the effects on different traits. There is good evidence for such flexibility in both deposition and response. Natural selection on hormone-mediated maternal effects may differ between mothers and offspring, because costs and benefits are not equally shared. Evolutionary changes in the deposition and effect of these hormones therefore depend upon the consequences for all family members. Gaps in our understanding of the adaptive benefits and their underlying physiological mechanisms offer opportunities for future research.

1. INTRODUCTION: IMPORTANCE OF THE TOPIC AND OUTLINE An avian egg contains all the substances needed to produce a fully functioning organism. In addition to basic resources (proteins, lipids, water, and minerals) eggs contain a range of other substances, such as vitamins, antibodies, and enzymes. These appear to fulfill important functions, acting as regulators of embryonic development and protecting the embryo against pathogens, or may represent metabolic waste products. In the early 1990s, it was shown that the freshly laid egg, especially the yolk, contains hormones (Schwabl, 1993). Hormones are chemical messengers, small molecules produced by specialized cells, that bind to specific receptors in their target tissues and either directly regulate gene activity or change the physiological state of the cells; for example, by acting on ion channels in the cell membrane. Yolk hormones are produced by the mother but

Hormones and Reproduction of Vertebrates, Volume 4dBirds Copyright Ó 2011 Elsevier Inc. All rights reserved.

act on the offspring. Since hormone levels are modulated by the maternal environment and her condition, hormones in avian eggs are highly interesting as a potential mechanism by which information experienced in one generation can be transmitted to the next generation and thereby allow flexible adjustment of development to prevailing environmental conditions. This is possible if the environment experienced by mothers correlates with the environment offspring experience later in life. Maternal hormones may thus act as adaptive maternal effects, comparable to a ‘weather forecast’ that provides offspring with timely information in order to increase chances of survival and reproduction. Maternal effects are defined as influences of the environment provided by mothers on offspring that act in addition to or in interaction with offspring genotype and other environmental influences on offspring. A maternal effect may depend on the maternal environment and on the genetic quality of the mother and interact with direct genetic and environmental effects on offspring phenotype (Figure 4.1) (Mousseau & Fox, 1998). Empirical data and theoretical models suggest that such intergenerational effects can have important consequences for evolutionary dynamics and may allow rapid adaptation to variable environments, but may also delay adaptation or even lead to temporary maladaptive responses to changing selection pressures (Kirkpatrick & Lande, 1989; Moore, Wolf, & Brodie, 1998). An adaptive maternal effect mediated by yolk hormones should provide a net benefit for mother and/ or offspring. This requires that the conditions inducing the maternal effect predict (i.e., correlate with) variation in offspring environment that is relevant for maternal and/or offspring fitness. Further, there must be a mechanism that allows mothers to regulate deposition of hormones in relation to the context and also a mechanism by which offspring respond to maternal hormones. This chapter reviews maternal hormones in avian eggs, their effects, their regulating mechanisms, and their potential Darwinian function; i.e., the way in which they maximize survival and/or reproductive success. Most attention will be given to variation in maternal hormones

91

92

FIGURE 4.1 Schematic representation of environmental and genetic maternal effects. Reprinted from Groothuis, M€ uller, von Engelhardt, Carere, & Eising (2005b) with permission from Elsevier Ltd.

that reflect the environment experienced by mothers and are therefore classified as indirect environmental effects, since genetic variation between mothers in the deposition of maternal hormones has only very recently started to attract interest. In oviparous species, the embryo develops outside the mother’s body, which allows descriptive and experimental studies not possible in mammalian species. In addition, behavior and ecology of birds can be studied easily. As a consequence, maternal hormones have been studied in a large number of species. The mechanisms of deposition and action and the functions of hormones in avian eggs have been reviewed (Schwabl, 1997b; Gil, 2003; Groothuis, Mu¨ller, von Engelhardt, Carere, & Eising, 2005; Gil, 2008; Carere & Balthazart, 2007; Mu¨ller, Lessells, Korsten, & von Engelhardt, 2007; Groothuis & Schwabl, 2008) and conceptual and methodological approaches and their problems and pitfalls have specifically been addressed (Groothuis & von Engelhardt, 2005; von Engelhardt & Groothuis, 2005). This chapter aims at a broad overview integrating mechanistic with functional and evolutionary approaches and includes recent findings. The main hormones found in avian eggs and the potential mechanisms of hormone transfer to the egg will be presented first. Next, effects of maternal hormones on offspring phenotype and the potential mechanisms by which maternal hormones act on offspring will be reviewed. Finally, the influence of a variety of factors on levels of hormones in the egg will be examined and the potential adaptive role of yolk hormones will discussed in the light of observed effects of these hormones on offspring phenotype.

2. HORMONES AND LEVELS 2.1. Which Hormones? The possible presence of hormones in avian eggs was suspected in the 1920s (Fellner, 1925; Kopec &

Hormones and Reproduction of Vertebrates

Greenwood, 1929), but analytical difficulties, especially problems with their extraction from the complex yolk matrix as well as the lack of immunoassays, prevented proof of their presence. It was even considered that the high proportion of feminized sons in a strain of hermaphrodite-producing ring doves (Streptopelia risoria) might be caused by high levels of estrogens in the eggs acting as a ‘nongenomic maternal effect’ transmitted across generations (Riddle & Dunham, 1942; Riddle, Hollander, & Schooley, 1945). However, definitive proof of their existence and roles in development was not established until the studies by Hubert Schwabl in the 1990s (Schwabl, 1993; 1996b). Several steroids are present in high concentrations in avian eggs, in particular the lipophilic steroids progesterone (P4), androstenedione (AND), testosterone (T), and dihydrotestosterone (DHT). Low levels of estradiol (E2) and corticosterone (CORT) also have been found (reviewed in Groothuis et al., 2005b; Gil, 2008). For example, Figure 4.2 shows steroid levels in great tit eggs (Groothuis et al., 2005b). Concentrations of P4 and androgens in the yolk can be much higher than in the maternal circulation (Carere & Balthazart, 2007), most likely because hormones accumulate in the yolk over several days and metabolism is much slower or absent in comparison with the maternal circulation. Thyroid hormones (THs), catecholamines, melatonin (MEL), growth hormone (GH), insulin, glucagon, and leptin are also present in eggs (Trenkle & Hopkins, 1971; De Pablo, Roth, Hernandez, & Pruss, 1982; Sechman & Bobek, 1988; Prati, Calvo, Morreale, & Morreale de Escobar, 1992; McNabb & Wilson 1997; Wilson &

FIGURE 4.2 Concentrations of steroid hormones (mean standard error in pg/mg yolk) in great tit (Parus major) eggs, showing androgens (open bars), androstenedione (AND), dihydrotestosterone (DHT), testosterone (T), estradiol (E2, grey bar), and corticosterone (CORT, black bar). Reprinted and modified from Groothuis, M€ uller, von Engelhardt, Carere, & Eising (2005b) with permission from Elsevier Ltd.

Chapter | 4

Maternal Hormones in Avian Eggs

McNabb, 1997; Hu, Ni, Ren, Dai, & Zhao, 2008). Hormones seem to be present primarily in the egg yolk, although some studies have detected low levels also in the albumen (McNabb & Wilson, 1997; Rettenbacher, Mo¨stl, Hackl, & Palme, 2005; Downing & Bryden, 2008). Only the presence of T has been identified by high performance liquid chromatography (HPLC) and mass spectrometry (Schwabl, 1993). Several other steroids have been measured only by immunoassays, which may be unspecific due to crossreactivity with structurally related substances, and a chromatographic separation may be necessary to obtain valid measures. For example, a study using chromatographic separation of steroids followed by immunoassays detected low levels of immunoreactive substances in fractions containing CORT but found high levels of immunoreactive substances in fractions not containing CORT, presumably because the antibody cross-reacted with some unknown substances, most likely gestagens (Rettenbacher, Mo¨stl, & Groothuis, 2009). This review will focus on yolk androgens, especially T, since they have been studied best, although other hormones are briefly discussed as well. The concepts and general principles of androgen roles should apply to other hormones, although there may be considerable differences regarding specific functions and mechanisms, such as, for example, between the mechanisms involving transfer of gonadal and other hormones to the egg.

2.2. What Determines Hormone Levels in Eggs? From a functional perspective, any predictors of conditions that influence maternal or offspring survival or reproductive success have the potential to become important regulators of yolk hormone levels. Such factors must be perceived by mothers before or during egg production and need to be correlated with factors influencing fitness once offspring have been produced. The first

93

factor that received attention as a determinant of yolk hormone levels was the position of the egg in the laying order (Schwabl, 1993). This study, which initiated and stimulated further research interest on maternal hormones in birds, found that T levels in the egg increased with each successive egg laid and that yolk T correlated positively with the social rank of juvenile domestic canaries (Serinus canaria) hatched from those eggs. Since young from lastlaid eggs hatch later and are therefore smaller than their siblings from earlier laid eggs, Schwabl speculated that yolk T might mitigate the disadvantage of last-hatching offspring in sibling competition. Subsequent studies found that yolk hormone levels vary both within and between clutches, between females, and between species, and have effects on various aspects of offspring development (reviewed in Groothuis et al., 2005b; Gil, 2008). Many studies report effects of the environment experienced by mothers, such as food quality, breeding density, and social interactions with mates or competitors (for specification see Section 6.2). Yolk hormone levels also may correlate with offspring characteristics, such as sex, the composition of the egg (e.g., yolk mass or carotenoid levels), or the position in the laying order (see Section 6.1). Finally, hormone levels may relate not to the current or recent environment but to the state of the mother herself in terms of, for example, her age, physical condition, past experiences, or genetic background (for further discussion see Section 6.2.5). Figure 4.3 shows the increase of yolk T over the laying sequence in domestic canaries (S. canaria) and the decrease over the laying sequence in zebra finches (Taeniopygia guttata), who in addition increased yolk T concentrations when paired to males wearing red leg bands, an artificial ornament that increases the attractiveness of the male for females (see also Section 6.2.2). The effects of yolk hormones on offspring are reviewed in detail in Section 4, their mechanisms of action in Section 5, and the effects of yolk hormones and their potential functions in Section 6.

FIGURE 4.3 Yolk testosterone (T) concentrations (mean standard error) increased over the laying sequence in domestic canaries (Serinus canaria) (left panel) and decreased in zebra finches (Taeniopygia guttata) (right panel). In zebra finches, females also increased yolk T concentrations when paired to males wearing red leg bands, which renders them more attractive to females in some studies. Left panel reprinted from Schwabl, (1993) with permission from the National Academy of Sciences, USA. Right panel reprinted from Gil, Graves, Hazon, & Wells (1999) with permission from the American Association for the Advancement of Science.

94

Hormones and Reproduction of Vertebrates

2.3. Conclusion Bird eggs contain substantial amounts of steroids and other hormones, some at higher concentrations and others at lower concentrations than in the maternal circulation. The presence of some hormones in the egg still requires verification, and probably some hormones found in the maternal circulation may not be present in the egg, whereas others that have not been identified yet may be in the yolk. Since yolk hormones vary with a range of maternal and environmental factors, they may function as indicators of biologically relevant conditions for offspring development.

3. MECHANISMS OF ACCUMULATION 3.1. Why Relevant? Understanding the mechanisms of hormone transfer to the egg is particularly relevant to answering the question of whether levels of hormones in the maternal circulation and in the yolk can be independently regulated. Flexible regulation would allow simultaneous optimization of effects of circulating hormones on mothers and later effects of yolk hormones on offspring. The mechanisms by which hormones in the circulation and the yolk are adjusted are therefore important potential constraints on the evolution of adaptive hormonal effects (Groothuis et al., 2005b; Mu¨ller et al., 2007b; Groothuis & Schwabl, 2008; Moore & Johnston, 2008).

FIGURE 4.4 Scheme of possible sources and regulation of maternal hormones in the oocyte. The circles represent two follicles, with the oocyte (future yolk) in the center, surrounded by the three steroidogenic cell layers producing primarily progesterone (P4; granulosa), androgens (AND, T, DHT; theca interna) or estradiol (E2; theca externa). The rectangles stand for other organs involved in production (adrenal (corticosterone (CORT) and androstenedione (AND)), thyroid gland (triiodothyronine (T3) and thyroxine (T4)), regulation (central nervous system (CNS), pituitary), transport (blood) and degradation (liver) of maternal hormones. Wide grey arrows designate secretion and transport of hormones, small grey arrows show synthesis pathways of ovarian steroids. Black arrows indicate regulation by external stimuli, by releasing hormones (gonadotropin-releasing hormone (GnRH), corticotropinreleasing hormone (CRH), thyrotropin-releasing hormone (TRH)), and by pituitary hormones (luteinizing hormone (LH) and follicle-stimulating hormone (FSH), corticotropin (ACTH), and thyrotropin (TSH)). Reprinted and modified from Groothuis, & Schwabl (2008) with permission from the Royal Society.

3.2. Hormone Production Hormone accumulation in the egg requires three main processes: perception of the external or internal state by the female; transduction of this information to the tissues producing, storing, releasing, and metabolizing hormones; and transfer of the hormones to the yolk, schematically shown in Figure 4.4 (Groothuis & Schwabl, 2008). External and internal stimuli modify the release of gonadotropinreleasing hormone (GnRH) from the hypothalamus. Gonadotropin-releasing hormone stimulates production and release of the gonadotropins (GTHs) follicle-stimulating hormone (FSH) and luteinizing hormone (LH) from the pituitary. Follicle-stimulating hormone and LH in turn are released into the circulation and regulate follicular growth and steroid hormone production in the ovarian follicles (Johnson, 2000) (Figure 4.4). Production of the adrenal steroids CORT and AND is similarly stimulated by the release of corticotropin-releasing hormone (CRH) via corticotropin (ACTH). Release of thyrotropin (TSH) is also stimulated by CRH with subsequent release of THs from the thyroid: thyroxine (T4) and triiodothyronine (T3). Within the ovarian follicle, different steroids are produced in different cell layers, depending upon the

stimulation by GTHs and the size or stage of development of each follicle, which changes during the reproductive cycle. Steroids are produced in granulosa (P4, AND, T) and theca (T, E2) cell layers in the follicles (Huang, Kao, & Nalbandov, 1979; Bahr, Wang, Huang, & Calvo, 1983; Porter, Hargis, Silsby, & Elhalawani, 1989; Kato, Shimada, Saito, Noda, & Ohta, 1995; Gomez, Velazquez, JuarezOropeza, & Pedernera, 1998). They diffuse or are actively transported into the circulation and potentially directly into the yolk during the rapid yolking phase of the oocyte. Small follicles produce primarily estrogens, larger follicles increasingly produce T and other androgens, and the largest follicles secrete primarily P4. Progesterone is produced in the granulosa cells, the inner layer of the follicle closest to the oocyte. Androgens are produced in the next cell layer, the inner theca, while estrogens are produced in the outer theca layers; i.e., closest to the circulation. Steroid hormones are not stored in the tissue, but diffuse through cell membranes into other tissues, the yolk, or the circulation, although specific proteins also appear to transport steroids across the cell membrane (Kralli, Bohen, & Yamamoto, 1995; Friesema, Jansen, Milici, & Visser, 2005;

Chapter | 4

Maternal Hormones in Avian Eggs

Visser, Frieserna, Jansen, & Visser, 2008). Androgens also can be produced in the adrenal gland, but female adrenals produce mainly CORT and express little 17a-hydroxylase/ C17,20-lyase (P450c17), needed to produce androgens (Schlinger, Lane, Grisham, & Thompson, 1999; Freking, Nazairians, & Schlinger, 2000).

3.3. Accumulation of Hormones in the Egg Gonadal steroids (estrogens, progestins, and androgens) may reach the yolk directly from the surrounding follicle wall, the principle source of these hormones, and indirectly from neighboring follicles and the circulation. Extragonadal steroids, such as corticosteroids, THs, insulin, or GH, must reach the yolk via the circulation. This may explain why CORT levels in maternal plasma are much higher than in the yolk whereas androgen levels are higher in yolk than in plasma. Steroidogenic activity of the follicle wall changes with follicle maturation (first E2, then T, then P4) and this is consistent with the concentration of these hormones in the different yolk layers (highest in the center for E2, the first layer to be deposited; highest in intermediate layers for T; and highest in the last-produced outer layers for P4) found in some (Lipar, Ketterson, Nolan, & Casto 1999; Mo¨stl, Spendier, & Kotrschal, 2001; Hackl, Bromundt, Daisley, Kotrschal, & Mo¨stl, 2003; Rettenbacher et al., 2005), but not all (Reed & Vleck, 2001), studies. Gonadal hormones also may enter the yolk from the circulation since experimental elevation of plasma hormone levels leads to increases in the yolk (Arcos, 1972; AdkinsRegan, Ottinger, & Park, 1995; Wilson & McNabb, 1997; Hackl et al., 2003; Hayward & Wingfield, 2004; Love, Chin, Wynne-Edwards, & Williams, 2005). However, this may not reflect the natural process since such manipulation leads often to supraphysiological blood levels. When injecting radioactively labeled T into the circulation, less than 1% is transferred to the yolk after injection (Hackl et al., 2003). Despite this, levels of T in the yolk are on average about 40 times higher than in the circulation (Carere & Balthazart, 2007; Groothuis & Schwabl, 2008). This may reflect an active uptake process, high affinity of yolk to lipophilic steroids, high local concentration of steroids in the follicles, and/or cumulative uptake over several days. Yolk hormone levels may thus not directly reflect levels in the circulation but rather local production within the follicle with potentially specific transfer to the yolk, a topic discussed further in the next section.

3.4. Differential Regulation of Yolk and Circulating Levels Groothuis and Schwabl (2008) distinguish three potential ways in which levels of hormones in the circulation and the

95

yolk may be linked. First, yolk hormones may simply reflect levels in the circulation regulating female reproductive physiology and behavior. According to this ‘physiological epiphenomenon’ hypothesis, yolk and circulating levels would be positively correlated. Secondly, the ‘flexible distribution hypothesis’ assumes that hormones may be allocated either to the circulation or to the yolk, resulting in a negative correlation between circulating and yolk levels. Third, the ‘independent regulation hypothesis’ suggests that both production and distribution can be regulated, so that circulating and yolk levels are not necessarily correlated. Only the last mechanism would allow an unconstrained evolution of separate adaptive effects on mother and offspring. Actual measures of levels in the circulation and the yolk find a positive correlation (domestic canary (Schwabl, 1996a); house finch (Carpodacus mexicanus) (Badyaev et al., 2005)), no correlation (domestic canary (Tanvez, Beguin, Chastel, Lacroix, & Leboucher, 2004); domestic pigeon (Columba livia f. domesticus) (Goerlich, Dijkstra, Schaafsma, & Groothuis, 2009)), or a negative correlation (black-backed gull (Larus fuscus) (Verboven et al. 2003); house finch (Navara, Siefferman, Hill, & Mendonc¸a, 2006)) between circulating and yolk hormone levels, suggesting that independent regulation is at least potentially possible (for a detailed discussion see Groothuis & Schwabl, 2008). Finally, in house sparrows (Passer domesticus) (Mazuc, Bonneaud, Chastel, & Sorci, 2003) there were opposite correlations at different levels: both yolk and circulating levels increased with breeding density, but within females a negative correlation between yolk and circulating levels was found. When the gonadal axis of female dark-eyed juncos (Junco hyemalis) was stimulated by GnRH during different phases of the reproductive cycle (Jawor et al., 2007), circulating T increased only in the week before egg laying and, although yolk and circulating levels were not correlated, the magnitude of the response to GnRH correlated with yolk T levels, suggesting that the responsiveness of the reproductive axis influences steroid levels in both mother and offspring. Perhaps the strongest evidence for a differential regulation is the fact that relative levels of different hormones differ strongly between circulation and the yolk (Groothuis et al., 2005b). Estradiol and CORT are found only in very low concentrations in the egg, but in relatively high concentrations in the circulation, and the ratio of P4 to different androgens differs between maternal circulation and yolk. Overall, this indicates that various factors contribute to hormone levels in the circulation and the yolk and that there is no simple relationship. A direct comparison between plasma and yolk concentrations is also not easy because of the different dynamics of circulating concentrations, which can fluctuate rapidly, and yolk concentrations, which accumulate over several days. Therefore, single blood

96

Hormones and Reproduction of Vertebrates

samples taken at specific stages during egg laying may not reflect the accumulation of hormones in the yolk. Further, plasma levels are the product of all follicles, whereas levels in each follicle may depend mostly upon production in the follicle itself and less by adjacent follicles. Finally, as mentioned before, conclusions from implants demonstrating transfer to the egg are difficult to draw, since circulating levels are generally increased above the physiological range, which could result in a transfer to the yolk that would normally not occur. However, even in the case that hormone levels in the mother and egg correlate, this does not rule out potential specific adaptive roles for these hormones both in the circulation and in the yolk: if external factors are functionally relevant for both mothers and offspring, correlated levels of hormones in circulation and yolk may carry useful information for both. Processes that could affect relative levels in the circulation and the yolk are differences in solubility between hormones, presence of converting enzymes in the yolk, differential degradation of hormones in the circulation (liver) and yolk, and specific binding proteins or binding of steroids to lipids that are transported into the egg (Groothuis & Schwabl, 2008). In birds, androgens are bound to corticosteroid-binding globulins (CBGs) and to albumin since there is no specific protein binding sex steroids. Binding globulins therefore can regulate hormone levels, and circulating CORT levels may influence free T levels or vice versa by competing for CBG (Swett & Breuner, 2008). Several proteins that bind THs are thought to be involved in active transport of these hormones into the yolk (McNabb & Wilson, 1997).

physiology, anatomy, and morphology (Nelson, 2000; see also Volume 5, Chapter 1). In birds, contrary to mammals, embryonic estrogens feminize and demasculinize the reproductive system and reproductive behavior, whereas lack of exposure to estrogens results in a male phenotype (see discussions of sex determination in Chapters 2 and 3, this volume); hence, low E2 in the egg does not interfere with sexual differentiation. Paradoxically, estrogens masculinize the song system early posthatching in altricial birds. As androgens are converted to estrogens by aromatase (P450aro), androgens can have feminizing effects if P450aro and estrogen receptors (ERs) are present in the target tissues. Therefore, the same steroid can have different effects due to changes in metabolizing enzymes and receptors at different stages in development and in different tissues. Most studies on the effects of steroid hormones on avian embryonic development have focused on sexual differentiation that occurs as a response to hormones produced by the embryo itself. These studies generally use dosages several orders of magnitude higher than levels of maternal hormones in the egg. This overview will be limited to the effects of androgens (and other hormones) on offspring within the physiological range. Tables 4.1 and 4.2 summarize early developmental effects and long-lasting effects respectively of androgens, but other hormones will be briefly discussed too.

3.5. Conclusion

Many studies have demonstrated effects of yolk hormones on offspring pre- or posthatching growth by injecting freshly laid eggs with T, AND, or a combination of both. In black-headed gulls (Larus ridibundus), yolk androgens shortened time until hatching (Eising, Eikenaar, Schwabl, & Gro, 2001; Eising & Groothuis, 2003), while hatching time was increased in American kestrels (Falco sparverius) and zebra finches (Sockman & Schwabl, 2000; von Engelhardt, Carere, Dijkstra, & Groothuis, 2006) and there was no effect in starlings (Sturnus vulgaris) (Pilz, Quiroga, Schwabl, & Adkins-Regan, 2004) and yellow-legged gulls (Larus michahellus) (Rubolini, Romano, Martinelli, & Saino, 2006). Generally these are slight effects of 0.5e1 days of delay or advance, but since the time interval between the hatching of the first and last chick of these species is usually 1e4 days this can result in a significant advantage or disadvantage in sibling competition. Effects on hatching time may be mediated by effects on the hatching muscle (musculus complexus), which enlarges after androgen treatment and decreases in size after antiandrogen (flutamide) administration to eggs of red-winged blackbirds (Agelaius phoeniceus) (Lipar & Ketterson,

From a functional perspective, it is important to understand whether circulating and yolk hormone levels and their effects can be independently regulated. Circulating hormones affect the mother, whereas yolk hormones affect offspring. A lack of independence would therefore impose a constraint on the evolution of hormones as adaptive regulators of offspring development. Although some evidence points to a differential regulation of hormone levels in mothers and offspring, current evidence is not sufficient to understand the extent of independence. More studies on the physiological regulation of hormone accumulation in the egg are needed to better understand where hormones originate, how their levels are regulated, and whether this affects levels in the circulation and the yolk differentially.

4. EFFECTS ON OFFSPRING Gonadal hormones have long been known for their organizational and activational effects on brain, behavior,

4.1. Early Development 4.1.1. Time until hatching and growth

Chapter | 4 Maternal Hormones in Avian Eggs

TABLE 4.1 Effects of yolk androgens on early offspring development Effect On

Increase

Decrease 31

No/Inconsistent Effect 4

Hatching time

American kestrel Zebra finch7

Black-headed gull European starling20 Comparative11,30

Yellow-legged gull26 European starling24 Comparative8(R)

Growth

Domestic canary29 Black-headed gull4 Eastern Bluebird21(D) European starling24 House finch22 Red-winged blackbird13 Spotless starling16

American kestrel31(S) Yellow-legged gull26

Zebra finch7(S) Barn swallow28(S) Black-headed gull14(S) Domestic canary17,19(S) Partridge3(D) European starling20 Ring-necked pheasant25 Comparative8, 11(R)

Begging/ competitiveness

Domestic canary29 Black-headed gull5,18 Yellow-legged gull2 Zebra finch7(S) Spotless starling16

Barn swallow28 European starling24 Domestic canary17

Metabolic rate

Zebra finch32

Black-headed gull5

Immune response

House finch22

Endocrine system

Spotless starling16

Black-headed gull12,15 Eastern bluebird21(D) Chinese painted quail1(R)

Great tit33 Yellow-legged gull26 Partridge3(D) Black-headed gull14(S) Spotless starling16 Ring-necked pheasant25 Eastern bluebird21 Lesser black-backed gull35 (Continued)

97

98

TABLE 4.1 Effects of yolk androgens on early offspring developmentdcont’d Effect On

Increase

Decrease 6

Survival

Black-headed gull Zebra finch7 European starling24 Spotless starling16

Sex-ratio Primary Secondary

Spotless starling34 Zebra finch27 Homing pigeon (E)9 Yellow-legged gull26

No/Inconsistent Effect 31

American kestrel Domestic canary16,19(S) Eastern bluebird21

Yellow-legged gull26 Black-headed gull14(S) Ring-necked pheasant25 Japanese quail23 Homing pigeon10

Modifying factors: S, sex; D, dosage; E, egg number; R, growth; C, clutch size.

Hormones and Reproduction of Vertebrates

Effects of other hormones mentioned in the chapter are not in the table. Traits are indicated in the first column, positive effects on offspring traits are shown in the second column, negative effects in the third column, and cases where no effects or both positive and negative effects were observed are shown in the last column. ‘Comparative’ indicates correlations across several species. Modifying factors that resulted in increased, reduced, or reversed effects are indicated in brackets adjacent to the species name and are detailed below the table. References: 1 Andersson et al., 2004; 2 Boncoraglio et al., 2006; 3 Cucco et al., 2008; 4 Eising et al., 2001; 5 Eising et al., 2003b; 6 Eising & Groothuis, 2003; 7 von Engelhardt et al., 2006; 8 Gil et al., 2007; 9 Goerlich et al., 2009, 10 Goerlich et al., 2010; 11 Gorman & Williams, 2005; 12 Groothuis et al., 2005a; 13 Lipar et al., 2000; 14 M€ u ller et al., 2005a, 15 M€ u ller et al., 2005b; 16 M€ u ller et al., 2007a; 17 M€ u ller et al., 2008; 18 M€ u ller et al., 2009a; 19 M€ u ller et al., 2009b; 20 M€ u ller & Eens, 2009; 21 Navara et al., 2005; 22 Navara et al., 2006b; 23 Pike & Petrie, 2006; 24 Pilz et al., 2004; 25 Rubolini et al., 2006a; 26 Rubolini et al., 2006b; 27 Rutkowska & Cicho n, 2006; 28 Saino et al., 2006; 29 Schwabl 1996b; 30 Schwabl et al., 2007; 31 Sockman et al., 2008; 32 Tobler et al., 2007b; 33 Tschirren et al., 2005; 34 Veiga et al., 2004; 35 Verboven et al., 2003.

Chapter | 4

99

Maternal Hormones in Avian Eggs

TABLE 4.2 Long-term effects of yolk androgens on offspring phenotype Effect On

Increase

Decrease

No/Inconsistent Effect

House sparrow11 Ring-necked pheasant12 Chinese quail21 European starling9

15

Dominance/competition

Domestic canary House sparrow11,17(S) Black-headed gull3

Dispersal

Great tit18

Sexual traits Coloration Morphology Song

House sparrow17(S) Black-headed gull4 Comparative5

Ring-necked pheasant12 Domestic canary7 Comparative5

Reproduction Female Male

Domestic canary8

Ring-necked pheasant13 Chinese quail21

Behavioral syndromes Boldness Neophobia

Japanese quail1,10 Zebra finch20 House sparrow11 Japanese quail2

Endocrine system Levels Black-headed gull6

Survival Family members Siblings Parents

Great tit19(S)

Black-headed gull3

American kestrel16 Collared flycatcher14

Effects of other hormones mentioned in the chapter are not in the table. Traits are indicated in the first column, positive effects on offspring traits are shown in the second column, negative effects in the third column, and cases where no effects or both positive and negative effects were observed are shown in the last column. ‘Comparative’ indicates correlations across several species. Modifying factors that resulted in increased, reduced, or reversed effects are indicated in brackets adjacent to the species name and are detailed below the table. References: 1 Bertin et al., 2009; 2 Daisley et al., 2005; 3 Eising et al., 2001; 4 Eising et al., 2006; 5 Garamszegi et al., 2007; 6 Groothuis et al., 2005b; 7 M€ u ller et al., 2008; 8 M€ u ller et al., 2009b; 9 M€ u ller & Eens, 2009; 10 Okuliarova et al., 2007; 11 Partecke & Schwabl, 2008; 12 Rubolini et al., 2006a; 13 Rubolini et al., 2007; 14 Ruuskanen et al., 2009; 15 Schwabl, 1996b; 16 Sockman & Schwabl, 2000; 17 Strasser & Schwabl, 2004; 18 Tschirren et al., 2007; 19 Tschirren & Richner, 2008; 20 Tobler & Sandler 2007; 21 Uller et al., 2005 Modifying factors: S, sex.

2000). Two comparative studies found a negative relation between incubation time and yolk androgen levels among different songbird species (Gorman & Williams, 2005; Schwabl et al., 2007) although another study could not confirm this relationship (Gil et al., 2007). Posthatching growth was enhanced by yolk androgens in domestic canaries (Figure 4.5) (Schwabl, 1996b), and in

one (Eising et al., 2001), but not another (Mu¨ller, Dijkstra, & Groothuis, 2009), study on black-headed gulls; in European starlings (Pilz et al., 2004); and house finches (Navara, Hill, & Mendonc¸a, 2006b). It was reduced in American kestrels (Sockman & Schwabl, 2000) and yellow-legged gulls (Rubolini et al., 2006b). These effects on posthatching growth may in some studies depend

100

indirectly upon effects on hatching time, since hatching was advanced and posthatching growth increased in blackheaded gulls, whereas hatching time was delayed and posthatching growth reduced in American kestrels, which would be in line with an advantage or disadvantage, respectively, in sibling competition. However, there are also effects independent of hatching time, since the effect in offspring of black-headed gulls was found when offspring were size-matched at hatching (Eising et al., 2001), whereas hatching in zebra finches was delayed in both sexes, but growth of daughters was increased while growth of sons was slightly reduced (von Engelhardt et al., 2006). Contrasting effects between studies may depend upon methodological differences, such as dosage or context, or, for example, offspring sex. In Grey partridges (Perdix perdix) (Cucco, Guasco, Malacarne, Ottonelli, & Tanvez, 2008) and Eastern bluebirds (Sialia sialis) (Navara, Hill, & Mendonc¸a, 2005), low dosages of T enhance growth, whereas higher dosages have no effect. However, in Grey partridges, the highest dosages used suppress growth. Positive effects or no effects on females and negative effects on males were observed in zebra finches (von Engelhardt et al., 2006) and the domestic canary (Mu¨ller, Vergauwen, & Eens, 2008), yet the opposite was found in barn swallows (Hirundo rustica) (Saino et al., 2006). Effects on growth may be restricted to early development, with no difference observed in final body weight.

4.1.2. Begging/competitiveness Most young birds engage in conspicuous acoustic and visual behavior that influences food allocation by parents (Kilner, 2002). Offspring can influence parental feeding in

Hormones and Reproduction of Vertebrates

several ways: they can respond faster to the arrival of the parents, open their beak more, stretch higher in the nest, shake their head or tongue, push other siblings to the side, or move to positions in the nest closer to the parental feeding position. Coloration and size of the mouth also can influence parental feeding of the nestlings. Injection in the egg of T or a combination of T and AND enhance visual or acoustic display or competitive behaviors in domestic canaries, black-headed gulls, and yellow-legged gulls (Figure 4.5) (Schwabl, 1996b; Eising et al., 2001; Boncoraglio, Rubolini, Romano, Martinelli, & Saino, 2006; Mu¨ller, Deptuch, Lo´pez-Rull, & Gil, 2007). In some studies, the effects were found only in one offspring sex (von Engelhardt et al., 2006), but others report either no effects on begging at all (Saino et al., 2006) or inconsistent results (Pilz et al., 2004). In black-headed gull nestlings, elevation of yolk T and AND levels increased aggression not towards siblings but toward nestlings of neigboring nests or adults intruding on the natal territory (Mu¨ller et al., 2009a).

4.1.3. Metabolic rate Effects on growth and begging behavior may be associated with changes in energy expenditure, but observations are varied. In adult birds, administration of T increased (male house sparrow (Buchanan, Evans, Goldsmith, Bryant, & Rowe, 2001)), reduced (male white-crowned sparrow (Zonotrichia leucophyrys gambelii) (Wikelski, Lynn, Breuner, Wingfield, & Kenagy, 1999)), or had no effect on metabolic rate (male house sparrow (Buttemer, Warne, Bech, & Astheimer, 2008)). The evidence for yolk androgens is also inconsistent since T þ AND injections in freshly laid eggs influenced growth but not metabolic rate in black-headed gulls (Eising, Visser, Mu¨ller, & Groothuis,

FIGURE 4.5 Experimental elevation of yolk testosterone (T) enhanced growth (mean standard error) and stimulated begging behavior in domestic canaries. The left panel shows tarsus length and body mass of nestlings from T-injected and control eggs. Growth curves did not differ significantly, but T-treated chicks reached 50% of final tarsus length earlier (t ¼ 2.4, p < 0.03) and had detectable eye slits (indicated by arrows) significantly earlier (t ¼ 2.9, p < 0.02). The right panel shows number of begging bouts per test (mean with range; defined as raising head and gaping), bout duration, and total duration of begging (mean and standard error) of nestlings tested within one hour of hatching. Significance levels from Mann-Whitney U tests comparing between treatments are indicated above the bars for controls (for details see Schwabl, 1996b). Reprinted from Schwabl (1996b) with permission from Elsevier Science Inc.

Chapter | 4

101

Maternal Hormones in Avian Eggs

2003) but in-ovo T injections increased metabolic rate with no effect on growth in nestling zebra finches (Tobler, Nilsson, & Nilsson, 2007).

4.1.4. Immune system Exposure to pharmacological levels of steroids during embryonic development inhibits development of the bursa of Fabricius, which regulates early humoral immunity in birds (Glick, 1962; Erickson & Pincus, 1966; Glick, Holbrook, & Perkins, 1977; Olah, Glick, & Toro, 1986), although lower dosages are stimulatory (Norton & Wira, 1977). When yolk androgen levels are manipulated within the natural range, they suppress both humoral immunity and cellular immunity in black-headed gulls, and blocking androgen receptors (ARs) with flutamide injections in the egg improves humoral immunity (Groothuis, Eising, Dijkstra, & Mu¨ller, 2005; Mu¨ller, Groothuis, Eising, & Dijkstra, 2005; Mu¨ller, 2005b). In Eastern bluebirds (Navara et al., 2005), cellular immune response was negatively affected by a relatively high dose of T injected in the eggs, but not by a moderate one. Since only the former suppressed growth, the results suggest a tradeoff between growth and immunity. In Chinese painted quail (Coturnix chinensis) (Andersson, Uller, Lo¨hmus, & Sundstro¨m, 2004), egg injection of T resulted in suppression of cell-mediated immunity in fast, but not slowgrowing, birds, suggesting again an interaction between effects on growth and immunocompetence. As in the Eastern bluebird, in Grey partridges (Cucco et al., 2008) a low dosage of T increased cellular immune reaction whereas a high dose was suppressive. However, in this case, enhancement of cell-mediated immunity took place together with enhanced body growth, as in house finches (Navara et al., 2006b). In both cases, improved immunity might therefore be related to better body condition; a further reason for this is that the measurement of cellular immunity taken is often correlated with body condition. Finally, immunity was not affected by elevating yolk T in yellow-legged gulls (Rubolini et al., 2006b) and great tits (Parus major) (Tschirren, Saladin, Fitze, Schwabl, & Richner, 2005).

4.1.5. Endocrine system Exposure to maternal hormones during prenatal development may directly affect circulating levels of these hormones in nestlings since yolk is still consumed during the first days after hatching. It may also affect a nestling’s own hormone production. Chick begging and competitive behavior are correlated to circulating androgen levels in several species (Ros, Dieleman, & Groothuis, 2002; Schwabl & Lipar, 2002; Buchanan, Goldsmith, Hinde, Griffith, & Kilner, 2007; Hinde, Buchanan, & Kilner,

2009), so there may be a direct link between yolk androgen levels, nestling androgen levels, and nestling behavior. Lesser black-backed gulls (Verboven et al., 2003) and Eastern bluebird nestlings (Navara et al., 2005) from Ttreated eggs and control eggs did not differ in plasma T, but spotless starling chicks (Sturnus unicolor) (Mu¨ller et al., 2007a) from T-treated eggs had higher T levels at day 15.

4.1.6. Survival Yolk androgens have weak positive effects on early survival in black-headed gulls, zebra finches, spotless starlings, and European starlings (Eising & Groothuis, 2003; Pilz et al., 2004; Groothuis et al., 2005b; von Engelhardt et al., 2006; Mu¨ller et al., 2007a). On the other hand, yolk androgens reduce nestling survival in American kestrels (Sockman & Schwabl, 2000) and domestic canaries (Mu¨ller, Vergauwen, & Eens, 2009b), reduce hatching success in Eastern bluebirds (Navara et al., 2005), but do not affect survival in yellow-legged gulls (Rubolini et al., 2006b). The negative effects of yolk T injections found in the American kestrel may be linked to its delaying effect on hatching, which would reduce the ability to compete with earlier-hatched siblings. In other studies, the hatching spread between the first and last hatching chick was controlled for by crossfostering (Eising et al., 2001) or by treating all of the eggs in the clutch similarly (Navara et al., 2005; Rubolini et al., 2006b; von Engelhardt et al., 2006), so that the effect of T injections in the egg could not come about by its effect on hatching and its subsequent effect on the nestling competitive hierarchy. The discrepancy in the abovementioned effects of yolk T on survival could be due to context-dependent effects of yolk hormones, which may have positive effects under good and negative effects under poor environmental conditions. This will be addressed again in Section 6.

4.1.7. Sex allocation In birds, females are the heterogametic sex and may therefore have control over the sex of the offspring. As mentioned earlier, female zebra finches are attracted to males wearing red leg bands, and when paired to these males produce male-biased offspring sex ratios (Burley, 1981; 1982; 1986) and deposit higher levels of T and DHT in their eggs (Gil, Graves, Hazon, & Wells, 1999). Maternal hormones may affect sex allocation by modifying offspring primary sex ratio (in theory at meiosis, but often measured after a few days of incubation, to obtain sufficient tissue for sexing), secondary sex ratio (via sex-specific survival), or sex-specific effects on development that can lead to differences in quality (and therefore fitness return) between the sexes (Pike & Petrie, 2003; Rutkowska & Badyaev,

102

2008). Elevating T levels in the maternal circulation leads to male-biased sex ratios in spotless starlings (Veiga, Vinuela, Cordero, Aparicio, & Polo, 2004), zebra finches (Rutkowska & Cicho n, 2006), and yellow-legged gulls (Rubolini et al., 2006b); in one (Goerlich et al., 2009) but not another (Goerlich, Dijkstra, & Groothuis, 2010) study on domestic pigeons; and not in Japanese quail (Pike & Petrie, 2006). Elevating E2 levels in breeding zebra finches (Williams, 1999; von Engelhardt, Dijkstra, Daan, & Groothuis, 2004), elevating P4 in domestic chickens (Correa, Adkins-Regan, & Johnson, 2005), and elevating CORT in Japanese quail and European starlings (Pike & Petrie, 2006; Love et al., 2005; Love & Williams, 2008) led to female-biased sex ratios. In the zebra finch and the starling study, this was not due to an effect on the primary sex ratio but to a sex-specific effect on survival, resulting in a female-biased secondary sex ratio (von Engelhardt et al., 2004; Love et al., 2005; Love & Williams, 2008). In addition to effects of manipulation of hormones in the maternal circulation on the sex ratio, direct experimental elevation of T in the yolk had sex-specific effects on development in several studies. In zebra finches, yolk androgens increased begging and growth in daughters and reduced growth of sons (von Engelhardt et al., 2006), while they had detrimental effects on daughters in barn swallows (H. rustica) (Saino et al., 2006) and yellow-legged gulls (Rubolini et al., 2006b) and detrimental effects on growth in male American kestrels (Sockman, Weiss, Webster, Talbott, & Schwabl, 2008) and nestling domestic canaries (Mu¨ller et al., 2008), suggesting that the balance of costs and benefits of androgens may depend upon species and sex differences in sensitivity to hormones. Finally, avian mothers may differentially allocate hormones with respect to the sex of the egg. Evidence for this will be discussed in Section 6.

4.2. Long-term Effects Long-term effects of maternal hormones may be an indirect consequence of effects on physiology, behavior, and morphology during early development or due to direct

Hormones and Reproduction of Vertebrates

organizational effects on the nervous and endocrine systems or target organs that then leads to differences in production and/or responses to hormones when birds are adults (Carere & Balthazart, 2007; Groothuis & Schwabl, 2008). An advantage of separate direct effects on multiple traits is the possibility for an independent evolution of each trait by adjustment of its sensitivity to maternal hormones.

4.2.1. Competitiveness In domestic canaries, rank order of juveniles correlated positively with androgen levels in biopsies of the eggs (Schwabl, 1996b), and manipulation of yolk T increased aggression and dominance in adult female and male house sparrows during feeding and in a sexual context (Figure 4.6) (Strasser & Schwabl, 2004; Partecke & Schwabl, 2008). In black-headed gulls, elevation of yolk T enhanced aggressive behavior and success in displacing other individuals at 10 months of age (Eising, Mu¨ller, & Groothuis, 2006).

4.2.2. Dispersal Maternal effects, including maternal hormones, appear to influence offspring dispersal in various animal species (De Fraipont, Clobert, John, & Alder, 2000; Meylan, Belliure, Clobert, & De Fraipont, 2002). The only study performed in birds found that yolk T increased dispersal distance in great tits (Tschirren, Fitze, & Richner, 2007).

4.2.3. Coloration, morphology, and song Expression of sexually dimorphic plumage has long been known to be steroid-dependent in many bird species, but this has been studied only in the context of sexual differentiation. There can be direct genetic effects on coloration, activational effects of circulating steroids, organizing effects due to early exposure to hormones, and a combination of these (Witschi, 1961; Mueller, 1977; Kimball & Ligon, 1999). Generally, exposure to estrogens results in female plumage, whereas a lack of estrogens results in male coloration. Embryonic exposure to steroids can

FIGURE 4.6 Elevation of yolk testosterone (T) increased aggression, sexual display, and access to the opposite sex in male house sparrows (Passer domesticus). Shown are means 95% confidence interval. Significant differences between T-injected and control eggs as determined by post hoc Sidak tests are indicated by asterisks (*, p < 0.05; **, p < 0.01). Weight and size-matched contestants were tested during the first reproductive season at 10e12 months of age during 120 minutes in outdoor aviaries with wild-caught caged stimulus birds. Reprinted from Partecke & Schwabl (2008) with permission from Wiley Periodicals Inc.

Chapter | 4

103

Maternal Hormones in Avian Eggs

permanently modify plumage coloration; e.g., in ducks (Anas platyrhynchos), where skin grafts of hatchlings from eggs treated with E2 during embryonic development develop female-type feathers while control transplants develop male-type feathers irrespective of the sex of the host (Mueller, 1976). Early posthatching E2 exposure masculinizes the song system in zebra finches (Gurney, 1981; 1982; Quaglino et al., 2002), and elevation of T during the juvenile song learning phase leads to earlier song crystallization (Korsia & Bottjer, 1991; Whaling, Nelson, & Marler, 1995). However, these studies used much higher concentrations of steroid hormones than those present in the egg. Elevation of yolk T in black-headed gulls resulted in a more developed black mask (the nuptial plumage) and adult wing plumage the following spring (Eising et al., 2006). The black chest badge in house sparrows was enhanced by elevating yolk T, although the latter result could not be repeated (Strasser & Schwabl, 2004; Partecke & Schwabl, 2008). In ring-necked pheasants (Phasianus colchicus), elevation of yolk T did not affect ornaments such as wattle size and plumage coloration, although the covariance between different traits was changed and spur length was reduced (Rubolini, Romano, Martinelli, Leoni, & Saino, 2006). No clear effects of yolk T manipulations on song were observed in male domestic canaries; if anything, their song development was somewhat delayed but there was no difference in the final song (Mu¨ller et al., 2008). In European starlings, no effects on song, beak color, or feather coloration could be found (Mu¨ller & Eens, 2009). Finally, a comparative study in passerines found a negative correlation of yolk T with song duration and repertoire size, and a positive correlation with the height of the song-post relative to the surrounding vegetation (Garamszegi, Biard, Eens, Mo¨ller, & Saino, 2007). Overall, there is thus some support for long-term effects of maternal hormones on morphology, coloration, and song, but the results are not consistent, which is also the conclusion of a meta-analysis of the small number of studies that have been published (Mu¨ller & Eens, 2009).

4.2.4. Reproduction Early exposure to steroids can affect several measures of reproductive function, which has been studied especially in the context of effects of estrogens on avian sexual differentiation and toxic effects of endocrine disruptors (see Chapter 9, this volume). Embryonic exposure to T propionate negatively affects male mating behavior in domestic chickens (Glick, 1965), and in the Japanese quail exposure to both E2 (Adkins, 1975) and T (Adkins-Regan, Pickett, & Koutnik, 1982) during embryonic development, and in zebra finches (Adkins-Regan & Ascenzi, 1987) after hatching, demasculinizes copulatory behavior.

Female domestic canaries hatching from eggs with elevated T levels within the physiological range produce more but not larger eggs (Mu¨ller et al., 2009b), whereas female ring-necked pheasants (Rubolini et al., 2007) lay fewer eggs and male Chinese painted quail (Uller, Eklof, & Andersson, 2005) have smaller testis sizes when hatching from T-treated eggs.

4.2.5. Behavioral syndromes or personalities Personality differences or behavioral syndromes, defined as consistent individual differences in behavior, are observed in many species and are thought to represent alternative behavioral strategies that may be equally successful depending upon the context or the frequency of other strategies (Gosling & John, 1999; Sih, Bell, Johnson, & Ziemba, 2004). Such differences often seem to have a genetic basis, but also can be modified epigenetically by early environmental conditions (Carere, Drent, Koolhaas, & Groothuis, 2005). Because of the strong effects of hormones on development and their pleiotropic effects on multiple traits, hormones may influence the development of personality differences. Japanese quail hatching from eggs treated with T were more proactive (Daisley, Bromundt, Mo¨stl, & Kotrschal, 2005; Okuliarova, Skrobanek, & Zeman, 2007), took shorter time for exploratory tasks, issued fewer distress calls, and were less likely to show tonic immobility (Daisley et al., 2005). In addition, Japanese quail breeding lines selected for high or low social reinstatement behavior or fearfulness had relatively high and low yolk T levels respectively (Gil & Faure, 2007; Bertin et al., 2009). Whether yolk hormones are the cause or effect of the differences in behavior is not known (Gil, 2008). Zebra finches exposed to elevated yolk T (Tobler & Sandell, 2007) approached food and ate faster in a novel context, but showed stronger neophobic responses. Early exposure to CORT increased fear response in chickens (Janczak, Braastad, & Bakken, 2006). Great tits that were selected for differences in boldness differed also in yolk T levels (Groothuis, Carere, Lipar, Drent, & Schwabl, 2008): levels of T and AND increased over the laying in the genetic line selected to be more bold when placed in a novel environment or when approaching a novel object, and decreased in the genetic line selected to be more cautious. Cautious individuals also laid eggs later in the year, so that increase and decrease may reflect brood survival and brood reduction strategies as an adjustment to seasonally changing food availability (see Section 6).

4.2.6. Endocrine system Early exposure to androgens may organize hormone production or responsiveness to hormones later in life.

104

Hormones and Reproduction of Vertebrates

Sex-specific organization of GnRH neurons and neural networks controlling GnRH are organized by early T in mammals (Padmanabhan, Manikkam, Recabarren, & Foster, 2006). Japanese quail from eggs with elevated T had nonsignificantly higher circulating T levels but lower CORT levels (Daisley et al., 2005) and there was no effect on circulating T levels in house sparrows (Partecke & Schwabl, 2008). Early exposure to hormones can also affect neurotransmitter systems involved in reproductive and aggressive behavior (Abdelnabi & Ottinger, 2003; Panzica et al., 2007) and the brainepituitaryeadrenal axis (McCormick, Furey, Child, Sawyer, & Donohue, 1998; Welberg, Seckl, & Holmes, 2001). Changes in these systems, or density of androgen receptors, may underlie the long-term effects of maternal androgens on social behavior, but this has not been studied.

4.2.7. Survival Long-term effects on survival have been studied only in black-headed gulls, where, in contrast to the positive effects on nestling survival of males, experimental elevation of yolk androgens reduces survival of juveniles and adults (Groothuis et al., 2005b).

4.3. Indirect Effects on Other Family Members Effects of yolk hormones on individual offspring may have indirect effects on siblings or parents by changing sibling competition, cooperation, or demand for food from parents. The costs and benefits of these indirect effects are important as they also influence selection and evolution of hormone-mediated maternal effects (Mu¨ller et al., 2007b), but have unfortunately rarely been investigated. Elevating yolk androgen levels in black-headed gulls has negative effects on growth of siblings (Eising et al., 2001), whereas sibling survival in American kestrels is not affected (Sockman & Schwabl, 2000). Most other studies have used between-clutch treatments, so that indirect effects on siblings could not be analyzed. Sex-specific effects (Saino et al., 2006; von Engelhardt et al., 2006; Sockman et al., 2008) observed in a between-clutch design also may be due to indirect influences of one sex on the other, if begging or growth is more strongly affected in one sex, which could lead to an advantage in competition with siblings of the other sex. Relative male feeding rates in collared flycatchers (Ficedula albicollis) are correlated positively with yolk androgen levels of cross-fostered eggs of conspecific females, but not with levels of the original eggs of their females. However, experimental elevation of yolk androgen levels does not affect male or female parental

FIGURE 4.7 Reducing effects of maternal androgens by injecting flutamide, an androgen receptor blocker, into great tit (Parus major) eggs did not affect male feeding rates (mean þ standard error), measured for 100 minutes at day 10 posthatching (upper panel) but reduced female feeding rates (mean standard error) in enlarged broods (lower panel), as shown by a significant interaction between brood size and treatment (F1,44 ¼ 8.7, p < 0.01). Reprinted from Tschirren & Richner (2008) with permission from the Association for the Study of Animal Behaviour.

feeding rates (Ruuskanen et al., 2009). Male parental care was not affected in great tits following blocking of androgen binding to ARs with flutamide, but females reduced parental investment (Figure 4.7) (Tschirren & Richner, 2008). However, flutamide also blocks the action of endogenously produced androgens, so it is not clear whether this effect can be attributed to maternal androgens.

4.4. Other Yolk Hormones While this review focuses on yolk androgens, especially yolk T, which has been studied most thoroughly, some effects of other yolk hormones shall be mentioned briefly.

Chapter | 4

105

Maternal Hormones in Avian Eggs

Of these, yolk CORT attracts the most interest (Love et al., 2005; Love & Williams, 2008) because of the interest in intergenerational effects of maternal stress, although there is some doubt as to whether it is present in biologically significant amounts in the egg (Rettenbacher et al., 2009). Corticosterone injections into eggs reduced survival and growth in barn swallows (Saino, Romano, Ferrari, Martinelli, & Møller, 2005), reduced growth in male Japanese quail and reduced female immune response (Hayward, Richardson, Grogan, & Wingfield, 2006), and prolonged longer hatching times and suppressed begging and immunity in yellow-legged gulls (Rubolini et al., 2005). Some studies that implanted mothers with CORT and found elevated yolk CORT also found negative effects on growth in Japanese quail together with an increase in the hormonal stress response (Hayward & Wingfield, 2004) and male embryonic survival and posthatching growth in European starlings (Love et al., 2005). Negative effects on males also may be responsible for a reduction in sex ratio (i.e., increased proportion of daughters) found after CORT treatment (Pike & Petrie, 2006). Effects of P4, which is the steroid hormone present in highest concentrations in the egg, have apparently not been studied. Finally, there are few studies on effects of other hormones of maternal origin, such as insulin, leptin, GH, and MEL (McNabb & Wilson, 1997; Flamant & Samarut, 1998; Lamosova´ & Zeman, 2001; Kova´cikova´, Kuncova´, Lamosova´, & Zeman, 2003; Lamosova´, Ma´cajova´, Zeman, Mo´zes, & Jezova´, 2003; Darras, Van Herck, Geysens, & Reyns, 2009). Increased amounts of T4 deposited in the egg by feeding mothers the hormone increased pelvic cartilage weight but not other measures of mass or size, and did not affect hatching success (Wilson & McNabb, 1997). Thyroid hormones stimulate differentiation of cartilage to bone (Burch & Lebovitz, 1982), but injection of T3 into the yolk leads to embryo malformations (Flamant & Samarut, 1998).

4.5. Conclusion Yolk hormones can have a wide array of effects on offspring development. The direction and strength of effects frequently differs between studies, so that both negative and positive effects on growth, survival, and the expression of adult traits are observed. Effects may depend upon offspring sex, the dosage used, or contextual variables such as offspring growth rate. The most consistent effect is probably an increase in early and later competitive behavior. However, overall, there are no consistent effects in a specific direction, indicating that effects depend upon the context and/or that different species may have evolved different responses to maternal hormones. From a functional evolutionary perspective, such context-

dependent and species-specific effects can be expected and yolk hormones should have beneficial effects for mother and/or offspring in contexts where natural levels are high and detrimental effects in contexts where natural levels are low. However, this context-dependency has unfortunately hardly been studied. It is also unclear to what extent these effects are directly induced by yolk hormones or are indirect consequences of effects on other traits. Finally, there is no evidence that endogenous yolk androgens affect sexual differentiation, since masculinization or feminization of behavior or plumage has not been reported.

5. MECHANISMS OF ACTION 5.1. Why Relevant? Understanding the mechanisms that regulate offspring responses to maternal hormones is especially relevant for understanding to what extent offspring can optimally respond to hormones of maternal origin (Mu¨ller et al., 2007b; Groothuis & Schwabl, 2008). Several processes can influence this response: hormones have to be taken up from the yolk, yolk hormones can be metabolized to substances that are inactive or have a different activity from the original substance, receptor expression at different stages in target organs can be changed, and different responses may be activated by the receptors. mRNA for hormone receptors, hormone transporters, and metabolizing enzymes are present within the first days of embryonic development (Figure 4.8) (Bruggeman, Van As, & Decuypere, 2002; Darras et al., 2009), even before hormones seem to be produced by the embryo itself, which occurs by about day three to four of incubation, suggesting specific responses to maternal hormones.

5.2. Activational and Organizational Effects Yolk hormones may have activational effects on embryos or hatchlings that disappear when the yolk has been used up within the first days of hatching, or they may have organizational effects that remain even when the inducing hormone is no longer present (Phoenix, Goy, Gerall, & Young, 1959). Yolk hormones may directly affect multiple traits due to the presence of receptors in each tissue, and this may indirectly affect other traits (Carere & Balthazart, 2007; Groothuis & Schwabl, 2008). This distinction is relevant from an evolutionary perspective, since multiple independently affected traits can separately evolve specific responses to maternal hormones, while all indirectly influenced traits will be simultaneously affected if there is a change in the primary trait responding directly to maternal hormones.

106

Hormones and Reproduction of Vertebrates

FIGURE 4.8 Appearance of enzymes, receptors, binding and transport proteins, endogenous hormones, and maternal hormones during the first half of the incubation period in chicken eggs (days 0e10), indicated by arrows. Shown are enzymes involved in synthesis and metabolism of thyroid hormones (deiodinases), and steroid hormones (P450 side-chain cleavage enzyme (P450scc), 3b- and 17b-hydroxysteroid dehydrogenase (3b-HSD and 17b-HSD), p450 17a-hydroxysteroid-dehydrogenase (p450c17), 5b-reductase and aromatase); receptors for thyroid hormones (TR), corticosteroids (CR), progesterone (PR), estrogens (ER), and androgens (AR); transporter proteins for thyroid hormone (organic anion transporting polypeptide (1c1OATP1c1)); and corticosteron (corticosteroid-binding protein (CBG)); and maternal or endogenous hormones (progesterone (P4), androstenedione (AND), dihydrotestosterone (DHT), testosterone (T), estradiol (E2), corticosterone (CORT), and thyroid hormones triiodothyronine (T3) and thyroxine (T4)). Time points with differences between females (F) and males (M) in T and E2 levels, their receptors, and in aromatase expression are also indicated.

5.3. Hormone Uptake Steroid hormones are taken up from the yolk early in development and can be detected in different embryonic tissues (Paitz & Bowden, 2008; von Engelhardt, Henriksen, & Groothuis, 2009). However, there are no detailed studies on the distribution within the embryo at different stages in development. The embryo continues to take up yolk until some days after hatching and is therefore at this stage most likely still directly exposed to maternal hormones. Since yolk hormones are not equally distributed within the yolk (Lipar et al., 1999; Hackl et al., 2003), different hormones may be taken up at different stages in development. The layered yolk structure remains intact for some days, so that initially the embryo presumably takes up the outer layers containing the highest concentrations of P4. Androgens concentrated in the intermediate layers would be taken up next, and estrogens in the center of the yolk would be taken up last. However, this layering of the yolk is at least partially modified during embryonic development due to the uptake of water from the albumen, and it is possible that, due to such mixing as well as secretion of enzymes by the embryo, the distribution and/or concentrations of the hormones present in the yolk are modified. We therefore do not know to what extent the initial distribution of yolk hormone levels within the yolk is of functional significance.

5.4. Hormone Metabolism Steroids are metabolized to both conjugated and other free steroids by enzymes released from the embryo very early in

development, even within the first two days after onset of incubation (Woods & Weeks, 1969; Parsons, 1970; Antila, Leikola, & Tahka, 1984; Nomura, Nakabayashi, Nishimori, Yasue, & Mizuno, 1999). Although some evidence suggests that steroid-metabolizing enzymes present in chicken egg yolk before the onset of incubation are of maternal origin (Delrio, Botte, & Diprisco, 1968), these results have not been confirmed. Since embryos do not produce steroids at this age, it was suggested that maternal steroids could be substrates for these enzymes (Parsons, 1970). Further, deiodinases, which convert the less-active T4 to active T3, are present during the first day of incubation (Darras et al., 2009). Such enzymatic activity may explain the rapid decrease of measured AND, T, DHT, and E2 within the first days of incubation (Elf & Fivizzani, 2002; Eising, Mu¨ller, Dijkstra, & Groothuis, 2003). In turtle eggs, free steroids were converted in yolk and embryos to sulfonated conjugates, possibly to increase solubility and transport into the embryo (Paitz & Bowden, 2008), suggesting that similar events may be occurring in bird eggs. Free steroids can be converted to inactive conjugates or to different unconjugated forms (e.g., conversion of androgens to estrogens), which may render them inactive or change their physiological activity, respectively. Conjugation increases solubility in water and may inactivate steroids and facilitate excretion (Pang, Schwab, Goresky, & Chiba, 1994), but may also facilitate uptake from the yolk via these now water-soluble forms via blood vessels into the embryo. Some steroid conjugates may even be active (Coughtrie, Sharp, Maxwell, & Innes, 1998); e.g., as neurosteroids (Baulieu & Robel, 1990; Compagnone & Mellon, 2000). Unconjugated steroids, such as 5b-reduced androgens,

Chapter | 4

107

Maternal Hormones in Avian Eggs

which are produced by two-day incubated embryos (Parsons, 1970; Antila, 1984), are frequently considered inactive metabolites, but are in fact active during embryonic development (Levere, Kappas, & Granick, 1967; Irving, Mainwaring, & Spooner, 1976; Aragones, Gonzalez, Spinedi, & Lantos, 1991). Thus, there is the potential for metabolism to modify the maternal hormonal signal in the egg, but it is not known how these metabolites act and thereby affect the embryo. Maternal steroid hormones also may regulate levels of steroid-metabolizing enzymes in the embryo, indirectly affecting levels of other maternal hormones or hormone production by the embryo itself (Balthazart, Baillien, Charlier, Cornil, & Ball, 2003). Testosterone and E2 do increase levels of P450aro in adult male and female Japanese quail (Schumacher & Hutchison, 1986), whereas other endogenous metabolites of T, such as 5a- and 5b-DHT, inhibit P450aro (Wozniak & Hutchison, 1993; Hutchison, Wozniak, Beyer, & Hutchison, 1996). Estradiol also downregulates 3b-hydroxysteroid dehydrogenase (3bHSD) (Schmidt et al., 2008), which is sexually dimorphic at specific stages in certain brain areas in Japanese quail (Aste, Watanabe, Shimada, & Saito, 2008). Such sex differences in metabolizing enzymes may explain sexspecific effects of maternal hormones. The most important enzymatic sex difference early in chicken development is for P450aro, which is expressed only in female embryonic gonads (Elbrecht & Smith, 1992). Therefore, only female embryonic gonads produce estrogens, resulting in sexual differentiation at this time. Later in development, males express P450aro in the brain, so that T is converted to E2, which is important in masculinizing the song system. Maternal androgens may therefore have androgenic effects on males and both estrogenic and androgenic effects on females during early embryonic development, as well as estrogenic effects on males when they start to express P450aro.

5.5. Binding Proteins As stated previously, birds have no specific sex hormonebinding globulin, so both CORT and androgens bind either to CBG or with low affinity to albumin. Levels of CORT may therefore indirectly influence free androgen levels or vice versa (Deviche, Breuner, & Orchinik, 2001; Breuner & Orchinik, 2002; Breuner et al., 2006). However, CBG is not present in embryos before day 10 (Siegel & Gould, 1976). Transthyretin (TTR), a thyroid hormone-binding protein, may influence uptake of THs from the yolk, and the thyroid hormone transporter organic anion transporting polypeptide 1c1 (OATP1c1) has been detected by day two of incubation (Darras et al., 2009). The role of binding proteins in uptake of maternal hormones by the embryo has not been studied.

5.6. Receptors (Time, Location) Receptors for steroid hormones are present by day three to four of incubation, as shown by immunohistochemical detection of P4 receptors (Guennoun et al., 1987) and for ERs (Andrews et al., 1997), by the presence of mRNA for ARs and ERs (Andrews et al., 1997; Smith, Andrews, & Sinclair, 1997; Endo et al., 2007), or by binding assays for corticosteroids (Pavlik, Novotna, & Jelinek, 1986). Thyroid hormone receptor mRNA is detectable within the first day of incubation (Flamant & Samarut, 1998), suggesting that receptors may be specifically expressed at this stage to respond to maternal hormones. Since some androgens can be converted to estrogens, they may act both on ARs and ERs. The spinal cord, spinal ganglia, and the glycogen body (corpus gelatinosum), a structure of unknown function associated with the lumbosacral region of the spinal cord and present only in birds, bind androgens in chicken embryos (Reid, Gasc, Stumpf, & Sar, 1981), and ARs were found in brain nuclei controlling muscles as well as in the syrinx (Godsave, Lohmann, Vloet, & Gahr, 2002; Veney & Wade, 2005). Androgen receptors in the ovary are important for ovarian development, possibly by upregulating P450aro levels in response to androgens, leading to an increase in E2 levels and feminization (Katoh, Ogino, & Yamada, 2006). Estrogen receptor-a is expressed in gonads and is important for sexual differentiation of the reproductive organs; in the brain at early stages both ERa and ERb are active, whereas later only ERa is expressed, and it seems to be more important for sexual differentiation of brain and behavior (Mattsson, Mura, Brunstro¨m, Panzica, & Halldin, 2008; Brunstro¨m, Axelsson, Mattsson, & Halldin, 2009; Mattsson & Brunstro¨m, 2010). Sex differences in steroid receptors occur in some brain areas and organs but not in others, although links to sex differences in behavior or morphology are not very clear (Veney & Wade, 2005; Voigt, Ball, & Balthazart, 2007; Ball & Balthazart, 2008). Early exposure to steroids may modify levels of hormone receptors in birds, since early T exposure in rats reduced ER expression (Kuhnemann, Brown, Hochberg, & Maclusky, 1995), and E2 administration to hatchlings upregulates AR expression in zebra finches (Kim, Perlman, & Arnold, 2004). There is thus potential for an influence of maternal hormones on the response to endogenously produced steroids or other hormones in the egg.

5.7. Embryonic Vs. Maternal Hormones Hormones of maternal and offspring origin are structurally identical, so that receptors cannot distinguish their origin and will respond equally to both. Before the onset of endogenous steroid hormone production, only maternal hormones can act on the receptors that are present already

108

at this stage. Therefore, this may be a special sensitive period for the effects of maternal hormones on offspring. Once embryos begin producing the same hormones, maternal hormones act with the endogenous hormones. Maternal hormones may have specific effects if the embryo does not yet produce a given hormone or if the maternal hormone is metabolized to a different form before, during, or after uptake by the embryo. Maternal hormones also may affect endogenous production of hormones through effects on synthesizing or metabolizing enzymes or alter the responsiveness to hormones due to effects on hormone receptors.

5.8. Conclusion Hormonal pathways that allow a response of the embryo to maternal hormones and a modification of the hormonal signal are present very early in development. So far these pathways have been studied primarily with respect to sexual differentiation in response to endogenously produced hormones or to understand the effects of endocrine disruptors taken up from the environment. Since these studies use far higher dosages and often long-lasting agonists or antagonists, their effects may be different from responses to maternal hormones, as exemplified by the strong effects of high levels of exogenous steroids on sexual differentiation, contrasting with the lack of effects of maternal androgens (for further discussion see Groothuis & Schwabl, 2008). Clearly, the specific roles of maternal hormones deposited in the egg require much more study in this context. Further, knowledge of the potential role of early sensitive phases for maternal hormones and of tissue-dependent metabolism and uptake of hormones is almost completely lacking. Finally, understanding the relevance of the pronounced decrease of maternal androgen concentrations in the yolk during early incubation is highly relevant: the decrease is too pronounced to be easily explained by dilution of the yolk with albumin. It is therefore very likely that metabolism of these hormones by the embryo, or by maternally derived enzymes, is involved. Finally, studies of the intriguing effects of both free and conjugated metabolites on the embryo are urgently needed.

6. FUNCTIONAL AND EVOLUTIONARY ASPECTS A maternal effect is the outcome of a coevolutionary process of the transfer of maternal signals or resources to the offspring and offspring responses to these substances. Maternal effects may be beneficial for mother and offspring, beneficial for one but detrimental for the other, or even detrimental for both (Marshall & Uller, 2007). It is often assumed that an adaptive maternal effect benefits

Hormones and Reproduction of Vertebrates

offspring, but maternal effects may reduce fitness of offspring while increasing maternal survival and thereby the number of her future offspring. Conversely, a maternal effect potentially can be adaptive for offspring survival even if maternal survival is negatively affected, but some constraint prevents the mother from adjusting the maternal effect. Finally, maternal effects, as in the example of a pathogen transmitted through the egg, may be detrimental for both mother and offspring. If maternal hormones are a mechanism of adaptive adjustment, it is implied that they have benefits in one context and costs in another context. If, for example, maternal hormones increase the use of resources for growth, these resources cannot be used for other processes such as maintenance of the immune system. Maternal hormones and the response to these hormones should thus be adjusted in such a way that costs and benefits of the responses are optimally matched to the given context. Further, the mechanism itself and its regulation produce costs, which have to be taken into account (Lessells, 2008). In the case of maternal hormones, this includes the cost of producing hormones and receptors and the regulatory system that allows the adjustment of yolk hormone levels to specific conditions and a specific response by offspring (Mu¨ller et al., 2007b). The cost of these processes is unknown, but since hormones are active at very small concentrations it may not be very costly to produce maternal hormones and the receptors. Hormonal mechanisms are also often thought to impose constraints on evolution, since they generally have effects on multiple traits, which reduces flexibility, since a change in one trait is not independent of changes in other traits. However, this is debatable, since it may also be possible to decouple effects on different traits over evolutionary time by changing the regulatory mechanisms (Hau, 2007; AdkinsRegan, 2008). Two nonexclusive evolutionary scenarios for the evolution of hormonally mediated maternal effects can be imagined. Yolk hormones may initially have been a sideeffect of elevated circulating levels, resulting in selection on offspring to respond to variation predicting important environmental conditions. This in turn creates a selection pressure on mothers to adjust yolk hormone levels depending upon the fitness consequences for mother and offspring. Alternatively, offspring may initially have expressed hormone receptors to respond to endogenously produced hormones that play a role in development. This could select for transfer of hormones to the egg to exploit the existing responsiveness to the benefit of mothers and/or offspring. At any rate, mechanisms of maternal and offspring control over the effects of maternal hormones ultimately coevolve depending upon the costs and benefits of the mechanisms and the effects for both mother and offspring.

Chapter | 4

Maternal Hormones in Avian Eggs

In this last section, the potential functions of variation of maternal hormones will be discussed in light of their effects on offspring development. Variation of yolk hormone levels in relation to various factors are reviewed at three levelsdwithin clutches, between clutches, and between species. Unfortunately, convincing experimental tests of their adaptive functions are few. Tables 4.3 and 4.4 show the major factors that influence yolk androgen levels within and between clutches.

6.1. Within-clutch Variation 6.1.1. Laying order and sibling competition Yolk androgen variation over the laying sequence is generally thought to play a role in sibling competition due to the beneficial effects on growth, begging, and competitiveness in some species. This idea was first raised by studies finding that concentrations of yolk androgens increase over the laying sequence in domestic canaries and stimulate growth and competitiveness (Schwabl, 1993; 1996b) whereas total amounts of yolk androgens decrease over the laying order in cattle egrets (Bubulcus ibis) (Schwabl, Mock, & Gieg, 1997) where last-hatching chicks rarely survive due to siblicidal behavior of the first chick. It was thus thought that yolk hormone levels increase with the position in the laying order in species with a brood survival strategy, while in species with a brood reduction strategy yolk hormone levels would decrease with the laying order. This idea has more recently become less clear, since in siblicidal blue-footed (Sula nebouxii) and brown (Sula leucogaster) boobies there were no consistent patterns across the laying order (Dentressangle, Boeck, & Torres, 2008; Drummond, Rodriguez, & Schwabl, 2008), and in kittiwakes (Rissa tridactyla), which are facultatively siblicidal, T levels even increase over the laying sequence (Gasparini et al., 2007). In all studied gull species and in homing pigeons, canaries, house sparrows, American kestrels, and communally breeding smooth-billed anis (Chrotophaga ani), T concentrations increase over the laying order (see Table 4.3). In one study on European starlings, yolk androgen concentrations increased over the laying order (Pilz, Smith, Sandell, & Schwabl, 2003), while, in another, variation over the laying order depended upon female mating status (Gwinner & Schwabl, 2005). Zebra finches (Gil et al., 1999), American coots (Fulica americana) (Reed & Vleck, 2001), and cattle egrets (Schwabl et al., 1997) are examples of species showing a decrease over the laying order, although in cattle egrets only total amounts of each androgen per egg are reported, so that it is unclear whether the decrease is the same for concentration of androgens per gram of yolk, since yolk mass often varies over the lay sequence. Finally, no overall species-specific pattern for

109

variation of T over the laying sequence is found in house wrens (Troglodytes aedon) (Ellis, Borst, & Thompson, 2001), Japanese quail (Hackl et al., 2003), tree swallows (Tachycineta bicolor) (Whittingham & Schwabl, 2002), great tits (Tschirren, Richner, & Schwabl, 2004), or blue tits (Cyanistes caeruleus) (Kingma et al., 2009). However, in two selection lines of great tits, T increased over the laying order for the bold genetic line and decreased for the shy genetic line, indicating that, even if there is no speciesspecific pattern, individuals may be consistent depending upon their genetic background (Groothuis et al., 2008). Interpretation of yolk androgens as modulators of sibling competition is complicated by the fact that effects on hatching time and growth are not always in the same direction. For example, yolk androgens delay hatching in American kestrels but lead to an advance in black-headed gulls. Although the increase of yolk androgen levels over the laying order is generally interpreted as a brood survival strategy, this would hold for gulls but not for American kestrels, where a delay in hatching time of higher-androgen eggs would reduce their ability to compete with siblings from earlier-laid eggs. Overall, evidence is weak that yolk hormones consistently mitigate or enhance the disadvantages of a sibling hierarchy. Unfortunately, there are no comparative studies on within-clutch variation, presumably because it has not been measured in enough species. Obviously, yolk androgens have important functions outside of sibling competition, since eggs of species that lay only one egg (therefore no sibling competition) still contain substantial levels of androgens (Go¨th, Eising, Herberstein, & Groothuis, 2008; Addison, Benowitz-Fredericks, Hipfner, & Kitaysky, 2008). Most interesting is perhaps that the effects of yolk androgens on growth and hatching time differ among species, suggesting that other costs and benefits of growth than those related to sibling competition may be important. Fast growth may have direct costs since insufficient resources would be allocated to other important processes (Metcalfe & Monaghan, 2001). Direct costs and benefits of developmental rate may thus be more important than the benefits in sibling competition. Another explanation for the inconsistency of results is that hormonal effects are context-dependent. For example, elevated androgen concentrations in last-laid eggs may only be beneficial under good environmental conditions where offspring can cope with the suppressive effects of androgens on immunity, resulting in increased brood survival; in contrast, brood reduction results when conditions are poor (Royle, Surai, & Hartley, 2001; Mu¨ller et al., 2005b). Often the question is raised as to why females should first induce a sibling hierarchy and then compensate for this competitive asymmetry by adding more hormones to the eggs. The hierarchy is created by starting incubation before

110

Hormones and Reproduction of Vertebrates TABLE 4.3 Parameters influencing within-clutch variation of yolk androgens for studies mentioned in the chapter Effect Of Laying order

Increase Domestic canary (T) American kestrel52(T) Starling37 Black-headed gull19,33(T,I) Lesser back-backed gull42 House sparrow50 Homing pigeon18 Black-legged kittiwake8 Smooth-billed ani47

Egg quality Sex (male ¼ higher)

Brood parasites/ communal breeders

Decrease 48,49

No/Inconsistent Effect 51

Cattle egret Zebra finch9,46(F) American coot41

Tree swallow60 House wren7 Japanese quail23 Brown and blue boobies3,4 Great tit21,56(G) Blue tit28 Zebra finch16,17(S,Q) Guira cuckoo2 Eastern bluebird35 European starling22(Q)

Black-headed gull20 Lesser black-backed gull42

Black-legged kittiwake8(B)

Peafowl35 House finch1

Barn swallow45 Zebra finch16,17(E,Q) Domestic chicken5,32(Q) Japanese quail39 Homing pigeon18 Lesser black-backed gull58 Peafowl29 Common cuckoo26

European starling40 Blue-tit57 Common cuckoo55 Brown-headed cowbird27,24 Guira cuckoo2 Smooth-billed anis47

Effects of other hormones mentioned in the chapter are not shown. Factors are indicated in the first column, positive effects on yolk androgens are shown in the second column, negative effects in the third column, and cases where no effects or both positive and negative effects were observed in the last column. ‘Comparative’ indicates correlations across several species. Modifying factors that resulted in increased, reduced, or reversed effects are indicated in brackets adjacent to the species name and are detailed below the table. References: 1 Badyaev et al., 2005; 2 Cariello et al., 2006; 3 Dentressangle et al., 2008; 4 Drummond et al., 2008; 5 Eising et al., 2003a;6Eising et al., 2008; 7 Ellis et al., 2001; 8 Gasparini et al., 2007; 9 Gil et al., 1999;10Gil et al., 2004a;11Gil et al., 2004b;12Gil et al., 2006a;13Gil et al., 2006b;14Gil et al., 2007;15Gil & Faure, 2007; 16 Gilbert et al., 2005;17Gilbert et al., 2007; 18 Goerlich et al., 2009; 19 Groothuis & Schwabl, 2002;20Groothuis et al., 2006;21Groothuis et al., 2008; 22 Gwinner & Schwabl, 2005;23Hackl et al., 2003; 24 Hahn et al., 2005;25Hargitai et al., 2009; 26 Hargitai et al., 2010; 27 Hauber & Pilz, 2003; 28 Kingma et al., 2009; 29 Loyau et al., 2007;30Mazuc et al., 2003;31Michl et al., 2005; 32 M€ u ller et al., 2002;33M€ u ller et al., 2004; 34 Navara et al., 2006a;35Navara et al., 2006c;36Petrie et al., 2001; 37 38 Pilz et al., 2003; Pilz & Smith, 2004; 39 Pilz et al., 2005a;40Pilz et al., 2005b; 41 Reed & Vleck, 2001; 42 Royle et al., 2001;43Rutstein et al., 2005;44Safran et al., 2008; 45 Saino et al., 2006; 46 Sandell et al., 2007; 47 Schmaltz et al., 2008; 48 Schwabl, 1993;49Schwabl, 1996a;50Schwabl, 1997a;51Schwabl et al., 1997; 52 Sockman et al., 2001;53Tanvez et al., 2004;54Tobler et al., 2007a; 55 To¨ro¨k et al., 2004; 56 Tschirren et al., 2004; 57 Vedder et al., 2007; 58 Verboven et al., 2003;59Verboven et al., 2005; 60 Whittingham & Schwabl, 2002. Modifying factors: S, sex; E, egg number; T, time of year; I, incubation onset; Q, female quality/male quality/dominance/nutrition; B, within/between broods; G, genetic background; F, food quality.

Chapter | 4

111

Maternal Hormones in Avian Eggs

TABLE 4.4 Parameters influencing between-clutch variation of yolk androgens for studies mentioned in the chapter Effect Of

Increase

Decrease 30,49

No/Inconsistent Effect Lesser black-backed gull59 Comparative14

Social stimulation

House sparrow Tree swallow60 American coot41 Black-headed gull19 Collared flycatcher25 Barn swallow13 Eastern bluebird35 European starling6,38

Male quality

Zebra finch9 Domestic canary11 Peafowl29 Blue-footed boobie3(Q) European starling22(E) Barn swallow13

House finch34 Collared flycatcher31

House sparrow30 Barn swallow44,45 Comparative14

Food

Zebra finch46 (E)

Lesser black-backed gull58

Zebra finch43(S)

Black-legged Kittiwake8 Season

Black-headed gull33(E) American kestrel52(E)

Barn swallow13 Domestic canary49 Pied flycatcher54(C)

Female quality

Zebra finch10 Domestic canary53 European starling37

Pied flycatcher54 Domestic chicken32 Lesser black-backed gull58 House martin12 Great tit55

Immune challenge Selection lines Sociality Boldness

European starling37* House sparrow30* Great tit21(G)*

Japanese quail15

Great tit21(G)

Effects of other hormones are not shown. Factors are indicated in the first column, positive effects on yolk androgens are shown in the second column, negative effects in the third column, and cases where no effects or both positive and negative effects were observed in the last column. ‘Comparative’ indicates correlations across several species. Modifying factors that resulted in increased, reduced or reversed effects are indicated in brackets behind the species name and are detailed below the table. For references, please see Table 4.3. *all three species increase early in the season and decrease later in the season. Modifying factors: S, sex; E, egg number; C, clutch number; G, genetic background; Q, year/environmental quality;

laying the last egg of the clutch, so that earlier-laid eggs hatch earlier and nestlings start to grow earlier. In principle, females should be able to regulate the hierarchy by delaying onset of incubation, as is typical for many temperate passerines such as great tits and blue tits. However, it may not always be possible to freely vary incubation onset since it may cause increased death of first-laid eggs due to detrimental influences of the environment such as heat, cold, infection, or predation. On the other hand, the asymmetry in competitiveness induced by early onset of incubation may have direct benefits by ensuring survival of first-hatched nestlings under suboptimal conditions, especially if these are not predictable at the time incubation starts. Yolk androgens may fine-tune the effects of incubation onset on the sibling hierarchy by increasing competitiveness of late-hatching nestlings so that they can

survive under good environmental conditions. In blackheaded gulls, e.g., yolk androgen levels increase more strongly over the laying sequence when incubation starts earlier, suggesting a mitigation of the negative effects of a strong sibling hierarchy (Mu¨ller, Eising, Dijkstra, & Groothuis, 2004). For a detailed discussion of this topic see Groothuis et al. (2005b).

6.1.2. Egg quality Variation in the allocation of different egg resources can be another mechanism to adjust competitiveness of siblings. Yolk hormone levels have often been found to be positively or negatively correlated with egg size or concentrations of egg components (e.g., carotenoids or antibodies). In the lesser black-backed gull and the black-headed gull,

112

nutrients and antibodies usually decrease over the laying order while androgen levels increase (Royle et al., 2001; Groothuis et al., 2006). Within- and between-clutch patterns can differ, as in black-legged kittiwakes where androgen levels and antibodies in yolk were negatively correlated within clutches but positively correlated between clutches (Gasparini et al., 2007). Such variation may reflect differences in overall investment in specific eggs, resulting in high and low quality eggs, or may indicate that different egg components are adaptively adjusted in relation to the amounts of other egg components (Royle et al., 2001; Groothuis et al., 2006). Resources such as antibodies, lipids, and carotenoids may be costly to acquire or to produce. A decrease of such components over the laying sequence may therefore suggest a constraint of maternal ability to acquire and allocate these resources throughout the laying period (Royle et al., 2001). Yolk hormones may be less costly to produce and transfer to the egg and have therefore been suggested as a relatively cheap way to compensate the offspring from these eggs for their lower overall quality (Groothuis et al., 2005b; Mu¨ller et al., 2007b). It is not clear to what extent the relationship between egg quality and yolk androgen levels is independent from the relationship with laying order, since both are confounded and have not been experimentally disentangled.

6.1.3. Parentage Even though most bird species are socially monogamous, a proportion of offspring is frequently fathered by different males. Since zebra finch females increase yolk androgen when paired to males with red leg bands that were supposedly more attractive (Gil et al., 1999), it might also be beneficial to invest in offspring of extra-pair males that are perceived to be of higher quality. However, a mechanism to modulate yolk hormone levels of individual eggs depending upon paternity is difficult to conceive (Birkhead, Schwabl, & Burke, 2000), since hormone accumulation of each egg is complete before ovulation and mating. The only possibility would seem to be an overall correlation with paternity, if, for example, the likelihood of extra-pair paternity decreases with the laying order (Magrath, Vedder, Van der Velde, & Komdeur, 2009), which could thus explain variations in yolk androgen levels with the laying sequence. However, this hypothesis has not been tested. It seems more likely that yolk androgens may be adjusted in relation to female parentage. Females may lay eggs in nests of conspecifics or, as in some cuckoo species, even in nests of a different species. It would be beneficial in such a situation for the brood parasite if her own offspring could outcompete the offspring of the host. Since many studies find that yolk androgens promote

Hormones and Reproduction of Vertebrates

offspring growth and competitiveness, eggs of broodparasitic females may contain higher levels of androgens. Unfortunately, the relation with conspecific brood parasitism has not been studied in species where it commonly occurs, and only in European starlings and blue tits, where it rarely happens and may therefore not be under strong selection. Yolk hormone levels were not consistently higher or lower in eggs of these species when laid in other females’ nests (Pilz, Smith, & Andersson, 2005b; Vedder et al., 2007). In interspecific brood parasites, no consistent pattern was found in brown-headed cowbirds (Molothrus ater) (Hauber & Pilz, 2003; Hahn et al., 2005), while androgens were not different or lower in eggs of common cuckoos (Cuculus canorus) (To¨ro¨k, Moska´t, Michl, & Pe´czely, 2004; Hargitai et al., 2010) compared with their hosts. Some data suggest that more vulnerable hosts may have higher androgen levels, suggesting that the evolution of host yolk androgens should be taken into account, which may change predictions (Hahn, Wingfield, Fox, Walker, & Richie, 2003). Further, the fact that more recently established brown-headed cowbird populations have the highest yolk T levels (Hahn et al., 2005) indicates that there may be some change in yolk androgen concentrations in parasitic and host species over evolutionary time. Finally, in communally breeding guira cuckoos (Guira guira) (Cariello, Macedo, & Schwabl, 2006) and smooth-billed anis (Schmaltz, Quinn, & Schoech, 2008), there was no evidence that certain females increased yolk androgen levels that would give an advantage to their own offspring competing with unrelated nestlings. Although adjustment of yolk androgen levels in relation to parentage would potentially be beneficial, this is not supported by data. It is also not very clear as to what to expect when considering the coevolution of hosts and parasites.

6.1.4. Sex When offspring reproductive value depends upon its sex, sex-ratio adjustment or differential parental investment with respect to offspring sex can be adaptive (Hamilton, 1967; Trivers & Willard, 1973; Charnov, 1982). As mentioned earlier, maternal hormones may affect the sex ratio at meiosis (primary sex ratio) as well as the secondary sex ratio later in embryonic and postnatal development due to sex-specific mortality. Primary sex-ratio adjustment is more attractive as an adaptive mechanism, since it is less costly than adjustment of the secondary sex ratio, which wastes the investment into eggs of the unwanted sex that are produced but do not result in surviving offspring. Despite the evidence for hormonal sex-ratio adjustment, it is not known whether this is indeed adaptive and results in increased Darwinian fitness.

Chapter | 4

113

Maternal Hormones in Avian Eggs

Maternal hormones may not only determine offspring sex but also depend upon sex, potentially by differential allocation depending upon growth of male and female follicles (Petrie, Schwabl, Brande-Lavridsen, & Burke, 2001; Young & Badyaev, 2004; Badyaev et al., 2005; Badyaev, Young, Hill, & Duckworth, 2008). However, sex differences of yolk hormones in incubated eggs may also be caused by sex differences in the metabolism and uptake of steroids from the yolk or at later stages by embryonic production of steroid hormones. This can especially be a problem when incubating eggs for several days to obtain tissue for sexing. Indeed, the hormone level results obtained at day 10 after the start of incubation (Petrie et al., 2001) could not be replicated in the same species when incubated for a much shorter time (Loyau, Saint Jalme, Mauget, & Sorci, 2007). Yolk hormone levels should therefore be measured as early as possible in the incubation period, which may make it difficult to also determine offspring sex due to lack of tissue for sex determination. In the majority of studies measuring yolk androgen levels after minimal incubation, sex differences were not found (Eising et al., 2003a; Verboven et al., 2003; Pilz, Adkins-Regan, & Schwabl, 2005; Saino et al., 2006; Loyau et al., 2007), or only in interaction with other factors (Mu¨ller, Eising, Dijkstra, & Groothuis, 2002; Gilbert, Rutstein, Hazon, & Graves, 2005), warranting some caution when considering some of these results. However, in the domestic chicken, the allocation of yolk androgens is consistent with expectations from sex-allocation theory. Dominant females were of higher quality and allocated more T to sons while subdominant females allocated more T to daughters (Mu¨ller et al., 2002). In such a polygynous social system, high-quality females are expected to invest in sons, since this can have a stronger impact on male reproductive success, which is more variable than female reproductive success and therefore increases much more strongly with male quality. Although there is thus support for an influence of maternal hormones on offspring primary or secondary sex ratios, and possibly for sex-specific hormone deposition in eggs, there is insufficient evidence that these represent mechanisms of adaptive sex allocation.

6.1.5. Bet-hedging Variation of offspring quality within clutches may represent a bet-hedging strategy in unpredictable environments by which overall variation in offspring phenotypes is increased, resulting in higher fitness of at least some offspring (Philippi & Seger, 1989; Crean & Marshall, 2009). Within-clutch variation in yolk hormone levels that is not related to any specific factor can potentially create such variation in offspring phenotype, but the advantages and disadvantages of such within-clutch variation have not been studied.

6.2. Between-clutch Variation Many studies have observed differences between clutches in relation to a variety of factors such as breeding density, adjustment to food availability, season, male or female quality, pathogens, and predation. Between-clutch or between-female variation in yolk androgen levels can be larger than within-female variation in yolk T concentrations in relation to laying order (Schwabl, 1996a; Groothuis & Schwabl, 2002; Williams, Kitaysky, & Vezina, 2004). This may reflect direct effects of the environment but also differences in female quality due to conditions experienced earlier in life or possibly to genetic differences between females (Groothuis et al., 2005b; Gil, 2008). Effects of between-clutch variation in yolk androgens may optimally adjust offspring to the conditions they experience during early development or later in life. Whether effects of yolk androgen variations are matched to the context has not been experimentally tested. Such a test should show that high hormone levels are beneficial in one context but detrimental in another context, while the reverse, i.e., detrimental effects in the former and beneficial in the latter context, should be true for low hormone levels (for details on the design of such an experiment see Groothuis & von Engelhardt, 2005). Since such studies are lacking, potential adaptive effects are discussed by exploring whether the observed effects of yolk hormones are consistent with the variation in conditions that influence yolk hormone levels.

6.2.1. Social interactions Several studies report a positive relationship between yolk androgen levels and social interactions, as shown by positive correlations with nest box density (house sparrow) and nest density (American coot, black-headed gull), intrusions at nest sites (tree swallow), and colony size in different species (Schwabl, 1997a; Reed & Vleck, 2001; Groothuis & Schwabl, 2002; Whittingham & Schwabl, 2002; Mazuc et al., 2003; Pilz & Smith, 2004). One question is whether social interactions increase androgen levels or whether female quality influences both androgen levels and social interactions, since, e.g., house sparrows in higher densities have a better body condition. In correlative studies, social interactions may thus not influence yolk androgen levels but females may choose or defend certain sites depending upon individual differences in androgen production and behavior. In the black-headed gull, yolk androgen levels were higher when females were breeding at the periphery of the colony at low nest densities. The authors suggested that this might be due to higher aggressiveness and androgen production of females defending larger and better territories (Groothuis & Schwabl, 2002). Experimental increase of nest density and simulated intrusions also increase yolk androgen levels (Gil et al.,

114

2006b; Navara et al., 2006c; Hargitai, Arnold, Herenyi, Prechl, & To¨ro¨k, 2009). Yolk androgens increase when simulating intrusions by presenting an unfamiliar male to a house sparrow pair (Mazuc et al., 2003), although the results of the study are difficult to interpret since they are corrected for female circulating levels and for nest-density effects. The only experimental study finding no effect was in lesser black-backed gulls (Verboven et al., 2005), but in this study social interactions but not female aggressive behavior increased. Increasing yolk androgen levels in relation to an increase in group size, density, or social interactions has been thought to represent an adaptation to increased competition. Offspring that develop faster and are more competitive should fare better under these conditions. Another potential benefit is increased dispersal, as observed in great tits hatching from eggs with elevated T (Tschirren et al., 2007). Conversely, yolk androgens tend to suppress immunity, which should be more problematic at higher densities. This was thought to be a possible explanation of why female black-headed gulls breeding in the center of the colony, where the risk of exposure to pathogens would seem to be higher, had lower androgen levels (Groothuis & Schwabl, 2002). There are unfortunately no studies on the effects of yolk androgens when offspring are reared in different social conditions.

6.2.2. Male quality Female zebra finches paired to males wearing red leg rings deposited higher levels of androgens in their eggs (Figure 4.3) (Gil et al., 1999). Since female zebra finches preferred males wearing red rings (Burley, Krantzberg, & Radman, 1982), it was thought that elevated yolk androgens indicate increased investment in offspring sired by these attractive males and are possibly causally involved in sex-ratio adjustments. Subsequently, several other studies also found effects of male quality. Yolk androgen levels increased with eyespot density in peafowl (Pavo cristatus) (Loyau et al., 2007), depended upon color and/or streamer length in barn swallows (Gil et al., 2006b; but see Saino et al., 2006; Safran, Pilz, McGraw, Correa, & Schwabl, 2008), and depended upon male song in domestic canaries (Gil, Leboucher, Lacroix, Cue, & Kreutzer, 2004; Tanvez et al., 2004). Rapid changes in yolk androgen levels were observed when male coloration was manipulated during egg laying. Blue-footed boobies laid smaller second eggs with less AND, but not less T, when the feet of their males were dulled (Dentressangle et al., 2008). In contrast, blue tits laid eggs with less T, but not less AND, following blocking ultraviolet (UV) reflectance of the males’ crown feathers (Kingma et al., 2009). For female European starlings, the pattern of yolk AND concentrations, but not of other hormones measured (T, DHT, E2), differed over the

Hormones and Reproduction of Vertebrates

laying order in relation to their mating status. Androstenedione levels increased when paired to monogynous males, decreased for primary females of polygynous males, and did not change for secondary females of polygynous males (Gwinner & Schwabl, 2005). Conversely, a negative relationship with male attractiveness was found in house finches (Navara, Hill, & Mendonc¸a, 2006a) and females paired to younger, presumably inexperienced, collared flycatchers deposited higher androgen levels in their eggs (Michl, To¨ro¨k, Pe´czely, Garamszegi, & Schwabl, 2005). Finally, house sparrow females (Mazuc et al., 2003) did not change yolk androgen levels when paired to androgenimplanted males, which should have affected their attractiveness by elevating song rate, aggressiveness, and size of the black badge, although no actual effect on male traits were reported. Across species, no relationship between yolk T and sexual dichromatism or mating system (monogamous/polygamous) was found (Gil et al., 2007), although monochromatic species had lower yolk T levels, but only when not controlling for phylogeny. Different functional explanations may elucidate a relationship between yolk androgen levels and male mate quality. It was suggested that females may increase investment when paired to high-quality males (Burley, 1988; Sheldon, 2000) or to compensate for the low quality of a male (Navara et al., 2006a; Moreno-Rueda, 2007). In fact, both may reflect a compensatory adjustment in relation to male parental care, which correlates positively with male attractiveness in house finches (Hill, 1991) but negatively in zebra finches (Burley, 1988). However, the single study testing this question did not find that yolk androgens stimulate male parental care (Tschirren & Richner, 2008). A third idea is that yolk androgens may be adjusted to offspring genetic quality, assuming that offspring of high genetic quality are better able to deal with the negative consequences of elevated yolk androgens on the immune system, for example (see Section 4.1.4). This could potentially explain negative effects of elevated yolk androgens on male growth and survival (Rutkowska & Cichon, 2006; von Engelhardt et al., 2006). If the genetic quality of sons influences their sensitivity to detrimental effects of yolk androgen, any increase in yolk androgen levels in eggs fathered by average-quality males should result in negative effects. This assumes that genetic sensitivity of daughters to androgens is not related to paternal quality. So far there have been no tests of whether sons of attractive males can deal better with the costs of elevated yolk androgens.

6.2.3. Food The availability or quality of food is important for offspring development and survival, either directly or indirectly, by influencing maternal condition and ability to care for

Chapter | 4

115

Maternal Hormones in Avian Eggs

offspring. Better maternal feeding conditions were related to overall reduced yolk androgen concentrations in lesser black-backed gulls and black-legged kittiwakes (Verboven et al., 2003; Gasparini et al., 2007). However, in zebra finches, average androgen levels did not change with food quality available for the mother, although yolk androgen levels decreased over the laying sequence under a lowquality diet but not under a high-quality diet (Sandell, Adkins-Regan, & Ketterson, 2007). In another study on zebra finches, yolk hormone levels in eggs depended in a complex way on diet, offspring sex, and treatment order (Rutstein, Gilbert, Slater, & Graves, 2005). Yolk androgen levels may be adjusted to potential competition for food in relation to feeding conditions. This is consistent with the positive effects of yolk androgens on survival of European starlings in a bad year (Pilz et al., 2004), although this study is based on a very small sample of 1 out of 22 vs. 5 out of 34 nestlings dying. Again, there are unfortunately no studies analyzing the consequences of variation in yolk androgens under different feeding conditions.

effects. Since food availability and offspring survival chances are often higher early in the season, earlier-laying birds may follow a brood survival strategy, while later in the season a brood reduction strategy may be more beneficial. This would fit with the observation that in some species yolk androgens increase with laying order early in the season (brood survival strategy) and decrease later in the season (brood reduction strategy), while the reverse has not been reported. Conversely, the decrease of average yolk androgens with season observed in some species does not fit with the hypothesis that yolk androgens increase competitiveness, since later-hatching young should face more competition. A seasonal decrease may alternatively be functionally related to a seasonal increase in the presence of pathogens, since yolk androgens suppress immunity in some studies. The consequences of exposure to yolk androgens at different times in the season are thus likely to depend upon species-specific differences in predation risk, pathogens, and competition, but actual costs and benefits still have to be measured.

6.2.5. Female quality 6.2.4. Season Several studies find seasonal variation in yolk androgen levels, mostly with higher amounts early in the season (Gil et al., 2006b; Tobler, Granbom, & Sandell, 2007) or an initial increase followed by a decrease in concentrations (Mazuc et al., 2003; Pilz et al., 2003). Similarly, in two genetic selection lines of great tit that differed in laying date, the earlier-laying genetic line showed an increase in yolk T and AND over the laying sequence, and the laterlaying genetic type showed a decrease of these yolk androgens over the laying sequence (Groothuis et al., 2008). Yolk androgen levels in pied flycatchers (Ficedula hypoleuca) increased over the laying order in first clutches and decreased or did not change with the laying order in replacement clutches (Tobler et al., 2007a), and in domestic canaries yolk androgen levels were lower and the increase over the laying sequence was less pronounced in later-laid clutches (Schwabl, 1996a). In contrast, in blackheaded gulls (Mu¨ller et al., 2004) and in American kestrels (Sockman, Schwabl, & Sharp, 2001), the increase over the laying order became more pronounced as the season progressed. In the black-headed gulls, this was related to an earlier onset of incubation and therefore more pronounced hatching asynchrony. This suggests, as indicated earlier when discussing egg quality (see Section 6.1.2), that enhanced yolk androgen levels may act to compensate for poor environmental conditions or higher competition. Many factors that change with season, such as competition, food availability, presence of pathogens, and predation risk may select for hormone-mediated maternal

Yolk androgen levels may relate to differences between females, independent of current environmental conditions. There is evidence that individual females of the same species differ consistently in how much androgen they deposit in their eggs. Although part of this consistency perhaps may be due to consistency in environmental factors, as in the study by Tobler et al. (2007a), this was less likely in a study measuring birds repeatedly across years (Eising, Pavlova, Groothuis, Eens, & Pinxten, 2008). These differences may be due to quality differences between females, age, environmental conditions experienced earlier in life, and genetic differences (Tschirren, Sendecka, Groothuis, Gustafsson, & Doligez, 2009; see also Section 4.2.4). Higher-quality females may be able to deposit higher levels of androgens, because they can cope better with the costs of high androgen levels (either in the female circulation or in offspring). However, there is evidence for both a negative and a positive relationship between yolk androgen levels and female quality. Female pied flycatchers (Tobler et al., 2007a) and lesser black-backed gulls (Verboven et al., 2003) in good condition deposit less yolk androgen in their eggs, while higher concentrations of yolk androgens were found in eggs of female zebra finches reared in small clutches that presumably were in better condition (Gil et al., 2004a). High-ranking chickens (Mu¨ller et al., 2002) have lower concentrations of androgens in their eggs than low-ranking hens, but high-ranking canaries (Tanvez et al., 2004) and older starlings (Pilz et al., 2003) deposit more androgens, so overall there is no clear pattern with respect to female quality. Some studies performed more short-term manipulations of female quality,

116

Hormones and Reproduction of Vertebrates

while other studies measured or manipulated more longterm aspects of female quality. However, female quality can encompass very different aspects, which may explain some of the differences.

6.2.6. Parasites A relation of yolk androgens with parasite prevalence has been proposed because androgens frequently affect the immune system negatively. Two studies report that an immune challenge in house martins (Gil, Marzal, De Lope, Puerta, & Møller, 2006) or parasite exposure in great tits (Tschirren et al., 2004) reduces yolk androgen levels. Reducing yolk androgen levels in relation to parasite prevalence would seem an adaptive strategy, since yolk androgens may suppress immunity (see Section 4.1.4; Mu¨ller et al., 2005b). However, yolk androgens did not affect immunity in great tits but instead increased natal dispersal, and individuals with higher natal dispersal had higher fitness (Figure 4.9) (Tschirren et al., 2007). Interestingly, this appeared to be an adaptive response, since, in areas with high pathogen levels (and thus lower androgen levels), individuals disperse less and exhibit greater fitness (Heeb et al., 1999; Tschirren et al., 2007). Why reduced dispersal should be beneficial in areas with higher pathogen levels is unclear, but the authors suggested that it might reflect a benefit of adapting to local parasites or a reduced ability of infected animals to cope with new environments.

6.3. Between-species Comparison Comparative studies allow us to analyze whether variations in certain conditions, such as predation risk or sociality of a species, are associated with variation in yolk hormone levels. However, species comparisons are correlative, so that cause and effect cannot easily be disentangled, and patterns do not necessarily reflect experimental effects within species. An example mentioned below is the association of high levels of blood parasites with a short incubation period, which has been interpreted either as indicating that there is selection for rapid development to protect from parasites, or the contrary: that offspring developing rapidly are less well defended against parasites. Another difficulty is that effects of yolk hormones are not consistent across species but can be quite variable, potentially because the response to maternal hormones is under selection and therefore evolving as well. This is a similar difficulty that is encountered when attempting to explain variation in plasma hormone levels, where average hormone levels seem to be less informative than the variation in hormonal responsiveness and variation in sensitivity of the organism to hormones (Ball & Balthazart, 2008). Nevertheless, several comparative studies report

FIGURE 4.9 Elevation of yolk testosterone (T) increased dispersal in great tits (Parus major) (mean standard error; upper panel) and larger dispersal distances were positively correlated with increased reproductive success in parasite-free nests but negatively correlated in parasitized nests (upper panel). Reprinted from Tschirren, Fitze, & Richner (2007) with permission from the University of Chicago Press.

interesting relationships; these have been included in Table 4.3 and are discussed below. There are no comparative studies on within-clutch variation, presumably because it has not been measured in a large enough number of species.

6.3.1. Social stimulation A relationship between circulating T levels and coloniality or group size was observed across species, as within species, and coloniality was related to AND, but not T levels in the egg (Gil et al., 2007).

6.3.2. Parasite exposure Effects on growth rate may also be an adaptation to parasite exposure, but the direction that such an effect should have is less clear. Within temperate species, shorter incubation periods and longer nestling periods are related to higher

Chapter | 4

117

Maternal Hormones in Avian Eggs

mortality through parasites (Møller, 2005). Incubation period was also negatively correlated with the prevalence of adult blood parasites (Ricklefs, 1992). Finally, passerines with higher blood parasite exposure appear to mount a better immune response, but species with longer incubation periods mount a weaker response (Schwabl, Palacios, & Martin, 2007). These results may indicate that either high prevalence of parasites selects for shorter incubation periods or the opposite; i.e., long incubation periods allow for a better defense. Across passerine species, short incubation periods were correlated with high T and DHT levels (see Figure 4.10) (Gorman & Williams, 2005; Schwabl et al., 2007), except for one study, when using a phylogenetic correction (Gil et al., 2007). Conversely, high AND correlated with a relatively long incubation period compared to the nestling period, suggesting that AND may increase time to hatching or shorten the nestling period (Gil et al., 2007). Experimental data are controversial since high yolk androgen levels both reduced (Eising

et al., 2001; Mu¨ller & Eens, 2009) and increased (Sockman & Schwabl, 2000; von Engelhardt et al., 2006) time to hatching. Effects of androgens on incubation time and their functional benefits in relation to parasite exposure are thus unclear.

6.3.3. Predation risk Relative predation risk for adult and young birds is thought to select for differences in developmental rate, which are influenced by maternal androgens. In tropical species, adult mortality is relatively low and incubation periods are long, whereas incubation periods are typically shorter and adult mortality is higher in temperate species (Martin, 2002; Martin & Schwabl, 2008). Rapid development may have detrimental short- and long-term effects (Metcalfe & Monaghan, 2001) so that slow growth may be favorable for tropical species that have a longer life-span due to lower adult mortality. Alternatively, parents of long-lived species may invest more in their own survival and reduce parental investment, including nest attendance, which could explain lower average egg temperatures found in tropical species (Martin & Schwabl, 2008). Under such conditions, development would require more resources and be more costly for embryos, so that in both cases it would seem beneficial to reduce growth-promoting effects of high androgen levels, which is in line with the finding that yolk androgen levels are lower in tropical species (Martin & Schwabl, 2008). In contrast, when nestling predation risk is high, rapid offspring development would seem beneficial. Elevating yolk androgens may be a mechanism to enhance offspring growth, which is supported by a positive correlation between nestling predation rate and yolk T, and between yolk T and offspring growth in a comparative study of temperate species (Figure 4.10) (Schwabl et al., 2007). Whether yolk hormone levels are also adjusted within species to predation risk is unknown.

6.4. Conclusion

FIGURE 4.10 Yolk testosterone (T) concentrations correlated negatively with the incubation period (upper panel) and the nestling period (middle panel), and positively with offspring growth rate (lower panel) in a comparative analysis using 25 passerine species. Reprinted from Schwabl, Palacios, & Martin, T. E. (2007) with permission from the University of Chicago Press.

Levels of yolk androgens and other yolk hormones of maternal origin are influenced by a range of factors that are potentially relevant for offspring survival and development. Yolk androgens and other yolk hormones may thus provide information regarding environmental conditions to offspring, allowing them to optimize their development. Evidence for the predominant hypothesis that within-clutch variation regulates sibling competition is not yet convincing. For between-clutch variation, only the effects of social density are consistent. Comparisons between species are relatively new and promising approaches but the interpretation is still difficult. Experiments should test

118

effects of yolk hormones both in the context where they are naturally high and in the context where they are naturally low and test whether a match is beneficial whereas a mismatch is detrimental.

6.5. ParenteOffspring Conflict and Coadaptation Reduced or elevated yolk hormone levels may not only have consequences for the offspring directly exposed to the hormones but also affect siblings and/or parents indirectly. Most studies have measured effects on offspring from treated eggs, but not indirect effects on the parents and siblings of current or future broods. For example, rearing offspring from eggs with high hormone levels may have costs that reduce future reproductive success. Unfortunately, most studies treat all eggs in a clutch equally and do not analyze effects on untreated siblings or parents. Constraints or costs associated with regulating yolk hormone levels also have to be taken into account. If levels in the circulation and the yolk are not independent, regulating yolk hormone levels will expose the mother to varying levels of circulating hormone levels, with potentially negative side-effects. From an evolutionary perspective, there is a conflict between parents and offspring over the distribution of investment to different offspring (Trivers, 1974). Each individual offspring benefits from obtaining a larger proportion of parental investment, while for parents more equal allocation of resources over all offspring is optimal. Evolution of hormone-mediated maternal effects depends upon selection on maternal mechanisms regulating hormone transfer in relation to environmental

Hormones and Reproduction of Vertebrates

conditions (Figure 4.11(a)) and on offspring mechanisms regulating development in relation to yolk hormone levels in the egg (Figure 4.11(b)). Together, this results in an overall relationship between environmental conditions and offspring development (Figure 4.11(c)), which determines the fitness consequences for mother and offspring (for details see Mu¨ller et al., 2007b). One can therefore ask to what extent effects of maternal hormones on offspring maximize maternal or offspring fitness, and thus whether mothers or offspring may ‘win’ a potential conflict over the outcome of a maternal effect (Mu¨ller et al., 2007b). Theoretical and empirical studies suggest that offspring benefit directly from this transfer of information while mothers benefit only indirectly through enhanced offspring fitness (Hinde, Johnstone, & Kilner, 2010). It has also been argued that offspring cannot ‘win’ parenteoffspring conflict, since they have no information about the environment and the costs of countermeasures to maternal influences are too high (Sockman, Sharp, & Schwabl, 2006; Groothuis & Schwabl, 2008). Although it is true that offspring may have no independent information, hormones could provide this information indirectly, which would select for a mechanism allowing offspring to respond to this information. Obviously the reality is likely to be even more complex, since mothers may have other ways to influence offspring development and fathers may contribute a large amount of parental investment and may be influenced by hormonal effects (for more on this issue see Mu¨ller et al., 2007b). Maternal adjustment of yolk hormones and offspring adjustment of development are therefore expected to coevolve, depending upon the fitness consequences for all family members.

FIGURE 4.11 The relationship between yolk hormone levels and the environment is represented by the curve in panel (a) and the relationship between yolk hormone levels and offspring development by the curve in panel (b). In a given environment ei, the amount of hormone deposited by the mother is given by hi, and an amount hi of yolk hormone results in a developmental response di by offspring. From these two curves, the relationship between environment and offspring development shown in panel (c) can be derived by plotting each pair of points ei and di. The evolution of hormone-mediated maternal effects depends upon selection on the mechanisms under maternal control that shape the curve in panel (a) and the mechanisms under offspring control that shape the curve in panel (b), which together determine the relationship between environment and offspring development (panel (c)). Reprinted from M€ uller, Lessells, Korsten, & von Engelhardt (2007b) (For details, see M€ uller et al., 2007b) with permission from the University of Chicago Press.

Chapter | 4

119

Maternal Hormones in Avian Eggs

7. CONCLUSION, GAPS, AND PERSPECTIVES Many factors influence avian yolk hormone levels, and yolk hormones affect a wide range of offspring traits. Patterns of variation and effects within and between clutches and between species suggest that maternal hormones may act as adaptive maternal effects, but so far few studies have actually tested adaptive hypotheses experimentally. An adaptive function of yolk hormones implies that the net consequences of yolk hormones are positive when yolk hormone levels are naturally high and negative when yolk hormone levels are naturally low. In other words, positive effects should outweigh negative effects when levels of yolk hormones match the respective environmental conditions. Therefore, both hormone levels and context need to be manipulated to test adaptive hypotheses. Assuming that hormone levels in the egg are optimized, elevating hormone levels always induces a deviation from this optimum and therefore produces detrimental effects, unless the context is also changed. This can be difficult to test if yolk hormone levels are adjusted to parameters that are hard to manipulate in the wild, such as egg composition or offspring genetic quality. Moreover, fitness estimates have almost always been measured on the effect for the offspring, and effects on parents and siblings have been neglected. These indirect effects, however, are also relevant for natural selection to act on maternal hormones. On the other hand, yolk hormones may not be adaptive. Mothers may regulate circulating hormone levels to respond to variations in the environment, and hormones may ‘leak’ into the egg. In this case, yolk hormones might be informative only about environmental conditions relevant for the mother and not for offspring, so that offspring would not necessarily benefit from responding to maternal hormones. Further, effects of maternal hormones on offspring may not be specific, but a sideeffect of a response to their own endogenously produced hormones. If mothers cannot specifically regulate the transfer of hormones to the egg and offspring cannot specifically regulate responses to maternal hormones, the evolution of adaptive maternal effects mediated by yolk hormones is constrained and effects may even be detrimental for both mother and offspring. Adaptive adjustment thus requires some degree of flexibility in regulating yolk and circulating levels, and in responding to yolk hormones and endogenously produced hormones. The best evidence that mothers regulate yolk hormone levels is the large variation in relative amounts of different steroids in eggs and circulation and the large species differences in relative amounts in the yolk when exposed to different conditions. The best support for an

ability of offspring to regulate their responses to maternal hormones is provided by the large change of yolk hormone levels over the course of incubation, by the evidence for metabolism of yolk hormones, and by sex and species differences in the strength and even direction of effects of yolk hormones on offspring. However, very little is known about the mechanisms regulating hormone transfer to the egg and regulation of offspring responses. As this chapter was limited mostly to the effects of yolk T and other androgens, reflecting the focus of most research, a number of other steroids and nonsteroidal hormones that are present have not received much attention. Yolk hormones correlate with a variety of factors and may therefore play a role in adjusting offspring development optimally to the context. Before concluding that they have such an adaptive function, however, it is necessary to show that benefits indeed outweigh costs in the appropriate context. To some extent this depends upon the constraints of the regulatory mechanisms, which are still poorly understood. While maternal hormones thus represent an intriguing possible mechanism of adaptive intergenerational phenotypic plasticity, many basic questions regarding their function and mechanism still need to be addressed.

ABBREVIATIONS 3b-HSD ACTH AND AR CBG CORT CRH DHT E2 ER FSH GH GnRH GTH HPLC LH MEL mRNA OATP1c1 P4 P450aro P450C17 T T3 T4 TH TTR TSH UV

3b-hydroxysteroid dehydrogenase Corticotropin Androstenedione Androgen receptor Corticosteroid-binding globulin Corticosterone Corticotropin-releasing hormone Dihydrotestosterone Estradiol Estrogen receptor Follicle-stimulating hormone Growth hormone Gonadotropin-releasing hormone Gonadotropin High performance liquid chromatography Luteinizing hormone Melatonin Messenger ribonucleic acid Organic anion transporting polypeptide 1c1 Progesterone Aromatase 17a-hydroxylase/17,20-lyase Testosterone Triiodothyronine Thyroxine Thyroid hormone Transthyretin Thyrotropin Ultraviolet

120

REFERENCES Abdelnabi, M. A., & Ottinger, M. A. (2003). Hypothalamic indolamines during embryonic development and effects of steroid exposure. Gen. Comp. Endocrinol., 130, 13e19. Addison, B., Benowitz-Fredericks, Z. M., Hipfner, J. M., & Kitaysky, A. S. (2008). Are yolk androgens adjusted to environmental conditions? A test in two seabirds that lay single-egg clutches. Gen Comp Endocrinol, 158, 5e9. Adkins-Regan, E. (2008). Do hormonal control systems produce evolutionary inertia? Philos Trans R Soc Lond B Biol Sci., 363, 1599e1609. Adkins-Regan, E., & Ascenzi, M. (1987). Social and sexual behavior of male and female zebra finches treated with estradiol during the nestling period. Anim Behav, 35, 1100e1112. Adkins-Regan, E., Ottinger, M. A., & Park, J. (1995). Maternal transfer of estradiol to egg yolks alters sexual differentiation of avian offspring. J Exp Zool, 271, 466e470. Adkins-Regan, E., Pickett, P., & Koutnik, D. (1982). Sexual differentiation in quaildconversion of androgen to estrogen mediates testosterone-induced demasculinization of copulation but not other male characteristics. Horm Behav, 16, 259e278. Adkins, E. K. (1975). Hormonal basis of sexual differentiation in Japanese quail. J Comp Physiol Psychol, 89, 61e71. Andrews, J. E., Smith, C. A., & Sinclair, A. H. (1997). Sites of estrogen receptor and aromatase expression in the chicken embryo. Gen. Comp. Endocrinol., 108, 182e190. Andersson, S., Uller, T., Lo˜hmus, M., & Sundstro¨m, F. (2004). Effects of egg yolk testosterone on growth and immunity in a precocial bird. J Evol Biol, 17, 501e505. Antila, E. (1984). Steroid conversion by oocytes and early embryos of Salmo gairdneri. Ann Zool Fenn, 21, 465e471. Antila, E., Leikola, A., & Tahka, S. (1984). Early steroid metabolism by chick blastoderm in vitro. Steroids, 43, 315e323. Aragones, A., Gonzalez, C. B., Spinedi, N. C., & Lantos, C. P. (1991). Regulatory effects of 5-beta-reduced steroids. J Steroid Biochem Mol Biol, 39, 253e263. Arcos, M. (1972). Steroids in egg-yolk. Steroids, 19, 25. Aste, N., Watanabe, Y., Shimada, K., & Saito, N. (2008). Sex- and agerelated variation in neurosteroidogenic enzyme mRNA levels during quail embryonic development. Brain Res, 1201, 15e22. Badyaev, A. V., Schwabl, H., Young, R. L., Duckworth, R. A., Navara, K. J., & Parlow, A. F. (2005). Adaptive sex differences in growth of preovulation oocytes in a passerine bird. Proc R Soc B, 272, 2165e2172. Badyaev, A. V., Young, R. L., Hill, G. E., & Duckworth, R. A. (2008). Evolution of sex-biased maternal effects in birds. IV. Intra-ovarian growth dynamics can link sex determination and sex-specific acquisition of resources. J Evol Biol, 21, 449e460. Bahr, J. M., Wang, S. C., Huang, M. Y., & Calvo, F. O. (1983). Steroid concentrations in isolated theca and granulosa layers of preovulatory follicles during the ovulatory cycle of the domestic hen. Biol Reprod, 29, 326e334. Ball, G. F., & Balthazart, J. (2008). Individual variation and the endocrine regulation of behaviour and physiology in birds: a cellular/molecular perspective. Philos Trans R Soc, B, 363, 1699e1710. Balthazart, J., Baillien, M., Charlier, T. D., Cornil, C. A., & Ball, G. F. (2003). The neuroendocrinology of reproductive behavior in Japanese quail. Domest Anim Endocrinol, 25, 69e82. Baulieu, E. E., & Robel, P. (1990). Neurosteroidsda new brain function. J Steroid Biochem Mol Biol, 37, 395e403.

Hormones and Reproduction of Vertebrates

Bertin, A., Richard-Yris, M. A., Houdelier, C., Richard, S., Lumineau, S., Kotrschal, K., et al. (2009). Divergent selection for inherent fearfulness leads to divergent yolk steroid levels in quail. Behav, 146, 757e770. Birkhead, T., Schwabl, H., & Burke, T. (2000). Testosterone and maternal effectsdintegrating mechanisms and function. Trends Ecol Evol, 15, 86e87. Boncoraglio, G., Rubolini, D., Romano, M., Martinelli, R., & Saino, N. (2006). Effects of elevated yolk androgens on perinatal begging behavior in yellow-legged gull (Larus michahellis) chicks. Horm Behav, 50, 442e447. Breuner, C. W., & Orchinik, M. (2002). Plasma binding proteins as mediators of corticosteroid action in vertebrates. J Endocrinol, 175, 99e112. Breuner, C. W., Lynn, S. E., Julian, G. E., Cornelius, J. M., Heidinger, B. J., et al. (2006). Plasma-binding globulins and acute stress response. Horm Metab Res, 38, 260e268. Bruggeman, V., Van As, P., & Decuypere, E. (2002). Developmental endocrinology of the reproductive axis in the chicken embryo. Comp Biochem Physiol, Part A: Mol Integr Physiol, 131, 839e846. Brunstro¨m, B., Axelsson, J., Mattsson, A., & Halldin, K. (2009). Effects of estrogens on sex differentiation in Japanese quail and chicken. Gen Comp Endocrinol, 163, 97e103. Buchanan, K. L., Evans, M. R., Goldsmith, A. R., Bryant, D. M., & Rowe, L. V. (2001). Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc B, 268, 1337e1344. Buchanan, K. L., Goldsmith, A. R., Hinde, C. A., Griffith, S. C., & Kilner, R. M. (2007). Does testosterone mediate the trade-off between nestling begging and growth in the canary (Serinus canaria)? Horm Behav, 52, 664e671. Burch, W. M., & Lebovitz, H. E. (1982). Triiodothyronine stimulation of in-vitro growth and maturation of embryonic chick cartilage. Endocrinology, 111, 462e468. Burley, N. (1981). Sex-ratio manipulation and selection for attractiveness. Science, 211, 721e722. Burley, N. (1982). Facultative sex-ratio manipulation. Am Nat, 120, 81e107. Burley, N. (1986). Sex-ratio manipulation in color-banded populations of zebra finches. Evolution, 40, 1191e1206. Burley, N. (1988). The differential-allocation hypothesisdan experimental test. Am Nat, 132, 611e628. Burley, N., Krantzberg, G., & Radman, P. (1982). Influence of colorbanding on the conspecific preferences of zebra finches. Anim Behav, 30, 444e455. Buttemer, W. A., Warne, S., Bech, C., & Astheimer, L. B. (2008). Testosterone effects on avian basal metabolic rate and aerobic performance: facts and artefacts. Comp Biochem Physiol, Part A: Mol Integr Physiol, 150, 204e210. Carere, C., & Balthazart, J. (2007). Sexual versus individual differentiation: the controversial role of avian maternal hormones. Trends Endocrinol Metab, 18, 73e80. Carere, C., Drent, P. J., Koolhaas, J. M., & Groothuis, T. G. G. (2005). Epigenetic effects on personality traits: early food provisioning and sibling competition. Behaviour, 142, 1329e1355. Cariello, M. O., Macedo, R. H. F., & Schwabl, H. G. (2006). Maternal androgens in eggs of communally breeding guira cuckoos (Guira guira). Horm Behav, 49, 654e662.

Chapter | 4

Maternal Hormones in Avian Eggs

Charnov, E. L. (1982). The Theory of Sex Allocation. Princeton, NJ: Princeton University Press. Compagnone, N. A., & Mellon, S. H. (2000). Neurosteroids: biosynthesis and function of these novel neuromodulators. Front Neuroendocrinol, 21, 1e56. Correa, S. M., Adkins-Regan, E., & Johnson, P. A. (2005). High progesterone during avian meiosis biases sex ratios toward females. Biol Lett, 1, 215e218. Coughtrie, M. W. H., Sharp, S., Maxwell, K., & Innes, N. P. (1998). Biology and function of the reversible sulfation pathway catalysed by human sulfotransferases and sulfatases. Chem Biol Interact, 109, 3e27. Crean, A. J., & Marshall, D. J. (2009). Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Philos Trans R Soc, B, 364, 1087e1096. Cucco, M., Guasco, B., Malacarne, G., Ottonelli, R., & Tanvez, A. (2008). Yolk testosterone levels and dietary carotenoids influence growth and immunity of Grey partridge chicks. Gen Comp Endocrinol, 156, 418e425. Daisley, J. N., Bromundt, V., Mo¨stl, E., & Kotrschal, K. (2005). Enhanced yolk testosterone influences behavioral phenotype independent of sex in Japanese quail chicks Coturnix japonica. Horm Behav, 47, 185e194. Darras, V. M., Van Herck, S. L. J., Geysens, S., & Reyns, G. E. (2009). Involvement of thyroid hormones in chicken embryonic brain development. Gen Comp Endocrinol, 163, 58e62. De Fraipont, M., Clobert, J., John, H., & Alder, S. (2000). Increased prenatal maternal corticosterone promotes philopatry of offspring in common lizards Lacerta vivipara. J Anim Ecol, 69, 404e413. De Pablo, F., Roth, J., Hernandez, E., & Pruss, R. M. (1982). Insulin is present in chicken eggs and early chick embryos. Endocrinology, 111, 1909e1916. Delrio, G., Botte, V., & Diprisco, C. L. (1968). Research on enzymes of steroidogenesis in Gallus domesticus egg yolk. Atti Accad Naz Lincei, Mem, Cl Sci Fis, Mat Nat, Sez, 3, 616e619. Dentressangle, F., Boeck, L., & Torres, R. (2008). Maternal investment in eggs is affected by male feet colour and breeding conditions in the blue-footed booby, Sula nebouxii. Behav Ecol Sociobiol, 62, 1899e1908. Deviche, P., Breuner, C., & Orchinik, M. (2001). Testosterone, corticosterone, and photoperiod interact to regulate plasma levels of binding globulin and free steroid hormone in dark-eyed juncos, Junco hyemalis. Gen Comp Endocrinol, 122, 67e77. Downing, J. A., & Bryden, W. L. (2008). Determination of corticosterone concentrations in egg albumen: a non-invasive indicator of stress in laying hens. Physiol Behav, 95, 381e387. Drummond, H., Rodriguez, C., & Schwabl, H. (2008). Do mothers regulate facultative and obligate siblicide by differentially provisioning eggs with hormones? J Avian Biol, 39, 139e143. Eising, C. M., & Groothuis, T. G. G. (2003). Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Anim Behav, 66, 1027e1034. Eising, C. M., Eikenaar, C., Schwabl, H., & Groothuis, T. G. G. (2001). Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc B, 268, 839e846. Eising, C. M., Mu¨ller, W., Dijkstra, C., & Groothuis, T. G. G. (2003a). Maternal androgens in egg yolks: relation with sex, incubation time and embryonic growth. Gen Comp Endocrinol, 132, 241e247.

121

Eising, C. M., Mu¨ller, W., & Groothuis, T. G. G. (2006). Avian mothers create different phenotypes by hormone deposition in their eggs. Biol Lett, 2, 20e22. Eising, C. M., Pavlova, D., Groothuis, T. G. G., Eens, M., & Pinxten, R. (2008). Maternal yolk androgens in European starlings: affected by social environment or individual traits of the mother? Behaviour, 145, 51e72. Eising, C. M., Visser, G. H., Mu¨ller, W., & Groothuis, T. G. G. (2003b). Steroids for free? No metabolic costs of elevated maternal androgen levels in the black-headed gull. J Exp Biol, 206, 3211e3218. Elbrecht, A., & Smith, R. G. (1992). Aromatase enzyme activity and sex determination in chickens. Science, 255, 467e470. Elf, P. K., & Fivizzani, A. J. (2002). Changes in sex steroid levels in yolks of the leghorn chicken, Gallus domesticus, during embryonic development. J Exp Zool, 293, 594e600. Ellis, L. A., Borst, D. W., & Thompson, C. F. (2001). Hatching asynchrony and maternal androgens in egg yolks of house wrens. J Avian Biol, 32, 26e30. von Engelhardt, N., & Groothuis, T. G. G. (2005). Measuring hormones in avian eggs. Ann NY Acad Sci, 1046, 181e192. von Engelhardt, N., Carere, C., Dijkstra, C., & Groothuis, T. G. G. (2006). Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc R Soc B, 273, 65e70. von Engelhardt, N., Dijkstra, C., Daan, S., & Groothuis, T. (2004). Effects of 17-beta-estradiol treatment of female zebra finches on offspring sex ratio and survival. Horm Behav, 45, 306e313. von Engelhardt, N., Henriksen, R., & Groothuis, T. G. G. (2009). Steroids in chicken egg yolk: metabolism and uptake during early embryonic development. Gen Comp Endocrinol, 163, 175e183. Endo, D., Murakami, S., Akazome, Y., & Park, M. K. (2007). Sex difference in Ad4BP/SF-1 mRNA expression in the chick-embryo brain before gonadal sexual differentiation. ZoologSci, 24, 877e882. Erickson, A. E., & Pincus, G. (1966). Modification of embryonic development of reproductive and lymphoid organs in chick. J Embryol Exp Morphol, 16, 211. ¨ ber das vorkommen des femininen sexual-lipoids Fellner, O. O. (1925). U in vogeleiern und den eiersto¨cken der fische. Klin Wochenschr, 35, 1651e1652. Flamant, F., & Samarut, J. (1998). Involvement of thyroid hormone and its alpha receptor in avian neurulation. Dev Biol, 197, 1e11. Freking, F., Nazairians, T., & Schlinger, B. A. (2000). The expression of the sex steroid-synthesizing enzymes CYP11A1, 3 beta-HSD, CYP17, and CYP19 in gonads and adrenals of adult and developing zebra finches. Gen Comp Endocrinol, 119, 140e151. Friesema, E. C. H., Jansen, J., Milici, C., & Visser, T. J. (2005). Thyroid hormone transporters. Vitam Horm, 70, 137e167. Garamszegi, L. Z., Biard, C., Eens, M., Møller, A. P., & Saino, N. (2007). Interspecific variation in egg testosterone levels: implications for the evolution of bird song. J Evol Biol, 20, 950e964. Gasparini, J., Boulinier, T., Gill, V., Gil, D., Hatch, S., & Roulin, A. (2007). Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird. J Evol Biol, 20, 874e880. Gil, D. (2003). Golden eggs: maternal manipulation of offspring phenotype by egg androgen in birds. Ardeola, 50, 281e294. Gil, D. (2008). Hormones in avian eggs: physiology, ecology and behavior. Advances in the Study of Behavior, 38, 337e398.

122

Gil, D., & Faure, J. M. (2007). Correlated response in yolk testosterone levels following divergent genetic selection for social behaviour in Japanese quail. J Exp Zool Part A Ecol Genet Physiol, 307A, 91e94. Gil, D., Biard, C., Lacroix, A., Spottiswoode, C. N., Saino, N., Puerta, M., et al. (2007). Evolution of yolk androgens in birds: development, coloniality, and sexual dichromatism. Am Nat, 169, 802e819. Gil, D., Graves, J., Hazon, N., & Wells, A. (1999). Male attractiveness and differential testosterone investment in zebra finch eggs. Science, 286, 126e128. Gil, D., Heim, C., Bulmer, E., Rocha, M., Puerta, M., & Naguib, M. (2004a). Negative effects of early developmental stress on yolk testosterone levels in a passerine bird. J Exp Biol, 207, 2215e2220. Gil, D., Leboucher, G., Lacroix, A., Cue, R., & Kreutzer, M. (2004b). Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Horm Behav, 45, 64e70. Gil, D., Marzal, A., De Lope, F., Puerta, M., & Møller, A. P. (2006a). Female house martins (Delichon urbica) reduce egg androgen deposition in response to a challenge of their immune system. Behav Ecol Sociobiol, 60, 96e100. Gil, D., Ninni, P., Lacroix, A., De Lope, F., Tirard, C., Marzal, A., et al. (2006b). Yolk androgens in the barn swallow (Hirundo rustica): a test of some adaptive hypotheses. J Evol Biol, 19, 123e131. Gilbert, L., Bulmer, E., Arnold, K. E., & Graves, J. A. (2007). Yolk androgens and embryo sex: maternal effects or confounding factors? Horm Behav, 51, 231e238. Gilbert, L., Rutstein, A. N., Hazon, N., & Graves, J. A. (2005). Sex-biased investment in yolk androgens depends on female quality and laying order in zebra finches (Taeniopygia guttata). Naturwissenschaften, 92, 178e181. Glick, B. (1962). Effect of dipping eggs in testosterone propionate on bursa of Fabricius of chickens in immediate and future generations. Fed Proc, 21, 29. Glick, B. (1965). Embryonic exposure to testosterone propionate will adversely influence future mating behavior in male chickens. Fed Proc, 24, 700. Glick, B., Holbrook, K. A., & Perkins, W. D. (1977). Scanning electron microscopy of bursa of Fabricius from normal and testosterone-treated embryos. Developmental and Comparative Immunology, 1, 41e46. Godsave, S. F., Lohmann, R., Vloet, R. P. M., & Gahr, M. (2002). Androgen receptors in the embryonic zebra finch hindbrain suggest a function for maternal androgens in perihatching survival. J Comp Neurol, 453, 57e70. Goerlich, V. C., Dijkstra, C., & Groothuis, T. G. G. (2010). No evidence for selective follicle abortion underlying primary sex ratio adjustment in pigeons. Behav Ecol Sociobiol, 64, 599e606. Goerlich, V. C., Dijkstra, C., Schaafsma, S. M., & Groothuis, T. G. G. (2009). Testosterone has a long-term effect on primary sex ratio of first eggs in pigeonsdin search of a mechanism. Gen Comp Endocrinol, 163, 184e192. Gomez, Y., Velazquez, P. N., Juarez-Oropeza, M. A., & Pedernera, E. (1998). Steroid metabolism in granulosa and theca interna cells from preovulatory follicles of domestic hen (Gallus domesticus). Anim Reprod Sci, 52, 81e91. Gorman, K. B., & Williams, T. D. (2005). Correlated evolution of maternally derived yolk testosterone and early developmental traits in passerine birds. Biol Lett, 1, 461e464. Gosling, S. D., & John, O. P. (1999). Personality dimensions in nonhuman animals: a cross-species review. Curr Dir Psychol Sci, 8, 69e75.

Hormones and Reproduction of Vertebrates

Go¨th, A., Eising, C. M., Herberstein, M., & Groothuis, T. G. G. (2008). Consistent variation in yolk androgens in the Australian brush-turkey, a species without sibling competition or parental care. Gen Comp Endocrin 155, 742e748. Groothuis, T. G., & Schwabl, H. (2002). Determinants of within- and among-clutch variation in levels of maternal hormones in blackheaded gull eggs. Funct Ecol, 16, 281e289. Groothuis, T. G. G., & von Engelhardt, N. (2005). Investigating maternal hormones in avian eggs: measurement, manipulation and interpretation. Ann NY Acad Sci, 1046, 168e180. Groothuis, T. G. G., & Schwabl, H. (2008). Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philos Trans R Soc, B, 363, 1647e1661. Groothuis, T. G. G., Carere, C., Lipar, J., Drent, P. J., & Schwabl, H. (2008). Selection on personality in a songbird affects maternal hormone levels tuned to its effect on timing of reproduction. Biol Lett, 4, 465e467. Groothuis, T. G. G., Eising, C. M., Blount, J. D., Surai, P., Apanius, V., Dijkstra, C., et al. (2006). Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. J Evol Biol, 19, 1304e1313. Groothuis, T. G. G., Eising, C. M., Dijkstra, C., & Mu¨ller, W. (2005a). Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol Lett, 1, 78e81. Groothuis, T. G. G., Mu¨ller, W., von Engelhardt, N., Carere, C., & Eising, C. (2005b). Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev, 29, 329e352. Gurney, M. E. (1981). Hormonal control of cell form and number in the zebra finch song system. J Neurosci, 1, 658e673. Gurney, M. E. (1982). Behavioral correlates of sexual differentiation in the zebra finch song system. Brain Res, 231, 153e172. Guennoun, R., Reyss-Brion, M., & Jean-Marie, J.-M. (1987). Progesterone receptors in hypothalamus and pituitary during the embryonic development of the chick: regulation by sex steroid hormones. Dev brain res, 37, 1e9. Gwinner, H., & Schwabl, H. (2005). Evidence for sexy sons in European starlings (Sturnus vulgaris). Behav Ecol Sociobiol, 58, 375e382. Hackl, R., Bromundt, V., Daisley, J., Kotrschal, K., & Mo¨stl, E. (2003). Distribution and origin of steroid hormones in the yolk of Japanese quail eggs (Coturnix coturnix japonica). J Comp Physiol, B, 173, 327e331. Hahn, D. C., Hatfield, J. S., Abdelnabi, M. A., Wu, J. M., Igl, L. D., & Ottinger, M. A. (2005). Inter-species variation in yolk steroid levels and a cowbird-host comparison. J Avian Biol, 36, 40e46. Hahn, D. C., Wingfield, J. C., Fox, D. M., Walker, B. G., & Richie, J. T. (2003). Environmental endocrinology and invasive cowbird species. In: Abstracts of the Ecological Society of America 88th Annual Meeting, Savannah, GA. Washington, DC: Ecological Society of America. Hamilton, W. D. (1967). Extraordinary sex ratios. Science, 156, 477. Hargitai, R., Arnold, K. E., Herenyi, M., Prechl, J., & To¨ro¨k, J. (2009). Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher. Behav Ecol Sociobiol, 63, 869e882. Hargitai, R., Csaba, M., Miklo´s, B., Gil, D., Lo´pez-Rull, I., & Solymos, E. (2010). Eggshell characteristics and yolk composition in the common cuckoo Cuculus canorus: are they adapted to brood parasitism? J Avian Biol, 41, 177e185.

Chapter | 4

Maternal Hormones in Avian Eggs

Hau, M. (2007). Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. BioEssays, 29, 133e144. Hauber, M. E., & Pilz, K. M. (2003). Yolk testosterone levels are not consistently higher in the eggs of obligate brood parasites than their hosts. Am Midl Nat, 149, 354e362. Hayward, L. S., & Wingfield, J. C. (2004). Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen Comp Endocrinol, 135, 365e371. Hayward, L. S., Richardson, J. B., Grogan, M. N., & Wingfield, J. C. (2006). Sex differences in the organizational effects of corticosterone in the egg yolk of quail. Gen Comp Endocrinol, 146, 144e148. Heeb, P., Werner, I., Mateman, A. C., Kolliker, M., Brinkhof, M. W. G., Lessells, C. M., et al. (1999). Ectoparasite infestation and sex-biased local recruitment of hosts. Nature, 400, 63e65. Hill, G. E. (1991). Plumage coloration is a sexually selected indicator of male quality. Nature, 350, 337e339. Hinde, C. A., Buchanan, K. L., & Kilner, R. M. (2009). Prenatal environmental effects match offspring begging to parental provisioning. Proceedings of the Royal Society B-Biological Sciences, 276, 2787e2794. Hinde, C. A., Johnstone, R. A., & Kilner, R. M. (2010). Parenteoffspring conflict and coadaptation. Science, 327, 1373e1376. Hu, Y., Ni, Y., Ren, L., Dai, J., & Zhao, R. (2008). Leptin is involved in the effects of cysteamine on egg laying of hens, characteristics of eggs, and posthatch growth of broiler offspring. Poult Sci, 87, 1810e1817. Huang, E. S. R., Kao, K. J., & Nalbandov, A. V. (1979). Synthesis of sex steroids by cellular components of chicken follicles. Biol Reprod, 20, 454e461. Hutchison, J. B., Wozniak, A., Beyer, C., & Hutchison, R. E. (1996). Regulation of sex-specific formation of oestrogen in brain development: endogenous inhibitors of aromatase. J Steroid Biochem Mol Biol, 56, 201e207. Irving, R. A., Mainwaring, W. I. P., & Spooner, P. M. (1976). Regulation of hemoglobin synthesis in cultured chick blastoderms by steroids related to 5-beta-androstane. Biochem J, 154, 81e93. Janczak, A. M., Braastad, B. O., & Bakken, M. (2006). Behavioural effects of embryonic exposure to corticosterone in chickens. Appl Anim Behav Sci, 96, 69e82. Jawor, J. M., McGlothlin, J. W., Casto, J. M., Greives, T. J., Snajdr, E. A., Bentley, G. E., et al. (2007). Testosterone response to GnRH in a female songbird varies with stage of reproduction: implications for adult behaviour and maternal effects. Funct Ecol, 21, 767e775. Johnson, A. L. (2000). Reproduction in the female. In G. C. Whittow (Ed.), Sturkie’s Avian Physiology (pp. 569e596). San Diego, CA: Academic Press. Kato, M., Shimada, K., Saito, N., Noda, K., & Ohta, M. (1995). Expression of P450 (17-alpha-hydroxylase) and P450 (aromatase) genes in isolated granulosa, theca interna, and theca externa layers of chicken ovarian follicles during follicular growth. Biol Reprod, 52, 405e410. Katoh, H., Ogino, Y., & Yamada, G. (2006). Cloning and expression analysis of androgen receptor gene in chicken embryogenesis. Febs Letters, 580, 1607e1615. Kilner, R. M. (2002). The evolution of complex begging displays. In J. Wright, & M. L. Leonard (Eds.), ldquo;The Evolution of Begging: Competition, Cooperation and Communication (pp. 87e106). Dordrecht, Germany: Kluwer Academic Publishers.

123

Kim, Y. H., Perlman, W. R., & Arnold, A. P. (2004). Expression of androgen receptor mRNA in zebra finch song system: developmental regulation by estrogen. J Comp Neurol, 469, 535e547. Kimball, R. T., & Ligon, J. D. (1999). Evolution of avian plumage dimorphism from a proximate perspective. Am Nat, 154, 182e193. Kingma, S. A., Komdeur, J., Vedder, O., von Engelhardt, N., Korsten, P., & Groothuis, T. G. G. (2009). Manipulation of male attractiveness induces rapid changes in avian maternal yolk androgen deposition. Behav Ecol, 20, 172e179. Kirkpatrick, M., & Lande, R. (1989). The evolution of maternal characters. Evolution, 3, 485e503. Kopec, S., & Greenwood, A. W. (1929). The effect of yolk injections on the plumage of an ovariotomised brown leghorn hen. Wilhelm Roux Archiv f€ ur Entwicklungsmechanik der Organismen, 121, 87e95. Korsia, S., & Bottjer, S. W. (1991). Chronic testosterone treatment impairs vocal learning in male zebra finches during a restricted period of development. J Neurosci, 11, 2362e2371. Kova´cikova´, Z., Kuncova´, T., Lamosova´, D., & Zeman, M. (2003). Embryonic and post-embryonic development of Japanese quail after in-ovo melatonin treatment. Acta Vet Brno, 72, 157e161. Kralli, A., Bohen, S. P., & Yamamoto, K. R. (1995). Lem1, an ATPbinding-cassette transporter, selectively modulates the biological potency of steroid-hormones. Proc Natl Acad Sci USA, 92, 4701e4705. Kuhnemann, S., Brown, T. J., Hochberg, R. B., & Maclusky, N. J. (1995). Sexual differentiation of estrogen-receptor concentrations in the rat braindeffects of neonatal testosterone exposure. Brain Res, 691, 229e234. & Jezova´, D. Lamosova´, D., Ma´cajova´, M., Zeman, M., Mozes, S., (2003). Effect of in-ovo leptin administration on the development of Japanese quail. Physiol Res, 52, 201e209. Lamosova´, D., & Zeman, M. (2001). Effect of leptin and insulin on chick embryonic muscle cells and hepatocytes. Physiol Res, 50, 183e189. Lessells, C. M. (2008). Neuroendocrine control of life histories: what do we need to know to understand the evolution of phenotypic plasticity? Philos Trans R Soc, B, 363, 1589e1598. Levere, R., Kappas, A., & Granick, S. (1967). Induction of hemoglobin formation in erythroid cell culture by 5-beta-H steroid metabolites. J Clin Invest, 46, 1084. Lipar, J. L., & Ketterson, E. D. (2000). Maternally derived yolk testosterone enhances the development of the hatching muscle in the redwinged blackbird Agelaius phoeniceus. Proc R Soc B, 267, 2005e2010. Lipar, J. L., Ketterson, E. D., Nolan, V., & Casto, J. M. (1999). Egg yolk layers vary in the concentration of steroid hormones in two avian species. Gen Comp Endocrinol, 115, 220e227. Love, O. P., & Williams, T. D. (2008). The adaptive value of stressinduced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness. Am Nat, 172, E135eE149. Love, O. P., Chin, E. H., Wynne-Edwards, K. E., & Williams, T. D. (2005). Stress hormones: a link between maternal condition and sexbiased reproductive investment. Am Nat, 166, 751e766. Loyau, A., Saint Jalme, M., Mauget, R., & Sorci, G. (2007). Male sexual attractiveness affects the investment of maternal resources into the eggs in peafowl (Pavo cristatus). Behav Ecol Sociobiol, 61, 1043e1052.

124

Magrath, M. J. L., Vedder, O., van der Velde, M., & Komdeur, J. (2009). Maternal effects contribute to the superior performance of extra-pair offspring. Curr Biol, 19, 792e797. Marshall, D. J., & Uller, T. (2007). When is a maternal effect adaptive? Oikos, 116, 1957e1963. Martin, T. E. (2002). A new view of avian life-history evolution tested on an incubation paradox. Proc R Soc B, 269, 309e316. Martin, T. E., & Schwabl, H. (2008). Variation in maternal effects and embryonic development rates among passerine species. Philos Trans R Soc, B, 363, 1663e1674. Mattsson, A., & Brunstro¨m, B. (2010). Effects on differentiation of reproductive organs and sexual behaviour in Japanese quail by excessive embryonic ER alpha activation. Reprod Fertil Dev, 22, 416e425. Mattsson, A., Mura, E., Brunstro¨m, B., Panzica, G., & Halldin, K. (2008). Selective activation of estrogen receptor alpha in Japanese quail embryos affects reproductive organ differentiation but not the male sexual behavior or the parvocellular vasotocin system. Gen Comp Endocrinol, 159, 150e157. Mazuc, J., Bonneaud, C., Chastel, O., & Sorci, G. (2003). Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol Lett, 6, 1084e1090. McCormick, C. M., Furey, B. F., Child, M., Sawyer, M. J., & Donohue, S. M. (1998). Neonatal sex hormones have ‘organizational’ effects on the hypothalamicepituitaryeadrenal axis of male rats. Dev Brain Res, 105, 295e307. McNabb, F. M. A., & Wilson, C. M. (1997). Thyroid hormone deposition in avian eggs and effects on embryonic development. Am Zool, 37, 553e560. Metcalfe, N. B., & Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? Trends Ecol Evol, 16, 254e260. Meylan, S., Belliure, J., Clobert, J., & De Fraipont, M. (2002). Stress and body condition as prenatal and postnatal determinants of dispersal in the common lizard (Lacerta vivipara). Horm Behav, 42, 319e326. Michl, G., To¨re´k, J., Peczely, P., Garamszegi, L. Z., & Schwabl, H. (2005). Female collared flycatchers adjust yolk testosterone to male age, but not to attractiveness. Behav Ecol, 16, 383e388. Møller, A. P. (2005). Parasites, predators and the duration of developmental periods. Oikos, 111, 291e301. Moore, M. C., & Johnston, G. I. H. (2008). Toward a dynamic model of deposition and utilization of yolk steroids. Integr Comp Biol, 48, 411e418. Moore, A. J., Wolf, J. B., & Brodie, E. D. (1998). The influence of direct and indirect genetic effects on the evolution of behaviour. In T. A. Mousseau & Ch. W. Fox (Eds.), Maternal effects as adaptations (pp. 22e41). Oxford, UK: Oxford University Press. Moreno-Rueda, G. (2007). Yolk androgen deposition as a female tactic to manipulate paternal contribution. Behav Ecol, 18, 496e498. Mo¨stl, E., Spendier, H., & Kotrschal, K. (2001). Concentration of immunoreactive progesterone and androgens in the yolk of hens’ eggs (Gallus domesticus). Wiener Tiera¨rztliche Monatsschrift, 88, 62e65. Mousseau, T. A., & Fox, C. W. (1998). Maternal Effects as Adaptations. Oxford, UK: Oxford University Press. Mueller, N. S. (1976). Influence of embryonic estrogens on adult feather coloration in duck Anas platyrhynchos. J Exp Zool, 195, 207e213. Mueller, N. S. (1977). Control of sex differences in plumage of house sparrow, Passer domesticus. J Exp Zool, 202, 45e48.

Hormones and Reproduction of Vertebrates

Mu¨ller, W., & Eens, M. (2009). Elevated yolk androgen levels and the expression of multiple sexually selected male characters. Horm Behav, 55, 175e181. Mu¨ller, W., Dijkstra, C., & Groothuis, T. G. G. (2009a). Maternal yolk androgens stimulate territorial behaviour in black-headed gull chicks. Biol Lett, 5, 586e588. Mu¨ller, W., Deptuch, K., Lo´pez-Rull, I., & Gil, D. (2007a). Elevated yolk androgen levels benefit offspring development in a between-clutch context. Behav Ecol, 18, 929e936. Mu¨ller, W., Eising, C. M., Dijkstra, C., & Groothuis, T. G. G. (2002). Sex differences in yolk hormones depend on maternal social status in leghorn chickens (Gallus gallus domesticus). Proc R Soc B, 269, 2249e2255. Mu¨ller, W., Eising, C. M., Dijkstra, C., & Groothuis, T. G. G. (2004). Within-clutch patterns of yolk testosterone vary with the onset of incubation in black-headed gulls. Behav Ecol, 15, 893e897. Mu¨ller, W., Groothuis, T. G. G., Eising, C. M., & Dijkstra, C. (2005a). An experimental study on the causes of sex-biased mortality in the blackheaded gulldthe possible role of testosterone. J Anim Ecol, 74, 735e741. Mu¨ller, W., Groothuis, T. G. G., Kasprzik, A., Dijkstra, C., Alatalo, R. V., & Siitari, H. (2005b). Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc R Soc B, 272, 1971e1977. Mu¨ller, W., Lessells, M., Korsten, P., & von Engelhardt, N. (2007b). Manipulative signals in family conflict? On the function of maternal yolk hormones in birds. Am Nat, 169, E84eE96. Mu¨ller, W., Vergauwen, J., & Eens, M. (2008). Yolk testosterone, postnatal growth and song in male canaries. Horm Behav, 54, 125e133. Mu¨ller, W., Vergauwen, J., & Eens, M. (2009b). Long-lasting consequences of elevated yolk testosterone levels on female reproduction. Behav Ecol Sociobiol, 63, 809e816. Navara, K. J., Hill, G. E., & Mendonc¸a, M. T. (2005). Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol Biochem Zool, 78, 570e578. Navara, K. J., Hill, G. E., & Mendonc¸a, M. T. (2006a). Yolk androgen deposition as a compensatory strategy. Behav Ecol Sociobiol, 60, 392e398. Navara, K. J., Hill, G. E., & Mendonc¸a, M. T. (2006b). Yolk testosterone stimulates growth and immunity in house finch chicks. Physiol Biochem Zool, 79, 550e555. Navara, K. J., Siefferman, L. M., Hill, G. E., & Mendonc¸a, M. T. (2006c). Yolk androgens vary inversely to maternal androgens in eastern bluebirds: an experimental study. Funct Ecol, 20, 449e456. Nelson, R. J. (2000). An Introduction to Behavioural Endocrinology. Sunderland, MA: Sinauer Associates Inc, Sunderland Publishers. Nomura, O., Nakabayashi, O., Nishimori, K., Yasue, H., & Mizuno, S. (1999). Expression of five steroidogenic genes including aromatase gene at early developmental stages of chicken male and female embryos. J Steroid Biochem Mol Biol, 71, 103e109. Norton, J. M., & Wira, C. R. (1977). Dose-related effects of sex hormones and cortisol on growth of bursa of Fabricius in chick embryos. J Steroid Biochem Mol Biol, 8, 985e987. Okuliarova, M., Skrobanek, P., & Zeman, M. (2007). Effect of increasing yolk testosterone levels on early behaviour in Japanese quail hatchlings. Acta Vet Brno, 76, 325e331.

Chapter | 4

Maternal Hormones in Avian Eggs

Olah, I., Glick, B., & Toro, I. (1986). Bursal development in normal and testosterone-treated chick embryos. Poult Sci, 65, 574e588. Padmanabhan, V., Manikkam, M., Recabarren, S., & Foster, D. (2006). Prenatal testosterone excess programs reproductive and metabolic dysfunction in the female. Mol Cell Endocrinol, 246, 165e174. Paitz, R. T., & Bowden, R. M. (2008). A proposed role of the sulfotransferase/sulfatase pathway in modulating yolk steroid effects. Integr Comp Biol, 48, 419e427. Pang, K. S., Schwab, A. J., Goresky, C. A., & Chiba, M. (1994). Transport, binding, and metabolism of sulfate conjugates in the liver. Chem-Biol Interact, 48, 419e427. Panzica, G. C., Viglietti-Panzica, C., Mura, E., Quinn, M. J., Lavoie, E., Palanza, P., et al. (2007). Effects of xenoestrogens on the differentiation of behaviorally-relevant neural circuits. Front Neuroendocrinol, 28, 179e200. Parsons, I. C. (1970). Metabolism of testosterone by early chick embryonic blastoderm. Steroids, 16, 59e65. Partecke, J., & Schwabl, H. (2008). Organizational effects of maternal testosterone on reproductive behavior of adult house sparrows. Dev Neurobiol, 68, 1538e1548. Pavlik, A., Novotna, B., & Jelinek, R. (1986). Glucocorticoid receptormediated teratogenesis and cell proliferation in the limbs and face of the chick embryo. Teratog Carcinog Mutagen, 6, 441e450. Petrie, M., Schwabl, H., Brande-Lavridsen, N., & Burke, T. (2001). Maternal investmentdsex differences in avian yolk hormone levels. Nature, 412. 498e498. Philippi, T., & Seger, J. (1989). Hedging ones evolutionary bets, revisited. Trends Ecol Evol, 4, 41e44. Phoenix, C. H., Goy, R. W., Gerall, A. A., & Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology, 65, 369e382. Pike, T. W., & Petrie, M. (2003). Potential mechanisms of avian sex manipulation. Biol. Revi., 78, 553e574. Pike, T. W., & Petrie, M. (2006). Experimental evidence that corticosterone affects offspring sex ratios in quail. Proc R Soc B, 273, 1093e1098. Pilz, K. M., Adkins-Regan, E., & Schwabl, H. (2005a). No sex difference in yolk steroid concentrations of avian eggs at laying. Biol Lett, 1, 318e321. Pilz, K. M., Smith, H. G., & Andersson, M. (2005b). Brood parasitic European starlings do not lay high-quality eggs. Behav Ecol, 16, 507e513. Pilz, K. M., Smith, H. G., Sandell, M. I., & Schwabl, H. (2003). Interfemale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more? Anim Behav, 65, 841e850. Pilz, K. M., Quiroga, M., Schwabl, H., & Adkins-Regan, E. (2004). European starling chicks benefit from high yolk testosterone levels during a drought year. Horm Behav, 46, 179e192. Pilz, K. M., & Smith, H. G. (2004). Egg yolk androgen levels increase with breeding density in the European starling, Sturnus vulgaris. Funct Ecol, 18, 58e66. Porter, T. E., Hargis, B. M., Silsby, J. L., & Elhalawani, M. E. (1989). Differential steroid-production between theca interna and theca externa cellsda 3 cell model for follicular steroidogenesis in avian species. Endocrinology, 125, 109e116. Prati, M., Calvo, R., Morreale, G., & Morreale de Escobar, G. (1992). L-thyroxine and 3,5,3’-triiodothyronine concentrations in the chicken

125

egg and in the embryo before and after the onset of thyroid function. Endocrinology, 130, 2651e2659. Quaglino, A. E., Craig-Veit, C. B., Viant, M. R., Erichsen, A. L., Fry, D. M., & Millam, J. R. (2002). Oral estrogen masculinizes female zebra finch song system. Horm Behav, 41, 236e241. Reed, W. L., & Vleck, C. M. (2001). Functional significance of variation in egg-yolk androgens in the American coot. Oecologia, 128, 164e171. Reid, F. A., Gasc, J. M., Stumpf, W. E., & Sar, M. (1981). Androgen targets cells in spinal cord, spinal ganglia, and glycogen body of chick embryosdautoradiographic localization. Exp Brain Res, 44, 243e248. Rettenbacher, S., Mo¨stl, E., & Groothuis, T. G. G. (2009). Gestagens and glucocorticoids in chicken eggs. Gen Comp Endocrinol, 164, 125e129. Rettenbacher, S., Mo¨stl, E., Hackl, R., & Palme, R. (2005). Corticosterone in chicken eggs. Ann NY Acad Sci, 1046,193e203. Ricklefs, R. E. (1992). Embryonic development period and the prevalence of avian blood parasites. Proc Natl Acad Sci USA, 89, 4722e4725. Riddle, O., & Dunham, H. H. (1942). Transformation of males to intersexes by estrogen passed from blood of ring doves to their ovarian eggs. Endocrinology, 30, 959e968. Riddle, O., Hollander, W. F., & Schooley, J. P. (1945). A race of hermaphrodite-producing pigeons. Anat Rec, 92, 401e423. Ros, A. F. H., Dieleman, S. J., & Groothuis, T. G. G. (2002). Social stimuli, testosterone, and aggression in gull chicks: support for the challenge hypothesis. Horm Behav, 41, 334e342. Royle, N. J., Surai, P. F., & Hartley, I. R. (2001). Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol, 12, 381e385. Rubolini, D., Martinelli, R., von Engelhardt, N., Romano, M., Groothuis, T. G. G., Fasola, M., et al. (2007). Consequences of prenatal androgen exposure for the reproductive performance of female pheasants (Phasianus colchicus). Proc R Soc B, 274, 137e142. Rubolini, D., Romano, M., Boncoraglio, G., Ferrari, R. P., Martinelli, R., Galeotti, P., et al. (2005). Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks. Horm Behav, 47, 592e605. Rubolini, D., Romano, M., Martinelli, R., Leoni, B., & Saino, N. (2006a). Effects of prenatal yolk androgens on armaments and ornaments of the ring-necked pheasant. Behav Ecol Sociobiol, 59, 549e560. Rubolini, D., Romano, M., Martinelli, R., & Saino, N. (2006b). Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks. Behav Ecol Sociobiol, 59, 344e352. Rutkowska, J., & Badyaev, A. V. (2008). Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds. Philos Trans R Soc, B, 363, 1675e1686. Rutkowska, J., & Cichon, M. (2006). Maternal testosterone affects the primary sex ratio and offspring survival in zebra finches. Anim Behav, 71, 1283e1288. Rutstein, A. N., Gilbert, L., Slater, P. J. B., & Graves, J. A. (2005). Sexspecific patterns of yolk androgen allocation depend on maternal diet in the zebra finch. Behav Ecol, 16, 62e69. Ruuskanen, S., Doligez, B., Tschirren, B., Pitala, N., Gustafsson, L., Groothuis, T. G. G., et al. (2009). Yolk androgens do not appear to mediate sexual conflict over parental investment in the collared flycatcher Ficedula albicollis. Horm Behav, 55, 514e519.

126

Safran, R. J., Pilz, K. M., McGraw, K. J., Correa, S. M., & Schwabl, H. (2008). Are yolk androgens and carotenoids in barn swallow eggs related to parental quality? Behav Ecol Sociobiol, 62, 427e438. Saino, N., Ferrari, R. P., Romano, M., Martinelli, R., Lacroix, A., Gil, D., et al. (2006). Maternal allocation of androgens and antagonistic effects of yolk androgens on sons and daughters. Behav Ecol, 17, 172e181. Saino, N., Romano, M., Ferrari, R. P., Martinelli, R., & Møller, A. P. (2005). Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. J Exp Zool A Comp Exp Biol, 303, 998e1006. Sandell, M. I., Adkins-Regan, E., & Ketterson, E. D. (2007). Pre-breeding diet affects the allocation of yolk hormones in zebra finches Taeniopygia guttata. J Avian Biol, 38, 284e290. Schlinger, B. A., Lane, N. I., Grisham, W., & Thompson, L. (1999). Androgen synthesis in a songbird: a study of Cyp17 (17 alphahydroxylase/C17,20-lyase) activity in the zebra finch. Gen Comp Endocrinol, 113, 46e58. Schmaltz, G., Quinn, J. S., & Schoech, S. J. (2008). Do group size and laying order influence maternal deposition of testosterone in smoothbilled ani eggs? Horm Behav, 53, 82e89. Schmidt, K. L., Pradhan, D. S., Shah, A. H., Charlier, T. D., Chin, E. H., & Soma, K. K. (2008). Neurosteroids, immunosteroids, and the Balkanization of endocrinology. Gen Comp Endocrinol, 157, 266e274. Schumacher, M., & Hutchison, J. B. (1986). Testosterone induces hypothalamic aromatase during early development in quail. Brain Res, 377, 63e72. Schwabl, H. (1993). Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA, 90, 11446e11450. Schwabl, H. (1996a). Environment modifies the testosterone levels of a female bird and its eggs. J Exp Zool, 276, 157e163. Schwabl, H. (1996b). Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol A Physiol, 114, 271e276. Schwabl, H. (1997a). The contents of maternal testosterone in house sparrow Passer domesticus eggs vary with breeding conditions. Naturwissenschaften, 84, 406e408. Schwabl, H. (1997b). Maternal steroid hormones in the egg. In S. Harvey, & R. J. Etches (Eds.), Perspectives in Avian Endocrinology (pp. 3e14). Bristol, UK: Society for Endocrinology. Schwabl, H., & Lipar, J. L. (2002). Hormonal regulation of begging behaviour. In J. Wright, & M. Leonard (Eds.), The Evolution of Begging: Competition, Cooperation, and Communication (pp. 221e244). Dordrecht, The Netherlands: Kluwer Academic. Schwabl, H., Mock, D. W., & Gieg, J. A. (1997). A hormonal mechanism for parental favouritism. Nature, 386, 231e231. Schwabl, H., Palacios, M. G., & Martin, T. E. (2007). Selection for rapid embryo development correlates with embryo exposure to maternal androgens among passerine birds. Am Nat, 170, 196e206. Sechman, A., & Bobek, S. (1988). Presence of iodothyronines in the yolk of the hen’s egg. Gen Comp Endocrinol, 69, 99e105. Sheldon, B. C. (2000). Differential allocation: tests, mechanisms and implications. Trends Ecol Evol, 15, 397e402. Siegel, H. S., & Gould, N. R. (1976). Chick embryonic plasma proteins and binding capacity for corticosterone. Dev Biol, 50, 510e516. Sih, A., Bell, A. M., Johnson, J. C., & Ziemba, R. E. (2004). Behavioral syndromes: an integrative overview. Q Rev Biol, 79, 241e277.

Hormones and Reproduction of Vertebrates

Smith, C. A., Andrews, J. E., & Sinclair, A. H. (1997). Gonadal sex differentiation in chicken embryos: expression of estrogen receptor and aromatase genes. J Steroid Biochem Mol Biol, 60, 295e302. Sockman, K. W., & Schwabl, H. (2000). Yolk androgens reduce offspring survival. Proc R Soc B, 267, 1451e1456. Sockman, K. W., Schwabl, H., & Sharp, P. J. (2001). Regulation of yolkandrogen concentrations by plasma prolactin in the American kestrel. Horm Behav, 40, 462e471. Sockman, K. W., Sharp, P. J., & Schwabl, H. (2006). Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition. Biol Rev Cambridge Philos Soc, 81, 629e666. Sockman, K. W., Weiss, J., Webster, M. S., Talbott, V., & Schwabl, H. (2008). Sex-specific effects of yolk-androgens on growth of nestling American kestrels. Behav Ecol Sociobiol, 62, 617e625. Strasser, R., & Schwabl, H. (2004). Yolk testosterone organizes behavior and male plumage coloration in house sparrows (Passer domesticus). Behav Ecol Sociobiol, 56, 491e497. Swett, M. B., & Breuner, C. W. (2008). Interaction of testosterone, corticosterone and corticosterone binding globulin in the whitethroated sparrow (Zonotrichia albicollis). Comp Biochem Physiol, Part A: Mol Integr Physiol, 151, 226e231. Tanvez, A., Beguin, N., Chastel, O., Lacroix, A., & Leboucher, G. (2004). Sexually attractive phrases increase yolk androgens deposition in Canaries (Serinus canarias). Gen Comp Endocrinol, 138, 113e120. Tobler, M., & Sandell, M. I. (2007). Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata. Horm Behav, 52, 640e645. Tobler, M., Granbom, M., & Sandell, M. I. (2007a). Maternal androgens in the pied flycatcher: timing of breeding and within-female consistency. Oecologia, 151, 731e740. Tobler, M., Nilsson, J. A., & Nilsson, J. F. (2007b). Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch. Biol Lett, 3, 408e410. To¨ro¨k, J., Moska´ct, C., Michl, G., & Pe´czely, P. (2004). Common cuckoos (Cuculus canorus) lay eggs with larger yolk but not more testosterone than their great reed warbler (Acrocephalus arundinaceus) hosts. Ethol Ecol Evol, 16, 271e277. Trenkle, A., & Hopkins, K. (1971). Immunological investigation of an insulinlike substance in chicken egg. Gen Comp Endocrinol, 16, 493e497. Trivers, R. L. (1974). Parenteoffspring conflict. Am Zool, 14, 249e264. Trivers, R. L., & Willard, D. E. (1973). Natural selection of parental ability to vary sex ratio of offspring. Science, 179, 90e92. Tschirren, B., & Richner, H. (2008). Differential effects of yolk hormones on maternal and paternal contribution to parental care. Anim Behav, 75, 1989e1994. Tschirren, B., Fitze, P. S., & Richner, H. (2007). Maternal modulation of natal dispersal in a passerine bird: an adaptive strategy to cope with parasitism? Am Nat, 169, 87e93. Tschirren, B., Richner, H., & Schwabl, H. (2004). Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc R Soc B, 271, 1371e1375. Tschirren, B., Saladin, V., Fitze, P. S., Schwabl, H., & Richner, H. (2005). Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J Anim Ecol, 74, 675e682. Tschirren, B., Sendecka, J., Groothuis, T. G. G., Gustafsson, L., & Doligez, B. (2009). Heritable variation in maternal yolk hormone transfer in a wild bird population. Am Nat, 174, 557e564.

Chapter | 4

Maternal Hormones in Avian Eggs

Uller, T., Eklof, J., & Andersson, S. (2005). Female egg investment in relation to male sexual traits and the potential for transgenerational effects in sexual selection. Behav Ecol Sociobiol, 57, 584e590. Vedder, O., Kingma, S. A., von Engelhardt, N., Korsten, P., Groothuis, T. G. G., & Komdeur, J. (2007). Conspecific brood parasitism and egg quality in blue tits Cyanistes caeruleus. J Avian Biol, 38, 625e629. Veiga, J. P., Vinuela, J., Cordero, P. J., Aparicio, J. M., & Polo, V. (2004). Experimentally increased testosterone affects social rank and primary sex ratio in the spotless starling. Horm Behav, 46, 47e53. Veney, S. L., & Wade, J. (2005). Post-hatching syrinx development in the zebra finch: an analysis of androgen receptor, aromatase, estrogen receptor alpha and estrogen receptor beta mRNAs. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 191, 97e104. Verboven, N., Evans, N. P., D’Alba, L., Nager, R. G., Blount, J. D., Surai, P. F., et al. (2005). Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus). Behav Ecol Sociobiol, 57, 357e365. Verboven, N., Monaghan, P., Evans, D. M., Schwabl, H., Evans, N., Whitelaw, C., et al. (2003). Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus). Proc R Soc B, 270, 2223e2232. Visser, W. E., Frieserna, E. C. H., Jansen, J., & Visser, T. J. (2008). Thyroid hormone transport in and out of cells. Trends Endocrinol Metab, 19, 50e56. Voigt, C., Ball, G. F., & Balthazart, J. (2007). Neuroanatomical specificity of sex differences in expression of aromatase mRNA in the quail brain. J Chem Neuroanat, 33, 75e86. Welberg, L. A. M., Seckl, J. R., & Holmes, M. C. (2001). Prenatal glucocorticoid programming of brain corticosteroid receptors and

127

corticotrophin-releasing hormone: possible implications for behaviour. Neuroscience, 104, 71e79. Whaling, C. S., Nelson, D. A., & Marler, P. (1995). Testosterone-induced shortening of the storage phase of song development in birds interferes with vocal learning. Dev Psychobiol, 28, 367e376. Whittingham, L. A., & Schwabl, H. (2002). Maternal testosterone in tree swallow eggs varies with female aggression. Anim Behav, 63, 63e67. Wikelski, M., Lynn, S., Breuner, C., Wingfield, J. C., & Kenagy, G. J. (1999). Energy metabolism, testosterone and corticosterone in whitecrowned sparrows. J Comp Physiol, A, 185, 463e470. Williams, T. D. (1999). Parental and first generation effects of exogenous 17beta-estradiol on reproductive performance of female zebra finches (Taeniopygia guttata). Horm Behav, 35, 135e143. Williams, T. D., Kitaysky, A. S., & Vezina, F. (2004). Individual variation in plasma estradiol-17 beta and androgen levels during egg formation in the European starling Sturnus vulgaris: implications for regulation of yolk steroids. Gen Comp Endocrinol, 136, 346e352. Wilson, C. M., & McNabb, F. M. A. (1997). Maternal thyroid hormones in Japanese quail eggs and their influence on embryonic development. Gen Comp Endocrinol, 107, 153e165. Witschi, E. (1961). Sex and secondary sexual characters. In A. J. Marshall (Ed.), Biology and Comparative Physiology of Birds (pp. 115e168). Academic Press. Woods, J. E., & Weeks, R. L. (1969). Ontogenesis of the pituitaryegonadal axis in chick embryo. Gen Comp Endocrinol, 13, 242e254. Wozniak, A., & Hutchison, J. B. (1993). Action of endogenous steroid inhibitors of brain aromatase relative to fadrozole. J Steroid Biochem Mol Biol, 44, 641e645. Young, R. L., & Badyaev, A. V. (2004). Evolution of sex-biased maternal effects in birds: I. Sex-specific resource allocation among simultaneously growing oocytes. J Evol Biol, 17, 1355e1366.

Chapter 5

Stress and Reproduction in Birds Creagh W. Breuner University of Montana, Missoula, MT, USA

SUMMARY There is intrinsic conflict between survival and reproduction. This conflict can be viewed from the perspective of the pace-of-life framework (an ultimate view), trading off many offspring per year over a short life against few offspring per year over a longer life; it can also be viewed from a resource-utilization perspective (a proximate view), increasing current reproductive effort vs. selfmaintenance. The hypothalamicepituitaryeadrenal (HPA) axis controls the production of glucocorticoids (GCs) primarily responsible for mediating this proximate decision-making process. In field studies, GCs tend to decrease performance measures associated with reproduction, and increase measures associated with immediate survival. This chapter investigates the role of GCs in regulating reproductive effort (the proportion of available energy expended on reproductionda proximate query), approaching this question from an ultimate pace-of-life framework.

1. INTRODUCTION Animals face an intrinsic tradeoff between survival and reproduction. This tradeoff manifests both on ultimate (e.g. pace of life) and proximate (e.g. resource utilization) levels. From an ultimate or pace-of-life perspective, animals face tradeoffs between longevity and the number of offspring they produce, so that some animals produce few offspring over a long life and others produce many offspring over a shorter life. A proximate or resource-utilization view highlights the tradeoff in resource allocation; animals have a limited amount of resources that they must divide between self-maintenance and reproduction. Although the consequences of trading off survival and reproduction can be dampened when resources are not limited (as in highquality individuals), the conflict between these two components of fitness is virtually ubiquitous. How is this conflict mediated within individuals? More specifically, what proximate physiological mechanisms translate external and internal cues into the decision-making process of reproductive effort? Hormones and Reproduction of Vertebrates, Volume 4dBirds Copyright Ó 2011 Elsevier Inc. All rights reserved.

Glucocorticoids (GCs) are primary candidates for mediating this decision-making process (Wingfield & Sapolsky, 2003). Glucocorticoids are normally maintained in the blood at relatively low levels that fluctuate on circadian and circannual cycles to regulate energy availability and use (Dallman et al., 1994). However, as the level of challenge increases, the hypothalamus upregulates the hormone cascade, resulting in further release of GCs from the adrenal gland into the plasma. Elevated GCs then act through receptors in target tissue to alter behavior and physiology in a variety of ways, including glucose mobilization through gluconeogenesis (Dallman, Darlington, Suemaru, Cascio, & Levin, 1989; Plaschke, Muller, & Hoyer, 1996), increased lipogenesis (Cherrington, 1999; Landys, Piersma, Ramenofsky, & Wingfield, 2004), and fat deposition (Dittami, Meran, Bairlein, Totzke, 2006; Yuan, Lin, Jiang, Jiao, & Song, 2008); reduction or abandonment of the reproductive effort (e.g., Silverin, 1986; Wingfield & Silverin, 1986; Love, Breuner, Vezina, & Williams, 2004); promotion of escape behavior (Breuner, Greenberg, & Wingfield, 1998; Wingfield et al., 1998; Breuner & Hahn, 2003); and increases in locomotor activity, foraging behavior, and food intake (see Landys, Ramenofsky, & Wingfield, 2006 for review). Altogether, elevated GCs are thought to appropriately redirect energy and behavior from noncritical energy expenditure (e.g., reproduction) towards self-maintenance, making them a good tool for the examination of tradeoffs between reproduction and survival.

1.1. Allostasis Historically, the GC-driven stress response has been viewed as a response to unpredictable events, and distinct from the circadian rhythm in baseline GC levels (Wingfield et al., 1998). In the last five to ten years, McEwen and Wingfield (2003) have been promoting the movement away from ‘stress’ terminology towards the idea of allostasis, which they define as ‘stability through change.’ Generally, the argument behind allostasis rests on the concept that, as an animal faces challenge, there are homeostatic mechanisms 129

130

that regulate physiology and behavior to maintain homeostasis. Allostasis incorporates large and small challenges into this framework, so that basal homeostatic regulation and ‘responding to stress’ are put on a continuum instead of considered separately. Allostasis also incorporates the current state of the animal in defining the response, including large-scale differences such as breeding vs. wintering, as well as small-scale differences such as current parasite load. This can be argued to be an elegant framework from which to evaluate GC physiology for two reasons. First, ‘stressors’ do not occur in a vacuum. One cannot expect that a decline in food availability will have similar physiological or behavioral outcomes whether an animal is feeding young or foraging in a flock. Accounting for the current state of the animal allows for greater refinement of predictions, and greater explanation for variation in response measured. Second, it is unclear whether a GC ‘stress response’ is a distinctly different beast from baseline changes in GCs. In field studies, we see incredible variation in what constitutes baseline (called ‘baseline’ and not basal because the GC axis is very rarely quiescent in free-living animals). We also see incredible variation in GC responses to challenge: presentation of a static predator has very little effect on GC secretion and presentation of a moving predator increases GC levels slightly (e.g., Silverin, 1998); food removal increases GC levels to about double baseline levels (e.g., Lynn, Breuner, & Wingfield, 2003); changes in weather can have very little effect (Romero, Reed, & Wingfield, 2000), intermediate activation (Wingfield, Moore, & Farner, 1983), or can maximally activate the hypothalamicepituitaryeadrenal (HPA) axis (Smith, Wingfield, & Veit, 1994). Which of these conditions represents ‘stress’? This semantic argument is avoided if one considers the response to challenges on a continuum, and not from a dichotomous viewpoint. Three reviews postulate that baseline and stress-induced GC secretion are two entirely separate issues (Romero, 2004; Bo´kony et al., 2009; Bonier, Martin, Moore, & Wingfield, in press). This opinion is based on the fact that there are two GC receptors, high-affinity mineralocorticoid receptors (MRs) and low-affinity GC receptors (GRs). This author disagrees for several key reasons. First, as described above, hormone secretion in response to challenge varies continuously from slightly elevated to maximal HPA activation. Splitting baseline and stress-induced levels into two separate traits ignores much of the range of GC secretion. Second, while there are two separate intracellular receptors, separating GC secretion into two discrete traits is an unwarranted oversimplification. As GC levels rise above baseline, both MR and GR occupation increase. The inverted-U dose-response curve common to many GCinduced processes is explained through initial increases in GCs (above baseline) activating MR-driven processes, and

Hormones and Reproduction of Vertebrates

higher levels acting through GR, often having an opposite effect (Hayden-Hixon & Ferris, 1991a; 1991b; Diamond, Bennett, Fleshner, & Rose, 1992). Hence, both MR and GR are active in driving processes regulated by elevated GCs. Lastly, MR cannot be considered independently of stressinduced levels of GCs, as it plays a major role in both tonic inhibition of GC levels (setting baseline and immediate GC reactivity to a stressor) and negative feedback on elevated levels of GCs after the stressor begins (Dallman et al., 1987; Sapolsky, Zolamorgan, & Squire, 1991). Therefore, this author believes that it is important to consider baseline to stress-induced levels along a continuum, within the framework of allostasis.

1.2. Pace-of-life This section discusses the role of GCs in regulating reproductive effort (the proportion of energy spent on reproduction). However, this proximate mechanism (GC secretion) will be shaped by life history (ultimate) differences among species. For example, GC responses should vary along a continuum, such that species with high survival rates and high residual reproductive value should pass the cost of a current stress challenge onto their offspring (they will respond to the stressor with elevated GCs and then reduce parental care), whereas species with low survival rates and therefore low residual reproductive value should take the cost of challenge on themselves (through suppression of GCs to maintain parental care) (Ghalambor & Martin, 2001; Martin, 2002). Greater GC levels are thought to drive the reproduction/survival tradeoff towards survival, and so greater GC response should be associated with high survival and high residual reproductive value. This continuum is elegantly demonstrated through the ‘pace-of-life’ framework (Ricklefs & Wikelski, 2002; Martin, 2004; for discussion see Hasselquist, 2007; Martin, Weil, & Nelson, 2007; Stutchbury & Morton, 2008; Wiersma, Ro, & Williams, 2009). This framework puts number of eggs per breeding season against survival probability for that species (see Figure 5.1). The ‘fast’-pace-of-life animals (those on the upper left of the continuum) have many offspring over a short lifespan, and so should optimize every reproductive opportunity, despite challenges experienced. The ‘slow’ species (those on the lower right of the continuum) have few offspring per year over a longer lifespan, and so should optimize self-maintenance and reduce reproductive effort in the face of challenge. This reiteration of the classic reproduction vs. survival tradeoff presents a valuable framework from which to formulate predictions regarding whether, during challenge, GCs will move an animal away from the current reproductive bout towards survival. For example, fast species from that clade should bear the cost of the challenge to ensure success of the

Chapter | 5

131

Stress and Reproduction in Birds

chapter considers relationships between environment, GC physiology, reproductive output, and survival in birds.

1.3. Categorization of Glucocorticoid (GC) Studies

FIGURE 5.1 Pace-of-life framework for visualizing reproduction/ survival tradeoffs. Each point is a single species. The group consists of 47 species for which we have data on corticosterone, survival probability, and number of eggs/breeding season. Circles, passerines; triangles, raptors, including two Strigiformes and one Accipitriformes; squares, ‘other,’ including Anseriformes, Charadriiformes, Procellariiformes, Sphenisciformes, Pelicaniformes, and Ciconiiformes.

current reproductive effort; hence, the slow species would be expected to suppress GC secretion. Alternatively, slow species within a clade should pass the cost of current challenge onto their offspring, and so would be expected to have a robust GC response to challenge, moving energy expenditure away from current reproduction towards selfmaintenance. Are GCs primary mediators of the tradeoff between avian reproduction and survival? Does increasing GCs during the reproductive life-history stage necessarily lead to a decline in reproductive success that season? This chapter approaches this question from a ‘pace-of-life’ viewpoint, to evaluate how the above relationships may differ between slow- and fast-pace-of-life species. This

The field of comparative GC physiology has expanded rapidly since the early 1990s. An evaluation of those studies shows a straightforward categorization (Figure 5.2). The majority of papers evaluate physiological, behavioral, or environmental correlates of GC secretion, either examining baseline GC levels or GC response to capture and handling stress (Figure 5.2, light gray arrows). Other studies evaluate the relationship between endogenous or experimentally manipulated GCs and performance (Figure 5.2, dark gray arrow). Performance measures range from behavior (e.g., parental feeding rates, song production, territory defense) to immune function, and can be categorized as physiological, behavioral, or morphological changes resulting from altered GC level. The least common, but potentially most important, category evaluates the effect of GC level on direct fitness measures, such as reproductive output or survival (Figure 5.2, black arrow). A recent review highlighted the commonalities of studies within each category, noting the need for more direct fitness measures in studies of stress physiology (Breuner, Patterson, & Hahn, 2009). This chapter is structured using these categories, evaluating relationships from a pace-oflife perspective.

1.4. Pace-of-life and Brood Value For the purposes of this chapter, approximately 120 references dealing with avian GC physiology were used to measure interactions with the internal/external environment (category one), intermediate performance

FIGURE 5.2 Framework illustrating the relationships between environment, glucocorticoid (GC) secretion, intermediate performance measures, and fitness.

132

Hormones and Reproduction of Vertebrates

(performance measures that do not measure reproductive output or survival; category two), and direct fitness measures (measures of reproductive output or survival; category three). Demographic information from each species was obtained in order to determine pace-of-life (Table 5.1): average clutch size, number of broods per season, and annual adult survival probability (preferably

calculated using MARK (a model estimating survival using mark-recapture data)) (White & Burnham, 1999). If there were multiple populations for which data were available, the population was chosen that was closest to the one for which GC data was available. The pace-of-life framework offers a visualization of relationships among species (Figure 5.1). However, there is

TABLE 5.1 Demographic data for pace-of-life and brood value Common name

Species

Clutch Broods Total eggs Survival size per season per season probabilitya

Brood Valueb

References

Adelie penguin

Pygoscelis adeliae

1

1

1

0.76

0.38

Jenouvrier et al. (2006)

American tree sparrow

Spizella arborea

4.96

1

4.96

0.39

0.79

Naugler (1993)

Barn owl

Tyto alba

5.28

1

5.28

0.465

0.73

Marti et al. (2005)

Barn swallow

Hirundo rustica

6.875

2

13.75

0.35

0.51

Brown and Brown (1999)

Black-browed albatross

Thallasarche melanophris

1

1

1

0.765

0.37

Nevoux et al. (2007)

Black-legged kittiwake

Rissa tridactyla

1.5

1

1.5

0.86

0.15

Saether (1989); Hatch et al. (2009)

Blue tit

Cyanistes caeruleus

10.8

1

10.8

0.416

0.77

Martin and Clobert (1996)

Blue-footed booby

Sula nebouxii

2

1

2

0.9

0.00

Nelson (2006)

Cactus wren

Campylorhynchus brunneicapillus

3.45

2.54

8.73

0.5

0.30

Proudfoot et al. (2000)

Cliff swallow

Petrochelidon pyrrhonota

3.5

1

3.5

0.595

0.61

Brown and Brown (1995; 1998)

Common eider

Somateria mollissima

4.5

1

4.5

0.89

0.04

Hanssen et al. (2003); Descamps et al. (2009)

Common murre

Uria aalge

1

1

1

0.89

0.04

Ainley et al. (2002); Lee et al. (2008)

Common redpoll

Carduelis flammea

5

1

5

0.425

0.76

Knox and Lowther (2000)

Common tern

Sterna hirundo

2.5

1

2.5

0.73

0.43

Saether (1989); Knox and Lowther (2000)

Curve-billed thrasher

Toxostoma curvirostre

2.7

2.2

5.94

0.79

0.02

Twit (1996)

Dark-eyed junco

Junco hyemalis

4

1

4

0.45

0.74

Nolan et al. (2002)

Dusky flycatcher

Empidonax oberholseri

3.6

1

3.6

0.577

0.63

Pereyra and Wingfield (2003)

Eurasian tree sparrow

Passer montanus

4.95

2

9.9

0.439

0.45

Martin and Clobert (1996)

European blackbird Turdus merula

4.04

2.5

10.1

0.531

0.27

Martin and Clobert (1996)

European starling

Sturnus vulgaris

4.71

2

9.42

0.47

0.42

Cabe (1993); Martin (1995)

Florida scrub-jay

Aphelocoma coerulescens

4.5

1

4.5

0.774

0.35

Martin (1995); Woolfenden and Fitzpatrick (1996); Mumme et al. (2000)

Chapter | 5

133

Stress and Reproduction in Birds

TABLE 5.1 Demographic data for pace-of-life and brood valuedcont’d Common name

Species

Clutch Broods Total eggs Survival size per season per season probabilitya

Brood Valueb

References

Greylag goose

Anser anser

6

1

6

0.75

0.40

Saether (1989)

Harris’ hawk

Parabuteo unicinctus

3.5

1.5

5.25

0.817

0.09

Bednarz (1995)

Herring gull

Larus argentatus

3

1

3

0.76

0.38

Pierotti; Saether (1989)

House finch

Carpodacus mexicanus

4.4

2

8.8

0.552

0.35

Hill (1993); Martin (1995)

House sparrow

Passer domesticus

4.6

2

9.2

0.55

0.35

Martin and Clobert (1996)

Lapland longspur

Calcarius lapponicus

5.06

1

5.06

0.677

0.51

Custer and Pitelka (1977); Martin (1995)

Mallard

Anas platyrhynchos

8.91

1

8.91

0.53

0.67

Saether (1989); Krapu et al. (2004)

Mountain chickadee

Poecile gambeli

7

2

14

0.52

0.38

McCallum et al. (1999)

Northern pintail

Anas acuta

7.66

1

7.66

0.72

0.45

McCallum et al. (1999); Krapu et al. (2004)

Northern spotted owl

Strix occidentalis caurina

1.83

1

1.83

0.82

0.26

Gutierrez et al. (1995); Seamans and Gutierrez (2007)

Pied flycatcher

Fidecula hypoleuca

6.5

1

6.5

0.499

0.70

Martin and Clobert (1996)

Red-footed booby

Sula sula

1

1

1

0.9

0.00

Schreiber et al. (1996)

Red-winged blackbird

Agelaius phoeniceus

3.49

2

6.98

0.53

0.37

Martin (1995)

Semipalmated sandpiper

Calidris pusilla

4

1

4

0.62

0.58

Gratto-Trevor (1992); Rice et al. (2007)

Smith’s longspur

Calcarius pictus

3.8

1

3.8

0.61

0.59

Briskie (2009)

Snow bunting

Plectrophenax nivalis

5.23

1

5.23

0.37

0.80

Lyon and Montgomerie (1995); Martin, (1995)

Snow petrel

Pagadroma nivea

1

1

1

0.9

0.00

Barbraud et al. (2000)

Song sparrow

Melospiza melodia

4.1

2.5

10.25

0.576

0.23

Arcese et al. (2002)

Wandering albatross

Diomedea exulans

1

1

1

0.972

0.55

Weimerskirch (1992)

Western sandpipers

Calidris mauri

4

1

4

0.51

0.69

Wilson (1994); Fernandez et al. (2004)

White stork

Ciconia ciconia

4.6

1

4.6

0.784

0.33

Nevoux et al. (2008)

White-crowned sparrow

Zonotrichia leucophrys pugetensis

3.56

2.5

8.9

0.544

0.26

Martin (1995)

Willow warbler

Pyhylloscopus trochilus

6

1

6

0.45

0.74

Peach et al. (1995)

Yellow warbler

Dendroica petechia

4.3

1.5

6.45

0.573

0.45

Martin (1995)

Yellow-eyed penguin

Megadyptes antipodes

1

1

1

0.9

0.00

Ratz et al. (2004)

Zebra finch

Taeniopygia guttata

5

2

10

0.24

0.58

Zann and Runciman (1994)

a

Annual survival probability of adults. Brood value ¼ log10(clutch size/(clutch size broods per year (1/1adult survival probability))þ1.

b

134

Hormones and Reproduction of Vertebrates

no absolute value associated with each point, to enable numerical comparisons between species. Bo´kony et al. (2009) used the demographic data to calculate a ‘brood value’ for the current brood: log10 ðclutch size=ðclutch size broods per year average reproductive lifespanÞÞ where reproductive lifespan represents the inverse of adult mortality probability (1/1-adult survival probability). This calculation represents the value of current reproductive output relative to the lifetime reproductive output of a species. The majority of values resulting from this calculation range from 1 and 0, which can be confusing to assess. To simplify evaluation of brood value, þ1 has been added to each value so that the numbers range from 0e1. Higher brood values are found in species where the current brood represents a larger proportion of the total number of young produced in a lifetime. Hence, the fast-pace-of-life individuals (upper left in Figure 5.1) would have higher brood values and slow-pace-of-life individuals (lower right in Figure 5.1) would have lower brood values.

2. REGULATION OF GLUCOCORTICOID (GC) SECRETION This chapter asks how stress affects reproduction, or, how the GC response to stress mediates the allocation of resources between current and future reproductive events. As such, one would expect this chapter to focus solely on how GCs regulate reproductive function. However, the majority of literature on stress and reproduction concerns factors explaining variation in GC secretion. The authors of these papers approach this topic with a view to understanding how GCs will affect reproductive output, but ties to actual performance or fitness measures used are few. None-the-less, after 30 years of study, several strongly supported hypotheses elucidating how external (e.g., environment/social) and internal (e.g., body condition/immune status) factors affect GC reactivity, and, therefore, how animals will respond to stressors under varied conditions, have emerged. This section (1) briefly reviews how GC levels relate to annual seasonality, length of breeding season, and body condition and (2) goes further in depth on how GC levels change within the breeding cycle, especially in relation to parental care and pace-of-life differences. The discussion of these studies rests on the assumption that greater hormone levels measured during challenge will reflect greater change in physiology and behavior. This primary assumption drives the fitness expectations discussed in most of the ‘regulation of secretion’ studies. There is evidence to support this assumption. For example,

corticosterone (CORT) contained within silastic tubing and implanted into pied flycatchers reduced parental visits to the nest, while CORT implants with a hole punched in the side of the tubing caused nest desertion (Silverin, 1986). However, several studies in both birds and rats have demonstrated significant changes downstream of total CORT secretion in terms of binding globulins, intracellular degratory enzymes, and receptor number (Dhabhar, McEwen, & Spencer, 1993; Spencer et al., 1996; Breuner et al., 2003; Love et al., 2004). A study evaluating nest abandonment rates within 12 hours of sampling determined that free (unbound to corticosteroid-binding globulin (CBG)) CORT levels predict female starling nest abandonment, whereas total CORT does not (Lakshmi, Sakai, McEwen, & Monder, 1991; Love et al., 2004). Unfortunately it is exceedingly difficult to obtain measures of these downstream regulators, especially at the tissue level. The ‘greater hormone ¼ greater output’ hypothesis rests solidly on the assumption that hormone-behavior doseresponse curves are linear or monotonic in nature. There is very little evidence for this, and in fact overwhelming evidence exists for alternative dose-response curves, such as inverted-U-shaped or threshold-dependent curves (Hayden-Hixon & Ferris 1991a; 1991b; Diamond et al., 1992; Breuner & Wingfield, 2000). Hence, we expect total plasma hormone levels to offer an estimate of organismal effects during challenge, but one that lacks the fine-tuning of downstream regulators or consideration of a nonlinear dose-response curve.

2.1. Parental Care and Within-breedingseason Regulation How does brood value affect the GC response to stress? Bo´kony et al. (2009) reviewed the relationship between parental care and brood value across 64 species, incorporating data from 104 studies. Based on the brood value hypothesis, they predicted that (1) GC reactivity should be lower in species with a higher brood value and (2) sexbiased investment in parental care should be inversely related to sex differences in GC levels. They found that baseline CORT levels were strongly positively associated with brood value, while maximal CORT levels (corrected for changes in baseline and breeding latitude) were negatively associated with brood value (Figure 5.3). This author interprets this to mean that, when brood value is high, baseline levels are upregulated, allowing for greater flexibility in energy expenditure (Sapolsky, Romero, & Munck, 2000; Romero, 2002). Therefore, stress reactivity is suppressed, decreasing the likelihood of lower feeding rates or nest abandonment. The relationship shown in Figure 5.3 may be dependent on three data points, two from extremely long-lived sea birds (upper left) and one from a species that shows an incredibly small increase in

Chapter | 5

Stress and Reproduction in Birds

FIGURE 5.3 Regression of brood value against maximal corticosterone (CORT) levels corrected for variation in baseline CORT and latitude of population. Brood values reported here are all one unit lower than brood values in this chapter, as they were not corrected upward for ease of evaluation. Reproduced from Bo´kony et al. (2009), with permission.

stress-induced CORT (~10% increase to maximal stress levels). However, these data reflect patterns seen in several smaller studies, where expected brood value correlates with GC secretion. The first is described in detail in Section 2.3 (Breuner & Hahn, 2003), where three subspecies with different amounts of time to breed, and therefore a different brood value for each individual clutch, show a direct relationship between number of clutches and stress-induced free CORT (unbound to CBG). Specifically, as estimated clutch value increases

135

(fewer clutches per season), maximal CORT levels decrease. This relationship shows up repeatedly in latitudinal studies, where populations further north, with higher expected brood value, show suppression of the stress response (Silverin, Arvidsson, & Wingfield, 1997; Silverin & Wingfield, 1998; O’Reilly & Wingfield, 2001; Wilson & Holberton, 2004; however, see Section 2.3; Martin, Gilliam, Han, Lee, & Wikelski, 2005; Goymann et al., 2006). According to Bo´kony et al. (2009), sex-biased investment relates to maximal CORT levels in females. Specifically, as relative investment of male care increases, female maximal CORT levels increase but male CORT levels are unaffected. Hence, when females are responsible for the majority of care, they suppress CORT levels, increasing the likelihood of brood survival. Alternatively, when care is equal or primarily maledriven, female maximal levels rise, allowing the female to invest in self-maintenance. This effect in females is illustrated well by a study on several species of shorebird (O’Reilly & Wingfield, 2001) that exhibit three mating systems representing three different strategies for parental care: the polygamous pectoral sandpiper (Calidris fulicaria), the monogamous semipalmated sandpiper (Calidris pusilla), and the polyandrous red phalarope (Calidris fulicaria). The authors predicteddas did Bo´kony et al. (2009)dthat the sex responsible for the majority of parental care would suppress GC reactivity during incubation and nestling phases. Their predictions were supported, as GC response is suppressed in female pectoral sandpipers, equal in male and female semipalmated sandpipers, and suppressed in male red phalaropes (Figure 5.4). FIGURE 5.4 Three species of shorebird, each with different roles for males and females in raising the young. In the polygynous pectoral sandpiper (Calidris melanotos), the female raises the brood; in the monogamous semipalmated sandpiper (Calidris pusilla), parental care is shared; in the polyandrous red phalarope (Phalaropus fulicaria), the male raises the brood (parental care denoted by egg above bar). Stress-induced corticosterone secretion is inversely related to the load of parental care in each species. Redrawn from O’Reilly and Wingfield (2001), with permssion. See color plate section.

136

2.2. Annual Regulation of Glucocorticoids (GCs) Most seasonal species regulate GC secretion over the annual cycle. Romero (2002) reviewed baseline and stress-induced CORT levels across seasons, comparing prebreeding, breeding, and postbreeding data (the last was often represented by winter sampling). In birds (29 separate studies, 14 species), baseline CORT is upregulated during breeding compared to winter, whereas stress-induced CORT is static over the cycle except for a marked decline during molt. On average the species show no change in the GC response to stress, but that average is a result of eight species that increase GC response during breeding compared to winter, 13 species that decrease, and one that does not change. However, evaluation of these data from a pace-of-life perspective does not produce clear patterns. Based on the slow-to-fast continuum, we would expect that fast birds, taking the cost of challenge on themselves, would show a reduced response to stress during breeding (as compared to winter, when brood value is not a selective factor), whereas slow birds, passing the cost of challenge onto their offspring, would have equal or greater response to stress between breeding and winter. This author estimated brood values for most of the bird species reviewed by Romero (2002) (where data were available), also including 17 studies completed since 2002. All studies evaluated stress-induced GC levels during breeding and winter in a species for which clutch size, number of broods per season, and annual survival probability were known. This analysis ended up with 30 studies represented by only 11 species (Wingfield, Vleck, & Moore, 1992; Wingfield, Suydam, & Hunt, 1994; Astheimer, Buttemer, & Wingfield, 1995; Breuner & Orchinik, 2001; O’Reilly & Wingfield, 2001; Lindstrom, Hawley, Davis, & Wikelski, 2005; Romero, Cyr, & Romero, 2006; Lynn & Porter, 2008; Rubenstein, Parlow, Hutch, & Martin, 2008; Fokidis & Deviche, 2009; Newman & Soma, 2009). These data show no relationship between brood value and seasonal fluctuations of the GC response to stress. In fact, the data are completely overlapping (species with lower GCs during breeding have a brood value of 0.29 0.08; species with higher or equal GCs during breeding have a brood value of 0.33 0.04; brood values averaged across species from Table 5.1). To rigorously explore the relationship between brood value and seasonal change in GCs, one would need many more species representeddenough to perform a phylogenetic comparison of results. At present, those studies are not available.

2.3. ‘Latitudinal’ Regulation of Glucocorticoids (GCs) In the temperate and subtropical zones, there is an inverse relationship between latitude and time available to breed.

Hormones and Reproduction of Vertebrates

With less time to produce young (less opportunity for a second brood), each brood becomes more valuable. Hence, stress-induced GCs may be differentially regulated across species or populations with similar lifespans that breed at different latitudes, with higher GC secretion expected in populations at lower latitudes and lower GC secretion expected in populations at higher latitudes. However, the relationship between latitude and GCs is complicated by elevation and hemisphere differences. First, elevation complicates the relationship because higher elevation shortens available breeding time independently of latitude. As an extreme example, Eurasian woodcocks (Scolopax rusticola) breeding in the Himalayas (31 N; up to 3500 m elevation) will have a much shorter breeding season than Eurasian woodcocks breeding further north, around the Mediterranean (36 N; sea level). Second, climate changes more slowly through the southern latitudes than it does through the Northern latitudes. Therefore, a 7 shift north in the northern hemisphere (e.g., O’Reilly & Wingfield, 2001) will have a much more dramatic effect on the length of the breeding season than a similar shift in the southern hemisphere. For these reasons, it is best to avoid a scale of absolute latitude; one way towards that is to simply use the number of broods possible. In passerines and other short-lived species, number of broods represents the length of the breeding season, which is the relevant factor, independent of latitude, altitude, or hemisphere. Five subspecies of white-crowned sparrows (Zonotrichia leucophrys) breed from above the arctic circle down to southern California. Breuner et al. (2003) determined GC responses to stress in three separate populations, representing three of the five subspecies. The Z. l. gambelii population, breeding north of the Brooks Range (68 N; 720 m elevation) is severely limited in the amount of time in which to raise a clutch, and is therefore obligatorily single-brooded. Z. l. oriantha, breeding in the high Sierras (38 N; 2940 m), is somewhat less limited and may have years where two full broods are possible. Z. l. pugetensis, breeding in the Puget Sound area (47 N; 275 m), can raise up to three broods per season (Chilton, Baker, Barrentine, & Cunningham, 1995). Breuner et al. (2003) collected baseline and stress-induced GCs from males during the nesting period in all three populations, comparing total and free GC levels. The expectation was that stress-induced GC levels would be highest in the Z. l. pugetensis population (with a lower brood value) and lowest in the Z. l. gambelii population (with the highest brood value). Surprisingly, total stress-induced GC levels were similar among the three populations; however, binding-globulin affinity and capacity changed, so that estimations of free GC levels were highest in Z. l. pugetensis, intermediate in Z. l. oriantha, and lowest in Z. l. gambelii. Hence, the level of free stress-induced GCs is inversely correlated with the length of the current breeding effort (Figure 5.5). In this

Chapter | 5

Stress and Reproduction in Birds

137

FIGURE 5.5 Population location and total corticosterone (CORT), corticosterone-binding globulin (CBG), and free CORT levels in three populations of white-crowned sparrows with varied amounts of time to breed. Blue, Zonotrichia leucophrys gambelii; green, Zonotrichia leucophrys pugetensis; black, Zonotrichia leucophrys oriantha. Redrawn from Breuner et al. (2003), with permission. See color plate section.

study, by using brood number instead of latitude, the relationship between GCs and each reproductive attempt could be evaluated more clearly. A review of the studies published on latitude over the last 10 years provides marginal support for the effects of latitude on GC reactivity. Across 10 passerines and two seabirds, six species show suppressed GC reactivity at more northern latitudes, three show no difference, and two show higher GC reactivity in the north (Wingfield, Kubokawa, Ishida, Ishii, & Wada, 1995; Silverin et al., 1997; O’Reilly & Wingfield, 2001; Wilson & Holberton, 2004; Lindstrom et al., 2005; Martin et al., 2005; Goymann et al., 2006). However, one of these two counterexamples is from male bush warblers (Cettia diphone), the only polygynous

species represented; if a male is not involved in parental care, one would not expect a suppression of GC reactivityd see above. In contrast to this, Bo´kony et al. (2009) found the opposite pattern when the latitude of each population of 64 species was added as a covariate in the analysis. Surprisingly, GC reactivity was directly related to latitude, and so increased as one moved away from the equator; Akaike’s Information Criterion identified latitude as the prominent explanatory variable in determining elevated GC levels. Can this be explained by difference in scale? Most of the studies on individual species are carried out over a 7e15 change, usually within one climate zone (though see Breuner et al., 2003; Goymann et al., 2006). The Bo´kony study covers a range of species from 66 to 82 N,

138

with a fairly good representation of tropical populations. It is possible that the small differences in elevated GCs measured over short distances are overwhelmed by largescale hormonal differences due to tropical vs. temperate habitat; hormone patterns are often less dynamic in the tropics (Hau, Gill, & Goymann, 2008). To clarify this, it would be helpful to use length of breeding season instead of latitude, in order to avoid confounding elevation and hemisphere, to determine whether the pattern persists.

2.4. Body Condition and Glucocorticoids (GCs) Glucocorticoid reactivity is often inversely related to body condition. Greater energetic reserves during challenge are thought to lessen the volume of GCs released, since the animal can often wait out whatever challenge occurs and move on to find more resources once the challenge has passed. Animals with fewer endogenous reserves secrete more GCs during a challenge, and so are more likely to redirect behavior away from the current reproductive effort towards survival. For example, low food availability in an income breeder (fueling reproduction from available food in the environment) may cause an increase in GC levels. Animals in good condition may only have a slight increase in GCs, and therefore spend less time feeding young and more time searching for food. In contrast, animals in poor condition may have a larger GC increase, inducing nest abandonment to ensure energy availability for the parent. However, there is incredible variation in the relationship between energetic reserves and GC elevation, with many studies showing no relationship at all. The pace-of-life hypothesis would predict that fast species would keep GC levels low, despite low body condition, to enable continuation of the current brood. Alternatively, slow species would be expected to vary GC elevation according to body condition, so that self-maintenance is prioritized over current reproduction. In terms of brood value, we then expect that animals with high brood value (high relative value of the current brood) would suppress the GC response, in spite of low energetic reserves, while animals with low brood value would allow for GC response to vary inversely with body condition. Of the 17 avian studies that include measures of body condition and GC reactivity during the breeding season, only 12 of them are in species with survival data (Wingfield et al., 1994; Schoech et al., 1997; Wingfield, Ramos-Fernandez, La Mora, & Drummond, 1999; Pravosudov, Kitaysky, Wingfield, & Clayton, 2001; Breuner & Hahn, 2003; Pereyra & Wingfield, 2003; Lindstrom et al., 2005; Moe, Angelier, Bech, & Chastel, 2007; Muller et al., 2007). Surprisingly, the results are exactly opposite to those predicted. Species with low brood value sort into the group that does not modulate GCs with

Hormones and Reproduction of Vertebrates

body condition, while species with high brood value do modulate GCs inversely to body condition (mean brood values: 0.18 0.09 vs. 0.54 0.07, respectively). Certainly, this relationship is complicated by the dichotomous strategies represented by income vs. capital breeders. Capital breeders fuel reproduction from endogenous stores, and so go through predictable fasts with radical change in body condition. If we remove the capital breeders from the relationship (leaving 10 species, all passerines), any directional relationship disappears, and species that vary GC secretion with body condition have similar brood values to those that do not. In the world of avian endocrinology, lower body condition is thought to be bad, while higher body condition is thought to be good. So, the greater the energetic reserves, the better. This is incredibly oversimplified. As body mass increases in a given skeletal size, it can significantly hamper maneuverability, increasing the risk of predation. In many bird species, chicks grow to be larger than adults and must lose weight to fledge. In both of these situations, lighter is better. Walsberg (2003) published a commentary on the use of energetics in stress physiology. His main point revolves around energy balance as only a small representation of what an animal may need, ignoring a wealth of other resources necessary for survival. He also argues that ‘energy balance’ is a temporally variable thing, wherein animals have periodic energy intake but constant power output. Hence, the timing of ‘balance’ will vary given the size and metabolic rate of the animal. Altogether, Walsberg argues for less attention to be spent on body condition and energy balance, as the saliency of the measure is not clear for the field of stress physiology.

3. INTERMEDIATE PERFORMANCE MEASURES In the evaluation of stress effects on reproduction, most measures fall short of direct fitness measures (e.g., nestling success or integration into the reproductive population in the next season). The majority of studies focus on intermediate measures of performance; i.e., measures that are expected to enhance or restrict reproductive success. This section covers morphological, physiological, and behavioral examples of intermediate performance measures that are known or thought to influence reproductive success.

3.1. Morphology Male morphological characteristics are thought to play an important role in female mate choice; hence, sexually selected characteristic development can have significant repercussions for reproductive success (Ferns & Lang,

139

Stress and Reproduction in Birds

3.2. Physiology

200

1.6

150

1.4

100

1.2

50

1.0

0

Flight muscle (g)

2003). Stressors have long been known to affect feather quality (King & Murphy, 1984; Murphy, King, & Lu, 1988), and recent experimental evidence has supported this finding. In male barn owls (Tyto alba), CORT implants reduced the level of pheomelanin (yellow to red coloration) of feathers growing while the implant was in place (Roulin et al., 2008). In white-crowned sparrows (Z. leucophrys), GC implants slowed individual feather growth (Romero, Strochlic, & Wingfield, 2005), while repeated acute bursts of GCs delayed the onset of molt (Busch, Sperry, Wingfield, & Boyd, 2008). In European starlings (S. vulgaris), GC implants slowed individual feather growth rate (Romero et al., 2005) and decreased feather quality, reducing coloration and increasing interbarb distance (DesRochers et al., 2009). There is also evidence for GCs reducing other sexually selected morphological traits in birds. In barn swallows, lower GC levels are associated with longer tails, a trait that is under current directional selection in this species (Saino, Incagli, Martinelli, Moller, 2002). In selected lines of the zebra finch (Taeniopygia guttata), males selected for higher GC reactivity had lower ultraviolet (UV) reflectance in both legs and cheek patches (Roberts, Buchanan, Hasselquist, Bennett, & Evans, 2007). Both structures are thought to be signals used by females to ascertain male quality.

Adipose tissue (mg)

Chapter | 5

0.8 Control

CORT

Adipose tissue

Control

CORT

Flight muscle

FIGURE 5.6 The change in adipose tissue and flight muscle after prolonged corticosterone (CORT) treatment in male dark-eyed juncos (Junco hymenalis). Reproduced from Gray, Yarian, and Ramenofsky (1990), with permission.

elevation does not raise GC levels high enough to increase fat load. Three recent captive studies show an overall loss of body mass in response to elevated GCs or chronic stress (El-Lethey, Huber-Eicher, & Jungi, 2003; Martin et al., 2005; Rich & Romero, 2005). However, this pattern does not hold for animals with endogenously higher GC response. Zebra finches selected for greater GC reactivity had the highest body mass index measured from all three groups (selected high, control, selected low) (Roberts et al., 2007a).

3.2.1. Body composition

3.2.2. Immune function

Glucocorticoids were named for their hyperglycemic properties. Gluconeogenesis is one pathway through which GCs increase blood glucose. Prolonged elevation of GCs reduces energetic stores across the body. In fasting mammals, elevated GCs reduce both muscle and fat. However, when elevated GCs are accompanied by nutrient intake, so that insulin and GCs are elevated at the same time, the nutrients are preferentially deposited as fat (Dallman et al., 1993), resulting in low muscle mass but incredibly high fat stores. This situation is similar in birds (Figure 5.6). Prolonged and repeated intermittent GC application results in a decline in muscle mass (Gray, Yarian, & Ramenofsky, 1990; Astheimer, Buttemer, & Wingfield, 2000; Bauchinger & Biebach, 2001; Busch et al., 2008), while GC implants increase fat stores in freeliving birds (Wingfield & Silverin, 1986; Wingfield, 1988; Gray et al., 1990). However, a recent study in captive whitecrowned sparrows (Z. leucophrys) showed no change in fat scores with repeated transient GC application compared to control birds (Busch et al., 2008). This may be because either (1) captive birds are already so overfed that further increase in fat level is difficult to detect or (2) repeated

The interaction of immune function and stress physiology is currently one of the most exciting areas in environmental endocrinology. With the onset of ecoimmunology, studies into relationships between hormones and immune function have proliferated (Martin, 2009). These studies have primarily focused on the immunosuppressive effects of GCs, which are interpreted as either (1) a brake on immune function in order to prevent autoimmune disease (Munck, Guyre, & Holbrook, 1984; Raberg, Grahn, Hasselquist, & Svensson, 1998; Sapolsky et al., 2000) or (2) a tradeoff of energy mobilization, such that costly behaviors during reproduction, or a shift in energy utilization during stress, cannot coexist with immune activity (Folstad & Carter, 1992; Lochmiller & Deerenberg, 2000; Martin et al., 2007). However, it is misleading to characterize GCs as solely immunosuppressive. In the mammalian literature, the enhancing vs. suppressive effects of GCs depend on the time frame of reference as well as the specific arm of the immune system (reviewed by Martin, 2009). The vertebrate immune system has both innate and adaptive arms, and each arm has humoral and cellular components. The innate arm is a rapid general defense

140

These studies, however, can be extremely difficult to carry out in free-living birds, especially the adaptive studies that require the investigator to repeatedly capture the same animal. As a result, the majority of avian studies in this area have associated GC treatment with one specific component of the immune system, such as measuring the secondary antibody response (adaptive/humoral), bactericidal activity (complement), or wing-web swelling (adaptive/cellular when given in a two-injection treatment). With only one component tested, it is difficult to truly assess tradeoffs within the immune system and to discern whether GC effects on the immune system are total or isolated to one specific component. Additionally, the bird immune system is not identical to the mammalian system, which limits our ability to extrapolate from mammalian systems. Birds lack lymph nodes (a key site of upregulation of the adaptive immune response), and they have a different set of inflammatory cytokines and different types of white blood cells (see Kaiser & Staheli, 2008 for a helpful review). Despite these limitations, a good number of avian studies address GC interaction with both cellular and humoral components of the immune system. The most in-depth studies have been done in chickens (Gallus domesticus). S. Shini, Kaiser, A. Shini, and Bryden (2008) demonstrated the temporal divergence of GC action on humoral immune function. Experimentally increased GC initially enhanced primary antibody response (after one hour) but decreased the response to below that of controls after three and 24 hours (Figure 5.7). Glucocorticoid increase also resulted in a decrease in immune tissue weight. In free-living birds, the results are much more

4.0

IBV titre (log 10)

*

3.5

*

*

3.0 Control Saline Corticosterone

2.5

hr 24

hr 3

hr 1

hr

2.0 0

against pathogens. It is composed of many cell types, such as macrophages, granulocytes, and natural killer cells. These cells fight infection directly and also secrete substances to fight pathogens extracellularly, such as complement, antimicrobial peptides, and destructive enzymes. The adaptive arm consists of the cells and antibodies generated to fight specific antigens of invading cells or organisms. The adaptive arm requires upregulation of helper T cells, killer T cells, or antibody-producing B cells specific to the pathogen present; mobilization of this arm of the immune system takes longer, but the arm is more potent once fully activated. At the base of the adaptive arm are helper T cells, which release cytokines to activate either the cellular or humoral components of the adaptive arm. Additionally, differential activation within the adaptive or the innate arm can subsequently alter the activation of the other arm. Hence, the vertebrate immune system is incredibly complex, with tradeoffs within and between arms. As a result, the strongest tests of GC-immune interactions assess multiple arms of the immune system, and illuminate possible tradeoffs between activation and suppression of cellular and humoral components in the innate and adaptive arms. Although studies of GC-immune interactions have been most common in mammals (because of their obvious medical applications), we can draw on this vast literature to direct our appraisal of GC-immune studies in birds. Two poignant examples of GC-immune interactions from mammalian systems highlight this application. First, it has long been apparent that stress causes a decline in the cellular component of the adaptive arm, measured as a decline in leukocytes in the blood (up to 50% loss within two hours of stress). However, Dhabhar and McEwen (1997) reviewed mammalian studies demonstrating a redistribution of leukocytes to the skin, as opposed to an overall loss. In fact, the inflammatory response in the skin increased when accompanied by moderate stress, and almost doubled when accompanied by severe stress. This enhancement of the cellmediated inflammatory response (regulated through Th1 helper cells) is time-sensitive. Two hours of restraint or shaking stress enhanced the inflammatory response, while three weeks of chronic stress reduced the same response (Dhabhar & McEwen, 1997). The second example focuses on the GC-induced tradeoff between the humoral and cellmediated components of the adaptive arm. Over extended time periods (days to weeks), GCs inhibit the activity of mammalian Th1 cells and enhance the activity of Th2 cells, thereby suppressing the cell-mediated response while enhancing the humoral (antibody) response (see Elenkov, 2004 for review). Both of these examples illustrate that variation in GC effect is dependent on the time course and branch of immune response measured; they also support the need for a robust experimental approach when studying GC-immune interactions.

Hormones and Reproduction of Vertebrates

Time after vaccination FIGURE 5.7 Primary antibody response to infectious bronchitis virus (IBV) vaccine in chickens given control (1 ml ethanol in 1 L) or corticosterone (20 mg in 1 ml ethanol in 1 L water) water to drink over 10 days before blood was drawn for assay. The saline group received plain water to drink and a saline injection on day one as a control for a different experiment. Redrawn from S. Shini, Kaiser, A. Shini, and Bryden (2008), with permission.

Chapter | 5

141

Stress and Reproduction in Birds

variable. Study of general immunity in house finches (Carpodacus mexicanus) showed that birds with higher maximal CORT in response to capture and handling are more likely to contract mycoplasma infection (Lindstrom et al., 2005). In fasting, incubating common eiders (Somateria mollissima), CORT implant reduced general immunoglobulin levels compared to control implanted females (Bourgeon & Raclot, 2006). Cutaneous immunity was measured in zebra finches (T. guttata) by injecting a foreign antigende.g., phytohemagglutinin (PHA)dinto the wing web and quantifying swelling 24 hours later. In individuals selected for greater GC reactivity, there was no line effect on PHA response, but endogenous stressinduced CORT levels were directly related to PHA response (greater GC levels indicate greater response) (Roberts et al., 2007a; Roberts, Buchanan, Hasselquist, Evans, 2007). In north temperate house sparrows (Passer domesticus), CORT implants reduced the PHA response, but there was no effect in tropical house sparrows (Martin et al., 2005). There was no effect of CORT implants on the PHA response in barn swallows (Hirundo rustica) (Saino et al., 2002) or in fasting common eiders (S. mollissima) (Bourgeon & Raclot, 2006). In zebra finches, stressinduced CORT levels were positively related with secondary antibody response against diphtheria, but negatively related to primary antibody response to tetanus (among individuals, not among selected lines; Roberts et al., 2007a; 2007b). In white-laying hens (Gallus gallus domesticus), GC treatment reduced the primary antibody response to both sheep red blood cells and tetanus toxoid, but not to human serum albumin (all three injected into hens eight days before primary antibody sampling) (ElLethey et al., 2003). Taken together, it is difficult to synthesize any overall effects of GCs on immune system function in birds. Based on mammalian studies, we expect extended GC application to enhance humoral immune function, but the evidence supports this in some species (e.g., zebra finches) and not in others (e.g., laying hens). In contrast, GC application should inhibit cell-mediated immune function, but, once again, support for this is equivocal. Additionally, a common immune test (PHA injection) in mammals is supposed to measure cell-mediated immunity, but in birds the tests all measure 24-hour responses to initial PHA injection, not the 24-hour response to the second PHA injection 8e12 days after the first. Hence PHA data do not truly measure a full cell-mediated adaptive immune response and so we cannot apply these measures to our expectations as outlined by mammalian studies. The way forward may lie in testing multiple aspects of immune function (innate, adaptive with humoral, and cell-mediated) within one species. Roberts et al. (2007a; 2007b) have obtained the most complete look at immune function in zebra finches. However, these

results are based on selected lines, not direct GC application, so the results are all correlational. While the results presented above are mixed, it is clear that GCs can have significant effects on immune function. This interaction is thought to have driven the evolution of CBGs, enabling delivery of GCs directly to sites of immune activity (Pemberton, Stein, Pepys, Potter, & Carrell, 1988). Corticosteroid-binding globulin is a glycoprotein present in the plasma with high affinity for GCs. It is thought to limit access of GCs to tissues, in that only free GCs can cross capillaries and enter tissues (Hammond, 1995; Breuner & Orchinik, 2002; Malisch & Breuner, 2010). This prevents approximately 95% of circulating GCs from accessing tissues and, hence, effecting a change in immune function. However, mammalian CBG is a member of the serine protease superfamily; this family of proteins is cleaved by elastase secreted by activated neutrophils. Hence, at sites of inflammation, CBG can be cleaved, resulting in a local increase in free CORT from 5 to 100% of total CORT in the plasma. If avian CBG is also a member of this family, immune activation could be highly regulated by CBG in the plasma.

3.3. Behavior 3.3.1. Singing and territorial behavior Several studies link GCs to reduced song performance. Greater CORT secretion as adults is correlated with lower song rates (Owen-Ashley, Turner, Hahn, & Wingfield, 2006; Wada et al., 2008), and food restriction (known to increase endogenous CORT levels (Lynn et al., 2003)) reduces undirected song in zebra finches by 67% (Johnson & Rashotte, 2002). Additionally, developmental nutritional stress is associated with poor song performance as adults. While CORT levels were not measured in these studies, nutritional stress increases endogenous CORT levels in several species (Kitaysky, Piatt, Wingfield, & Romano, 1999; Kitaysky, Kitaiskaia, Wingfield, & Piatt, 2001; Kitaysky, Romano, Piatt, Wingfield, & Kikuchi, 2005). As a result of early nutritional stress, there is a reduction in song repertoire (Nowicki, Searcy, & Peters, 2002; Spencer, Buchanan, Goldsmith, & Catchpole, 2004), number of song bouts, length of song bouts, and total time spent singing (Buchanan, Spencer, Goldsmith, & Catchpole, 2003). One song performance study experimentally increased CORT during development, resulting in a decrease in song complexity in adults (Spencer et al., 2004), similar to the results found with nutritional stress described above. Wingfield and Silverin (1986) examined GC effects on aggressive responses to simulated territorial intrusion (STI), which is a standardized method for obtaining unbiased measures of territorial behavior. Only three of the ten CORT-implanted males responded to STI at all; those three

142

spent less time within 5 m, took fewer flights over the decoy, and sang fewer songs as compared to control males. Surprisingly, this study has only been replicated and published three times, all within arctic passerines. As described above, arctic breeding seasons are necessarily shorter, limiting the number of broods a species can have. In fact, all three species studied (white-crowned sparrow (Z. leucophrys), Lapland longspur (Calcarius lapponicus), and tree sparrow (Spizella arborea)) are obligatorily single brooded when breeding in the arctic. Hence, the brood value of each individual brood should be higher for the three arctic populations as compared to the temperate song sparrow. Of the three, the Lapland longspur and the tree sparrow male responses to STI are insensitive to CORT (Astheimer et al., 2000; Meddle, Owen-Ashley, Richardson, & Wingfield, 2003). This indicates that the current brood is of high enough value that males have evolved behavioral insensitivity to CORT, making it less likely that they will abandon the current brood if circumstances deteriorate. Surprisingly, white-crowned sparrows are sensitive to CORT implant and show a reduction of aggressive behavior in response to STI when CORT is present (Meddle et al., 2002). From a pace-of-life perspective, we would expect calculated brood values for temperate song sparrows to be lower than those for Lapland longspurs and American tree sparrows because the latter two species have repressed their response to CORT during breeding. Brood values fall out as expected: song sparrow with the lowest at 0.23 and longspurs and tree sparrows higher at 0.59 and 0.79, respectively (see Table 5.1). In this case, brood value does predict behavioral response to CORT, in that two species with little time to breed, and thus high brood value, repress their response to stress and take the cost of stressors onto themselves (instead of passing it onto their young).

3.3.2. Foraging/feeding young Elevated GCs are thought to increase self-maintenance behavior at the cost of parental care. For example, parents may increase foraging without increasing food delivery to the young. This increase in foraging time usually results in a reduction of time spent with the young, which is especially important for altricial chicks before they reach thermoregulation. Subsets of this paradigm have been demonstrated in several studies. Chronic and transient CORT administration increases both foraging and food intake measures (Saldanha, Schlinger, & Clayton, 2000; Koch, Wingfield, & Buntin, 2002; Lohmus, Sundstrom, & Moore, 2006; Angelier, Clement-Chastel, Gabrielsen, & Chas, 2007). Higher endogenous CORT is linked to greater time spent away from the nest and greater weight gain while feeding young (Angelier et al., 2007a; Angelier, Shaffer, Weimerskirch, Trouve, & Chastel, 2007; Lendvai

Hormones and Reproduction of Vertebrates

& Chastel, 2008). Corticosterone implants increase time spent away from the young (Silverin, 1986; Kitaysky, Wingfield, & Piatt, 2001). Lastly, elevated CORT (endogenous or experimental) is associated with a reduction in chick feeding rate (Silverin, 1986; Almasi, Roulin, JenniEiermann, & Jenni, 2008). A few recent studies have, however, challenged the idea that CORT reduces offspring feeding rate. In common murres (Uria aalge) and Adelie penguins (Pygoscelis adeliae), elevated endogenous CORT levels are associated with behaviors that should benefit the young. First, common murres usually time breeding with the spawning period of capelin fish, matching food availability to the increased food requirement of their young. However, one year there was a mismatch, and the young hatched before the capelin spawned. As expected, average CORT levels were elevated in all of the parents that year; however, the birds who provisioned their young at higher rates were the individuals with higher endogenous CORT levels (Doody, Wilhelm, McKay, Walsh, & Storey, 2008). In Adelie penguins, preforaging CORT levels were compared to distance travelled. Individuals with higher pretrip CORT levels spent less time at sea, remained closer to the colony, and had lower mass gain over the trip (Angelier et al., 2008). These trip characteristics are usually associated with short trips made to feed young at the expense of selfmaintenance (Weimerskirch et al., 2003). Both of these examples indicate that elevated CORT may be associated with an increase in provisioning to the young, and have led to the formation of a new hypothesis on the relationship between CORT, foraging, and provisioning: under ideal conditions, parents can forage and feed their young as required; however, slight elevations in CORT levels may initially increase parental feeding behavior, whether through mobilization of greater energy stores to meet costs of foraging, increasing nest attentiveness, or some undescribed pathway. This suggests that moderately elevated CORT may be a necessary and inherent part of reproduction (Angelier et al., 2008). However, when endogenous CORT levels are greatly elevated above baseline (as is the case for most of the implant studies mentioned above), foraging behavior will become more directed towards selfmaintenance, at the cost of food delivery to the young.

4. DIRECT FITNESS METRICS How does stress affect reproduction? Thus far, this chapter has covered the regulation of CORT secretion and the effect of CORT on intermediate performance measures, but has not directly addressed the effect of CORT on reproductive output. As stated throughout this chapter, CORT is thought to redirect physiology and behavior away from reproductive activities and toward self-maintenance, mediating the tradeoff intrinsic to limited budgets of energy and time.

Chapter | 5

143

Stress and Reproduction in Birds

If this idea is true, then elevated CORT should be associated with diminished reproductive output. Bonier, Moore, Martin, and Robertson (2009) have addressed reproductive/survival issues with the CORTefitness hypothesis. This hypothesis states that increased CORT will result in a decline in fitness, independently of whether that fitness metric is reproductive output or survival. Their argument stems from the concept that, when comparing two populations, the one facing challenge will have lower reproductive success or survival than the one under ideal conditions. This author agrees with this argument (which is supported by several avian studies d see Section 4.1), but feels that it oversimplifies CORTd fitness interactions by neglecting the tradeoff between allocation of resources towards current vs. future reproduction. Within the CORTefitness hypothesis, there is no room for brood value, no consideration of tradeoffs, and no room for exploring selection for CORT reactivity as it modulates differential expression of physiology and behavior in individuals under similar conditions. The CORTefitness hypothesis was not well supported by previous work, possibly because variation among and within species is too great (Bonier et al., 2009). However, the example Bonier et al. use of the effect of CORT on reproduction and survival in side-blotched lizards (Uta stansburiana) (Lancaster, Hazard, Clobert, & Sinervo, 2008) actually supports the focus of this chapter: the utility of brood value. In side-blotched lizards, yellow slow-pace-of-life females have fewer larger young, while orange fast-pace-of-life females have many small young. Exogenous CORT elevation increases reproduction and decreases survival in orange females, while having the opposite effect in yellow females. This study is useful for a number of reasons. First, unlike most fitness studies, it measures both reproduction and survival, so it is possible to directly measure the tradeoff. Second, it demonstrates that alternative reproductive strategies (different brood values) show different sensitivity to CORT elevation, indicating the need for inclusion of brood value in further analyses.

4.1. Reproduction The majority of studies evaluating the effects of GCs on reproduction do so at a population level, evaluating correlations between reproductive success in one population facing a more challenging environment against reproductive success in a population not facing that challenge. It is important to realize that reproduction and survival will be reduced in the face of challenge, compared to an ‘ideal’ stress-free population. Instead of population comparisons, we need within-population investigations evaluating fitness parameters across individuals that react to challenges with different CORTebehaviorephysiology output.

We can, however, gain some initial insights from these population-level studies. The relationship between CORT and reproductive output between populations suggests that increased endogenous CORT predicts lower reproductive success (Wingfield et al., 1999; Scheuerlein, Van’t Hof, & Gwinner, 2001; Saino, Romano, Ferrari, Martinelli, & Moller, 2005; Ellenberg, Setiawan, Cree, Houston, & Seddon, 2007; Muller et al., 2007; Williams, Kitaysky, Kettle, & Buck, 2008). Further, experimentally increased CORT (implant) reduces breeding success in terms of number of young fledged, number of unhatched eggs, and nest abandonment (Silverin, 1986; 1998; Criscuolo et al., 2005; Almasi et al., 2008; Angelier & Chastel, 2009). Four other studies showed no relationship between endogenous CORT level and reproductive output (Beletsky, Orians, & Wingfield, 1992; Wingfield et al., 1999; Evans, Roberts, Buchanan, & Goldsmith, 2006; Almasi et al., 2008). In an interesting study, Cyr and Romero (2007) applied random, continuous acute stressors to female free-living starlings (Sturnus vulgaris). This treatment reduced CORT around 24 hours after completion of the last acute stressor; mothers experiencing chronic stress fledged fewer young compared to animals not receiving the treatment. Hence, it appears in this situation that a lower CORT level is associated with a loss of reproductive output. However, it is entirely possible that CORT levels were elevated during and immediately after the acute stressors were applied, but that the repeated elevation of the HPA axis downregulated overall CORT secretion, leading to lower CORT levels when measured the next day. Although we cannot evaluate overall CORT levels from this study, it does demonstrate that chronic stress lowers reproductive output in free-living starlings. Over the last two years, the number of within-population studies assessing CORTefitness relationships has increased significantly. Higher levels of endogenous CORT within a population predict lower reproductive success in six species (Love et al., 2004; Angelier, Weimerskirch, Dano, & Chastel, 2007; Bonier et al., 2007a; Bonier, Martin, & Wingfield, 2007b; Kitaysky, Piatt, & Wingfield, 2007). In one study, endogenous CORT levels predicted laying success, but not hatching or fledging success (Lanctot, Hatch, Gill, & Eens, 2003), and in another study higher endogenous CORT levels predicted lower fledging success if elevated CORT was observed early in the breeding season, but higher fledging success if elevation occurred later in the season (Bonier et al., 2009).

4.2. Survival Avian studies evaluating CORT relationship to survival in adults are still rare. In a declining colony of common murre (U. aalge), increased CORT level correlated with negative population growth, although this relationship was not

144

present in a growing colony (Kitaysky et al., 2007). In one colony of cliff swallows (Petrochelidon pyrrhonota), early CORT levels predicted lower survival rates to the next year (C. Brown, M. Brown, Raouf, Smith, & Wingfield, 2005).

4.3. Tradeoffs? To properly evaluate the adaptive significance of CORT effects on fitness, one needs to evaluate the effect on both reproduction and survival. A decline in reproductive output in one year is only adaptive if it increases survival probability to the next year. This tradeoff is elegantly illustrated in a study by Love and Williams (2008). In European starlings (S. vulgaris), greater CORT levels in mothers are associated with lower reproductive output but higher survival to the next year; however, the relationship is fairly

Hormones and Reproduction of Vertebrates

complex. Mothers in poor body condition have elevated CORT levels. When this level of CORT is injected into eggs, the resulting brood has a higher proportion of females, and the males grow at a slower rate than control males. To test whether this type of brood benefits the mother in poor condition, Love and Williams produced four groups of European starlings: control mothers with control broods, control mothers with CORT-treated broods (fewer and smaller males), ‘poor-condition’ mothers (wing feathers clipped to reduce foraging ability) with control broods, and ‘poor-condition’ mothers with CORT-treated broods. The salient comparison here is the survival rates of mothers in poor condition with and without CORT-treated broods. The wing clipping reduced the ability of mothers to feed their young. However, the broods with CORT treatment required less food, and so matched the ability of the

FIGURE 5.8 Matching clutch need to maternal ability: if a poor-condition mother (wing-clipped) produces a poor condition brood (corticosterone (CORT)-treated), she will raise fewer young that year (upper graph) but increase her survival probability 10-fold over poor-condition mothers raising a full brood (lower graph). Redrawn from Love and Williams (2008), with permission. See color plate section.

Chapter | 5

145

Stress and Reproduction in Birds

wing-clipped mothers. The reproductive output was lower for all poor-condition mothers, but survival to the next year was higher in those mothers whose brood matched their ability. That is, if a poor-condition mother produces a poorcondition brood, she will raise fewer young that year but increases her survival probability 10-fold over poorcondition mothers raising a full brood (Figure 5.8).

HPA MR PHA STI Th1 Th2 UV

5. SUMMARY

REFERENCES

How does stress affect reproduction in birds? We know that higher brood value predicts lower GC response, but does not predict seasonality of that response, and it appears that GCelatitude relationships vary by scale of enquiry (Section 2). There is strong evidence for a negative relationship between GCs and sexually selected traits (feather quality, song, and territorial defense); GCs may enhance attendance of young at low levels but suppress it at higher concentrations, and GC-immune interactions can depend on timing, arm of the immune system, species, and season (Section 3). Finally, populations with elevated GCs tend to have lower reproductive output and lower survival, but within-population studies produce much more complicated results (Section 4). To truly evaluate the role of GCs in allocating resources between reproduction and survival, we need more studies directly evaluating reproduction and survival within a population. At present, there are very few studies measuring CORTesurvival interactions in adult birds. Further, while there are more studies evaluating CORTereproduction interactions, the majority look between populations, demonstrating that a population facing challenge (stress) will have lower fitness than a population ‘without’ challenge. Additionally, the majority of studies are correlative, offering much less power to determine what effect is due to CORT elevation and what may simply be a byproduct of individual quality or a nonadaptive association. Only one study to date has evaluated the tradeoff between reproduction and survival to assess the adaptive benefit of the CORT effect, and found that the decline in reproductive output resulting from elevated CORT did indeed increase survival to the next breeding opportunity (Love and Williams, 2008, Figure 5.8). We have come a long way from measuring hormone eenvironment interactions, to directly assessing CORTefitness measures. However, there is a long way to go before we can fully support any directional effect of stress on reproduction.

Ainley, D., Nettleship, D., Carter, H., & Storey, A. (2002). Common Murre (Uria aalge). In A. Poole (Ed.), The Birds of North America, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/666. Almasi, B., Roulin, A., Jenni-Eiermann, S., & Jenni, L. (2008). Parental investment and its sensitivity to corticosterone is linked to melaninbased coloration in barn owls. Hormones and Behavior, 54, 217e223. Angelier, F., & Chastel, O. (2009). Stress, prolactin and parental investment in birds: a review. General and Comparative Endocrinology, 163, 142e148. Angelier, F., Bost, C. A., Giraudeau, M., Bouteloup, G., Dano, S., & Chastel, O. (2008). Corticosterone and foraging behavior in a diving seabird: the Adelie penguin, Pygoscelis adeliae. General and Comparative Endocrinology, 156, 134e144. Angelier, F., Clement-Chastel, C., Gabrielsen, G. W., & Chastel, O. (2007a). Corticosterone and time-activity budget: an experiment with black-legged kittiwakes. Hormones and Behavior, 52, 482e491. Angelier, F., Shaffer, S. A., Weimerskirch, H., Trouve, C., & Chastel, O. (2007b). Corticosterone and foraging behavior in a pelagic seabird. Physiological and Biochemical Zoology, 80, 283e292. Angelier, F., Weimerskirch, H., Dano, S., & Chastel, O. (2007c). Age, experience and reproductive performance in a long-lived bird: a hormonal perspective. Behavioral Ecology and Sociobiology, 61, 611e621. Arcese, P., Sogge, M., Marr, A., & Patten, M. (2002). Song Sparrow (Melospiza melodia). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/ species/704. Astheimer, L. B., Buttemer, W. A., & Wingfield, J. C. (1995). Seasonal and acute changes in adreoncortical responsiveness in an arcticbreeding bird. Hormones and Behavior, 29, 442e457. Astheimer, L. B., Buttemer, W. A., & Wingfield, J. C. (2000). Corticosterone treatment has no effect on reproductive hormones or aggressive behavior in free-living male tree sparrows, Spizella arborea. Hormones and Behavior, 37, 31e39. Barbraud, C., Weimerskirch, H., Guinet, C., & Jouventin, P. (2000). Effect of sea-ice extent on adult survival of an Antarctic top predator: the snow petrel Pagodroma nivea. Oecologia, 125, 483e488. Bauchinger, U., & Biebach, H. (2001). Differential catabolism of muscle protein in garden warblers (Sylvia borin): flight and leg muscle act as a protein source during long distance migration. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 171, 293e301. Bednarz, J. (1995). Harris’s hawk (Parabuteo unicinctus). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/146.

ABBREVIATIONS CBG CORT GC GR

Corticosteroid-binding globulin Corticosterone Glucocorticoid Glucocorticoid receptor

Hypothalamicepituitaryeadrenal Mineralocorticoid receptor Phytohemagglutinin Simulated territorial intrusion T-helper cells-1 T-helper cells-2 Ultraviolet

146

Beletsky, L. D., Orians, G. H., & Wingfield, J. C. (1992). Year-to-year patterns of circulating levels of testosterone and corticosterone in relation to breeding density, experience, and reproductive success of the polygynous red-winged blackbird. Hormones and Behavior, 26, 420e432. Bo´kony, V., Lendvai, A. Z., Liker, A., Angelier, F., Wingfield, J. C., & Chastel, O. (2009). Stress response and the value of reproduction: are birds prudent parents? American Naturalist, 173, 589e598. Bonier, F., Martin, P., Moore, I. T., & Wingfield, J. C. (in press). Do baseline glucocorticoids predict fitness? Trends in Ecology & Evolution. Bonier, F., Martin, P. R., Sheldon, K. S., Jensen, J. P., Foltz, S. L., & Wingfield, J. C. (2007a). Sex-specific consequences of life in the city. Behavioral Ecology, 18, 121e129. Bonier, F., Martin, P. R., & Wingfield, J. C. (2007b). Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird. Behavioral Ecology, 18, 1045e1050. Bonier, F., Moore, I. T., Martin, P. R., & Robertson, R. J. (2009). The relationship between fitness and baseline glucocorticoids in a passerine bird. General and Comparative Endocrinology, 163, 208e213. Bourgeon, S., & Raclot, T. (2006). Corticosterone selectively decreases humoral immunity in female eiders during incubation. Journal of Experimental Biology, 209, 4957e4965. Breuner, C. W., & Hahn, T. P. (2003). Integrating stress physiology, environmental change, and behavior in free-living sparrows. Hormones and Behavior, 43, 115e123. Breuner, C. W., & Orchinik, M. (2001). Seasonal regulation of membrane and intracellular corticosteroid receptors in the house sparrow brain. Journal of Neuroendocrinology, 13, 412e420. Breuner, C. W., & Wingfield, J. C. (2000). Rapid behavioral response to corticosterone varies with photoperiod and dose. Hormones and Behavior, 37, 23e30. Breuner, C. W., & Orchinik, M. (2002). Plasma binding proteins as mediators of corticosteroid action in vertebrates. Journal of Endocrinology, 175, 99e112. Breuner, C. W., Greenberg, A. L., & Wingfield, J. C. (1998). Noninvasive corticosterone treatment rapidly increases activity in Gambel’s whitecrowned sparrows (Zonotrichia leucophrys gambelii). General and Comparative Endocrinology, 111, 386e394. Breuner, C. W., Orchinik, M., Hahn, T. P., Meddle, S., Moore, I. T., Owen-Ashley, N., et al. (2003). Differential mechanisms for regulation of the stress response across latitudinal gradients. American Journal of Physiology: Regulatory, Comparative, and Integrative Physiology, 285, R594eR600. Breuner, C. W., Patterson, S. H., & Hahn, T. P. (2009). A ‘good’ stress response? Searching for relationships between the acute glucocorticoid response and fitness. Integrative and Comparative Biology, 49. E21eE21. Briskie, J. (2009). Smith’s Longspur (Calcarius pictus). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/034. Brown, C. R., & Brown, M. (1999). Barn Swallow (Hirundo rustica). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/452.

Hormones and Reproduction of Vertebrates

Brown, C. R., & Brown, M. B. (1995). Cliff Swallow (Petrochelidon pyrrhonota). In A. Poole (Ed.), The Birds of North America, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/149. Brown, C. R., & Brown, M. B. (1998). Fitness components associated with alternative reproductive tactics in cliff swallows. Behavioral Ecology, 9, 158e171. Brown, C. R., Brown, M. B., Raouf, S. A., Smith, L. C., & Wingfield, J. C. (2005). Effects of endogenous steroid hormone levels on annual survival in cliff swallows. Ecology, 86, 1034e1046. Buchanan, K. L., Spencer, K. A., Goldsmith, A. R., & Catchpole, C. K. (2003). Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proceedings of the Royal Society of London Series B-Biological Sciences, 270, 1149e1156. Busch, D. S., Sperry, T. S., Wingfield, J. C., & Boyd, E. H. (2008). Effects of repeated, short-term, corticosterone administration on the hypothalamoepituitaryeadrenal axis of the white-crowned sparrow (Zonotrichia leucophrys gambelii). General and Comparative Endocrinology, 158, 211e223. Cabe, P. (1993). European starling (Sturnus vulgaris). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/048. Cherrington, A. D. (1999). Control of glucose uptake and release by the liver in vivo. Diabetes, 48, 1198e1214. Chilton, G., Baker, M. C., Barrentine, C. D., & Cunningham, M. A. (1995). White-crowned sparrow (Zonotrichia leucophrys). In A. Poole, & F. B. Gill (Eds.), The Birds of North America: Life Histories for the 21st Century, Vol. 183. Philadelphia, Washington D.C: The Academy of Natural Sciences, The American Ornithologists’ Union. Criscuolo, F., Chastel, O., Bertile, F., Gabrielsen, G. W., Le Maho, Y., & Raclot, T. (2005). Corticosterone alone does not trigger a short term behavioural shift in incubating female common eiders Somateria mollissima, but does modify long term reproductive success. Journal of Avian Biology, 36, 306e312. Custer, T. W., & Pitelka, F. A. (1977). Demographic features of a lapland longspur population near barrow, Alaska. Auk., 94, 505e525. Cyr, N. E., & Romero, L. M. (2007). Chronic stress in free-living European starlings reduces corticosterone concentrations and reproductive success. General and Comparative Endocrinology, 151, 82e89. Dallman, M. F., Akana, S. F., Cascio, C. S., Darlington, D. N., Jacobson, L., & Levin, N. (1987). Regulation of acth-secretiond variations on a theme of B. Recent Progress in Hormone Research, 43, 113e173. Dallman, M. F., Akana, S. F., Levin, N., Walker, C. D., Bradbury, M. J., Suemaru, S., et al. (1994). Corticosteroids and the control of function in the hypothalamoepituitaryeadrenal (HPA) axis. In E. R. deKloet et al. (Eds.), Brain Corticosteroid ReceptorsdStudies on the Mechanism, Function, and Neurotoxicity of Corticosteroid Action, Vol. 746, (pp. 22e32). Dallman, M. F., Darlington, D. N., Suemaru, S., Cascio, C. S., & Levin, N. (1989). Corticosteroids in homeostasis. Acta Physiologica Scandinavica, 136, 27e34. Dallman, M. F., Strack, A. M., Akana, S. F., Bradbury, M. J., Hanson, E. S., Scribner, K. A., et al. (1993). Feast and famine: critical

Chapter | 5

Stress and Reproduction in Birds

role of glucocorticoids with insulin in daily energy flow. Frontiers in Neuroendocrinology, 14, 303e347. Descamps, S., Gilchrist, H. G., Bety, J., Buttler, E. I., & Forbes, M. R. (2009). Costs of reproduction in a long-lived bird: large clutch size is associated with low survival in the presence of a highly virulent disease. Biology Letters, 5, 278e281. DesRochers, D. W., Reed, J. M., Awerman, J., Kluge, J. A., Wilkinson, J., Van Griethuijsen, L. I., et al. (2009). Exogenous and endogenous corticosterone alter feather quality. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology, 152, 46e52. Dhabhar, F. S., & McEwen, B. S. (1997). Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain Behavior and Immunity, 11, 286e306. Dhabhar, F. S., McEwen, B. S., & Spencer, R. L. (1993). Stress response, adrenal steroid receptor levels and corticosteroid-binding globulin levelsda comparison between Sprague-Dawley, Fischer 344 and Lewis rats. Brain Research, 616, 89e98. Diamond, D. M., Bennett, M. C., Fleshner, M., & Rose, G. M. (1992). Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus, 2, 421e430. Dittami, J., Meran, I., Bairlein, F., & Totzke, U. (2006). Winter patterns of foraging, fat deposition and corticosterone differ between bearded and blue tits: is this an expression of egalitarian or depositic winter flocks? Journal of Ornithology, 147. 158. Doody, L. M., Wilhelm, S. I., McKay, D. W., Walsh, C. J., & Storey, A. E. (2008). The effects of variable foraging conditions on common murre (Uria aalge) corticosterone concentrations and parental provisioning. Hormones and Behavior, 53, 140e148. El-Lethey, H., Huber-Eicher, B., & Jungi, T. W. (2003). Exploration of stress-induced immunosuppression in chickens reveals both stressresistant and stress-susceptible antigen responses. Veterinary Immunology and Immunopathology, 95, 91e101. Elenkov, I. J. (2004). Glucocorticoids and the Th1/Th2 balance. In T. Kino et al. (Eds.), Glucocorticoid Action: Basic and Clinical Implications, Vol. 1024, (pp. 138e146). Ellenberg, U., Setiawan, A. N., Cree, A., Houston, D. M., & Seddon, P. J. (2007). Elevated hormonal stress response and reduced reproductive output in yellow-eyed penguins exposed to unregulated tourism. General and Comparative Endocrinology, 152, 54e63. Evans, M. R., Roberts, M. L., Buchanan, K. L., & Goldsmith, A. R. (2006). Heritability of corticosterone response and changes in life history traits during selection in the zebra finch. Journal of Evolutionary Biology, 19, 343e352. Fernandez, G., O’Hara, P. D., & Lank, D. B. (2004). Tropical and subtropical Western sandpipers (Calidris mauri) differ in life history strategies. Ornitologia Neotropical, 15, 385e394. Ferns, P. N., & Lang, A. L. (2003). The value of immaculate mates: relationships between plumage quality and breeding success in shelducks. Ethology, 109, 521e532. Fokidis, H. B., & Deviche, P. (2009). Sources of variation in the hypothalamicepituitaryeadrenal axis of urban and desert birds. Integrative and Comparative Biology, 49. E56. Folstad, I., & Carter, A. (1992). Parasites, bright males and the immunocompetence handicap. American Naturalist, 139, 603e622. Ghalambor, C. K., & Martin, T. E. (2001). Fecundity-survival trade-offs and parental risk-taking in birds. Science, 292, 494e497.

147

Goymann, W., Geue, D., Schwabl, I., Flinks, H., Schmidl, D., Schwabl, H., et al. (2006). Testosterone and corticosterone during the breeding cycle of equatorial and European stonechats (Saxicola torquata axillaris and S. t. rubicola). Hormones and Behavior, 50, 779e785. Gratto-Trevor, C. (1992). Semipalmated sandpiper (Calidris pusilla). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/006. Gray, J. M., Yarian, D., & Ramenofsky, M. (1990). Corticosterone, foraging behavior, and metabolism in dark-eyed juncos, Junco hyemalis. General and Comparative Endocrinology, 79, 375e384. Gutierrez, R. J., Franklin, A., & Lahaye, W. (1995). Spotted owl (Strix occidentalis). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/179. Hammond, G. L. (1995). Potential functions of plasma steroid-binding proteins. TEM, 6, 298e304. Hanssen, S. A., Erikstad, K. E., Johnsen, V., & Bustnes, J. O. (2003). Differential investment and costs during avian incubation determined by individual quality: an experimental study of the common eider (Somateria mollissima). Proceedings of the Royal Society of London Series B-Biological Sciences, 270, 531e537. Hasselquist, D. (2007). Comparative immunoecology in birds: hypotheses and tests. Journal of Ornithology, 148, S571eS582. Hatch, S., Robertson, G., & Baird, P. (2009). Black-legged kittiwake (Rissa tridactylaIa). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from The Birds of North America Online. http://bna.birds.cornell.edu/bna/ species/092. Hau, M., Gill, S. A., & Goymann, W. (2008). Tropical field endocrinology: ecology and evolution of testosterone concentrations in male birds. General and Comparative Endocrinology, 157, 241e248. Hayden-Hixon, D. M., & Ferris, C. F. (1991a). Cortisol exerts site-, context- and dose-dependent effects on agonistic responding in hamsters. Journal of Neuroendocrinology, 3, 613e622. Hayden-Hixson, D. M., & Ferris, C. F. (1991b). Steroid-specific regualtion of agonistic responding in the anterior hypothalamus of male hamsters. Physiology and Behavior, 50, 793e799. Hill, G. (1993). House finch (Carpodacus mexicanus). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/046. Jenouvrier, S., Barbraud, C., & Weimerskirch, H. (2006). Sea ice affects the population dynamics of Adelie penguins in Terre Adelie. Polar Biology, 29, 413e423. Johnson, F., & Rashotte, M. E. (2002). Food availability but not cold ambient temperature affects undirected singing in adult male zebra finches. Physiology & Behavior, 76, 9e20. Kaiser, P., & Staheli, P. (2008). Avian cytokines and chemokines. In F. Davison, B. Kaspers, & K. A. Schat (Eds.), Avian Immunology (1 ed.). (pp. 203e222) Amsterdam, The Netherlands: Elsevier. King, J. R., & Murphy, M. E. (1984). Fault bars in the feathers of whitecrowned sparrowsddietary deficiency or stress of captivity and handling. Auk., 101, 168e169. Kitaysky, A., Romano, M., Piatt, J., Wingfield, J., & Kikuchi, M. (2005). The adrenocortical response of tufted puffin chicks to nutritional deficits. Hormones and Behavior, 47, 606e619.

148

Kitaysky, A. S., Kitaiskaia, E. V., Wingfield, J. C., & Piatt, J. F. (2001a). Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 171, 701e709. Kitaysky, A. S., Piatt, J. F., & Wingfield, J. C. (2007). Stress hormones link food availability and population processes in seabirds. Marine Ecology-Progress Series, 352, 245e258. Kitaysky, A. S., Piatt, J. F., Wingfield, J. C., & Romano, M. (1999). The adrenocortical stress-response of black-legged kittiwake chicks in relation to dietary restrictions. Journal of Comparative Physiology B, 169, 303e310. Kitaysky, A. S., Wingfield, J. C., & Piatt, J. F. (2001b). Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behavioral Ecology, 12, 619e625. Knox, A., & Lowther, P. (2000). Common redpoll (Carduelis flammea). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/543. Koch, K. A., Wingfield, J. C., & Buntin, J. D. (2002). Glucocorticoids and parental hyperphagia in ring doves (Streptopelia risoria). Hormones and Behavior, 41, 9e21. Krapu, G. L., Reynolds, R. E., Sargeant, G. A., & Renner, R. W. (2004). Patterns of variation in clutch sizes in a guild of temperate-nesting dabbling ducks. Auk., 121, 695e706. Lakshmi, V., Sakai, R. R., McEwen, B. S., & Monder, C. (1991). Regional distribution of 11-beta-hydroxysteroid dehydrogenase in rat-brain. Endocrinology, 128, 1741e1748. Lancaster, L. T., Hazard, L. C., Clobert, J., & Sinervo, B. R. (2008). Corticosterone manipulation reveals hierarchical organization of multidimensional reproductive tradeoffs in r-strategist and K-strategist females. Journal of Evolutionary Biology, 21, 556e565. Lanctot, R. B., Hatch, S. A., Gill, V. A., & Eens, M. (2003). Are corticosterone levels a good indicator of food availability and reproductive performance in a kittiwake colony? Hormones and Behavior, 43, 489e502. Landys, M. M., Piersma, T., Ramenofsky, M., & Wingfield, J. C. (2004). Role of the low-affinity glucocorticoid receptor in the regulation of behavior and energy metabolism in the migratory red knot Calidris canutus islandica. Physiological and Biochemical Zoology, 77, 658e668. Landys, M. M., Ramenofsky, M., & Wingfield, J. C. (2006). Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. General and Comparative Endocrinology, 148, 132e149. Lee, D. E., Abraham, C. L., Warzybok, P. M., Bradley, R. W., & Sydeman, W. J. (2008). Age-specific survival, breeding success, and recruitment on common murres (Uria aalge) of the California Current System. Auk., 125, 316e325. Lendvai, A. Z., & Chastel, O. (2008). Experimental mate-removal increases the stress response of female house sparrows: the effects of offspring value? Hormones and Behavior, 53, 395e401. Lindstrom, K. M., Hawley, D. M., Davis, A. K., & Wikelski, M. (2005). Stress responses and disease in three wintering house finch (Carpodacus mexicanus) populations along a latitudinal gradient. General and Comparative Endocrinology, 143, 231e239.

Hormones and Reproduction of Vertebrates

Lochmiller, R. L., & Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 87e98. Lohmus, M., Sundstrom, F., & Moore, F. R. (2006). Non-invasive corticosterone treatment changes foraging intensity in red-eyed vireos Vireo olivaceus. Journal of Avian Biology, 37, 523e526. Love, O. P., Breuner, C. W., Vezina, F., & Williams, T. D. (2004). Mediation of corticosterone-induced reproductive conflict. Hormones and Behavior, 46, 59e65. Love, O. P., & Williams, T. D. (2008). The adaptive value of stressinduced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness. American Naturalist, 172, E135eE149. Lynn, S. E., & Porter, A. J. (2008). Trapping initiates stress response in breeding and non-breeding house sparrows Passer domesticus: implications for using unmonitored traps in field studies. Journal of Avian Biology, 39, 87e94. Lynn, S. E., Breuner, C. W., & Wingfield, J. C. (2003). The effects of short-term fasting on activity, corticosterone, and corticosteronebinding globulin in a migratory songbird, Gambel’s white-crowned sparrow (Zonotrichia leucophrys gambelii). Hormones and Behavior, 43, 150e157. Lyon, B., & Montgomerie, R. (1995). Snow bunting (Plectrophenax nivalis). In A. Poole (Ed.), The Birds of North America Online, Ithaca. Retrieved from the Birds of North America Online: http://bna.birds. cornell.edu/bna/species/198. Malisch, J. L., & Breuner, C. (2010). Steroid binding proteins and free steroids in birds. Molecular and Cellular Endocrinology, 316, 42e52. Marti, C., Poole, A., & Bevier, L. (2005). Barn owl (Tyto alba). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/001. Martin, L. B. (2009). Stress and immunity in wild vertebrates: timing is everything. General and Comparative Endocrinology, 163, 70e76. Martin, L. B., Gilliam, J., Han, P., Lee, K., & Wikelski, M. (2005). Corticosterone suppresses cutaneous immune function in temperate but not tropical house sparrows, Passer domesticus. General and Comparative Endocrinology, 140, 126e135. Martin, L. B., Weil, Z. M., & Nelson, R. J. (2007). Immune defense and reproductive pace of life in Peromyscus mice. Ecology, 88, 2516e2528. Martin, T. E. (1995). Avian life-history evolution in relation to nest sites, nest predation, and food. Ecological Monographs, 65, 101e127. Martin, T. E. (2002). A new view of avian life-history evolution tested on an incubation paradox. Proceedings of the Royal Society of London Series B-Biological Sciences, 269, 309e316. Martin, T. E. (2004). Avian life-history evolution has an eminent past: does it have a bright future? Auk., 121, 289e301. Martin, T. E., & Clobert, J. (1996). Nest predation and avian life-history evolution in Europe versus North America: a possible role of humans? American Naturalist, 147, 1028e1046. McCallum, D., Grundel, R., & Dahlsten, D. (1999). Mountain chickadee (Poecile gambeli). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/ species/453. McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43, 2e15.

Chapter | 5

Stress and Reproduction in Birds

Meddle, S. L., Owen-Ashley, N. T., Richardson, M. I., & Wingfield, J. C. (2003). Modulation of the hypothalamicepituitaryeadrenal axis of an Arctic-breeding polygynandrous songbird, the Smith’s longspur, Calcarius pictus. Proceedings of the Royal Society of London Series B-Biological Sciences, 270, 1849e1856. Meddle, S. L., Romero, L. M., Astheimer, L. B., Buttemer, W. A., Moore, I. T., & Wingfield, J. C. (2002). Steroid hormone interrelationships with territorial aggression in an arctic-breeding songbird, Gambel’s white-crowned sparrow, Zonotrichia leucophrys gambelii. Hormones and Behavior, 42, 212e221. Moe, B., Angelier, F., Bech, C., & Chastel, O. (2007). Is basal metabolic rate influenced by age in a long-lived seabird, the snow petrel? Journal of Experimental Biology, 210, 3407e3414. Muller, C., Jenni-Eiermann, S., Blondel, J., Perret, P., Caro, S. P., Lambrechts, M. M., et al. (2007). Circulating corticosterone levels in breeding blue tits Parus caeruleus differ between island and mainland populations and between habitats. General and Comparative Endocrinology, 154, 128e136. Mumme, R. L., Schoech, S. J., Woolfenden, G. W., & Fitzpatrick, J. W. (2000). Life and death in the fast lane: demographic consequences of road mortality in the Florida scrub-jay. Conservation Biology, 14, 501e512. Munck, A., Guyre, P. M., & Holbrook, N. J. (1984). Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocrine Reviews, 5, 25e44. Murphy, M. E., King, J. R., & Lu, J. (1988). Malnutrition during the postnuptial molt of white-crowned sparrowsdfeather growth and quality. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 66, 1403e1413. Naugler, C. (1993). American tree sparrow (Spizella arborea). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/037. Nelson, J., (2006). Pelicans, Cormorants, and Their RelativesdThe Pelecaniformes. Oxford. Nevoux, M., Barbraud, J. C., & Barbraud, C. (2008). Nonlinear impact of climate on survival in a migratory white stork population. Journal of Animal Ecology, 77, 1143e1152. Nevoux, M., Weimerskirch, H., & Barbraud, C. (2007). Environmental variation and experience-related differences in the demography of the long-lived black-browed albatross. Journal of Animal Ecology, 76, 159e167. Newman, A. E. M., & Soma, K. K. (2009). Corticosterone and dehydroepiandrosterone in songbird plasma and brain: effects of season and acute stress. European Journal of Neuroscience, 29, 1905e1914. Nolan, J., V., Ketterson, E., Cristol, D., Rogers, C., Clotfelter, E., et al. (2002). Dark-eyed Junco (Junco hyemalis). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http:// bna.birds.cornell.edu/bna/species/716. Nowicki, S., Searcy, W. A., & Peters, S. (2002). Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. Journal of Comparative Physiology a-Neuroethology Sensory Neural and Behavioral Physiology, 188, 1003e1014. O’Reilly, K. M., & Wingfield, J. C. (2001). Ecological factors underlying the adrenocortical response to capture stress in arctic-breeding shorebirds. General and Comparative Endocrinology, 124, 1e11.

149

Owen-Ashley, N. T., Turner, M., Hahn, T. P., & Wingfield, J. C. (2006). Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii). Hormones and Behavior, 49, 15e29. Peach, W. J., Crick, H. Q. P., & Marchant, J. H. (1995). The demography of the decline in the British willow warbler population. Journal of Applied Statistics, 22, 905e922. Pemberton, P. A., Stein, P. E., Pepys, M. B., Potter, J. M., & Carrell, R. W. (1988). Hormone binding globulins undergo serpin conformational change in inflammation. Nature, 336, 257e258. Pereyra, M. E., & Wingfield, J. C. (2003). Changes in plasma corticosterone and adrenocortical response to stress during the breeding cycle in high altitude flycatchers. General and Comparative Endocrinology, 130, 222e231. Pierotti, R., Herring gull (Larus argentatus). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology, Good, TP. Retrieved from the Birds of North America Online: http://bna.birds.cornell.edu/bna/species/124. Plaschke, K., Muller, D., & Hoyer, S. (1996). Effect of adrenalectomy and corticosterone substitution on glucose and glycogen metabolism in rat brain. Journal of Neural Transmission, 103, 89e100. Pravosudov, V. V., Kitaysky, A. S., Wingfield, J. C., & Clayton, N. S. (2001). Long-term unpredictable foraging conditions and physiological stress response in mountain chickadees (Poecile gambeli). General and Comparative Endocrinology, 123, 324e331. Proudfoot, G., Dawn, A., Johnson, S., & Johnson, S. (2000). Cactus wren (Campylorhynchus brunneicapillus). In A. Poole (Ed.), The Birds of North America, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/ bna/species/558. Raberg, L., Grahn, M., Hasselquist, D., & Svensson, E. (1998). On the adaptive significance of stress-induced immunosuppression. Proceedings of the Royal Society of London Series B-Biological Sciences, 265, 1637e1641. Ratz, H., Darby, J. T., Edge, K. A., & Thompson, C. (2004). Survival and breeding of yellow-eyed penguins (Megadyptes antipodes), at two locations on Otago Peninsula, South Island, New Zealand, 1991-96. New Zealand Journal of Zoology, 31, 133e147. Rice, S. M., Collazo, J. A., Alldredge, M. W., Harrington, B. A., & Lewis, A. R. (2007). Local annual survival and seasonal residency rates of semipalmated sandpipers (Calidris pusilla) in Puerto Rico. Auk., 124, 1397e1406. Rich, E. L., & Romero, L. M. (2005). Exposure to chronic stress downregulates corticosterone responses to acute stressors. American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 288, R1628eR1636. Ricklefs, R. E., & Wikelski, M. (2002). The physiology/life-history nexus. Trends in Ecology & Evolution, 17, 462e468. Roberts, M. L., Buchanan, K. L., Hasselquist, D., Bennett, A. T. D., & Evans, M. R. (2007a). Physiological, morphological and behavioural effects of selecting zebra finches for divergent levels of corticosterone. Journal of Experimental Biology, 210, 4368e4378. Roberts, M. L., Buchanan, K. L., Hasselquist, D., & Evans, M. R. (2007b). Effects of testosterone and corticosterone on immunocompetence in the zebra finch. Hormones and Behavior, 51, 126e134. Romero, L. M. (2002). Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. General and Comparative Endocrinology, 128, 1e24.

150

Romero, L. M. (2004). Physiological stress in ecology: lessons from biomedical research. Trends in Ecology & Evolution, 19, 249e255. Romero, L. M., Cyr, N. E., & Romero, R. C. (2006). Corticosterone responses change seasonally in free-living house sparrows (Passer domesticus). General and Comparative Endocrinology, 149, 58e65. Romero, L. M., Reed, J. M., & Wingfield, J. C. (2000). Effects of weather on corticosterone responses in wild free-living passerine birds. General and Comparative Endocrinology, 118, 113e122. Romero, L. M., Strochlic, D., & Wingfield, J. C. (2005). Corticosterone inhibits feather growth: potential mechanism explaining seasonal down regulation of corticosterone during molt. Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology, 142, 65e73. Roulin, A., Almasi, B., Rossi-Pedruzzi, A., Ducrest, A. L., Wakamatsu, K., Miksik, I., et al. (2008). Corticosterone mediates the condition-dependent component of melanin-based coloration. Animal Behaviour, 75, 1351e1358. Rubenstein, D. R., Parlow, A. F., Hutch, C. R., & Martin, L. B. (2008). Environmental and hormonal correlates of immune activity in a cooperatively breeding tropical bird. General and Comparative Endocrinology, 159, 10e15. Saether, B. E. (1989). Survival rates in relation to body-weight in European birds. Ornis Scandinavica, 20, 13e21. Saino, N., Incagli, M., Martinelli, R., & Moller, A. P. (2002). Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation. Behavioral Ecology, 13, 169e174. Saino, N., Romano, M., Ferrari, R. P., Martinelli, R., & Moller, A. P. (2005). Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. Journal of Experimental Zoology Part a-Comparative Experimental Biology, 303A, 998e1006. Saldanha, C. J., Schlinger, B. A., & Clayton, N. S. (2000). Rapid effects of corticosterone on cache recovery in mountain chickadees (Parus gambeli). Hormones and Behavior, 37, 109e115. Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21, 55e89. Sapolsky, R. M., Zolamorgan, S., & Squire, L. R. (1991). Inhibition of glucocorticoid secretion by the hippocampal-formation in the primate. Journal of Neuroscience, 11, 3695e3704. Scheuerlein, A., Van’t Hof, T. J., & Gwinner, E. (2001). Predators as stressors? Physiological and reproductive consequences of predation risk in tropical stonechats (Saxicola torquata axillaris). Proceedings of the Royal Society of London Series B-Biological Sciences, 268, 1575e1582. Schoech, S. J., Mumme, R. L., & Wingfield, J. C. (1997). Corticosterone, reproductive status, and body mass in a cooperative breeder, the Florida scrub-jay (Aphelocoma coerulescens). Physiological Zoology, 70, 68e73. Schreiber, E., Schreiber, R., & Schenk, G. (1996). Red-footed booby (Sula sula). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/241. Seamans, M. E., & Gutierrez, R. J. (2007). Sources of variability in spotted owl population growth rate: testing predictions using longterm mark-recapture data. Oecologia, 152, 57e70.

Hormones and Reproduction of Vertebrates

Shini, S., Kaiser, P., Shini, A., & Bryden, W. L. (2008). Biological response of chickens (Gallus gallus domesticus) induced by corticosterone and a bacterial endotoxin. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology, 149, 324e333. Silverin, B. (1986). Corticosterone-binding proteins and behavioral effects of high plasma levels of corticosterone during the breeding period in the pied flycatcher. General and Comparative Endocrinology, 64(1), 67e74. Silverin, B., & Wingfield, J. C. (1998). Adrenocortical responses to stress in breeding pied flycatchers Ficedula hypoleuca: relation to latitude, sex and mating status. Journal of Avian Biology, 29, 228e234. Silverin, B. (1998). Behavioural and hormonal responses of the pied flycatcher to environmental stressors. Animal Behavior, 55, 1411e1420. Silverin, B., Arvidsson, B., & Wingfield, J. (1997). The adrenocortical responses to stress in breeding willow warblers Phylloscopus trochilus in Sweden: effects of latitude and gender. Functional Ecology, 11, 376e384. Smith, G. T., Wingfield, J. C., & Veit, R. R. (1994). Adrenocortical response to stress in the common diving petrel, Pelecanoides urinatrix. Phys. Zool., 67, 526e537. Spencer, K. A., Buchanan, K. L., Goldsmith, A. R., & Catchpole, C. K. (2004). Developmental stress, social rank and song complexity in the European starling (Sturnus vulgaris). Proceedings of the Royal Society of London Series B-Biological Sciences, 271, S121eS123. Spencer, R. L., Miller, A. H., Moday, H., McEwen, B. S., Blanchard, R. J., Blanchard, D. C., et al. (1996). Chronic social stress produces reductions in available splenic type II corticosteroid receptor binding and plasma corticosteroid binding globulin levels. Psychoneuroendocrinology, 21, 95e109. Stutchbury, B. J. M., & Morton, E. S. (2008). Recent advances in the behavioral ecology of tropical birdsdThe 2005 Margaret Morse Nice Lecture. Wilson Journal of Ornithology, 120, 26e37. Twit, R. (1996). Curve-billed thrasher (Toxostoma curvirostre). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/235. Wada, H., Salvante, K. G., Stables, C., Wagner, E., Williams, T. D., & Breuner, C. W. (2008). Adrenocortical responses in zebra finches (Taeniopygia guttata): individual variation, repeatability, and relationship to phenotypic quality. Hormones and Behavior, 53, 472e480. Walsberg, G. E. (2003). How useful is energy balance as an overall index of stress in animals? Hormones and Bheavior, 43, 16e17. Weimerskirch, H. (1992). Reproductive effort in long-lived birdsdagespecific patterns of condition, reproduction and survival in the wandering albatross. Oikos, 64, 464e473. Weimerskirch, H., Ancel, A., Caloin, M., Zahariev, A., Spagiari, J., Kersten, M., et al. (2003). Foraging efficiency and adjustment of energy expenditure in a pelagic seabird provisioning its chick. Journal of Animal Ecology, 72, 500e508. White, G., & Burnham, K. (1999). Bird Study, 46(suppl), 120. Wiersma, P., Ro, J., & Williams, J. B. (2009). Small organ size contributes to the slow pace of life in tropical birds. Integrative and Comparative Biology, 49, E181. Williams, C. T., Kitaysky, A. S., Kettle, A. B., & Buck, C. L. (2008). Corticosterone levels of tufted puffins vary with breeding stage, body

Chapter | 5

Stress and Reproduction in Birds

condition index, and reproductive performance. General and Comparative Endocrinology, 158, 29e35. Wilson, C. M., & Holberton, R. L. (2004). Individual risk versus immediate reproductive success: a basis for latitudinal differences in the adrenocortical response to stress in Yellow warblers (Dendroica petechia). Auk., 121, 1238e1249. Wilson, W. (1994). Western sandpiper (Calidris mauri). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/species/090. Wingfield, J. C. (1988). Changes in reproductive function of free-living birds in direct response to environmental perturbations. In M. H. Stetson (Ed.), Processing of Environmental Information in Vertebrates (pp. 121e148). Berlin, Germany: Springer-Verlag. Wingfield, J. C., & Silverin, B. (1986). Effects of corticosterone on terrirorial behavior of free-living male song sparrows, Melospiza melodia. Hormones and Behavior, 20, 405e417. Wingfield, J. C., & Sapolsky, R. M. (2003). Reproduction and resistance to stress: when and how. Journal of Neuroendocrinology, 15, 711e724. Wingfield, J. C., Kubokawa, K., Ishida, K., Ishii, S., & Wada, M. (1995). The adrenocortical response to stress in male bush warblers, Cettia diphone: a comparison of breeding populations in Honshu and Hokkaido, Japan. Zoological Science, 12, 615e621. Wingfield, J. C., Maney, D. L., Breuner, C. W., Jacobs, J. D., Lynn, S., Ramenofsky, M., et al. (1998). Ecological bases of hormone-behavior interactions: the “emergency life history stage”. American Zoologist, 38, 191e206.

151

Wingfield, J. C., Moore, M. C., & Farner, D. S. (1983). Endocrine responses to inclement weather in naturally breeding populations of white-crowned sparrows (Zonotrichia leucophrys pugetensis). Auk, 100, 56e62. Wingfield, J. C., Ramos-Fernandez, G., la Mora, A. N. D., & Drummond, H. (1999). The effects of an “El Nino” Southern oscillation event on reproduction in male and female blue-footed boobies, Sula nebouxii. General and Comparative Endocrinology, 114, 163e172. Wingfield, J. C., Suydam, R., & Hunt, K. (1994). Adrenocortical responses to stress in snow buntings (Plectrophenax nivalis) and Lapland longspurs (Calcarius lapponicus) at Barrow, Alaska. Comparative Biochemistry and Physiology, 108, 299e306. Wingfield, J. C., Vleck, C. M., & Moore, M. C. (1992). Seasonal changes of the adrenocortical response to stress in birds of the Sonoran Desert. J. Exp. Zool., 264, 419e428. Woolfenden, G., & Fitzpatrick, J. W. (1996). Florida scrub-jay (Aphelocoma coerulescens). In A. Poole (Ed.), The Birds of North America Online, Vol. Ithaca: Cornell Lab of Ornithology. Retrieved from the Birds of North America Online. http://bna.birds.cornell.edu/bna/ species/228. Yuan, L., Lin, H., Jiang, K. J., Jiao, H. C., & Song, Z. G. (2008). Corticosterone administration and high-energy feed results in enhanced fat accumulation and insulin resistance in broiler chickens. British Poultry Science, 49, 487e495. Zann, R., & Runciman, D. (1994). Survivorship, dispersal, and sex-ratios of zebra finches Taeniopygia guttata in Southeast Australia. Ibis, 136, 136e146.

Chapter 6

Hormonal Regulation of Avian Courtship and Mating Behaviors Lauren V. Riters and Sarah J. Alger University of Wisconsin, Madison, WI, USA

SUMMARY Birds display some of the most elaborate and well-studied courtship and mating behaviors of the animal kingdom. The hormonal regulation of these behaviors has been detailed in multiple avian species. Courtship and mating behaviors are regulated to a large extent by the same hormones; however, the environmental cues that stimulate hormone synthesis and release, and the target brain regions in which they act, differ between males and females and among species. Further, hormones act within partially overlapping neural systems to regulate different components of courtship and mating.

1. INTRODUCTION Birds display remarkable species diversity and sex differences in courtship complexity, mating behaviors, and the neuroendocrine regulation of these behaviors. Courtship displays are typically performed by males and may combine songs, dances, wing and tail movements, plumage coloration displays, and nonvocal sounds (reviewed in Montgomerie & Doucet, 2007). Not every courtship display results in copulation, but most copulations are preceded by a courtship display. Birds are unusual among internally fertilizing vertebrates in that males of most species do not possess intromittent organs and transfer sperm through brief cloacal contact (Montgomerie & Briskie, 2007). Copulation typically involves a male mounting a female by placing his feet on her back, in some cases grasping the feathers at the nape of her neck, while the female lifts her tail, allowing cloacal contact. The entire sequence of copulatory events is typically completed within seconds. Although in some species females also display components of courtship similar to those observed in males (e.g., singing in female songbirds or aspects of courtship in ring doves), female courtship generally is not as elaborate as that displayed by males. It is clear, however, that female mating decisions are powerfully influenced by aspects of Hormones and Reproduction of Vertebrates, Volume 4dBirds Copyright Ó 2011 Elsevier Inc. All rights reserved.

male courtship. Females attend to male displays and use information provided therein to either reject a courting male or to respond by soliciting or accepting copulatory advances from the male. The endocrine basis of female courtship interactions and mating behavior in birds has received much less attention than that devoted to understanding male sexual behaviors, in part because female sexual behaviors are more subtle. Further, females require multiple supplemental cues (e.g., adequate food availability or appropriate temperatures) before engaging in copulatory behavior with a male (Ball & Ketterson, 2008), which adds an intriguing layer of complexity to studies of female sexual behavior. In this chapter, we define courtship behaviors as those occurring between a male and a female at close proximity and that persuade a member of the opposite sex to copulate. We expand this definition to include long-distance vocal signals that in some species are also used to attract members of the opposite sex to engage in copulation. We define mating behavior as copulation or physical contact between a male and a female that functions to bring the gametes together.

2. STEROID HORMONES SYNCHRONIZE COURTSHIP AND MATING BEHAVIORS WITH REPRODUCTIVE PHYSIOLOGY AND ENVIRONMENTAL FACTORS Courtship and mating are initiated in birds when sensory input from environmental and social stimuli trigger changes in activity within specific regions of the brain (Figure 6.1). The specific environmental cues that stimulate courtship and mating differ across avian species, but can include day length, resource availability, and/or the presence of potential mates (Wingfield et al., 1999). These environmental stimuli trigger the release of gonadotropinreleasing hormone (GnRH) from neurosecretory cells of 153

154

FIGURE 6.1 Schematic illustration highlighting interactions among environmental factors, gonadal steroid hormones, and the brain that underlie courtship and mating behaviors. POM, medial preoptic nucleus, a region in which steroid hormones play a central role in male sexual behavior; VMH, ventromedial hypothalamus, a region in which steroid hormones play a central role in female sexual behavior.

the hypothalamus, which stimulates release of the gonadotropins (GTHs)dluteinizing hormone (LH) and follicle stimulating hormone (FSH)dfrom the anterior pituitary gland. Luteinizing hormone and FSH travel through the circulatory system to target tissue in the gonads, where they stimulate gametogenesis and steroid hormone secretion from the gonads (e.g., testosterone (T) production and secretion from testes, and 17b-estradiol (E2) production and secretion from ovaries). Additionally, the recently discovered gonadotropin-inhibiting hormone (GnIH) appears to inhibit gonadal development, steroid hormone release, and reproductive behaviors (Bentley et al., 2006; Tsutsui et al., 2009). Both T and E2 are important, not only for gamete maturation and secondary sex characteristics, but also because they act within the brain to initiate courtship behaviors and mating. Thus, the hypothalamicepituitaryegonadal (HPG) axis plays a major role in coordinating environmental and social conditions with gonadal function and the onset of courtship and mating behaviors.

2.1. Steroid Control of Male Courtship and Mating Behaviors 2.1.1. Environmental and social stimuli influence male testosterone (T) It was recognized at the beginning of the 19th century that seasonally breeding male songbirds sing high rates of courtship song during the breeding season and that the testes are largest at this time (Montagu, 1802).

Hormones and Reproduction of Vertebrates

Subsequently, studies in a wide range of temperate-zone seasonally breeding birds have demonstrated that the gonads regress and recrudesce seasonally in response to changes in the length of the photophase (e.g., Wingfield & Farner, 1993; Dawson, King, Bentley, & Ball, 2001) and that breeding behavior, testis size, and circulating LH or T concentrations change annually in parallel (Beach & Inman, 1965; Adkins & Adler, 1972; Temple, 1974; Haase, Sharp, & Paulke, 1975; Balthazart & Hendrick, 1976; Robinson & Follett, 1982; Ball & Balthazart, 2004). Seasonal changes in T concentrations, courtship, and mating activity are most dramatic in temperate-zone species, but tropical species also show fluctuations in T and mating behaviors that correlate best with seasonal changes in resource availability rather than daylength (Wiley & Goldizen, 2003; Goymann et al., 2004; Day, McBroom, & Schlinger, 2006; Day et al., 2007; Hau, Gill, & Goymann, 2008). In addition to photoperiod, social stimuli influence T concentrations in male birds (Wingfield, Hegner, Dufty, & Ball, 1990). Evidence in multiple species shows that stimulation from receptive females increases testis size and elevates male T or LH concentrations (e.g., ring doves (Streptopelia risoria) (O’Connell, Reboulleau, Feder, & Silver, 1981), Japanese quail (Coturnix japonica) (Delville, Sulon, Hendrick, & Balthazart, 1984), multiple songbirds (e.g., brown-headed cowbirds (Molothrus ater), European starlings (Sturnus vulgaris), and white-crowned sparrows (Zonotrichia leucophrys) (Moore, 1982; Dufty & Wingfield, 1986; Gwinner, Van’t Hof, & Zeman, 2002; Pinxten, De Ridder, & Eens, 2003))). Testosterone release can also be influenced by the quality of social interaction with a female. For example, male ring doves presented with a gonadally intact female respond with higher levels of courtship behavior and T than males presented with an ovariectomized, nonsexually responsive female (O’Connell et al., 1981). Other studies show that the presence of a suitable nest site can influence T release and whether or not a bird engages in courtship activities. For example, providing male European starlings with appropriate nest sites (in this case nest boxes) elevated T concentrations in males housed alone (Gwinner et al., 2002). Further, males that won competitions over nest boxes displayed elevated concentrations of T and LH, and elevated rates of courtship behavior (singing and gathering nest material) compared to males who did not win (Riters et al., 2000; Gwinner et al., 2002). Male starlings that received implants containing T also occupied more nest boxes than controls (H. Gwinner & E. Gwinner, 1994), suggesting that possession of a nest box can enhance T, but also that T can enhance the ability of a male to acquire a nest box. Interestingly, only male starlings with nest boxes responded to the presence of a female with high rates of courtship song (Riters et al.,

Chapter | 6

155

Hormonal Regulation of Avian Courtship and Mating Behaviors

2000). These data indicate that multiple environmental factors, including photoperiod, the presence of a female, and an appropriate nesting territory, influence male reproductive endocrinology, so that a male has high T and is equipped to display courtship behavior when it is most likely to result in successful reproduction.

2.1.2. Hormone manipulations establish a role for testosterone (T) in male courtship and copulation The classic work of Berthold (1849) revealed that castrated male cockerels (Gallus gallus) failed to develop maletypical physical traits, such as a wattle and comb, or maletypical courtship and mating behaviors. These behaviors were rescued in cockerels that were castrated but reimplanted with their own testes or testes from another male. Although T, the steroid hormone responsible for these effects, was not isolated until the 1930s, this study is considered to be the first to demonstrate that a substance secreted from the testis is critical for male-typical sexual behaviors in any species. Subsequently, multiple studies in a variety of avian species have demonstrated that courtship and copulatory behaviors disappear or are substantially reduced after castration and can be restored by T treatment (e.g., Japanese quail (Beach & Inman, 1965; Adkins & Nock, 1976a), ring doves (Adkins-Regan, 1981), and songbird species (Arnold, 1975; Harding, Sheridan, & Walters, 1983; Pinxten, De Ridder, Balthazart, & Eens, 2002)). Further, during the mating season, T implants in gonadally intact males stimulate male courtship and can increase polygyny and extrapair copulations in birds studied in the wild (Wingfield, 1984; De Ridder, Pinxten, & Eens, 2000; Stoehr & Hill, 2000; Peters, 2002). Testosterone additionally appears to play a role in determining the stimuli to which males will respond with an increase in singing behavior. For example, the presence of a female conspecific induces high rates of courtship song production in male starlings with high T concentrations. In contrast, castrated male starlings or males with naturally low T concentrations sing at high rates when in large social flocks, but the presence of a female has no effect on the rate of male song (Riters et al., 2000; Pinxten et al., 2002). In addition to initiating male sexual behaviors, T appears to modify structural aspects of male behaviors observed within sexual and nonsexual social contexts so that they are most attractive to females within a breeding context. Male vocal behavior provides a good example. Some seasonally breeding male songbirds sing year-round, but the structure and function of song change seasonally in association with T concentrations. For example, in starlings and song sparrows (Melospiza melodia), males sing shorter or less stereotyped songs when T is low outside the breeding season but longer or more stereotyped songs when

T is high during the breeding season (Smith, Brenowitz, Beecher, & Wingfield, 1997; Riters et al., 2000). Several studies in a variety of species indicate that females prefer to select as mates males that sing long, stereotyped song (Searcy & Yasukawa, 1996), indicating a role for T in shifting song structure so that it is most attractive within a breeding context. More direct evidence for effects of T on vocal structure is provided by a study in which T treatment of male grey partridges (Perdix perdix) (a non-songbird species) in the winter nonbreeding season caused male call structure to shift from typical winter calls to springbreeding-season-typical calls similar to those used to attract females (Fusani, Beani, & Dessi-Fulgheri, 1994).

2.1.3. Many testosterone (T) effects on male courtship and copulation are mediated by its metabolites Originally it appeared that T was responsible for the activation of male sexual behavior and that estrogens primarily regulated female sexual behavior. However, similar to studies in mammals, in many bird species the effects of T on courtship and mating behaviors can be mimicked by E2 or blocked by inhibiting T conversion into E2 (e.g., Japanese quail (Adkins & Adler, 1972; Watson & Adkins-Regan, 1989c); ring dove (Hutchison, 1970a); zebra finch (Taeniopygia guttata) (Walters & Harding, 1988)). These findings led to the ‘aromatization hypothesis,’ which posits that T is converted in the brain into E2 by the enzyme aromatase (P450aro), which then binds to estrogen receptors (ERs) in the brain to activate male sexual behavior (Steimer & Hutchison, 1980; MacLusky & Naftolin, 1981; Steimer & Hutchison, 1981a; Balthazart & Foidart, 1993). Subsequent studies implicated three main T metabolites in the regulation

Cholesterol P450scc PREG P450c17 DHEA

3β-HSD

P4

P450c17 3β-HSD

AE

P450aro

17β-HSD

5α-DHT

red

5β-DHT

T

P450aro E1

d

-re

5α

17β-HSD

5β-

E2

FIGURE 6.2 Simplified diagram illustrating steroid synthetic pathways. Steroids are in boxes: 5a-DHT, 5a-dihydrotestosterone; 5b-DHT, 5b-dihydrotestosterone; AE, androstenedione; DHEA, dehydroepiandrosterone; E1, estrone; E2, 17b-estradiol; P4, progesterone; PREG, pregnenolone; T, testosterone. Enzymes are in italics: 17b-HSD, 17b-hydroxysteroid dehydrogenase; 3b-HSD, 3b-hydroxysteroid dehydrogenase/isomerase; 5a-red, 5a-reductase; 5b-red, 5b-reductase; P450aro, aromatase; P450c17, cytochrome P450 17a-hydroxylase/C17,20 lyase; P450scc, cytochrome P450 side-chain cleavage.

156

Hormones and Reproduction of Vertebrates

of avian sexual behavior (Figure 6.2). In the avian brain, P450aro transforms T into active estrogen metabolites (E2 or estrone) and 5a-reductase transforms T into the active androgen metabolite 5a-dihydrotestosterone (5a-DHT). Testosterone can also be converted by the enzyme 5breductase into 5b-dihydrotestosterone (5b-DHT), a metabolic pathway possibly serving to inactivate T. Dissociations have been identified in male birds between the effects of androgenic and estrogenic metabolites on different aspects of reproductive behavior (Figure 6.3). Courtship in male ring doves begins with aggressive components (chasing and bowing, which are also observed in the context of intermale aggression), shifting to nest-soliciting behaviors and eventually copulation. In male ring doves, T is released almost immediately in response to the presence of a female (Feder, Storey, Goodwin, Reboulleau, & Silver, 1977). The initial aggressive component of male ring dove courtship behavior is androgen-dependent with both T and 5a-DHT, but not E2, reinstating this aspect of courtship in castrated males (Hutchison, 1970a; Cheng & Lehrman, 1975b; AdkinsRegan, 1981; Hutchison, Steimer, & Duncan, 1981). In

with aggressive or male – male functions selectively directed towards females

Components of male courtship

CX

CX+ T

CX+AE or E2 + CX+ 5α-DHT 5α-DHT

CX+ E2 Aro inhib.

Ring dove Japanese quail Zebra finch Ring dove Japanese quail Zebra finch

FIGURE 6.3 Summary of findings for studies in ring doves (Streptopelia risoria), Japanese quail (Coturnix japonica), and zebra finches (Taeniopygia guttata) showing that androgenic and estrogenic metabolites differentially influence components of male courtship with an aggressive or maleemale function (e.g., hop charges in ring doves, crowing in quail, nonfemale-directed song in zebra finches) and courtship selectively directed towards females (e.g., nest solicitation in ring doves, approach or mounting in quail, female-directed song in zebra finches). Castration (CX) reduces all components of male courtship. Treatments providing aromatizable androgens such as testosterone (T), androstendione (AE), or both androgenic and estrogenic compounds (17b-estradiol þ 5a-dihydrotestosterone (E2 þ 5a-DHT)) restore all components of male courtship. The nonaromatizable androgen 5a-DHT selectively enhances only components of courtship with aggressive or maleemale functions. Estrogens increase only components of courtship directed exclusively towards females. Slash indicates data not found for these manipulations. Horizontal arrows indicate no change. See text for additional details and references.

contrast, nest-soliciting behaviors and copulation are both dependent upon the aromatization of T into E2 (Hutchison, 1970a; Cheng & Lehrman, 1975b; Adkins-Regan, 1981; Fusani, Gahr, & Hutchison, 2001). Studies in Japanese quail also demonstrate differential involvement of androgens and estrogens in the regulation of different components of male courtship and copulation (Figure 6.3). Specifically, E2 treatment restores measures of male sexual interest (e.g., looking at a female and cloacal gland movements) and copulation in castrated male quail. In contrast, T treatment fails to restore either component of sexual behavior in castrated males treated with an aromatase inhibitor (Adkins & Nock, 1976b; Balthazart, Reid, Absil, Foidart and Ball, 1995; Balthazart, Castagna, & Ball, 1997a; Cornil, Holloway, Taziaux, & Balthazart, 2004; Taziaux, Cornil, & Balthazart, 2004). These data indicate that the aromatization of T is critical for the activation of both sexual interest and copulation in male quail. In contrast to E2, 5a-DHT does not stimulate male sexual behavior in quail; however, this metabolite is critical for the activation of other precopulatory displays (strutting and crowing) and cloacal gland development (Adkins, 1977; Schumacher & Balthazart, 1983; Balthazart, Schumacher, & Malacarne, 1984). These observations suggest that E2 is involved in behavior specifically directed toward females, whereas 5a-reduced metabolites influence aspects of courtship also used during maleemale interactions. The 5b-reduction of androgens is considered a major T inactivation pathway in the avian brain (Hutchison & Steimer, 1984). Consistent with this idea, 5b-reduced metabolites of T are generally ineffective at stimulating courtship or copulation (Japanese quail (Adkins, 1977), ring doves (Steimer & Hutchison, 1981b)). Studies in male ring doves also show that 5b-reductase in the preoptic area (POA) (a brain region implicated in male sexual behavior, reviewed in Section 5.1.1) is lower in sexually active males but increases after castration. Testosterone additionally becomes less effective at stimulating vocal behavior in male ring doves as preoptic 5b-reductase activity rises (Hutchison & Steimer, 1981; 1984). Although the idea that the 5b-reduction of T serves as a T inactivation shunt is generally accepted, this view may be overly simplistic. For example, treating male quail with 5b-DHT in addition to subthreshold doses of T stimulates copulation in quail (Deviche, Bottoni, & Balthazart, 1982), and 5b-DHT in young chicks activates sexual behavior directed towards a human hand but not towards conspecifics (Balthazart, Malacarne, & Deviche, 1981). Together, the evidence gathered in ring doves and Japanese quail suggests that androgens may be critical for the regulation of components of courtship that also play a role in maleemale interactions (e.g., crowing in quail, chasing in doves) but that estrogens may underlie components of courtship that are highly sexually motivated and

Chapter | 6

Hormonal Regulation of Avian Courtship and Mating Behaviors

selectively directed towards the female (e.g., looking at and remaining near a female in quail, nest solicitation in ring doves) (Figure 6.3). This observation may provide insight into why different components of male courtship displays are controlled by different hormones. Possibly, ancestral behaviors that were used for purposes unrelated to courtship were stimulated by different hormones. As they evolved, these behaviors may have been co-opted and integrated into courtship displays but have maintained their original hormonal control mechanisms (Fusani, 2008). Similar to ring doves and Japanese quail, studies in songbirds (zebra finches and red-winged blackbirds (Agelaius phoenecius)) also indicate that full stimulation of male courtship song and associated behaviors requires aromatizable androgens (Harding et al., 1983; Harding, Walters, Collado, & Sheridan, 1988; Walters & Harding, 1988) (see Figure 6.3). Castrated male zebra finches were administered treatments containing nonaromatizable androgens, aromatizable androgens, or E2. Only treatments that included both a-androgenic and estrogenic compounds (i.e., T, androstenedione, or E2 plus 5a-DHT) (see Figure 6.2 for metabolic pathways) reinstated courtship displays, with androstenedione (an aromatizable androgen) raising courtship behavior to levels above those observed in gonadally intact males (Harding, Sheridan, & Walters, 1983). An additional study demonstrated a reduction in male courtship and copulation in males treated with androstenedione plus an aromatase inhibitor. This effect was reversed with the addition of E2, suggesting a role for the aromatization of androgens in male sexual behavior in zebra finches (Walters & Harding, 1988). Song in zebra finches has functions other than mate attraction. Interestingly, song that is not directed towards females does not appear to be as dependent upon estrogens (Walters, Collado, & Harding, 1991), a finding consistent with studies in ring doves and quail showing that selectively female-directed components of courtship are dependent upon estrogenic metabolites of T (Figure 6.3) but that behaviors that are not specifically female-directed are less E2-dependent.

2.2. Steroid Control of Female Courtship and Mating Behaviors 2.2.1. Estrogens and female sexual behavior In temperate-zone seasonally breeding birds, females display the highest levels of sexual receptivity in response to male courtship during the breeding season, when circulating LH and E2 are high (e.g., Dawson, 1983; Hegner & Wingfield, 1986). Ovariectomy reduces receptivity in female birds (e.g., Japanese quail (Adkins & Adler, 1972; Adkins & Nock, 1976a), ring dove (Cheng, 1973a; Cheng & Lehrman, 1975a)), whereas treatment with E2 can restore

157

female sexual behaviors, such as nest-coos in ring doves and receptive crouching in quail (e.g., Japanese quail (Adkins & Nock, 1976a), ring dove (Cheng, 1973a)). Antiestrogens suppress receptivity in female quail (Adkins & Nock, 1976b; Delville & Balthazart, 1987) and copulation solicitation displays in female canaries (Serinus canaria) hearing male courtship song (Leboucher, Beguin, Mauget, & Kreutzer, 1998). 17b-estradiol implants are routinely used to facilitate female courtship solicitation displays in a variety of songbird species (e.g., song sparrows (Searcy & Marler, 1981), white-crowned sparrows (Moore, 1982; 1983), and red-winged blackbirds (Searcy & Capp, 1997)) (reviewed in Searcy, 1992). 17b-estradiol from the ovaries appears to act directly on receptors in the brain, and its effects on courtship and mating do not depend upon local enzymatic conversion of T within target brain regions, unlike the case for males. However, there is some evidence for the involvement of estrogens produced in the brain in the reproductive behaviors of female ring doves (discussed in more detail in Section 4.2) (Belle, Sharp, & Lea, 2005).

2.2.2. Progestogens and female sexual behavior Some evidence also implicates progesterone (P4) in aspects of courtship in female birds. As with E2, serum P4 concentrations rise during female courtship behaviors, peaking in some species just prior to egg laying (e.g., canaries (Sockman & Schwabl, 1999)). Progesterone treatment alone in ovariectomized ring doves does not restore sexual behavior (Cheng & Silver, 1975). However, nest-cooing and nest-oriented behaviors are best restored in ovariectomized ring doves through synergistic effects of estrogens and progestogens (Cheng & Silver, 1975). In contrast, treatment with E2 alone is sufficient to activate female sexual behaviors in ovariectomized quail, and the addition of P4 has little or no additive effect (Noble, 1972; Delville & Balthazart, 1987). Although this suggests that progestogens do not play a strong stimulatory role in female sexual behavior in this species, it is possible that extragonadal sources of P4 (e.g., P4 from the adrenals or locally synthesized in neural tissue) do synergistically support female sexual behaviors, as suggested by data in female rats (Tennent, Smith, & Davidson, 1980; Frye, Bayon, Pursnan, & Purdy, 1998). Other data demonstrate that P4 can inhibit female courtship activity in canaries (Leboucher, Beguin, Lacroix, & Kreutzer, 2000) and may play a role in the transition from courtship to incubation behavior in turkey hens (Meleagris gallopavo) (El Halawani, Silsby, Behnke, & Fehrer, 1986). This inhibitory role for P4 in female receptive behavior has also been observed in lizards (Godwin, Hartman, Grammer, & Crews, 1996) and in E2-primed rats, in which P4 initially (i.e., within four hours) facilitates lordosis, but later (i.e., one to two days

158

after the initial P4 treatment) inhibits female receptivity (Blaustein & Wade, 1977a; 1977b; Gonzalez-Mariscal, Melo, & Beyer, 1993). Progesterone may affect female behavior by direct action on receptors. Progesterone can also be metabolized into other progestins, which in mammals influence GTH release and sexual receptivity in females (Zanisi, Messi, & Martini, 1984; Karavolas & Hodges, 2007). In birds, a role for P4 metabolites in female courtship and sexual behavior has not been explored.

2.2.3. Environmental and social stimuli influence female 17b-estradiol (E2) concentrations and behavior The presence of males or playback of male vocalizations can robustly stimulate female ovarian development, E2 release, nest building, egg laying, and sexual responsivity (e.g., budgerigars (Melopsittacus undulatus) (Brockway, 1965); song sparrows, canaries, and willow tits (Parus montanus) (Kroodsma, 1976; Silverin & Westin, 1995; Bentley, Wingfield, Morton, & Ball, 2000)). 17b-estradiol stimulates sexual interest and also appears to reduce fear responses inherent in social encounters. For example, female ring doves and Japanese quail with low concentrations of E2 actively avoid males (Adkins & Nock, 1976a; 1976b; reviewed in Cheng, 2008). Indeed a reduction in avoidance is used in some studies of female Japanese quail as an index of sexual responsivity (e.g., Adkins & Nock, 1976b). Further, female songbirds captured in the wild often do not display sexual behavior in captivity, presumably in part due to stress and a lack of supplemental cues. 17b-estradiol treatment of wild-caught, captive female songbirds stimulates responses to male song (Searcy & Marler, 1981; Moore, 1982; Searcy, 1992; Searcy & Capp, 1997), suggesting a role for E2 in shifting female social responses such that they are attracted to stimuli that they initially find stressful, or that they ignore or avoid. Classic research by Hinde and collaborators in female canaries also demonstrates that E2 release and ovarian development are coordinated with social and environmental stimuli required for successful reproduction (i.e., the presence of a courting male and an appropriate nest site). Playing male song to female canaries stimulated follicle development, and exposure to an appropriately long daylength plus male song also induced release of E2, resulting in nest-building behavior (Hinde & Steel, 1978). Male repertoire size differentially influenced female reproductive behavior, with playback of larger male song repertoires stimulating nest building and egg laying more than smaller repertoires (Kroodsma, 1976). In female ring doves, E2 stimulates sexual behaviors, nest-building activity, receptivity, and ovarian development in response to male courtship behavior (Cheng,

Hormones and Reproduction of Vertebrates

1973a; 1973b; 1974; reviewed in Cheng, 2008). Male vocalizations and the female’s own cooing vocalizations during courtship also stimulate release of LH (Cheng, Peng, & Johnson, 1998). Interestingly, female ring doves only undergo follicular maturation if the male is directing courtship at them, not under conditions in which they are able to view male courtship behaviors that appear to be directed towards another females (Friedman, 1977). Several studies indicate that the female’s own vocalizations are required for final follicle maturation (Cohen & Cheng, 1981; Cheng, 1986; Cheng, Desiderio, Havens, & Johnson, 1988). For example, female ovarian development is blocked by muting a female but can be restored through playbacks of the female’s own nest-coo (Cheng, 1986). In deafened females, proprioceptive feedback associated with performance of nest-coo behavior can also stimulate a moderate level of ovarian growth (Cheng et al., 1988). Prior to these studies, mating behavior was thought to be coordinated by the responses of one individual to another. The finding that females could stimulate themselves through their own vocal behavior caused a dramatic shift in the understanding of the coordination of courtship.

3. STEROID HORMONES ACT WITHIN DISTINCT BRAIN REGIONS TO INFLUENCE COURTSHIP AND MATING 3.1. Brain Regions Involved in Social and Sexual Behavior In both birds and mammals, a group of reciprocally connected, steroid-sensitive brain regions, sometimes referred to as the ‘social behavior network,’ has been implicated in multiple social behaviors ranging from aggression to courtship and mating behavior in both males and females (Newman, 1999; Goodson, 2005). This network includes the medial preoptic nucleus (often referred to as ‘POM’ in birds), extended medial amygdala [comprised of the amygdala (nucleus taenia of the amygdala in birds (TnA)), and medial bed nucleus of the stria terminalis (BSTm)], lateral septum (LS), the ventromedial hypothalamus (VMH), ventral tegmental area (VTA), periaqueductal (central) gray (PAG), and the anterior hypothalamus (AH). Newman (1999) proposed that variation in the pattern of activity within this network, rather than activity within any one region alone, controls all social behavior, including courtship and copulatory behaviors (Figure 6.4(a)). Each of these regions contains steroid receptors and participates in a variety of social behaviors in multiple vertebrate species, suggesting that a core group of brain structures underlies steroid-dependent social behaviors across vertebrate taxa (Goodson, 2005).

Chapter | 6

Hormonal Regulation of Avian Courtship and Mating Behaviors

(a)

LS

BSTm TnA

POM PAG VTA

AH

VMH

Androgen receptors Estrogen receptors

(b) HVC

RA

LMAN

Area X

DLM POM

nXIIts Ram/rVRG

PAG

DM

159

pathways that play roles in different aspects of song behavior. A forebrain pathway, which includes the HVC, area X, the medial nucleus of the dorsal lateral thalamus (DLM), and lateral portions of the magnocellular nucleus of the anterior nidopallium (LMAN), is involved in song learning (e.g., Bottjer, Miesner, & Arnold, 1984; Sohrabji, E. Nordeen, & K. Nordeen, 1990; Bottjer & Johnson, 1997; Doupe & Solis, 1997), perception (e.g., Brenowitz, 1991; Burt, Lent, Beecher, & Brenowitz, 2000; Riters & Teague, 2003), and the context in which a bird sings (Jarvis, Scharff, Grossman, Ramos, & Nottebohm, 1998; Hessler & Doupe, 1999). A second pathway includes HVC, the robust nucleus of the arcopallium (RA), and descending projections to the tracheosyringeal portion of the hypoglossal nucleus (nXIIts) and the dorsomedial nucleus of the nucleus intercollicularis (DM). This pathway plays a primary role in motor aspects of song production (e.g., Nottebohm, Stokes, & Leonard, 1976; Margoliash, 1997). Acoustic processing, discrimination, and perception are also performed by a separate set of steroid-sensitive auditory forebrain regions, including the caudomedial nidopallium (NCM) and the mesopallium caudomediale (CMM) (Gentner, 2004; Theunissen et al., 2004).

VTA

FIGURE 6.4 Illustration of key neural circuits implicated in aspects of male and female courtship and mating behaviors in birds. Lateral views of (a) reciprocally connected brain regions implicated in social (including sexual) behaviors common to all avian species investigated and (b) regions comprising the ‘song-control system,’ a group of brain regions unique to songbirds. Arrows represent neuroanatomical connections identified in tract-tracing studies. Open arrows identify a forebrain pathway involved in song learning. Gray arrows indicate a caudal pathway involved in song production. Small arrows highlight routes by which brain regions involved in social behavior and motivation access the song-control system. Areas containing androgen receptors are shaded with gray. Areas containing estrogen receptors contain stripes. See text for discussion of sex differences in these circuits, and references. AH, anterior hypothalamus; BSTm, medial bed nucleus of the stria terminalis; DLM, medial nucleus of the dorsal lateral thalamus; DM, dorsomedial nucleus of the nucleus intercollicularis; HVC, higher vocal center; LMAN, lateral portions of the magnocellular nucleus of the anterior nidopallium; nXIIts, tracheosyringeal portion of the hypoglossal nucleus; LS, lateral septum; PAG, periaqueductal (central) gray; POM, medial preoptic nucleus; RA, robust nucleus of the arcopallium; RAm/rVRG, nucleus retroambigualis/rostral ventral respiratory group; TnA, nucleus taenia of the amygdala; VMH, ventromedial hypothalamus; VTA, ventral tegmental area.

3.2. Brain Regions Involved in Song Control and Auditory Processing In songbirds, song production plays a critical role in bringing together males and females for copulation. Songbirds are unique in that they possess a specialized group of interconnected brain nuclei devoted exclusively to song, known as the song control system (Figure 6.4(b)). Briefly, this system consists of at least two distinct neural

3.3. Steroid Hormone Receptor Distribution in Males In male birds and other vertebrates, both androgens and estrogens participate in the regulation of courtship and mating behaviors by acting at receptors located within specific brain regions. The distribution of androgen receptors (ARs) and estrogen receptors (ERs) can serve as a guide to the specific regions in which steroid hormones act to influence these behaviors.

3.3.1. Androgen receptors (ARs) A single AR type has been identified in birds. The distribution of ARs has been examined in multiple songbird and non-songbird species. In general, the AR distribution across avian species is similar to that observed in other vertebrates (Morrell, Kelley, & Pfaff, 1975; Stumpf & Sar, 1978; Ball, 1990; Metzdorf, Gahr, & Fusani, 1999; Ball & Balthazart, 2002). In birds, ARs are found at high densities within each of the regions considered to be part of the social behavior network (Figure 6.4(a)) and, additionally, the hippocampus (HP), nucleus intercollicularis (ICo) (a region implicated in vocal production across avian species), and hypothalamus, including the tuberal complex (Tu) and infundibular area (regions implicated in GnRH release) (Konishi, Foster, & Follett, 1987). Androgen receptors have also been identified in regions involved in general arousal, attention, and motivation, including the locus coeruleus, the substantia nigra, and the VTA (Arnold, Nottebohm, & Pfaff, 1976; Barfield,

160

Ronay, & Pfaff, 1978; Harding, Walters, & Parsons, 1984; Balthazart, Foidart, Wilson, & Ball, 1992; Smith, Brenowitz, & Prins, 1996; Gahr & Metzdorf, 1997; Balthazart, Foidart, Houbart, Prins, & Ball, 1998; Metzdorf, Gahr, & Fusani, 1999; Soma, Hartman, Wingfield, & Brenowitz, 1999; Gahr, 2000; Belle & Lea, 2001; Maney, Bernard, & Ball, 2001; Matsunaga & Okanoya, 2008). These regions may regulate male arousal, attention, and motivated responses to females during courtship and copulation. In songbirds, the song control system and regions implicated in vocal perception also contain ARs (Figure 6.4 (b)). Androgen receptors are specifically found within the HVC, RA, LMAN, medial portion of the MAN (mMAN), nucleus interfacialis (Nif), premotor neurons, vocal respiratory regions, and nXIIts (Arnold, Nottebohm, & Pfaff, 1976; Harding, Walters, & Parsons, 1984; Balthazart et al., 1992a; Smith, Brenowitz, & Prins, 1996; Gahr & Metzdorf, 1997; Gahr & Wild, 1997; Bernard, Bentley, Balthazart, Turek, & Ball, 1999; Metzdorf, Gahr, & Fusani, 1999; Soma, Hartman, Wingfield, & Brenowitz, 1999; Gahr, 2000). Anna’s hummingbird (Calypte anna), a species that learns vocal behavior and has neural circuitry presumably analogous to the oscine song-control system, has immunoreactive ARs in the nXIIts and nucleus retroambigualis (a region implicated in the coordination of vocal and respiratory muscles (Wild, Kubke, & Mooney, 2009)) and areas equivalent to the HVC and LMAN (Gahr, 2000). Recent data suggest that the vocal-learning budgerigar also possesses AR expression in the forebrain and nXIIts (Matsunaga & Okanoya, 2008). The presence of ARs in discrete forebrain regions devoted to vocal production distinguishes songbirds and other vocal learners from all other vertebrates.

3.3.2. Estrogen receptors (ERs) Only one ER type was known until Kuiper reported a second type in rats in 1996 (Kuiper, Enmark, Pelto-Huikko, Nilsson, & Gustafsson, 1996). This second ER type was named ERb, and the first discovered form was renamed ERa. Estrogen receptor-a and ERb display distinct distribution patterns within the brain, suggesting that they may play distinct roles in physiology and behavior (Kuiper, Shughrue, Merchenthaler, & Gustafsson, 1998; Ball, Bernard, Foidart, Lakaye, & Balthazart, 1999). Studies of ERa distributions have included several avian species; ERb distributions in the brain have not been mapped as extensively.

Hormones and Reproduction of Vertebrates

regions, including the Tu and infundibular area (MartinezVargas, Stumpf, & Sar, 1976; Balthazart, Gahr, & Surlemont, 1989; Watson & Adkins-Regan, 1989b; Gahr, Guttinger, & Kroodsma, 1993; Jacobs, Arnold, & Campagnoni, 1996; Metzdorf, Gahr, & Fusani, 1999; Griffin, Flouriot, Sharp, Greene, & Gannon, 2001; Maney, Bernard, & Ball, 2001; Halldin, Axelsson, Holmgren, & Brunstrom, 2006) (Figure 6.4(a)). The microdistribution of ERa differs among families and species (Gahr, Guttinger, & Kroodsma, 1993). For example, Japanese quail have more ER in the ventrolateral POA than do domestic chickens (of the same order) and other avian species (Gahr & Balaban, 1996). Further, in addition to the regions listed above, in songbirds ERa is found within the NCM, HVC (Figure 6.4(b)), dorsal surround of the RA, and in portions of the rostral forebrain, all areas that so far have not been found to contain ERa in nonpasserines or passerine suboscines (K. Nordeen, E. Nordeen, & Arnold, 1987; Brenowitz & Arnold, 1989; Gahr, Guttinger, & Kroodsma, 1993; Jacobs, Arnold, & Campagnoni, 1996; Gahr & Metzdorf, 1997; Metzdorf, Gahr, & Fusani, 1999; Fusani, Van’t Hof, Hutchison, & Gahr, 2000). 3.3.2.2. Estrogen receptor-b (ERb) Estrogen receptor-b mRNA is present in several brain regions involved in sexual and social behavior (the POM, BSTm, TnA, LS, and ICo), the Tu, and parts of the thalamus, similar to the distribution of ERa (Foidart, Lakaye, Grisar, Ball, & Balthazart, 1999; Halldin et al., 2006) (Figure 6.4(a)). Unlike ERa, ERb mRNA in starlings was not expressed at detectable levels in the HVC and was expressed at low levels in the NCM in a pattern distinct from that of ERa (Bernard et al., 1999). It has been proposed based in part on the results of knockout studies in mice that ERa may play a more crucial role in reproductive function than ERb (Wersinger et al., 1997; Krege et al., 1998; Kuiper et al., 1998). However, given the identification in birds of ERb within multiple regions with known reproductive functions, additional research is required to determine the extent to which this hypothesis applies to birds (Ball et al., 1999).

3.4. Steroid Hormone Receptor Distribution in Females

3.3.2.1. Estrogen receptor-a (ERa)

3.4.1. Androgen receptors (ARs) and estrogen receptors (ERs)

The distribution of ERa in all avian species studied to date is fairly similar to that of AR. In both songbirds and nonsongbirds, ERa is found within each of the nuclei considered to be part of the social behavior network, and additionally in the HP, ICo, locus coeruleus, and hypothalamic

In general, the brain regions in which ARs and ERs are found during development and adulthood appear to be remarkably similar in male and female birds (Figure 6.4) (Kawashima, Kamiyoshi, & Tanaka, 1987; Balthazart et al., 1989; Gahr & Metzdorf, 1997; Griffin et al., 2001; Halldin

Chapter | 6

Hormonal Regulation of Avian Courtship and Mating Behaviors

et al., 2006). However, sex differences have been found for measures of receptor numbers or density in several brain areas. For example, numbers of cells labeled for ERa in the POM, LS, hypothalamic regions, and Tu, among others, in Japanese quail were lower in females than males (Balthazart et al., 1989). Further, in zebra finches, measures of AR are lower in females in the HVC and MAN compared to males (Gahr & Metzdorf, 1997; K. Nordeen, E. Nordeen, & Arnold, 1986). Interestingly, in zebra finches and Anna’s hummingbirds (both vocal learners in which males sing but females never sing), steroid receptors are notably lower in the forebrain vocal control areas of the female brain (Nordeen et al., 1986; Gahr, 2000).

3.4.2. Progesterone (P4) receptors (PRs) In addition to androgens and estrogens, in females P4 may participate in components of courtship behavior in some avian species (reviewed in Section 2.2.2). Progesterone receptor (PR) distributions have been examined in domestic hens and female ring doves (Sterling et al., 1987; Askew, Georgiou, Sharp, & Lea, 1997; Belle, Sharp, & Lea, 2005). In adult hens, PRs are found in several preopticehypothalamic areas (including the VMH, POM, and the Tu/infundibular area), the BSTm, the medial septum, and the dorsomedial thalamus (Sterling et al., 1987). Progesterone receptors have also been reported in preoptic and hypothalamic regions in female ring doves (Askew et al., 1997).

3.5. Receptor Dynamics Relate to Breeding Behaviors The sensitivity of tissue to a particular hormone depends upon receptor numbers and binding affinity. Androgen receptor, ER, and PR densities change dynamically in relation to season and reproductive activity. For example, during courtship, when T is high, compared to the brooding period, when T is low in both male and female ring doves, the density of ARs is substantially elevated within multiple brain regions, including areas implicated in sexual motivation and social behavior such as the POM, hypothalamus, LS, TnA, VTA, ICo, and PAG (Belle & Lea, 2001; Lea, Clark, & Tsutsui, 2001). Further, in male ring doves, measures of AR are elevated within the POM during early androgen-dependent aggressive components of courtship but then decline during estrogen-dependent nest-soliciting and copulation (Belle & Lea, 2001; Belle, Tsutsui, & Lea, 2003). Treating male or female ring doves with an aromatase inhibitor reduces both courtship behavior and the numbers of both ARs and PRs in the POM and hypothalamus (Belle et al., 2005). Fluctuations in the densities of ARs and ERs in the song control system parallel seasonal changes in song function

161

in songbirds. For example, AR and ER mRNA in the HVC in canaries are elevated in the fall, when males sing high rates of noncourtship song, but peak at the onset of the breeding season, when males are singing to attract females (Gahr & Metzdorf, 1997). Similarly, in Gambel’s whitecrowned sparrows (Zonotrichia leucophrys gambelii), the density and numbers of AR-immunopositive cells in the HVC was greatest during the spring breeding season (Soma et al., 1999). These data suggest that increases in ARs or ERs may increase the brain’s sensitivity to T or its metabolites to ensure that courtship and mating behaviors occur at an appropriate time of year. A final interesting example of the way in which differences in receptor densities can shape sexual behavior is illustrated by the African black coucal (Centropus grillii), a sex-role-reversed species. In this species, females are highly aggressive and compete over males, yet males and females have sex-traditional steroid hormone concentrations (i.e., circulating androgens are higher in males than females) (Goymann & Wingfield, 2004). Although the reversal in male- and female-typical behavior is not reflected in circulating androgen concentrations, in a study using in-situ hybridization, the mean AR mRNA expression level in TnA was significantly higher in female coucals compared to males (Voigt & Goymann, 2007). These data indicate that androgens may underlie sex-role-reversed courtship behavior in this species but that these effects manifest themselves through increased AR numbers or binding affinity in females.

4. STEROID HORMONE SYNTHETIC ENZYMES AND METABOLITES IN THE BRAIN 4.1. Enzyme and Metabolite Distribution in Males The gonads, adrenal glands, and brain contain cells equipped to synthesize steroids. Several studies have demonstrated that T originating from the gonads reaches the male brain, where it can be extensively metabolized by enzymes located within cells in the brain (Ball & Balthazart, 2004; Fusani & Gahr, 2006; Trainor, Kyomen, & Marler, 2006). The resulting products then bind to their own receptors in the brain to cause many of the cellular effects that modify male courtship and mating activities. The activity and distribution of T-metabolizing enzymes changes in association with the breeding season and plasma concentrations of T, representing another means by which endocrine mechanisms underlying sexual behaviors can be well matched to an environment predictive of a successful reproductive outcome.

162

Early studies in Japanese quail and ring doves established the importance of gonadal T metabolism within the medial preoptic-hypothalamic (POA-H) region in the control of male sexual behavior (Hutchison, 1970a; Adkins & Adler, 1972; Cheng & Lehrman, 1975a; Adkins et al., 1980; Hutchison & Steimer, 1984; 1985; Hutchison, Steimer, & Hutchison, 1986; Schlinger & Callard, 1987; Watson & Adkins-Regan, 1989c). Studies examining the metabolism of T in microdissected regions of the avian brain demonstrate high levels of P450aro activity within the diencephalon, with the highest levels in the POM (a crucial brain region involved in male courtship and copulation, detailed in Section 5.1.1) of male Japanese quail and ring doves (Steimer & Hutchison, 1980; Schlinger & Callard, 1987; Schumacher & Balthazart, 1987; Balthazart, 1991; Hutchison, 1993). A separate study in sexually mature male Japanese quail demonstrated that 5a-reductase was highest and 5b-reductase lowest in the POM and hypothalamic regions (Balthazart, Schumacher, & Evrard, 1990). High aromatase and 5a-reductase activity and lower 5b-reductase activity have also been identified in preoptic and hypothalamic regions of a songbird (Vockel, Prove, & Balthazart, 1990b). The distribution of P450aro highlights neural circuits in which P450aro activity may act to influence male sexual behavior. Dense clusters of neurons containing P450aro protein and mRNA are found in male quail in multiple regions involved in sexual behavior, including the POM, BSTm, VMH, and Tu. Scattered P450aro neurons are also found in the TnA and PAG (Balthazart, Foidart, & Harada, 1990; Foidart et al., 1995; Aste, Panzica, Viglietti-Panzica, Harada, & Balthazart, 1998). The patterns of P450aro distribution identified in quail overlap with those observed in several other non-songbirds (e.g., ring dove, budgerigar, swift (Apus apus), grey partridge, and barn owl (Tyto alba)) as well as in multiple songbirds (e.g., zebra finches, pied flycatchers (Ficedula hypoleuca), canaries, and house sparrows (Passer domesticus)) (Ball & Balthazart, 1990; Balthazart et al., 1996; Foidart, Silverin, Baillien, Harada, & Balthazart, 1998; Metzdorf et al., 1999; Silverin et al., 2000). Songbirds additionally have high amounts of P450aro mRNA and protein in the forebrain compared not only to other avian species but also to multiple other vertebrate groups (Balthazart et al., 1996; Foidart et al., 1998; Metzdorf, Gahr, & Fusani, 1999; Silverin, Baillien, Foidart, & Balthazart, 2000; Forlano, Schlinger, & Bass, 2006).

4.1.1. Aromatase (P450aro) is regulated by testosterone (T) Multiple studies show that the activity of P450aro in the diencephalon is regulated by plasma concentrations of T (Balthazart, 1991; Hutchison, 1993). In quail, ring doves,

Hormones and Reproduction of Vertebrates

and zebra finches, castration results in a reduction in P450aro activity in the POAeH (Steimer & Hutchison, 1981a; Schumacher & Balthazart, 1986; Balthazart et al., 1990b; Vockel, Prove, & Balthazart, 1990a) and a loss of immunoreactivity for P450aro protein or mRNA within the POM (Aste et al., 1998; Balthazart et al., 1990a). These effects are all reversed by T treatment. In seasonally breeding songbirds, P450aro activity changes seasonally within the diencephalon in parallel with changes in T. For example, in male European starlings and song sparrows, P450aro activity was highest in the diencephalon in spring, when this region is critical for the activation of courtship and copulation (Riters et al., 2001; Soma et al., 2003). In male European starlings, the POM was also found to be rich in P450aro protein during the spring breeding season but not outside the breeding season in fall (Riters et al., 2000) (Figure 6.5). These data demonstrate that changes in plasma T observed in response to seasonal changes in daylength or in response to other environmental factors (e.g., the presence of an appropriate nest site) can alter P450aro within the POAeH to optimize conversion of T into estrogens at the time of year and within an environment conducive to breeding success.

4.1.2. Studies of aromatase (P450aro) reveal nontraditional steroid effects Recent studies in Japanese quail and zebra finches support and expand upon what is known about the mechanisms of steroid action in the brain. In Section 2.1.3 we described the traditional route of steroid action, which involves T released from the gonads entering the brain, where it may be metabolized into estrogens, which then bind to intranuclear receptors to activate relatively slow gene transcription processes. 17b-estradiol also rapidly alters neuronal activity through cell membrane effects in rodents (McEwen & Alves, 1999; Kelly, Qiu, Wagner, & Ronnekleiv, 2002). In Japanese quail, rapid effects of estrogens on male sexual behavior are initiated within minutes by changes in brain P450aro (Balthazart, Baillien, Cornil, & Ball, 2004; Cornil, Taziaux, Baillien, Ball, & Balthazart, 2006). Thus, in addition to their conventional effects at intranuclear receptors, estrogens also influence male sexual behavior through nongenomic routes. Studies in songbirds have revealed other nontraditional routes of steroid action. Although the results of studies of P450aro in the songbird diencephalon generally match those obtained from non-songbirds such as quail and doves, there are notable differences observed within forebrain regions. Aromatase concentration is much denser within the telencephalon of songbirds compared to non-songbirds (Vockel et al., 1990a; Saldanha, Popper, Micevych, & Schlinger, 1998; Silverin et al., 2000), and P450aro activity within the telencephalon in songbirds is not highly T-dependent

Chapter | 6

Mean Volume (mm3 + sem)

(a)

.6

FIGURE 6.5 Data supporting a role for testosterone (T) and the medial preoptic nucleus (POM) in male courtship in European starlings (Sturnus vulgaris). (a) The mean volume of the POM is largest in males with nest boxes and high T in spring (black bar), as compared to males with low T in fall (white bar) and in males without nest boxes in spring that had intermediate concentrations of T (gray bar) (Riters et al., 2000). (bec) Photomicrographs showing a low density of immunolabeled aromatase cells in the POM of males in fall (b) and a high density in spring (c) (Riters et al., 2000). (d) Numbers of immediate early gene-immunolabeled cells in the POM relate positively to courtship song production (Heimovics & Riters, 2005). (e) Lesions to the POM disrupt male courtship song (Alger, Maasch, & Riters, 2009).

POM

.5 .4 .3 .2 .1 0

(b)

(c)

120 100

r2=0.61 p=0.02*

(e)

Songs Produced 40 35

80

*

30 60

Mean + SEM

Number of IEG (cFOS) labeled cells

(d)

163

Hormonal Regulation of Avian Courtship and Mating Behaviors

40 20

25 20 15 10

0

5

-20 -.02 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4

0

n = 12

n = 12

Control

POM Lesion

Songs Produced

(Vockel et al., 1990a). All steroid synthetic enzymes and precursors are located within the brain, and the brain itself forms steroids de novo from cholesterol, even in adults (Baulieu, 1997; Tsutsui, Ukena, Takase, Kohchi, & Lea, 1999; Schlinger & London, 2006). Such brain-derived steroids are called neurosteroids. Neurosteroidogenesis appears to be crucial during the development of the songcontrol system and for plasticity of this system in adult birds (Schlinger & London, 2006). The role of neurosteroidogenesis in the control of courtship and mating behavior has not been examined extensively, but it is possible that local changes in bioavailability of steroids may modulate aspects of sexual behavior.

4.2. Enzyme and Metabolite Distribution in Females In females, estrogens released into circulation from the gonads are thought to act directly at target receptors in the brain. Consistent with the idea that locally synthesized estrogens may be less important in females compared to males, P450aro activity has been found to be lower within the POA-H in females than males of multiple avian species (Schumacher & Balthazart, 1986; Schlinger & Callard, 1987; Vockel, Prove, & Balthazart, 1988; Balthazart et al., 1990b). However, there is some evidence in females that estrogens derived from the brain, in addition to those released from the

164

ovaries, play a role in courtship. This idea is based on studies in female ring doves demonstrating that ovarian development changes in parallel with P450aro activity within the POA and basal hypothalamus, regions implicated in courtship behaviors (Hutchison, Wozniak, & Hutchison, 1992). Although these changes in P450aro are reduced by ovariectomy and restored with E2 treatment, females with undeveloped ovaries that interacted with males had elevated P450aro activity in the brain. This elevation in P450aro activity was not observed in females with similarly undeveloped ovaries when these birds were visually isolated. These findings suggest that interactions with a male directly influence brain P450aro, independently of the ovary (Hutchison et al., 1992). Differences between the sexes in terms of both 5a- and 5b-reductase activity have also been identified. In quail, 5a-reductase activity is higher in the AH of males than females in gonadally intact animals. In contrast, 5breductase activity in the POA is higher in females than males. Sex differences in both 5a- and 5b-reductase activity are lost with gonadectomy but cannot be restored with T treatment, suggesting that they are not induced by differences in circulating T alone (Balthazart et al., 1990b; Schumacher & Balthazart, 1984). In male zebra finches, 5a-reductase activity is higher within song or vocal control regions (MAN, HVC, RA, and ICo) but lower in the POA (Vockel et al., 1990b) as compared to females. In contrast, 5b-reductase activity is higher in song-control regions (area X and RA) in females compared to males (Vockel et al., 1990b). These findings are consistent with data suggesting 5a- and 5b-reductase activities work in opposition to fine tune T effects on the brain and behavior. Although females of the sex-role-reversed species studied display many male-typical behaviors, such as vocal advertisement and territorial aggression, males have higher T concentrations than females, similar to birds with traditional sex-roles (Rissman & Wingfield, 1984; Fivizzani, Colwell, & Oring, 1986; Fivizzani & Oring, 1986; GrattoTrevor, Fivizzani, Oring, & Cooke, 1990). Wilson’s phalarope (Phalaropus tricolor), a sex-role-reversed species, also has patterns for androgen-metabolizing enzymes (P450aro, 5a-, and 5b-reductase) similar to patterns seen in bird species with traditional sex-roles (Schlinger et al., 1989). This suggests that sex-role-reversed behavior is not directly regulated by circulating T concentrations or local androgen metabolism, but instead perhaps by differential hormone sensitivity (e.g., differences in receptor numbers or binding affinity) between males and females.

5. NEUROENDOCRINE REGULATION OF MALE SEXUAL BEHAVIOR The neuroendocrine control of avian male sexual behavior has been intensely examined in Japanese quail and ring

Hormones and Reproduction of Vertebrates

doves, with more recent work in songbirds linking brain regions involved in sexual motivation to male courtship song (Figure 6.4(b)). Evidence from each of these species demonstrates that steroid hormone activity within the POM is crucially involved in the regulation of male sexual behavior. Although not as intensely studied, other steroid hormone-sensitive regions, including multiple brain regions implicated in social behavior (Figure 6.4(a)), also appear to be sites in which steroid hormones act to influence courtship and copulation.

5.1. Male Ring Doves and Japanese Quail 5.1.1. Steroid hormones act within the medial preoptic nucleus to regulate male sexual behavior The POM is a T-sensitive, sexually dimorphic nucleus that is larger in males than females (Viglietti-Panzica et al., 1986). In ring doves and quail, early studies demonstrated a central role for T activity within the POM in male copulatory behavior. As reviewed in Section 4.1.1, castration completely abolishes male copulatory behavior and reduces P450aro activity and labeling density in the POM, both of which can be restored by T treatment (Steimer & Hutchison, 1981a; Schumacher & Balthazart, 1986; Balthazart et al., 1990b; Vockel et al., 1990a). Placing a Treleasing implant into the POM of a castrated male quail or ring dove is necessary and sufficient for the activation of male copulatory behavior (Hutchison, 1970b; Barfield, 1971; Hutchison, 1971; Balthazart & Surlemont, 1990b; Riters, Absil, & Balthazart, 1998; Watson & AdkinsRegan, 1989c). Testosterone implants located within or near the POM that activate male sexual behavior also increase both the volume of the POM and the numbers of P450aro-immunolabeled cells in the POM (Balthazart, Surlemont, & Harada, 1992). The aromatization of T specifically within the POM underlies T activation of male sexual behavior. Male copulatory behavior is positively correlated with both the volume of the POM and the numbers of P450aro-immunoreactive cells located within the caudal POM (Balthazart et al., 1992b). Only implants releasing estrogens or aromatizable androgens into the POM stimulate male sexual behavior in castrated quail (Watson & Adkins-Regan, 1989a; 1989c; Balthazart & Surlemont, 1990a). Similarly, implants containing P450aro inhibitors aimed at the POM, but not the surrounding POA, inhibit the induction by T of male sexual behavior (Balthazart, Evrard, & Surlemont, 1990; Balthazart & Surlemont, 1990a). These results demonstrate that T must be aromatized within the POM to exert its behavioral effects. This is further supported by the fact that electrolytic POA lesions only disrupt male

Chapter | 6

Hormonal Regulation of Avian Courtship and Mating Behaviors

copulatory behavior if they damage P450aro-immunoreactive cells in the POM (Balthazart et al., 1992b).

5.1.2. Appetitive and consummatory sexual behavior rely on partially distinct neuronal mechanisms Male sexual behavior can be divided into two components that are regulated by at least partially distinct neuroendocrine mechanisms. Appetitive sexual behavior consists of behaviors immediately prior to and in anticipation of copulation, such as maintaining close proximity to a female, courting, or looking at a female. Consummatory sexual behavior consists of actual physical contact between the male and female during copulation (Beach, 1956; Balthazart et al., 1995). In rats, lesions to the medial POA abolish male copulation, but lesioned males continue to display sexual interest in females (Everitt & Stacey, 1987; Everitt, 1990; Liu, Salamone, & Sachs, 1997). These data suggest that, at least in rodents, the POA is crucial for the act of copulation but that other brain areas contribute to the control of appetitive components of sexual behavior. The extent to which distinct neural circuits regulate appetitive and consummatory components of sexual behavior in birds has been a focus of research in Japanese quail. In castrated male quail, T implants in the POM alone are sufficient to activate both appetitive and consummatory components of male sexual behavior (Riters et al., 1998), and lesions to the POM disrupt both components of sexual behavior (Balthazart et al., 1998a). However, more refined analyses reveal that lesions confined to the rostral POM most profoundly disrupted appetitive sexual behavior, whereas lesions restricted to the caudal POM more effectively disrupted consummatory components of behavior (Balthazart et al., 1998a). Further, studies in which immediate early gene (IEG) immunolabeling was used as an indirect marker of neuronal activity revealed elevations in IEG-labeled cells restricted to the rostral POM in male quail allowed to display appetitive but not consummatory sexual behavior (Taziaux et al., 2006). In contrast, numbers of IEG-labeled cells were elevated along the full rostralcaudal extent of the POM in male quail allowed to engage in both appetitive and consummatory components of behavior (Meddle et al., 1997; Taziaux et al., 2006). Thus, it appears that, similar to studies in rodents, appetitive and consummatory components of male sexual behavior rely on at least partially distinct neural mechanisms.

5.1.3. The medial preoptic nucleus is part of a neural circuit that regulates male sexual behavior The POM is well situated neuroanatomically to function as an integrative node in a neural circuit underlying both male

165

courtship and copulation. The POM is reciprocally connected to multiple steroid-sensitive, P450aro-rich brain regions that have been implicated in social and sexual behavior (including the septum, BSTm, TnA, VMH, PAG, and VTA) (Figure 6.4(a)) and modulation of endocrine state (Tu) (Balthazart et al., 1994). The POM sends a P450arorich projection to the PAG, which may control premotor aspects of male copulation (Absil, Riters, & Balthazart, 2001). The POM also receives input from areas implicated in motivation and arousal, including the VTA, PAG, substantia nigra, and locus coeruleus (Balthazart & Absil, 1997; Absil, Papello, Viglietti-Panzica, Balthazart, & Panzica, 2002). The role of these regions in male sexual behavior has not been as well characterized as that of the POM. Some data implicate the TnA in appetitive components of male sexual behavior. For example, lesions to the posterior-medial TnA, but not the anterior TnA, in quail increase the amount of time a male takes to approach a female, and reduce both appetitive cloacal gland movements in response to a female and copulation (Thompson, Goodson, Ruscio, & Adkins-Regan, 1998; Absil, Braquenier, Balthazart, & Ball, 2002). In males presented with a view of a female or stimuli predicting access to a female, IEG-immunolabeling was elevated within the LS, TnA, and BSTm. In addition to these regions, activity was also elevated within the PAG in males allowed to copulate with a female (Meddle et al., 1997; Charlier, Ball, & Balthazart, 2005; Taziaux et al., 2006; Can, Domjan, & Delville, 2007; Taziaux, Lopez, Cornil, Balthazart, & Holloway, 2007; Taziaux, Kahn, Moore, Balthazart, & Holloway, 2008). The way in which these regions interact with the POM and contribute to the regulation of male courtship and copulation must be defined in future research.

5.2. Male Songbirds 5.2.1. Testosterone (T) stimulates male courtship song In male songbirds, singing behavior plays a crucial role in courtship and mate attraction. Seasonally breeding or opportunistically breeding male songbirds with high T respond to the introduction of female conspecifics with high rates of song accompanied by courtship displays (Wingfield & Farner, 1993; Catchpole & Slater, 1995; Ball, Riters, MacDougall-Shackleton, & Balthazart, 2008). Song in this context can be considered to be highly sexually motivated. When T concentrations are low, some species continue to sing at high rates, however; song is used for purposes other than immediate mate attraction (e.g., for maintaining large overwintering flocks (Smith et al., 1997; Riters et al., 2000). When T is low, males do not produce courtship song in response to females (e.g., Riters et al., 2000; Pinxten et al., 2002). These observations suggest that

166

T plays a role in regulating the motivation to sing in a breeding context.

5.2.2. Testosterone (T) may act within the songcontrol system to influence sensorimotor aspects of song As outlined in Section 3.3.1, ARs are found within several brain regions comprising the song-control system, and ERs have been identified within the HVC (Figure 6.4(b)). Nuclei of the song-control system play well-studied roles in aspects of song such as learning and sensorimotor processing (Ziegler & Marler, 2008); however, much less attention has been devoted to understanding what activates the song-control system or how the brain regulates the motivation to sing. Lesions to song-control regions RA and HVC result in severe deficits in song production, but lesioned birds continue to assume a singing posture and display motor behaviors associated with song production, indicating an intact motivation to sing (Nottebohm et al., 1976). It is likely that T and its metabolites act within the song-control system to regulate aspects of song such as learning or sensorimotor processing, whereas the motivation to sing is regulated by T activity in regions outside the song-control system.

5.2.3. Evidence that testosterone (T) acts in the medial preoptic nucleus (POM) to motivate male courtship song Given that song during the breeding season can be highly sexually motivated, brain areas involved in the anticipation of copulatory behavior (e.g., the POM) or motivation in general (e.g., the VTA) are also likely to play important roles in this type of singing behavior. Indeed, multiple studies highlight a role for the POM in courtship song production (Figure 6.5). As compared to male starlings observed outside of the breeding season, during the breeding season the POM was rich in P450aro and larger in males with high T that successfully acquired nest sites and sang high rates of courtship song (Riters et al., 2000). Males in this study also sang longer songs in spring, when a longer song bout serves to attract mates and repel competitors (Eens et al., 1991; Mountjoy & Lemon, 1995; Gentner & Hulse, 2000). The volume of the POM related positively to song bout length (Riters et al., 2000), providing further evidence for POM involvement in sexually motivated communication. Lesions to the POM in male starlings block song and other courtship behaviors specifically within a sexually motivated context (Figure 6.5) but result in the production of context-inappropriate elevations in song in other nonsexually motivated contexts (Riters & Ball, 1999; Alger & Riters, 2006; Alger, Maasch, & Riters, 2009). Additional

Hormones and Reproduction of Vertebrates

data reveal positive relationships between the number of cells labeled for the IEG cFOS within the POM and sexually motivated song, but not other types of song, in two studies of different species (starlings (Figure 6.5) and house sparrows (Riters, Teague, Schroeder, & Cummings, 2004; Heimovics & Riters, 2005). Labeling within rostral but not caudal portions of the POM related best to sexually motivated song in house sparrows (Riters et al., 2004), suggesting that, as in quail, the rostral POM is specialized for the regulation of appetitive aspects of sexual behavior. Together, these data suggest that, similar to what has been described in quail, the volume of the POM and P450aro levels within the POM are T-dependent, and the POM plays a critical role in the regulation of courtship behavior that also extends to sexually motivated birdsong (Figure 6.5). It is likely that T acts within the song-control system to regulate structural aspects of song but that T acts within the POM to influence the motivation to sing within the context of courtship.

5.2.4. The medial preoptic nucleus (POM) is part of a neural circuit that regulates male courtship song In addition to the POM, studies using IEG-labeling as a marker for neuronal activity have identified several steroid-sensitive brain regions implicated in social behavior, including the BSTm, LS, VMH, VTA, and AH, in sexually motivated song production in male starlings (Heimovics and Riters, 2005; 2006; 2007). In songbirds, as in quail, the POM is reciprocally connected to multiple regions involved in social and sexual behavior, including the BSTm, LS, hypothalamic regions, PAG, and VTA. One direct route (through the DM) and multiple indirect routes (e.g., through the VTA, PAG, and locus coeruleus) have been identified by which the POM can influence the song system (Riters & Alger, 2004) (Figure 6.4(b)). Lesions to the POM disrupt relationships between sexually motivated song and patterns of neuronal activity within limbic, hypothalamic, and midbrain regions identified using IEGs, consistent with the neuroanatomical data highlighting the POM as well situated to interact with multiple regions (Figure 6.6) (Alger et al., 2009). The precise way in which the POM interacts with these regions to regulate courtship song has yet to be determined.

5.3. How Does Testosterone (T) Modulate Activity Within Regions Underlying Courtship and Copulation in Males? In addition to steroid hormones, several neuromodulators are implicated in the regulation of male courtship and mating behaviors in both birds and mammals, including the

Chapter | 6

167

Hormonal Regulation of Avian Courtship and Mating Behaviors

HVC Mean # of Labeled Cells + SEM

(a)

LS 100

2400

90

*

*

80

2000

70 1600

60 50

1200

40 800

30 n = 11

400

n = 12

n=8

20

n=8

Control POM Lesion Condition

Control POM Lesion Condition

(b) Number of Labeled Cells

Area X

VMH

3500

160

3000

140

2500

120 100

2000

80

1500

60 1000 40 500

20

0

0 0

20 40 60 Control

80

0

20 40 60 POM Lesion

80

0

20 40 Control

60

0

20 40 POM Lesion

60

Number of Songs Produced

Number of Songs Produced IEG label in VMH

(c) No Song

High Song

Control

vIII DSV

vIII DSV

POM Lesion

FIGURE 6.6 Evidence indicating that the medial preoptic nucleus (POM) plays a role in integrating networks of steroid-sensitive brain regions to coordinate courtship in male European starlings (Sturnus vulgaris). Examples of data showing that lesions to the POM (a) significantly reduce numbers of immediate early gene-immunolabeled cells and (b) disrupt correlations between measures of song production and numbers of immediate early geneimmunolabeled cells within song-control regions (e.g., the HVC and area X) and areas involved in social behavior (e.g., the lateral septum (LS) and ventromedial hypothalamus (VMH)). (c) Photomicrographs showing immediate early gene-immunolabeled cells within the VMH in control (top panels) and POM-lesioned (bottom panels) birds. Left images are of birds that did not sing. Right images are of birds that sang at high rates (the control bird sang 52 songs; the lesioned bird sang 49 songs. DSV, ventral supraoptic decussation; vIII, third ventricle. Reproduced from Alger, Maasch, and Riters (2009).

168

catecholamines dopamine (DA) and norepinephrine (Hull et al., 1986; Hull, Balthazart, Libioulle, & Sante, 1988; Pfaus et al., 1990; Du, Lorrain, & Matuszewich, 1995; Balthazart, Castagn, & Ball, 1997b; Schroeder & Riters, 2006), opioid neuropeptides (Agmo & Paredes, 1988; Agmo & Berenfeld, 1990; Kotegawa, Abe, & Tsutsui, 1997; Riters et al., 2005; Schroeder & Riters, 2006), and arginine vasopressin in mammals or its avian homolog arginine vasotocin (AVT) (Castagna, Absil, Foidart, & Balthazart, 1998; Harding & Rowe, 2003). Steroid hormone receptors and P450aro fibers colocalize in several brain regions with neurotransmitter receptors, mRNA, or fibers (e.g., Balthazart & Absil, 1997; Maney, Bernard, & Ball, 2001; Balthazart, Baillien, & Ball, 2002; Appeltants, Ball, & Balthazart, 2004). It is generally assumed that T or its metabolites alter neurochemical activity within specific brain regions to influence male sexual behavior, and some evidence supports this assumption. For example, AVT is nearly absent in several brain regions of castrated male quail, but is restored in T-treated animals (VigliettiPanzica, Aste, Balthazart, & Panzica, 1994; Panzica, GarciaOjeda, Viglietti-Panzica, Thompson, & Ottinger, 1996), suggesting that T may alter male sexual behavior by altering AVT activity. Androgens also influence DA activity, stimulating DA turnover within both the song system (area X and RA) and the POA in male zebra finches (Barclay & Harding, 1988; 1990). Further, androgens influence tyrosine hydroxylase (the rate-limiting enzyme for the synthesis of both DA and norepinephrine) labeling density in birds and rodents in a complex time- and regionspecific manner, indicating that steroid hormones can affect DA synthesis (Simerly, Swanson, Handa, & Gorski, 1985; Adler, Vescovo, Robinson, & Kritzer, 1999; Kritzer, Adler, Marotta, & Smirlis, 1999; King, Barkley, Delville, & Ferris, 2000; King, Kelly, & Delville, 2000; Kritzer, 2000; Appeltants, Ball, & Balthazart, 2003; Kritzer, 2003). These data support the idea that steroid hormones can influence components of male sexual behavior by altering neurochemical activity. Further, there is evidence that neurochemical activity can influence steroid hormones. For example, in male Japanese quail, studies show that DA depletion increases P450aro activity and that DA can rapidly inhibit P450aro activity (Baillien & Balthazart, 1997; Balthazart, Baillien, & Ball, 2002). Thus, many of the effects of T on sexual activity are likely modulated by its interactions with neurochemical systems.

6. NEUROENDOCRINE REGULATION OF FEMALE SEXUAL BEHAVIOR Surprisingly few studies are available on the neuroendocrine control of female courtship and mating in birds. This is in stark contrast to studies in female mammals, for which

Hormones and Reproduction of Vertebrates

detailed data on the neurocircuitry and endocrine mechanisms underlying the female lordosis response are available (for reviews see Etgen et al., 1999; Frye, 2001; Pfaff, Kow, Loose, & Flanagan-Cato, 2008). In mammals, the ER-rich VMH is a critical node in a network of nuclei underlying female receptivity. In birds, data also implicate the VMH as a critical site for the regulation of female receptivity; however, the integrative neuronal circuitry regulating female sexual behavior in birds has yet to be defined.

6.1. Female Ring Doves and Japanese Quail 6.1.1. 17b-estradiol (E2) acts within the ventromedial hypothalamus to regulate female sexual behavior The effects of lesions and E2 implants in the brain on female responses to male courtship have been examined extensively only in ring doves (Gibson & Cheng, 1979). In this study, ovariectomized female ring doves were treated with E2 and the effects of lesions on different portions of the POA and hypothalamus on courtship activity were examined. Lesions specifically to the posterior medial hypothalamus, containing the VMH, disrupted female courtship behavior. Gibson and Cheng (1979) also systematically placed implants containing E2 into regions of the female brain spanning the rostral POA to regions caudal to the VMH in ovariectomized ring doves. Implants in the region containing the VMH most effectively stimulated female crouching in response to nest-soliciting behaviors by males. Other less-reliable sexual responses were elicited by implants located within the preopticanterior hypothalamus, a possible homolog to the mammalian nucleus accumbens (a region shown in mammals to be centrally involved in reward). In adult female Japanese quail, a study using immunolabeling for the IEG cFOS also highlighted the VMH as being prominently active during sexual interactions with males (Meddle, Foidart, Wingfield, Ramenofsky, & Balthazart, 1999).

6.1.2. Pathways underlying vocal self-stimulation in ring doves During an extended period of courtship, female ring doves begin to respond to male nest-coos with nest-coos of their own. Production of nest-coos powerfully influences a female’s own reproductive endocrinology and ovarian development (Cohen & Cheng, 1981; Cheng, 1986; Cheng et al., 1988). The neuroendocrine circuits linking a female’s own vocal behavior to the stimulation of hypothalamic GnRH neurons, LH release, and consequent release of ovarian hormones have been identified and mapped using lesions, neuroanatomical tract-tracing studies, and

Chapter | 6

Hormonal Regulation of Avian Courtship and Mating Behaviors

electrophysiological recordings (reviewed in Cheng, 2005). Specifically, a population of neurons that responds to female nest-coos has been identified within the shell region of the auditory thalamic nucleus ovoidalis (Ov) (Cheng & Peng, 1997). The shell of the Ov receives projections from the midbrain auditory nucleus ICo and sends dense projections to hypothalamic regions containing GnRH, including the preoptic and anterior-medial hypothalamus (POA/AMH) and the VMH (Durand, Tepper, & Cheng, 1992; Cheng & Zuo, 1994; Cheng & Peng, 1997). Luteinizing hormone concentrations were dramatically elevated in association with the activation of female nest-cooresponsive units in the POA/AMH. These findings suggest that female nest-coo stimulation triggers GnRH release through projections from the Ov shell to the POA/AMH (Cheng, Peng, & Johnson, 1998). In this manner, females self-stimulate the release of LH and consequently E2 release from the gonads into the bloodstream, which can then activate female sexual behavior by acting within the VMH.

6.2. Female songbirds 6.2.1. Estrogen-sensitive circuits regulate female songbird responses to male courtship song In songbirds, females with high E2 concentrations attend to differences in male song structure, such as complexity or bout length, and display stereotyped courtship-solicitation displays or motivated approach behaviors in response to attractive, typically longer or more complex, songs (Searcy & Yasukawa, 1996). In seasonally breeding birds, such responses are not observed during the nonbreeding season, when E2 concentrations are low (e.g., LeBlanc, Goode, MacDougall-Shackleton, & Maney, 2007). Most studies of female responses to male song focus on auditory forebrain regions that respond to species-typical song. 17b-estradiol acts within these regions to influence aspects of song perception or discrimination. 17b-estradiol may additionally influence activity within diencephalic brain regions, such as the VMH, to induce receptive behavior in response to male song. Overall, the data suggest that female selective behavioral and neuronal responses to male song require activity within E2-sensitive regions involved in song perception to be integrated with activity in areas involved in hormonal state, courtship, and mating behavior.

6.2.2. Endocrine influences on auditory responses to male song In female songbirds, conspecific male song stimuli influence two auditory forebrain regions, the NCM and the CMM. In male canaries, IEG expression in the CMM was

169

higher in females presented with sexually attractive male song compared to females that were played less attractive song (Leitner, Voigt, Metzdorf, & Catchpole, 2005). In female white-throated sparrows (Zonotrichia albicollis), the selectivity of an IEG response within these two regions and also a part of the auditory pathway, the nucleus mesencephalicus lateralis pars dorsalis, is dependent upon breeding condition concentrations of E2 (Maney, Cho, & Goode, 2006). In this study, E2 appeared to modulate responses to male song by inhibiting neuronal responses to behaviorally irrelevant synthetic tones. Other brain areas involved in song processing are part of the song-control system. The HVC and LMAN are largest in females that respond strongly to sexually stimulating male conspecific songs in cowbirds, canaries, and starlings (Hamilton, King, Sengelaub, & West, 1997; Leitner & Catchpole, 2002; Riters & Teague, 2003). Lesion and electrophysiology studies in female canaries demonstrate that the HVC is involved in estrogen-dependent female copulation solicitation displays to sexually attractive elements of male canary song (Brenowitz, 1991; Del Negro et al., 1998; Burt et al., 2000; Del Negro, Kreutzer, & Gahr, 2000). Female canaries with lesions to the LMAN also showed deficits in discrimination among acoustic stimuli, including between canary and heterospecific song (Burt et al., 2000). As reviewed above, E2 receptors are located within the auditory forebrain and HVC. Thus, some of the effects of E2 may occur through its activity directly within these areas. Interestingly, lesions to auditory processing regions such as the HVC and LMAN do not reduce female solicitation displays overall. Instead, females with lesions to the HVC and LMAN continue to respond at high rates to song stimuli; however, they no longer discriminate (Brenowitz, 1991; Burt et al., 2000). For example, HVC lesions in female canaries did not reduce responses to attractive male song, but resulted in increased responses to stimuli that were normally only weakly sexually stimulating (Del Negro et al., 1998). These studies indicate that nuclei involved in song processing are critical for song discrimination but do not participate in the sexually motivated behavioral responses of females to male song. What motivates females to respond to sexually attractive male song is not well known. It is likely that E2 acts within acoustic and song-control regions to influence song perception, but acts outside of this system to influence endocrine physiology and sexually motivated responses to male courtship songs.

6.2.3. Neuroendocrine regulation of female sexually motivated responses to courtship song Females of many songbird species do not sing as part of courtship. Thus, vocal self-stimulation in such species

170

Hormones and Reproduction of Vertebrates

likely does not play a role in altering female neuroendocrine state and reproductive behavior. However, some data from a monogamous duetting songbird species, the robin chat (Cossypha heuglini), are at least consistent with a role for vocal self-stimulation in reproductive behavior (Todt & Hultsch, 1982). In this study, deafened females no longer participated in vocal duets with their mates, although they did continue to vocalize within other contexts. Although males and females in the study remained paired for the two years of the study, pairs in which the female was deafened did not build nests, a behavior typically initiated by females. It is likely that the failure to reproduce related to a lack of acoustic input from the male. However, it is also possible that, as in ring doves, a female’s own vocal production may feed back to her hypothalamus to stimulate reproductive behavior. Recent studies in female songbirds show that regions implicated in social behavior are sensitive to male song and that the response to male song varies depending upon a female’s endocrine state. In contrast to female whitethroated sparrows with low E2, the numbers of IEG-labeled cells in E2-treated females were substantially elevated in response to male song compared to biologically relevant tones within each of the brain regions considered part of the social behavior network (Figure 6.7). In this study, some of the E2-treated females displayed copulation solicitation displays in response to male song. The numbers of solicitation displays were correlated with the numbers of

IEG-labeled cells in the HP, POM, and TnA (Maney, Goode, Lange, Sanford, & Solomon, 2008).

6.3. How Does 17b-estradiol (E2) Modulate Activity Within Regions Underlying Female Responses to Male Courtship? Studies in female songbirds also support the assumption that steroid hormones, in this case E2, alter neurochemical activity within specific brain regions to influence sexual behavior. The role of the catecholamines norepinephrine and DA has been a focus of recent work on the neuroendocrine control of female responses to male courtship song (LeBlanc et al., 2007; Riters, Olesen, & Auger, 2007; Riters & Pawlisch, 2007; Sockman & Salvante, 2008). Although the results of some studies suggest an inhibitory role and others a stimulatory role, catecholamines clearly influence female responses to male courtship song (Appeltants, Del Negro, & Balthazart, 2002; Riters, Olesen, & Auger, 2007; Riters & Pawlisch, 2007; Vyas, Harding, McGowan, Snare, & Bogdan, 2008). Evidence suggests that E2 may influence female responses to song by altering catecholamine activity within specific brain regions. Specifically, in female starlings, a role for E2-sensitive catecholaminergic nuclei and female responses to song was assessed using immunohistochemistry to identify tyrosine hydroxylase in its phosphorylated form (pTH), a method for examining catecholamine synthesis occurring in the brain immediately

Social Behavior Network

Egr-1 cells/mm2

BSTm

TnA

600

AM

*

VTA

*

*

*

song tones

400

* 200

*

0 blank

Egr-1 cells/mm2

2000

E2

blank

VMH-m

E2

VMH-I

blank

E2

blank

LSc.vl.

E2

POM

GCt

*

1500

*

1000

*

*

*

* *

500 0 blank

E2

blank

E2

blank

E2

blank

E2

blank

E2

FIGURE 6.7 Counts of immediate early gene-immunolabeled cells within each brain region considered to be part of the vertebrate social behavior network in female white-throated sparrows (Zonotrichia albicollis) receiving empty (blank) or 17b-estradiol (E2)-filled subcutaneous implants. Females were either presented with male song stimuli or biologically irrelevant tones. AM, anterior hypothalamus; BSTm, medial bed nucleus of the stria terminalis; GCt, central gray; LSc.vl., ventrolateral subdivision of the caudal lateral septum; POM, medial preoptic nucleus; TnA, nucleus taenia of the amygdala; VMH-l, lateral portion of the ventromedial hypothalamus; VMH-m, medial portion of the ventromedial hypothalamus; VTA, ventral tegmental area. Reproduced from Maney, Goode, Lange, Sanford, and Solomon (2008).

Chapter | 6

Hormonal Regulation of Avian Courtship and Mating Behaviors

prior to the time of sacrifice (Riters, Olesen, & Auger, 2007). Exposure to male courtship song in E2-treated females reduced pTH density in brain regions involved in sexual and social behavior (VMH and LS). In contrast, labeling densities were elevated in the same regions in females with low concentrations of E2. Catecholamine synthesis in the VTA was also implicated in female responses to male song in a complex fashion. These data suggest that catecholamine activity within these E2-sensitive regions may modulate female responses to male song and that endocrine state and catecholamines interact to regulate female responses to male courtship song. Data also demonstrate that E2 influences the numbers of catecholaminergic cells in regions implicated in female responses to male song. In white-throated sparrows, E2 treatment enhanced tyrosine hydroxylase innervation of the auditory forebrain (NCM) and the numbers of tyrosine hydroxylase-immunolabeled cells in the locus coeruleus and VTA (LeBlanc et al., 2007). These data are similar to findings in female rats, which show E2 regulation of catecholamine activity (Petitti, Karkanias, & Etgen, 1992; Karkanias & Etgen, 1993; Shimizu & Bray, 1993; Bazzett & Becker, 1994; Etgen & Karkanias, 1994; Karkanias & Etgen, 1994; Karkanias, Li, & Etgen, 1997; Becker, 1999; Kritzer, 2003; Kritzer, Adler, & Bethea, 2003) and highlight ways in which steroid hormones might influence song processing and responses to song or other mate signals through effects on catecholamines.

7. CLOSING REMARKS In this chapter, we have reviewed multiple studies demonstrating that environmental and social stimuli strongly influence steroid hormones to coordinate gametogenesis, hormone production and release, and mating activities so that breeding behaviors are initiated within a context conducive to a successful reproductive outcome. However, many questions about the neuroendocrine regulation of avian courtship and mating activities remain. For example, the neuroendocrine regulation of sexual behavior in females has not been as well characterized as that of males. It is clear that females require many cues in addition to a breedingappropriate photoperiod to initiate courtship. This sex difference provides an excellent opportunity to examine sex differences in the transduction of environmental cues to hormonal secretions and sexual behavior. Further, little is known about the way in which multiple hormone-sensitive brain regions interact to coordinate courtship and mating activities in either male or female birds. There is also a dearth of knowledge about how steroid hormones influence and are influenced by other neurochemical systems to stimulate mating activities, and the genes regulated by hormones remain to be identified. The combination of a detailed understanding of behavioral aspects of avian

171

courtship and mating behaviors and the environmental stimuli that influence these behaviors make birds ideal for studying how environmental factors, hormones, and the brain interact to regulate courtship and mating activities.

ACKNOWLEDGMENTS Support from the National Institute of Mental Health MH080225 and the National Science Foundation NSF0717004 is gratefully acknowledged. We thank Bill Feeny and Dr. Deborah Duffy for assistance with illustrations and figures.

ABBREVIATIONS 5a-DHT 5b-DHT AH AMH AR AVT BSTm CMM DA DLM DM E2 ER FSH GCt GnIH GnRH GTH HP HPG HVC ICo IEG LH LMAN LS MAN mMAN NCM Nif nXIIts Ov P4 P450aro PAG POA POA/AMH POA-H POM PR pTH RA

5a-dihydrotestosterone 5b-dihydrotestosterone Anterior hypothalamus Anterior/medial hypothalamus Androgen receptor Arginine vasotocin Medial bed nucleus of the stria terminalis Mesopallium caudomediale Dopamine Medial nucleus of the dorsal lateral thalamus Dorsomedial nucleus of the nucleus intercollicularis 17b-estradiol Estrogen receptor Follicle-stimulating hormone Central gray Gonadotropin-inhibiting hormone Gonadotropin-releasing hormone Gonadotropin Hippocampus Hypothalamicepituitaryegonadal Higher vocal centre Nucleus intercollicularis Immediate early gene Luteinizing hormone Lateral magnocellular nucleus of the anterior nidopallium Lateral septum Magnocellular nucleus of the anterior nidopallium Medial portion of the magnocellular nucleus of the anterior nidopallium Caudomedial nidopallium Nucleus interfacialis Tracheosyringeal portion of the hypoglossal nucleus Nucleus ovoidalis Progesterone Aromatase Periaqueductal (central) gray Preoptic area Preoptic and anterior-medial hypothalamus Medial preoptic-hypothalamic Medial preoptic nucleus Progesterone receptor Phosphorylated tyrosine hydroxylase Robust nucleus of the arcopallium

172

RAm/rVRG T TnA Tu VMH VT VTA

Hormones and Reproduction of Vertebrates

Nucleus retroambigualis/rostral ventral respiratory group Testosterone Nucleus taenia of the amygdala Tuberal complex Ventromedial hypothalamus Vasotocin Ventral tegmental area

REFERENCES Absil, P., Braquenier, J. B., Balthazart, J., & Ball, G. F. (2002). Effects of lesions of nucleus taeniae on appetitive and consummatory aspects of male sexual behavior in Japanese quail. Brain Behav. Evol., 60, 13e35. Absil, P., Papello, M., Viglietti-Panzica, C., Balthazart, J., & Panzica, G. (2002). The medial preoptic nucleus receives vasotocinergic inputs in male quail: a tract-tracing and immunocytochemical study. J Chem Neuroanat., 24, 27e39. Absil, P., Riters, L. V., & Balthazart, J. (2001). Preoptic aromatase cells project to the mesencephalic central gray in the male Japanese quail (Coturnix japonica). Horm Behav., 40, 369e383. Adkins-Regan, E. (1981). Effect of sex steroids on the reproductive behavior of castrated male ring doves (Streptopelia sp.). Physiol Behav., 26, 561e565. Adkins, E. K. (1977). Effects of diverse androgens on the sexual behavior and morphology of castrated male quail. Horm Behav., 8, 201e207. Adkins, E. K., & Adler, N. T. (1972). Hormonal control of behavior in the Japanese quail. Journal of Comparative and Physiological Psychology, 81, 27e36. Adkins, E. K., & Nock, B. (1976a). Behavioural responses to sex steroids of gonadectomized and sexually regressed quail. J Endocrinol., 68, 49e55. Adkins, E. K., & Nock, B. L. (1976b). The effects of the antiestrogen CI-628 on sexual behavior activated by androgen or estrogen in quail. Horm Behav., 7, 417e429. Adkins, E. K., Boop, J. J., Koutnik, D. L., Morris, J. B., & Pniewski, E. E. (1980). Further evidence that androgen aromatization is essential for the activation of copulation in male quail. Physiol Behav., 24, 441e446. Adler, A., Vescovo, P., Robinson, J. K., & Kritzer, M. F. (1999). Gonadectomy in adult life increases tyrosine hydroxylase immunoreactivity in the prefrontal cortex and decreases open field activity in male rats. Neuroscience, 89, 939e954. Agmo, A., & Berenfeld, R. (1990). Reinforcing properties of ejaculation in the male rat: role of opioids and dopamine. Behav Neurosci., 104, 177e182. Agmo, A., & Paredes, R. (1988). Opioids and sexual behavior in the male rat. Pharmacol Biochem Behav., 30, 1021e1034. Alger, S. J., & Riters, L. V. (2006). Lesions to the medial preoptic nucleus differentially affect singing and nest box-directed behaviors within and outside of the breeding season in European starlings (Sturnus vulgaris). Behav Neurosci., 120, 1326e1336. Alger, S. J., Maasch, S. N., & Riters, L. V. (2009). Lesions to the medial preoptic nucleus affect immediate early gene immunolabeling in brain regions involved in song control and social behavior in male European starlings. European Journal of Neuroscience, 29, 970e982. Appeltants, D., Ball, G. F., & Balthazart, J. (2003). Song activation by testosterone is associated with an increased catecholaminergic

innervation of the song control system in female canaries. Neuroscience, 121, 801e814. Appeltants, D., Ball, G. F., & Balthazart, J. (2004). Catecholaminergic inputs to aromatase cells in the canary auditory forebrain. Neuroreport, 15, 1727e1730. Appeltants, D., Del Negro, C., & Balthazart, J. (2002). Noradrenergic control of auditory information processing in female canaries. Behav Brain Res., 133, 221e235. Arnold, A. P. (1975). The effects of castration and androgen replacement on song, courtship, and aggression in zebra finches (Poephila guttata). J Exp Zool., 191, 309e326. Arnold, A. P., Nottebohm, F., & Pfaff, D. W. (1976). Hormone concentrating cells in vocal control and other areas of the brain of the zebra finch (Poephila guttata). J Comp Neurol., 165, 487e511. Askew, J. A., Georgiou, G. C., Sharp, P. J., & Lea, R. W. (1997). Localization of progesterone receptor in brain and pituitary of the ring dove: influence of breeding cycle and estrogen. Horm Behav., 32, 105e113. Aste, N., Panzica, G. C., Viglietti-Panzica, C., Harada, N., & Balthazart, J. (1998). Distribution and effects of testosterone on aromatase mRNA in the quail forebrain: a non-radioactive in-situ hybridization study. J Chem Neuroanat., 14, 103e115. Baillien, M., & Balthazart, J. (1997). A direct dopaminergic control of aromatase activity in the quail preoptic area. J Steroid Biochem Mol Biol., 63, 99e113. Ball, G. F. (1990). Chemical neuroanatomical studies of the steroidsensitive songbird vocal control system: A comparative approach. In J. Balthazart (Ed.), Hormones, Brain and Behavior in Vertebrates, Vol. 8. Basel, Switzerland: Karger. Ball, G. F., & Balthazart, J. (1990). Steroid modulation of muscarinic cholinergic and alpha2-adrenergic receptor density in the nucleus intercollicularis of the Japanese quail. Eur J Neurosci., 2, 828e835. Ball, G. F., & Balthazart, J. (2002). Neuroendocrine mechanisms regulating reproductive cycles and reproductive behavior in birds. In D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach, & R. T. Rubin (Eds.), Hormones, Brain and Behavior, Vol. 2 (pp. 649e798). Academic Press. Ball, G. F., & Balthazart, J. (2004). Hormonal regulation of brain circuits mediating male sexual behavior in birds. Physiol Behav., 83, 329e346. Ball, G. F., & Ketterson, E. D. (2008). Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philos Trans R Soc Lond B Biol Sci., 363, 231e246. Ball, G. F., Bernard, D. J., Foidart, A., Lakaye, B., & Balthazart, J. (1999). Steroid sensitive sites in the avian brain: does the distribution of the estrogen receptor alpha and beta types provide insight into their function? Brain Behav Evol., 54, 28e40. Ball, G. F., Riters, L. V., MacDougall-Shackleton, S. A., & Balthazart, J. (2008). Sex differences in brain and behavior and the neuroendocrine control of the motivation to sing. In H. P. Zeigler, & P. Marler (Eds.), Neuroscience of Birdsong. (pp. 320e331). New York, NY: Cambridge University Press. Balthazart, J. (1991). Testosterone metabolism in the avian hypothalamus. J Steroid Biochem Mol Biol., 40, 557e570. Balthazart, J., & Absil, P. (1997). Identification of catecholaminergic inputs to and outputs from aromatase-containing brain areas of the Japanese quail by tract tracing combined with tyrosine hydroxylase immunocytochemistry. J Comp Neurol., 382, 401e428.

Chapter | 6

Hormonal Regulation of Avian Courtship and Mating Behaviors

Balthazart, J., & Foidart, A. (1993). Brain aromatase and the control of male sexual behavior. J Steroid Biochem Mol Biol., 44, 521e540. Balthazart, J., & Hendrick, J. (1976). Annual variation in reproductive behavior, testosterone, and plasma FSH levels in the Rouen duck, Anas platyrhynchos. Gen Comp Endocrinol., 28, 171e183. Balthazart, J., & Surlemont, C. (1990a). Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol Behav., 48, 599e609. Balthazart, J., & Surlemont, C. (1990b). Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail POA. Brain Res Bull., 25, 7e14. Balthazart, J., Absil, P., Foidart, A., Houbart, M., Harada, N., & Ball, G. F. (1996). Distribution of aromatase-immunoreactive cells in the forebrain of zebra finches (Taeniopygia guttata): implications for the neural action of steroids and nuclear definition in the avian hypothalamus. J Neurobiol., 31, 129e148. Balthazart, J., Absil, P., Gerard, M., Appeltants, D., & Ball, G. F. (1998). Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J Neurosci., 18, 6512e6527. Balthazart, J., Baillien, M., & Ball, G. F. (2002). Interactions between aromatase (estrogen synthase) and dopamine in the control of male sexual behavior in quail. Comp Biochem Physiol B Biochem Mol Biol., 132, 37e55. Balthazart, J., Baillien, M., Cornil, C. A., & Ball, G. F. (2004). Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol Behav., 83, 247e270. Balthazart, J., Castagna, C., & Ball, G. F. (1997a). Aromatase inhibition blocks the activation and sexual differentiation of appetitive male sexual behavior in Japanese quail. Behav Neurosci., 111, 381e397. Balthazart, J., Castagna, C., & Ball, G. F. (1997b). Differential effects of D1 and D2 dopamine-receptor agonists and antagonists on appetitive and consummatory aspects of male sexual behavior in Japanese quail. Physiol Behav., 62, 571e580. Balthazart, J., Dupiereux, V., Aste, N., Viglietti-Panzica, C., Barrese, M., & Panzica, G. C. (1994). Afferent and efferent connections of the sexually dimorphic medial preoptic nucleus of the male quail revealed by in-vitro transport of DiI. Cell Tissue Res., 276, 455e475. Balthazart, J., Evrard, L., & Surlemont, C. (1990). Effects of the nonsteroidal inhibitor R76713 on testosterone-induced sexual behavior in the Japanese quail. (Coturnix coturnix japonica). Horm. Behav., 24, 510e531. Balthazart, J., Foidart, A., & Harada, N. (1990). Immunocytochemical localization of aromatase in the brain. Brain Res., 514, 327e333. Balthazart, J., Foidart, A., Houbart, M., Prins, G. S., & Ball, G. F. (1998). Distribution of androgen receptor-immunoreactive cells in the quail forebrain and their relationship with aromatase immunoreactivity. J Neurobiol., 35, 323e340. Balthazart, J., Foidart, A., Wilson, E. M., & Ball, G. F. (1992). Immunocytochemical localization of androgen receptors in the male songbird and quail brain. J Comp Neurol., 317, 407e420. Balthazart, J., Gahr, M., & Surlemont, C. (1989). Distribution of estrogen receptors in the brain of the Japanese quail: an immunocytochemical study. Brain Res., 501, 205e214. Balthazart, J., Libioulle, J. M., & Sante, P. (1988). Stimulatory effects of the noradrenergic neurotoxin DSP4 on sexual behavior in male quail. Behavioural Processes, 17, 27e44.

173

Balthazart, J., Malacarne, G., & Deviche, P. (1981). Stimulatory effects of 5 beta-dihydrotestosterone on the sexual behavior in the domestic chick. Horm Behav., 15, 246e258. Balthazart, J., Reid, J., Absil, P., Foidart, A., & Ball, G. F. (1995). Appetitive as well as consummatory aspects of male sexual behavior in quail are activated by androgens and estrogens. Behav Neurosci., 109, 485e501. Balthazart, J., Schumacher, M., & Evrard, L. (1990). Sex differences and steroid control of testosterone-metabolizing enzyme activity in the quail brain. J Neuroendocrinol., 2, 675e683. Balthazart, J., Schumacher, M., & Malacarne, G. (1984). Relative potencies of testosterone and 5 alpha-dihydrotestosterone on crowing and cloacal gland growth in the Japanese quail (Coturnix coturnix japonica). J Endocrinol., 100, 19e23. Balthazart, J., Surlemont, C., & Harada, N. (1992). Aromatase as a cellular marker of testosterone action in the preoptic area. Physiol Behav., 51, 395e409. Barclay, S. R., & Harding, C. F. (1988). Androstenedione modulation of monoamine levels and turnover in hypothalamic and vocal control nuclei in the male zebra finch: steroid effects on brain monoamines. Brain Res., 459, 333e343. Barclay, S. R., & Harding, C. F. (1990). Differential modulation of monoamine levels and turnover rates by estrogen and/or androgen in hypothalamic and vocal control nuclei of male zebra finches. Brain Res., 523, 251e262. Barfield, R. J. (1971). Activation of sexual and aggressive behavior by androgen implanted into the male ring dove brain. Endocrinology, 89, 1470e1476. Barfield, R. J., Ronay, G., & Pfaff, D. W. (1978). Autoradiographic localization of androgen-concentrating cells in the brain of the male domestic fowl. Neuroendocrinology, 26, 297e311. Baulieu, E. E. (1997). Neurosteroids: of the nervous system, by the nervous system, for the nervous system. Recent Prog Horm Res., 52, 1e32. Bazzett, T. J., & Becker, J. B. (1994). Sex differences in the rapid and acute effects of estrogen on striatal D2 dopamine receptor binding. Brain Res., 637, 163e172. Beach, F. A. (1956). Characteristics of masculine “sex drive”. In M. R. Jones (Ed.), Nebraska symposium on motivation, Vol. 4 (pp. 1e32). Lincoln, NE: University of Nebraska Press. Beach, F. A., & Inman, N. G. (1965). Effects of castration and androgen replacement on mating in male quail. Proc Natl Acad Sci USA, 54, 1426e1431. Becker, J. B. (1999). Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav., 64, 803e812. Belle, M. D., & Lea, R. W. (2001). Androgen receptor immunolocalization in brains of courting and brooding male and female ring doves (Streptopelia risoria). Gen Comp Endocrinol., 124, 173e187. Belle, M. D., Sharp, P. J., & Lea, R. W. (2005). Aromatase inhibition abolishes courtship behaviours in the ring dove (Streptopelia risoria) and reduces androgen and progesterone receptors in the hypothalamus and anterior pituitary gland. Mol Cell Biochem., 276, 193e204. Belle, M. D., Tsutsui, K., & Lea, R. W. (2003). Sex steroid communication in the ring dove brain during courtship. Can J Physiol Pharmacol., 81, 359e370. Bentley, G. E., Jensen, J. P., Kaur, G. J., Wacker, D. W., Tsutsui, K., & Wingfield, J. C. (2006). Rapid inhibition of female sexual behavior by

174

gonadotropin-inhibitory hormone (GnIH). Horm Behav., 49, 550e555. Bentley, G. E., Wingfield, J. C., Morton, M. L., & Ball, G. F. (2000). Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song. Horm Behav., 37, 179e189. Bernard, D. J., Bentley, G. E., Balthazart, J., Turek, F. W., & Ball, G. F. (1999). Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinology, 140, 4633e4643. Berthold, A. A. (1849). Transplantation der Hoden. Arch Anat Physiol Wissenschr. Med., 42e46. Blaustein, J. D., & Wade, G. N. (1977a). Concurrent inhibition of sexual behavior, but not brain [3H]estradiol uptake, by progesterone in female rats. J Comp Physiol Psychol., 91, 742e751. Blaustein, J. D., & Wade, G. N. (1977b). Sequential inhibition of sexual behavior by progesterone in female rats: comparison with a synthetic antiestrogen. J Comp Physiol Psychol., 91, 752e760. Bottjer, S. W., & Johnson, F. (1997). Circuits, hormones, and learning: vocal behavior in songbirds. J Neurobiol., 33, 602e618. Bottjer, S. W., Miesner, E. A., & Arnold, A. P. (1984). Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science, 224, 901e903. Brenowitz, E. A. (1991). Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science, 251, 303e305. Brenowitz, E. A., & Arnold, A. P. (1989). Accumulation of estrogen in a vocal control brain region of a duetting song bird. Brain Res., 480, 119e125. Brockway, B. F. (1965). Stimulation of ovarian development and egg laying by male courtship vocalization in budgerigars (Melopsittacus undulatus). Anim Behav., 13, 575e578. Burt, J. M., Lent, K. L., Beecher, M. D., & Brenowitz, E. A. (2000). Lesions of the anterior forebrain song control pathway in female canaries affect song perception in an operant task. J Neurobiol., 42, 1e13. Can, A., Domjan, M., & Delville, Y. (2007). Sexual experience modulates neuronal activity in male Japanese quail. Horm Behav., 52, 590e599. Castagna, C., Absil, P., Foidart, A., & Balthazart, J. (1998). Systemic and intracerebroventricular injections of vasotocin inhibit appetitive and consummatory components of male sexual behavior in Japanese quail. Behav Neurosci., 112, 233e250. Catchpole, C., & Slater, P. J. B. (1995). Bird song: biological themes and variations. New York NY: Cambridge University Press. Cambridge, [England]. Charlier, T. D., Ball, G. F., & Balthazart, J. (2005). Sexual behavior activates the expression of the immediate early genes c-fos and Zenk (egr-1) in catecholaminergic neurons of male Japanese quail. Neuroscience, 131, 13e30. Cheng, M. (1973a). Effect of estrogen on behavior of ovariectomized ring doves (Streptopelia risoria). J Comp Physiol Psychol., 83, 234e239. Cheng, M. (1973b). Effect of ovariectomy on the reproductive behavior of female ring doves (Streptopelia risoria). J Comp Physiol Psychol., 83, 221e233. Cheng, M. F. (1974). Ovarian development in the female ring dove in response to stimulation by intact and castrated male ring doves. J Endocrinol., 63, 43e53.

Hormones and Reproduction of Vertebrates

Cheng, M. F. (1986). Female cooing promotes ovarian development in ring doves. Physiol Behav., 37, 371e374. Cheng, M. F. (2005). Audioevocal pathways controlling GnRH release. In A. Dawson, & P. J. Sharp (Eds.), Functional Avian Endocrinology (pp. 113e128). New Delhi, India: Narosa House. Cheng, M. F. (2008). The role of vocal self-stimulation in female responses to males: implications for state-reading. Horm Behav., 53, 1e10. Cheng, M. F., & Lehrman, D. (1975a). Gonadal hormone specificity in the sexual behavior of ring doves. Psychoneuroendocrinology, 1, 95e102. Cheng, M. F., & Lehrman, D. S. (1975b). Gonadal hormone specificity in the sexual behavior of ring doves. Psychoneuroendocrinology, 1, 95e102. Cheng, M. F., & Peng, J. P. (1997). Reciprocal talk between the auditory thalamus and the hypothalamus: an antidromic study. Neuroreport, 8, 653e658. Cheng, M. F., & Silver, R. (1975). Estrogen-progesterone regulation of nest-building and incubation behavior in ovariectomized ring doves (Streptopelia risoria). J Comp Physiol Psychol., 88, 256e263. Cheng, M. F., & Zuo, M. (1994). Proposed pathways for vocal selfstimulation: met-enkephalinergic projections linking the midbrain vocal nucleus, auditory-responsive thalamic regions and neurosecretory hypothalamus. J Neurobiol., 25, 361e379. Cheng, M. F., Desiderio, C., Havens, M., & Johnson, A. (1988). Behavioral stimulation of ovarian growth. Horm Behav., 22, 388e401. Cheng, M. F., Peng, J. P., & Johnson, P. (1998). Hypothalamic neurons preferentially respond to female nest coo stimulation: demonstration of direct acoustic stimulation of luteinizing hormone release. J Neurosci., 18, 5477e5489. Cohen, J., & Cheng, M. F. (1981). The role of the midbrain in courtship behavior of the female ring dove (Streptopelia risoria): evidence from radiofrequency lesion and hormone implant studies. Brain Res., 207, 279e301. Cornil, C. A., Holloway, K. S., Taziaux, M., & Balthazart, J. (2004). The effects of aromatase inhibition on testosterone-dependent conditioned rhythmic cloacal sphincter movements in male Japanese quail. Physiol Behav., 83, 99e105. Cornil, C. A., Taziaux, M., Baillien, M., Ball, G. F., & Balthazart, J. (2006). Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail. Horm Behav., 49, 45e67. Dawson, A. (1983). Plasma gonadal steroid levels in wild starlings (Sturnus vulgaris) during the annual cycle and in relation to the stages of breeding. Gen Comp Endocrinol., 49, 286e294. Dawson, A., King, V. M., Bentley, G. E., & Ball, G. F. (2001). Photoperiodic control of seasonality in birds. J Biol Rhythms, 16, 365e380. Day, L. B., Fusani, L., Hernandez, E., Billo, T. J., Sheldon, K. S., Wise, P. M., et al. (2007). Testosterone and its effects on courtship in golden-collared manakins (Manacus vitellinus): seasonal, sex, and age differences. Horm Behav., 51, 69e76. Day, L. B., McBroom, J. T., & Schlinger, B. A. (2006). Testosterone increases display behaviors but does not stimulate growth of adult plumage in male golden-collared manakins (Manacus vitellinus). Horm Behav., 49, 223e232. De Ridder, E., Pinxten, R., & Eens, M. (2000). Experimental evidence of a testosterone-induced shift from paternal to mating behavior in a facultatively polygynous songbird. Behav Ecol Sociobiol., 49, 24e30.

Chapter | 6

Hormonal Regulation of Avian Courtship and Mating Behaviors

Del Negro, C., Gahr, M., Leboucher, G., & Kreutzer, M. (1998). The selectivity of sexual responses to song displays: effects of partial chemical lesion of the HVC in female canaries. Behav Brain Res., 96, 151e159. Del Negro, C., Kreutzer, M., & Gahr, M. (2000). Sexually stimulating signals of canary (Serinus canaria) songs: evidence for a femalespecific auditory representation in the HVc nucleus during the breeding season. Behav Neurosci., 114, 526e542. Delville, Y., & Balthazart, J. (1987). Hormonal control of female sexual behavior in the Japanese quail. Horm Behav., 21, 288e309. Delville, Y., Sulon, J., Hendrick, J. C., & Balthazart, J. (1984). Effect of the presence of females on the pituitaryetesticular activity in male Japanese quail (Coturnix coturnix japonica). Gen Comp Endocrinol., 55, 295e305. Deviche, P., Bottoni, L., & Balthazart, J. (1982). 5 beta-Dihydrotestosterone is weakly androgenic in the adult Japanese quail (Coturnix coturnix japonica). Gen Comp Endocrinol., 48, 421e424. Doupe, A. J., & Solis, M. M. (1997). Song- and order-selective neurons develop in the songbird anterior forebrain during vocal learning. J Neurobiol., 33, 694e709. Dufty, A. M., Jr., & Wingfield, J. C. (1986). The influence of social cues on the reproductive endocrinology of male brown-headed cowbirds: field and laboratory studies. Horm Behav., 20, 222e234. Durand, S. E., Tepper, J. M., & Cheng, M. F. (1992). The shell region of the nucleus ovoidalis: a subdivision of the avian auditory thalamus. J Comp Neurol., 323, 495e518. Eens, M., Pinxten, R., & Verheyen, R. F. (1991). Male song as a cue for mate choice in the European starling. Behaviour, 116, 210e238. El Halawani, M. E., Silsby, J. L., Behnke, E. J., & Fehrer, S. C. (1986). Hormonal induction of incubation behavior in ovariectomized female turkeys (Meleagris gallopavo). Biol Reprod., 35, 59e67. Etgen, A. M., & Karkanias, G. B. (1994). Estrogen regulation of noradrenergic signaling in the hypothalamus. Psychoneuroendocrinology, 19, 603e610. Etgen, A. M., Chu, H. P., Fiber, J. M., Karkanias, G. B., & Morales, J. M. (1999). Hormonal integration of neurochemical and sensory signals governing female reproductive behavior. Behav Brain Res., 105, 93e103. Everitt, B. J. (1990). Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci Biobehav Rev., 14, 217e232. Everitt, B. J., & Stacey, P. (1987). Studies of instrumental behavior with sexual reinforcement in male rats (Rattus norvegicus): II. Effects of preoptic area lesions, castration, and testosterone. J Comp Psychol., 101, 407e419. Feder, H. H., Storey, A., Goodwin, D., Reboulleau, C., & Silver, R. (1977). Testosterone and “5alpha-dihydrotestosterone” levels in peripheral plasma of male and female ring doves (Streptopelia risoria) during and reproductive cycle. Biol Reprod., 16, 666e677. Fivizzani, A. J., & Oring, L. W. (1986). Plasma steroid hormones in relation to behavioral sex role reversal in the spotted sandpiper, Actitis macularia. Biol Reprod., 35, 1195e1201. Fivizzani, A. J., Colwell, M. A., & Oring, L. W. (1986). Plasma steroid hormone levels in free-living Wilson’s phalaropes, Phalaropus tricolor. Gen Comp Endocrinol., 62, 137e144. Foidart, A., Lakaye, B., Grisar, T., Ball, G. F., & Balthazart, J. (1999). Estrogen receptor-beta in quail: cloning, tissue expression and neuroanatomical distribution. J Neurobiol., 40, 327e342.

175

Foidart, A., Reid, J., Absil, P., Yoshimura, N., Harada, N., & Balthazart, J. (1995). Critical re-examination of the distribution of aromataseimmunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme. J Chem Neuroanat., 8, 267e282. Foidart, A., Silverin, B., Baillien, M., Harada, N., & Balthazart, J. (1998). Neuroanatomical distribution and variations across the reproductive cycle of aromatase activity and aromatase-immunoreactive cells in the pied flycatcher (Ficedula hypoleuca). Horm Behav., 33, 180e196. Forlano, P. M., Schlinger, B. A., & Bass, A. H. (2006). Brain aromatase: new lessons from non-mammalian model systems. Front Neuroendocrinol., 27, 247e274. Friedman, M. B. (1977). Interactions between visual and vocal courtship stimuli in the neuroendocrine response of female doves. J. Comp. Physiol. Psychol., 91, 1408e1416. Frye, C. A. (2001). The role of neurosteroids and non-genomic effects of progestins and androgens in mediating sexual receptivity of rodents. Brain Res Brain Res Rev., 37, 201e222. Frye, C. A., Bayon, L. E., Pursnani, N. K., & Purdy, R. H. (1998). The neurosteroids, progesterone and 3alpha,5alpha-THP, enhance sexual motivation, receptivity, and proceptivity in female rats. Brain Res., 808, 72e83. Fusani, L. (2008). Testosterone control of male courtship in birds. Horm Behav., 54, 227e233. Fusani, L., & Gahr, M. (2006). Hormonal influence on song structure and organization: the role of estrogen. Neuroscience, 138, 939e946. Fusani, L., Beani, L., & Dessi-Fulgheri, F. (1994). Testosterone affects the acoustic structure of the male call in the grey partridge (Perdix perdix). Behaviour, 128, 301e310. Fusani, L., Gahr, M., & Hutchison, J. B. (2001). Aromatase inhibition reduces specifically one display of the ring dove courtship behavior. Gen Comp Endocrinol., 122, 23e30. Fusani, L., Van’t Hof, T., Hutchison, J. B., & Gahr, M. (2000). Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens. J Neurobiol., 43, 254e268. Gahr, M. (2000). Neural song control system of hummingbirds: comparison to swifts, vocal learning (songbirds) and nonlearning (suboscines) passerines, and vocal learning (budgerigars) and nonlearning (dove, owl, gull, quail, chicken) nonpasserines. J Comp Neurol., 426, 182e196. Gahr, M., & Balaban, E. (1996). The development of a species difference in the local distribution of brain estrogen receptive cells. Brain Res Dev Brain Res., 92, 182e189. Gahr, M., & Metzdorf, R. (1997). Distribution and dynamics in the expression of androgen and estrogen receptors in vocal control systems of songbirds. Brain Res Bull., 44, 509e517. Gahr, M., & Wild, J. M. (1997). Localization of androgen receptor mRNA-containing cells in avian respiratory-vocal nuclei: an in-situ hybridization study. J Neurobiol., 33, 865e876. Gahr, M., Guttinger, H. R., & Kroodsma, D. E. (1993). Estrogen receptors in the avian brain: survey reveals general distribution and forebrain areas unique to songbirds. J Comp Neurol., 327, 112e122. Gentner, T. Q. (2004). Neural systems for individual song recognition in adult birds. Ann NY Acad Sci., 1016, 282e302. Gentner, T. Q., & Hulse, S. H. (2000). Female European starling preference and choice for variation in conspecific male song. Anim Behav., 59, 443e458.

176

Gibson, M. J., & Cheng, M. F. (1979). Neural mediation of estrogendependent courtship behavior in female ring doves. J. Comp. Physiol. Psychol., 93, 855e867. Godwin, J., Hartman, V., Grammer, M., & Crews, D. (1996). Progesterone inhibits female-typical receptive behavior and decreases hypothalamic estrogen and progesterone receptor messenger ribonucleic acid levels in whiptail lizards (genus Cnemidophorus). Horm Behav., 30, 138e144. Gonzalez-Mariscal, G., Melo, A. I., & Beyer, C. (1993). Progesterone, but not LHRH or prostaglandin E2, induces sequential inhibition of lordosis to various lordogenic agents. Neuroendocrinology, 57, 940e945. Goodson, J. L. (2005). The vertebrate social behavior network: evolutionary themes and variations. Horm Behav., 48, 11e22. Goymann, W., & Wingfield, J. C. (2004). Competing females and caring males. Sex steroids in African black coucals, Centropus grillii. Anim. Behav., 68, 733e740. Goymann, W., Moore, I. T., Scheuerlein, A., Hirschenhauser, K., Grafen, A., & Wingfield, J. C. (2004). Testosterone in tropical birds: effects of environmental and social factors. Am Nat., 164, 327e334. Gratto-Trevor, C. L., Fivizzani, A. J., Oring, L. W., & Cooke, F. (1990). Seasonal changes in gonadal steroids of a monogamous versus a polyandrous shorebird. Gen Comp Endocrinol., 80, 407e418. Griffin, C., Flouriot, G., Sharp, P., Greene, G., & Gannon, F. (2001). Distribution analysis of the two chicken estrogen receptor-alpha isoforms and their transcripts in the hypothalamus and anterior pituitary gland. Biol Reprod., 65, 1156e1163. Gwinner, H., & Gwinner, E. (1994). Effects of testosterone on nest-box occupation and associated behaviours by male European starlings (Sturnus vulgaris). Behaviour, 129, 141e148. Gwinner, H., Van’t Hof, T., & Zeman, M. (2002). Hormonal and behavioral responses of starlings during a confrontation with males or females at nest boxes during the reproductive season. Horm Behav., 42, 21e31. Haase, E., Sharp, P. J., & Paulke, E. (1975). Annual cycle of plasma luteinizing hormone concentrations in wild mallard drakes. J Exp Zool., 194, 553e558. Halldin, K., Axelsson, J., Holmgren, C., & Brunstrom, B. (2006). Localization of estrogen receptor-alpha and -betamRNA in brain areas controlling sexual behavior in Japanese quail. J Neurobiol., 66, 148e154. Hamilton, K. S., King, A. P., Sengelaub, D. R., & West, M. J. (1997). A brain of her own: a neural correlate of song assessment in a female songbird. Neurobiol Learn Mem., 68, 325e332. Harding, C. F., & Rowe, S. A. (2003). Vasotocin treatment inhibits courtship in male zebra finches; concomitant androgen treatment inhibits this effect. Horm Behav., 44, 413e418. Harding, C. F., Sheridan, K., & Walters, M. J. (1983). Hormonal specificity and activation of sexual behavior in male zebra finches. Horm Behav., 17, 111e133. Harding, C. F., Walters, M. J., Collado, D., & Sheridan, K. (1988). Hormonal specificity and activation of social behavior in male redwinged blackbirds. Horm Behav., 22, 402e418. Harding, C. F., Walters, M. J., & Parsons, B. (1984). Androgen receptor levels in hypothalamic and vocal control nuclei in the male zebra finch. Brain Res., 306, 333e339. Hau, M., Gill, S. A., & Goymann, W. (2008). Tropical field endocrinology: ecology and evolution of testosterone concentrations in male birds. Gen Comp Endocrinol., 157, 241e248.

Hormones and Reproduction of Vertebrates

Hegner, R. E., & Wingfield, J. C. (1986). Behavioral and endocrine correlates of multiple brooding in the semicolonial house sparrow Passer domesticus. II. Females. Horm Behav., 20, 313e326. Heimovics, S. A., & Riters, L. V. (2005). Immediate early gene activity in song control nuclei and brain areas regulating motivation relates positively to singing behavior during, but not outside of, a breeding context. J Neurobiol., 65, 207e224. Heimovics, S. A., & Riters, L. V. (2006). Breeding-context-dependent relationships between song and cFOS labeling within social behavior brain regions in male European starlings (Sturnus vulgaris). Horm Behav., 50, 726e735. Heimovics, S. A., & Riters, L. V. (2007). ZENK labeling within social behavior brain regions reveals breeding context-dependent patterns of neural activity associated with song in male European starlings (Sturnus vulgaris). Behav Brain Res., 176, 333e343. Hessler, N. A., & Doupe, A. J. (1999). Social context modulates singingrelated neural activity in the songbird forebrain. Nat Neurosci., 2, 209e211. Hinde, R. A., & Steel, E. A. (1978). The influence of daylength and male vocalizations on the estrogen-dependent behavior of female canaries and budgerigars, with discussion of data from other species. Adv. Study Behav., 8, 39e73. Hull, E. M., Bitran, D., Pehek, E. A., Warner, R. K., Band, L. C., & Holmes, G. M. (1986). Dopaminergic control of male sex behavior in rats: effects of an intracerebrally-infused agonist. Brain Res., 370, 73e81. Hull, E. M., Du, J., Lorrain, D. S., & Matuszewich, L. (1995). Extracellular dopamine in the medial preoptic area: implications for sexual motivation and hormonal control of copulation. J Neurosci., 15, 7465e7471. Hutchison, J. B. (1970a). Differential effects of testosterone and oestradiol on male courtship in Barbary doves (Streptopelia risoria). Anim. Behav., 18, 41e51. Hutchison, J. B. (1970b). Influence of gonadal hormones on the hypothalamic integration of courtship behaviour in the Barbary dove. J Reprod Fertil, (Suppl. 11) 15þ. Hutchison, J. B. (1971). Effects of hypothalamic implants of gonadal steroids on courtship behaviour in Barbary doves (Streptopelia risoria). J Endocrinol., 50, 97e113. Hutchison, J. B. (1993). Aromatase: neuromodulator in the control of behavior. J Steroid Biochem Mol Biol., 44, 509e520. Hutchison, J. B., & Steimer, T. (1981). Brain 5beta-reductase: a correlate of behavioral sensitivity to androgen. Science, 213, 244e246. Hutchison, J. B., & Steimer, T. (1984). Androgen metabolism in the brain: behavioural correlates. Prog Brain Res., 61, 23e51. Hutchison, J. B., & Steimer, T. (1985). Preoptic formation of 17 betaoestradiol is influenced by behavioural stimuli in the dove. Brain Res., 360, 366e369. Hutchison, J. B., Steimer, T., & Duncan, R. (1981). Behavioural action of androgen in the dove: effects of long-term castration on response specificity and brain aromatization. J Endocrinol., 90, 167e178. Hutchison, J. B., Steimer, T. J., & Hutchison, R. E. (1986). Formation of behaviorally active estrogen in the dove brain: induction of preoptic aromatase by intracranial testosterone. Neuroendocrinology, 43, 416e427. Hutchison, R. E., Wozniak, A. W., & Hutchison, J. B. (1992). Regulation of female brain aromatase activity during the reproductive cycle of the dove. J Endocrinol., 134, 385e396.

Chapter | 6

Hormonal Regulation of Avian Courtship and Mating Behaviors

Jacobs, E. C., Arnold, A. P., & Campagnoni, A. T. (1996). Zebra finch estrogen receptor cDNA: cloning and mRNA expression. J Steroid Biochem Mol Biol., 59, 135e145. Jarvis, E. D., Scharff, C., Grossman, M. R., Ramos, J. A., & Nottebohm, F. (1998). For whom the bird sings: context-dependent gene expression. Neuron, 21, 775e788. Karavolas, H. J., & Hodges, D. R. (2007). Neuroendocrine metabolism of progesterone and related progestins. In K. W. Derek Chadwick (Ed.), Ciba Foundation Symposium 153-Steroids and Neuronal Activity, (pp. 22e55). Karkanias, G. B., & Etgen, A. M. (1993). Estradiol attenuates alpha 2adrenoceptor-mediated inhibition of hypothalamic norepinephrine release. J Neurosci., 13, 3448e3455. Karkanias, G. B., & Etgen, A. M. (1994). Estradiol reduction of the agonist high affinity form of the alpha 2-adrenoceptor in the hypothalamus of female rats: identification as the alpha 2D subtype. Mol Pharmacol., 45, 509e516. Karkanias, G. B., Li, C. S., & Etgen, A. M. (1997). Estradiol reduction of alpha 2-adrenoceptor binding in female rat cortex is correlated with decreases in alpha 2A/D-adrenoceptor messenger RNA. Neuroscience, 81, 593e597. Kawashima, M., Kamiyoshi, M., & Tanaka, K. (1987). Presence of estrogen receptors in the hen hypothalamus and pituitary. Endocrinology, 120, 582e588. Kelly, M. J., Qiu, J., Wagner, E. J., & Ronnekleiv, O. K. (2002). Rapid effects of estrogen on G protein-coupled receptor activation of potassium channels in the central nervous system (CNS). J Steroid Biochem Mol Biol., 83, 187e193. King, J. A., Barkley, R. A., Delville, Y., & Ferris, C. F. (2000). Early androgen treatment decreases cognitive function and catecholamine innervation in an animal model of ADHD. Behav Brain Res., 107, 35e43. King, J. A., Kelly, T. A., & Delville, Y. (2000). Adult levels of testosterone alter catecholamine innervation in an animal model of attention-deficit hyperactivity disorder. Neuropsychobiology, 42, 163e168. Konishi, H., Foster, R. G., & Follett, B. K. (1987). Evidence for a daily rhythmicity in the acute release of luteinizing hormone in response to electrical stimulation in the Japanese quail. J Comp Physiol [A]., 161, 315e319. Kotegawa, T., Abe, T., & Tsutsui, K. (1997). Inhibitory role of opioid peptides in the regulation of aggressive and sexual behaviors in male Japanese quails. J Exp Zool., 277, 146e154. Krege, J. H., Hodgin, J. B., Couse, J. F., Enmark, E., Warner, M., Mahler, J. F., et al. (1998). Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci USA, 95, 15677e15682. Kritzer, M. F. (2000). Effects of acute and chronic gonadectomy on the catecholamine innervation of the cerebral cortex in adult male rats: insensitivity of axons immunoreactive for dopamine-beta-hydroxylase to gonadal steroids, and differential sensitivity of axons immunoreactive for tyrosine hydroxylase to ovarian and testicular hormones. J Comp Neurol., 427, 617e633. Kritzer, M. F. (2003). Long-term gonadectomy affects the density of tyrosine hydroxylase- but not dopamine-beta-hydroxylase-, choline acetyltransferase- or serotonin-immunoreactive axons in the medial prefrontal cortices of adult male rats. Cereb Cortex, 13, 282e296.

177

Kritzer, M. F., Adler, A., & Bethea, C. L. (2003). Ovarian hormone influences on the density of immunoreactivity for tyrosine hydroxylase and serotonin in the primate corpus striatum. Neuroscience, 122, 757e772. Kritzer, M. F., Adler, A., Marotta, J., & Smirlis, T. (1999). Regionally selective effects of gonadectomy on cortical catecholamine innervation in adult male rats are most disruptive to afferents in prefrontal cortex. Cereb Cortex, 9, 507e518. Kroodsma, D. E. (1976). Reproductive development in a female songbird: differential stimulation by quality of male song. Science, 192, 574e575. Kuiper, G. G., Enmark, E., Pelto-Huikko, M., Nilsson, S., & Gustafsson, J. A. (1996). Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA, 93, 5925e5930. Kuiper, G. G., Shughrue, P. J., Merchenthaler, I., & Gustafsson, J. A. (1998). The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front Neuroendocrinol., 19, 253e286. Lea, R. W., Clark, J. A., & Tsutsui, K. (2001). Changes in central steroid receptor expression, steroid synthesis, and dopaminergic activity related to the reproductive cycle of the ring dove. Microsc Res Tech., 55, 12e26. LeBlanc, M. M., Goode, C. T., MacDougall-Shackleton, E. A., & Maney, D. L. (2007). Estradiol modulates brainstem catecholaminergic cell groups and projections to the auditory forebrain in a female songbird. Brain Res., 1171, 93e103. Leboucher, G., Beguin, N., Lacroix, A., & Kreutzer, M. (2000). Progesterone inhibits female courtship behavior in domestic canaries (Serinus canaria). Horm Behav., 38, 123e129. Leboucher, G., Beguin, N., Mauget, R., & Kreutzer, M. (1998). Effects of fadrozole on sexual displays and reproductive activity in the female canary. Physiol Behav., 65, 233e240. Leitner, S., & Catchpole, C. K. (2002). Female canaries that respond and discriminate more between male songs of different quality have a larger song control nucleus (HVC) in the brain. J Neurobiol., 52, 294e301. Leitner, S., Voigt, C., Metzdorf, R., & Catchpole, C. K. (2005). Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J Neurobiol., 64, 275e284. Liu, Y. C., Salamone, J. D., & Sachs, B. D. (1997). Lesions in medial preoptic area and bed nucleus of stria terminalis: differential effects on copulatory behavior and noncontact erection in male rats. J Neurosci., 17, 5245e5253. MacLusky, N. J., & Naftolin, F. (1981). Sexual differentiation of the central nervous system. Science, 211, 1294e1302. Maney, D. L., Bernard, D. J., & Ball, G. F. (2001). Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem. Neurosci Lett., 311, 189e192. Maney, D. L., Cho, E., & Goode, C. T. (2006). Estrogen-dependent selectivity of genomic responses to birdsong. Eur J Neurosci., 23, 1523e1529. Maney, D. L., Goode, C. T., Lange, H. S., Sanford, S. E., & Solomon, B. L. (2008). Estradiol modulates neural responses to song in a seasonal songbird. J Comp Neurol., 511, 173e186. Margoliash, D. (1997). Functional organization of forebrain pathways for song production and perception. J Neurobiol., 33, 671e693. Martinez-Vargas, M. C., Stumpf, W. E., & Sar, M. (1976). Anatomical distribution of estrogen target cells in the avian CNS: a comparison with the mammalian CNS. J Comp Neurol., 167, 83e103.

178

Matsunaga, E., & Okanoya, K. (2008). Vocal area-related expression of the androgen receptor in the budgerigar (Melopsittacus undulatus) brain. Brain Res., 1208, 87e94. McEwen, B. S., & Alves, S. E. (1999). Estrogen actions in the central nervous system. Endocr Rev., 20, 279e307. Meddle, S. L., Foidart, A., Wingfield, J. C., Ramenofskyand, M., & Balthazart, J. (1999). Effects of sexual interactions with a male on fos-like immunoreactivity in the female quail brain. J Neuroendocrinol., 11, 771e784. Meddle, S. L., King, V. M., Follett, B. K., Wingfield, J. C., Ramenofsky, M., Foidart, A., et al. (1997). Copulation activates Foslike immunoreactivity in the male quail forebrain. Behavioural Brain Research, 85, 143e159. Metzdorf, R., Gahr, M., & Fusani, L. (1999). Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds. J Comp Neurol., 407, 115e129. Montagu, G. (1802). Ornithological Dictionary. London, UK: J. White. Montgomerie, R., & Briskie, J. (2007). Anatomy and evolution of copulatory structures. In B. G. M. Jamieson (Ed.), Reproductive Biology and Phylogeny of Birds, Vol. 6A (pp. 116e179). Enfield, NH: Science Publishers. Montgomerie, R., & Doucet, S. M. (2007). Courtship and Copulation. In B. G. M. Jamieson (Ed.), Reproductive Biology and Phylogeny of Birds, Vol. 6B (pp. 161e238). Enfield, NH: Science Publishers. Moore, M. C. (1982). Hormonal response of free-living male whitecrowned sparrows to experimental manipulation of female sexual behavior. Horm Behav., 16, 323e329. Moore, M. C. (1983). Effect of female sexual displays on the endocrine physiology and behavior of male white-crowned sparrows, Zonotrichia leucophrys. Journal of Zoology (London), 199, 137e148. Morrell, J. I., Kelley, D. B., & Pfaff, D. W. (1975). Sex steroid binding in the brain of vertebrates. In K. M. Knigge, D. E. Scott, H. Kobayashi, S. Miura, & S. Ishii (Eds.), Brain-endocrine interactions II (pp. 230e256). Basel, Switzerland: Karger. Mountjoy, D. J., & Lemon, R. E. (1995). Female choice for complex song in the European starling. Behavioral Ecology and Sociobiology, 38, 65e71. Newman, S. W. (1999). The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann NY Acad Sci., 877, 242e257. Noble, R. (1972). The effects of estrogen and progesterone on copulation in female quail (Coturnix coturnix japonica) housed in continuous dark. Horm Behav., 3, 199e204. Nordeen, K. W., Nordeen, E. J., & Arnold, A. P. (1986). Estrogen establishes sex differences in androgen accumulation in zebra finch brain. J Neurosci., 6, 734e738. Nordeen, K. W., Nordeen, E. J., & Arnold, A. P. (1987). Estrogen accumulation in zebra finch song control nuclei: implications for sexual differentiation and adult activation of song behavior. J Neurobiol., 18, 569e582. Nottebohm, F., Stokes, T. M., & Leonard, C. M. (1976). Central control of song in the canary, Serinus canarius. J Comp Neurol., 165, 457e486. O’Connell, M. E., Reboulleau, C., Feder, H. H., & Silver, R. (1981). Social interactions and androgen levels in birds. I. Female characteristics associated with increased plasma androgen levels in the male ring dove (Streptopelia risoria). Gen Comp Endocrinol, 44, 454e463. Panzica, G. C., Garcia-Ojeda, E., Viglietti-Panzica, C., Thompson, N. E., & Ottinger, M. A. (1996). Testosterone effects on vasotocinergic

Hormones and Reproduction of Vertebrates

innervation of sexually dimorphic medial preoptic nucleus and lateral septum during aging in male quail. Brain Res., 712, 190e198. Peters, A. (2002). Testosterone and the trade-off between mating and paternal effort in estrapair-mating superb fairy wrens. Animal Behaviour, 64, 103e112. Petitti, N., Karkanias, G. B., & Etgen, A. M. (1992). Estradiol selectively regulates alpha 1B-noradrenergic receptors in the hypothalamus and preoptic area. J Neurosci., 12, 3869e3876. Pfaff, D. W., Kow, L. M., Loose, M. D., & Flanagan-Cato, L. M. (2008). Reverse engineering the lordosis behavior circuit. Horm Behav., 54, 347e354. Pfaus, J. G., Damsma, G., Nomikos, G. G., Wenkstern, D. G., Blaha, C. D., Phillips, A. G., et al. (1990). Sexual behavior enhances central dopamine transmission in the male rat. Brain Res., 530, 345e348. Pinxten, R., De Ridder, E., Balthazart, J., & Eens, M. (2002). Contextdependent effects of castration and testosterone treatment on song in male European starlings. Horm Behav., 42, 307e318. Pinxten, R., De Ridder, E., & Eens, M. (2003). Female presence affects male behavior and testosterone levels in the European starling (Sturnus vulgaris). Horm Behav., 44, 103e109. Rissman, E. F., & Wingfield, J. C. (1984). Hormonal correlates of polyandry in the spotted sandpiper, Actitis macularia. Gen Comp Endocrinol., 56, 401e405. Riters, L. V., & Alger, S. J. (2004). Neuroanatomical evidence for indirect connections between the medial preoptic nucleus and the song control system: possible neural substrates for sexually motivated song. Cell Tissue Res., 316, 35e44. Riters, L. V., & Ball, G. F. (1999). Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris). Horm Behav., 36, 276e286. Riters, L. V., & Pawlisch, B. A. (2007). Evidence that norepinephrine influences responses to male courtship song and activity within song control regions and the ventromedial nucleus of the hypothalamus in female European starlings. Brain Research, 127e140. Riters, L. V., & Teague, D. P. (2003). The volumes of song control nuclei, HVC and lMAN, relate to differential behavioral responses of female European starlings to male songs produced within and outside of the breeding season. Brain Research., 978, 91e98. Riters, L. V., Absil, P., & Balthazart, J. (1998). Effects of brain testosterone implants on appetitive and consummatory components of male sexual behavior in Japanese quail. Brain Res Bull., 47, 69e79. Riters, L. V., Baillien, M., Eens, M., Pinxten, R., Foidart, A., Ball, G. F., et al. (2001). Seasonal variation in androgen-metabolizing enzymes in the diencephalon and telencephalon of the male European starling (Sturnus vulgaris). J Neuroendocrinol., 13, 985e997. Riters, L. V., Eens, M., Pinxten, R., Duffy, D. L., Balthazart, J., & Ball, G. F. (2000). Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm Behav., 38, 250e261. Riters, L. V., Olesen, K. M., & Auger, C. J. (2007). Evidence that female endocrine state influences catecholamine responses to male courtship song in European starlings. Gen Comp Endocrinol., 154, 137e149. Riters, L. V., Schroeder, M. B., Auger, C. J., Eens, M., Pinxten, R., & Ball, G. F. (2005). Evidence for opioid involvement in the regulation of song production in male European starlings. Behavioral Neuroscience, 119, 245e255. Riters, L. V., Teague, D. P., Schroeder, M. B., & Cummings, S. E. (2004). Vocal production in different social contexts relates to variation in

Chapter | 6

Hormonal Regulation of Avian Courtship and Mating Behaviors

immediate early gene immunoreactivity within and outside of the song control system. Behav Brain Res., 155, 307e318. Robinson, J. E., & Follett, B. K. (1982). Photoperiodism in Japanese quail: the termination of seasonal breeding by photorefractoriness. Proc R Soc Lond B Biol Sci., 215, 95e116. Saldanha, C. J., Popper, P., Micevych, P. E., & Schlinger, B. A. (1998). The passerine hippocampus is a site of high aromatase: inter- and intraspecies comparisons. Horm Behav., 34, 85e97. Schlinger, B. A., & Callard, G. V. (1987). A comparison of aromatase, 5 alpha-, and 5 beta- reductase activities in the brain and pituitary of male and female quail (C. c. japonica). J Exp Zool., 242, 171e180. Schlinger, B. A., & London, S. E. (2006). Neurosteroids and the songbird model system. J Exp Zoolog A Comp Exp Biol., 305, 743e748. Schlinger, B. A., Fivizzani, A. J., & Callard, G. V. (1989). Aromatase, 5 alpha- and 5 beta-reductase in brain, pituitary and skin of the sexrole reversed Wilson’s phalarope. J Endocrinol., 122, 573e581. Schroeder, M. B., & Riters, L. V. (2006). Pharmacological manipulations of dopamine and opioids have differential effects on sexually motivated song production in male European starlings. Physiology and Behavior, 88, 575e584. Schumacher, M., & Balthazart, J. (1983). The effects of testosterone and its metabolites on sexual behavior and morphology in male and female Japanese quail. Physiol Behav., 30, 335e339. Schumacher, M., & Balthazart, J. (1984). Sexual dimorphism in the hypothalamic metabolism of testosterone in the Japanese Quail (Coturnix coturnix japonica). Prog Brain Res., 61, 53e61. Schumacher, M., & Balthazart, J. (1986). Testosterone-induced brain aromatase is sexually dimorphic. Brain Res., 370, 285e293. Schumacher, M., & Balthazart, J. (1987). Neuroanatomical distribution of testosterone-metabolizing enzymes in the Japanese quail. Brain Res., 422, 137e148. Searcy, W. A. (1992). Measuring responses of female birds to male song. In P. K. McGregor (Ed.), Playback and studies of animal communication (pp. 175e189). New York, NY: Plenum Press. Searcy, W. A., & Capp, M. S. (1997). Estradiol dosage and the solicitation display assay in red-winged blackbirds. Condor, 99, 826e828. Searcy, W. A., & Marler, P. (1981). A test for responsiveness to song structure and programming in female sparrows. Science, 213, 926e928. Searcy, W. A., & Yasukawa, K. (1996). Song and female choice. In D. E. Kroodsma, & H. E. Miller (Eds.), Ecology and Evolution of Acoustic Communication in Birds (pp. 454e473). Ithaca, NY: Cornell University Press. Shimizu, H., & Bray, G. A. (1993). Effects of castration, estrogen replacement and estrus cycle on monoamine metabolism in the nucleus accumbens, measured by microdialysis. Brain Res., 621, 200e206. Silverin, B., & Westin, J. (1995). Influence of the opposite sex on photoperiodically induced LH and gonadal cycles in willow tit (Parus montanus). Horm Behav., 29, 207e215. Silverin, B., Baillien, M., Foidart, A., & Balthazart, J. (2000). Distribution of aromatase activity in the brain and peripheral tissues of passerine and nonpasserine avian species. Gen Comp Endocrinol., 117, 34e53. Simerly, R. B., Swanson, L. W., Handa, R. J., & Gorski, R. A. (1985). Influence of perinatal androgen on the sexually dimorphic distribution of tyrosine hydroxylase-immunoreactive cells and fibers in the anteroventral periventricular nucleus of the rat. Neuroendocrinology, 40, 501e510.

179

Smith, G. T., Brenowitz, E. A., Beecher, M. D., & Wingfield, J. C. (1997). Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J Neurosci., 17, 6001e6010. Smith, G. T., Brenowitz, E. A., & Prins, G. S. (1996). Use of PG-21 immunocytochemistry to detect androgen receptors in the songbird brain. J Histochem Cytochem., 44, 1075e1080. Sockman, K. W., & Salvante, K. G. (2008). The integration of song environment by catecholaminergic systems innervating the auditory telencephalon of adult female European starlings. Dev Neurobiol., 68, 656e668. Sockman, K. W., & Schwabl, H. (1999). Daily estradiol and progesterone levels relative to laying and onset of incubation in canaries. Gen Comp Endocrinol, 114, 257e268. Sohrabji, F., Nordeen, E. J., & Nordeen, K. W. (1990). Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. Behav Neural Biology, 53, 51e63. Soma, K. K., Hartman, V. N., Wingfield, J. C., & Brenowitz, E. A. (1999). Seasonal changes in androgen receptor immunoreactivity in the song nucleus HVc of a wild bird. J Comp Neurol., 409, 224e236. Soma, K. K., Schlinger, B. A., Wingfield, J. C., & Saldanha, C. J. (2003). Brain aromatase, 5 alpha-reductase, and 5 beta-reductase change seasonally in wild male song sparrows: relationship to aggressive and sexual behavior. J Neurobiol., 56, 209e221. Steimer, T., & Hutchison, J. B. (1980). Aromatization of testosterone within a discrete hypothalamic area associated with the behavioral action of androgen in the male dove. Brain Res., 192, 586e591. Steimer, T., & Hutchison, J. B. (1981a). Androgen increases formation of behaviourally effective oestrogen in dove brain. Nature, 292, 345e347. Steimer, T., & Hutchison, J. B. (1981b). Metabolic control of the behavioural action of androgens in the dove brain: testosterone inactivation by 5 beta-reduction. Brain Res., 209, 189e204. Sterling, R. J., Gasc, J. M., Sharp, P. J., Renoir, J. M., Tuohimaa, P., & Baulieu, E. E. (1987). The distribution of nuclear progesterone receptor in the hypothalamus and forebrain of the domestic hen. Cell Tissue Res., 248, 201e205. Stoehr, A. M., & Hill, G. E. (2000). Testosterone and the allocation of reproductive effort in male house finches (Carpodacus mexicanus). Behav Ecol Sociobiol., 48, 407e411. Stumpf, W. E., & Sar, M. (1978). Anatomical distribution of estrogen, androgen, progestin, corticoid and thyroid hormone target sites in the brain of mammals: phylogeny and ontogeny. Am. Zool., 18, 435e445. Taziaux, M., Cornil, C. A., & Balthazart, J. (2004). Aromatase inhibition blocks the expression of sexually-motivated cloacal gland movements in male quail. Behav Processes, 67, 461e469. Taziaux, M., Cornil, C. A., Dejace, C., Arckens, L., Ball, G. F., & Balthazart, J. (2006). Neuroanatomical specificity in the expression of the immediate early gene c-fos following expression of appetitive and consummatory male sexual behaviour in Japanese quail. Eur J Neurosci., 23, 1869e1887. Taziaux, M., Kahn, A., Moore, J., 3rd, Balthazart, J., & Holloway, K. S. (2008). Enhanced neural activation in brain regions mediating sexual responses following exposure to a conditioned stimulus that predicts copulation. Neuroscience, 151, 644e658. Taziaux, M., Lopez, J., Cornil, C. A., Balthazart, J., & Holloway, K. S. (2007). Differential c-fos expression in the brain of male Japanese

180

quail following exposure to stimuli that predict or do not predict the arrival of a female. Eur J Neurosci., 25, 2835e2846. Temple, S. A. (1974). Plasma testosterone titers during the annual reproductive cycle of starlings (Sturnus vulgaris). Gen Comp Endocrinol., 22, 470e479. Tennent, B. J., Smith, E. R., & Davidson, J. M. (1980). The effects of estrogen and progesterone on female rat proceptive behavior. Horm Behav., 14, 65e75. Theunissen, F. E., Amin, N., Shaevitz, S. S., Woolley, S. M., Fremouw, T., & Hauber, M. E. (2004). Song selectivity in the song system and in the auditory forebrain. Ann NY Acad Sci., 1016, 222e245. Thompson, R. R., Goodson, J. L., Ruscio, M. G., & Adkins-Regan, E. (1998). Role of the archistriatal nucleus taeniae in the sexual behavior of male Japanese quail (Coturnix japonica): a comparison of function with the medial nucleus of the amygdala in mammals. Brain Behav Evol., 51, 215e229. Todt, D., & Hultsch, H. (1982). Impairment of vocal signal exchange in the monogamous duet singer Cossypha-heuglini turdidae effects on pair bond maintenance. Ethology, 60, 265e274. Trainor, B. C., Kyomen, H. H., & Marler, C. A. (2006). Estrogenic encounters: how interactions between aromatase and the environment modulate aggression. Front Neuroendocrinol., 27, 170e179. Tsutsui, K., Saigoh, E., Yin, H., Ubuka, T., Chowdhury, V. S., Osugi, T., et al. (2009). A new key neurohormone controlling reproduction, gonadotrophin-inhibitory hormone in birds: discovery, progress and prospects. J Neuroendocrinol., 21, 271e275. Tsutsui, K., Ukena, K., Takase, M., Kohchi, C., & Lea, R. W. (1999). Neurosteroid biosynthesis in vertebrate brains. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol., 124, 121e129. Viglietti-Panzica, C., Aste, N., Balthazart, J., & Panzica, G. C. (1994). Vasotocinergic innervation of sexually dimorphic medial preoptic nucleus of the male Japanese quail: influence of testosterone. Brain Res., 657, 171e184. Viglietti-Panzica, C., Panzica, G. C., Fiori, M. G., Calcagni, M., Anselmetti, G. C., & Balthazart, J. (1986). A sexually dimorphic nucleus in the quail preoptic area. Neurosci Lett., 64, 129e134. Vockel, A., Prove, E., & Balthazart, J. (1988). Changes in the activity of testosterone-metabolizing enzymes in the brain of male and female zebra finches during the post-hatching period. Brain Res., 463, 330e340. Vockel, A., Prove, E., & Balthazart, J. (1990a). Effects of castration and testosterone treatment on the activity of testosterone-metabolizing enzymes in the brain of male and female zebra finches. J Neurobiol., 21, 808e825. Vockel, A., Prove, E., & Balthazart, J. (1990b). Sex- and age-related differences in the activity of testosterone-metabolizing enzymes in microdissected nuclei of the zebra finch brain. Brain Res., 511, 291e302. Voigt, C., & Goymann, W. (2007). Sex-role reversal is reflected in the brain of African black coucals (Centropus grillii). Dev Neurobiol., 67, 1560e1573. Vyas, A., Harding, C., McGowan, J., Snare, R., & Bogdan, D. (2008). Noradrenergic neurotoxin, N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine

Hormones and Reproduction of Vertebrates

hydrochloride (DSP-4), treatment eliminates estrogenic effects on song responsiveness in female zebra finches (Taeniopygia guttata). Behav Neurosci., 122, 1148e1157. Walters, M. J., & Harding, C. F. (1988). The effects of an aromatization inhibitor on the reproductive behavior of male zebra finches. Horm Behav., 22, 207e218. Walters, M. J., Collado, D., & Harding, C. F. (1991). Oestrogenic modulation of singing in male zebra finches: differential effects on directed and undirected songs. Animal Behaviour, 42, 445e452. Watson, J. T., & Adkins-Regan, E. (1989a). Activation of sexual behavior by implantation of testosterone propionate and estradiol benzoate into the preoptic area of the male Japanese quail (Coturnix japonica). Horm Behav., 23, 251e268. Watson, J. T., & Adkins-Regan, E. (1989b). Neuroanatomical localization of sex steroid-concentrating cells in the Japanese quail (Coturnix japonica): autoradiography with [3H]-testosterone, [3H]estradiol, and [3H]-dihydrotestosterone. Neuroendocrinology, 49, 51e64. Watson, J. T., & Adkins-Regan, E. (1989c). Testosterone implanted in the preoptic area of male Japanese quail must be aromatized to activate copulation. Horm Behav., 23, 432e447. Wersinger, S. R., Sannen, K., Villalba, C., Lubahn, D. B., Rissman, E. F., & De Vries, G. J. (1997). Masculine sexual behavior is disrupted in male and female mice lacking a functional estrogen receptor alpha gene. Horm Behav., 32, 176e183. Wild, J. M., Kubke, M. F., & Mooney, R. (2009). Avian nucleus retroambigualis: cell types and projections to other respiratory-vocal nuclei in the brain of the zebra finch (Taeniopygia guttata). J Comp Neurol., 512, 768e783. Wiley, C. J., & Goldizen, A. W. (2003). Testosterone is correlated with courtship but not aggression in the tropical buff-banded rail, Gallirallus philippensis. Horm Behav., 43, 554e560. Wingfield, J. C. (1984). Androgens and mating systems: testosteroneinduced polygyny in normally monogamous birds. Auk, 101, 665e671. Wingfield, J. C., & Farner, D. S. (1993). Endocrinology of reproduction in wild species. In D. S. Farner, J. R. King, & K. C. Parkes (Eds.), Avian Biology, Vol. 9 (pp. 163e247). London, UK: Academic Press. Wingfield, J. C., Hegner, R. E., Dufty, A. M., & Ball, G. F. (1990). The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist, 136, 829e846. Wingfield, J. C., Jacobs, J. D., tramontin, A. D., Perfito, N., Meddle, S., Maney, D. L., et al. (1999). Toward an ecological basis of hormonebehavior interactions in reproduction of birds. In K. Wallen, & J. Schneider (Eds.), Reproduction in context (pp. 85e128). Cambridge, MA: M.I.T. Press. Zanisi, M., Messi, E., & Martini, L. (1984). Physiologioal role of 5areduced metabolites of progesterone. In L. Martini (Ed.), Metabolism of hormonal steroids in the neuroendocrine structures. New York, NY: Raven Press. Ziegler, H. P., & Marler, P. (Eds.). (2008). Neuroscience of Birdsong. Cambridge, UK: Cambridge University Press.

Chapter 7

Hormones and Regulation of Parental Behavior in Birds Carol M. Vleck and David Vleck Iowa State University, Ames, IA, USA

SUMMARY Birds display high levels of parental behavior in caring for eggs and young; both males and females participate in most species. A variety of social, environmental, physiological, and experiential factors influence parental behavior, but the most important hormonal factor is elevated prolactin (PRL), often reinforced by previous elevation of the sex steroids. Prolactin secretion and parental behavior appear to be mutually reinforcing as contact with eggs or chicks often elevates PRL. Elevated testosterone (T) and paternal behavior are generally mutually exclusive. Environmental stress, which elevates corticosterone (CORT) and decreases PRL, can decrease parental behavior while elevating survival behaviors in adults. Despite general similarities in the control of parental behavior, there are obvious species differences associated with environmental conditions, maturity of the young at hatch, and other differences in life-history strategies. Additional studies of free-living birds under a variety of ecological conditions will continue to inform us about the regulation of parental behavior in birds.

1. INTRODUCTION Birds are the only major class of vertebrates characterized by a single reproductive mode: oviparity. Birds, like mammals, are endothermic homeotherms and generate enough body heat through their metabolism to maintain a constant and high body temperature. Developing embryos are not endothermic, yet successful maturation to hatching generally requires temperatures higher than the nest’s surroundings. Additional heat input to maintain egg temperatures compatible with development must therefore be provided by the parents, usually by incubating the eggs in a protective nest and in contact with a specialized brood patch that facilitates heat transfer from parent to eggs. Hatchlings of birds vary from extremely precocialdable to feed themselves, thermoregulate, and even fly shortly after hatchingdto extremely altricialdeyes closed, few

Hormones and Reproduction of Vertebrates, Volume 4dBirds Copyright Ó 2011 Elsevier Inc. All rights reserved.

feathers, and able to do little except beg for food (Nice, 1962; Starck & Ricklefs, 1998). Hatchlings of most species receive additional parental care, including guarding, feeding, and brooding to aid in posthatching temperature regulation, although the total time of dependency is often shorter than in mammals (Immelmann & Sossinka, 1986). The ubiquity and extent of parental care in birds and its variation between species provide a powerful system for understanding the hormonal control of parental behavior. In birds, development of young occurs completely outside the female parent’s body. Other individuals can therefore provide as much or more postlaying care as the laying female. As a result, birds have a much higher incidence of pair bonding and male parental care compared to mammals, and cooperative breeding, in which nonbreeders help to raise the young of breeding birds, is relatively common. The oviparous mode of reproduction also facilitates brood parasitism, in which birds lay their eggs in the nests of other birds (sometimes of their own species and sometimes of others) and thus transfer the entire parental care burden to another individual. External eggs are more vulnerable to physical and biological influences (especially predation) than embryos of mammals. The commercial egg industry and much of culinary development in many cultures has followed from humans’ ability to exploit bird eggs. Birds can abandon or neglect their eggs or chicks, however, so female birds can be more flexible in adjusting their reproductive burden than can a pregnant or lactating female mammal. Reproductive effort can be adjusted by changes in clutch size or rate of feeding chicks. Adults can also differentially affect their young by adjusting incubation to change hatching synchrony and thus relative developmental age and size of chicks within a brood. Consequently, much of what we understand about tradeoffs in parental effort and reproductive success, the mechanisms (often hormonal) that mediate these tradeoffs, and implications for adult phenotype and survival has been gleaned from the study of birds. 181

182

More recently, the demonstrations that females of many species deposit variable quantities of hormones, antibodies, and other nutrients such as carotenoids in the eggs of a given clutch has generated tremendous interest in the physiological and behavioral implications of disparities in embryo provisioning (Groothuis & Schwabl, 2008). For the most part, birds are diurnal animals like us, so their behavior is easily observed compared to many other vertebrate groups. They can often be easily trapped and sampled to measure hormone levels, which can then be correlated with observed behavior. Experimental manipulation of hormone levels in the field to directly test hypotheses about effects of hormones on behavior was pioneered in birds (Ketterson, Nolan, Wolf, & Ziegenfus, 1992). Coupled with a large body of knowledge about reproductive endocrinology in important domesticated species, these features have allowed studies of birds to contribute a large fraction of current knowledge of the hormonal control of parental behavior in general.

2. NEST BUILDING Nest building in birds is connected with both the sexual and the parental phases of the nesting cycle. Nest site choice, structure, and construction are often important in courtship and mate selection. The ultimate function of most bird nests, however, is to provide physical protection to the eggs and incubating adult, and so nest structure provides insight into the essential requirements for the successful development of eggs and young. Nests can vary from simple scrapes on the ground to elaborate burrows, huge accumulations of material, and complex domed and woven structures, some of which can be used communally or for many years (reviewed in N. Collias & E. Collias, 1984). Nests of species within the galliform family Megapodiidae are exceptional in that these birds often build structures such as large mounds, and use heat sources including solar radiation, geothermal energy, and organic decomposition for incubation of the eggs, although the ancestral condition was undoubtedly parental contact incubation (Jones, Dekker, & Roselaar, 1995).

2.1. Behavioral PatternsdRoles of the Sexes The male, the female, or both members of a pair may carry out nest-site selection and building behavior. The latter is the usual pattern in nonpasserines. In general, if the male helps incubate the eggs, he also helps build the nest. Cooperation in nest building is usually associated with long-term pair bonds and sharing of parental care between the sexes. Male-only nest building is often associated with sex-role reversal, in which only the male cares for the young, but, when nests are constructed by the female only, male contributions to parental care may vary from none,

Hormones and Reproduction of Vertebrates

as in hummingbirds (Trochilidae), to considerable, as in many passerine finches (N. Collias & E. Collias, 1984).

2.2. Interaction with Courtship Behavior In some species, especially the Columbiformes (doves and quail), we know that nest-building behavior is associated with elevated levels of reproductive hormones, and in turn the act of nest building further stimulates the hormones associated with courtship (Cheng & Silver, 1975). Recent work has characterized how courtship interactions increase secretion of gonadotropin-releasing hormone (GnRH), followed by luteinizing hormone (LH) release in male ring doves (Streptopelia risoria), which suggests that the entire hypothalamicepituitaryegonadal (HPG) axis is involved in the extended period of courtship and nest-building activity in doves (Mantei, Ramakrishnan, Sharp, & Buntin, 2008). Male house wrens (Tryoglodytes troglodytes) build multiple nests, sometimes weeks before a female chooses the male and lays eggs. Variation in the male’s nest-building behavior is correlated with testis size, suggesting that testicular recrudescence and resulting testosterone (T) secretion probably stimulate nest building (Evans & Goldsmith, 2000). In the bowerbirds of the passerine family Ptilonorhynchidae, males do not provide any parental care and females build their own simple nest in which to incubate the eggs. Males do, however, build elaborate bowers for courtship, and bower-building behavior is thought to be derived from nest-building behavior (N. Collias & E. Collias, 1984). In satin bowerbirds (Ptilonorhynchus violaceus), bower building, bower quality, and courtship success are all positively correlated with T levels (Borgia & Wingfield, 1991), suggesting that the same hormonal mechanism stimulates both courtship and building behavior. Without an adequate nest, females of many species may not reach the egg-laying stage, so the nest can be viewed as part of the subsidiary information used to regulate final priming of the ovary (Wingfield & Farner, 1993; Ball & Ketterson, 2008).

2.3. Hormonal CorrelatesdSex Steroids Gonadal sex steroids not only stimulate courtship and sexual behavior but probably also stimulate nest-building behavior (N. Collias & E. Collias, 1984). In ring doves, females build a platform nest while the male gathers and brings nest material to her. In early work with ovariectomized ring doves, both estrogen and progesterone (P4) treatment were required for the display of nest building and incubation in females, and nest-related activities in male doves depended on behavioral cues from the females (Cheng & Silver, 1975). Males that have been gonadectomized also require T replacement to show nest-building behavior (Martinez-Vargas, 1974). In canaries (Serinus canaria), only the female builds the nest, although the

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

male provides some nest material. Nest building can be stimulated in ovariectomized females by injecting the birds with estradiol (E2), particularly in birds exposed to long photoperiods (Hinde, Steel, & Follet, 1974). This effect can be augmented by T treatment as well (Steel & Hinde, 1972), although whether this result would be found with the purer hormones now available is not known. Testosterone can be converted to E2 by aromatase (P450aro) enzyme so it is possible that behavioral responses of females to exogenous androgens may be due at least in part to their conversion to estrogens. Ovariectomized female budgerigars (Melopsittacus undulates) treated with E2 in combination with prolactin (PRL) increase nesting behavior (time spent in a nest box) relative to that of intact birds, and these treated birds ultimately incubate artificial eggs (Hutchison, 1975b). Testosterone supplementation increases the nest-building activity in male red-billed weavers (Quelea quelea) (Crook & Butterfield, 1968) and castrated village weavers (Ploceus cucullatus) (N. Collias & E. Collias, 1984). In bantam hens (Gallus gallus), there is some indication that rising PRL plays a role in nesting behavior because its level increases with the time spent on the nest before incubation commences, as LH levels are falling (Lea, Dods, Sharp, & Chadwick, 1981), although this behavior may signal the onset of incubation rather than actual nest-building behavior. The male zebra finch (Taeniopygia guttata) tends to build the superstructure of the nest with coarser materials, and the female lines the nest with finer materials. In an interesting experiment on the indirect behavioral effects of hormones, Rochester, Heiblum, Rozenboim, and Millam (2008) reported that exposure of growing zebra finch chicks to moderate doses of E2 elevated nest-building behavior when they were adults in both sexes; treated birds built larger nests and at a faster rate than controls. In contrast, exposure of chicks to low levels of E2 decreased nest building as adults. Further, E2 treatment during development masculinized nest-building behavior of females compared to controls. It is the male tree swallow (Tachycineta bicolor), however, that lines the nest with feathers after the female constructs a grass cup. Following exposure as adults to estrogenic polychlorinated biphenyl (PCB) compounds, swallows build smaller and lighter nests with fewer feathers (McCarty & Secord, 1999). Exposure of adult zebra finches to Aroclor 1248, a mixture of PCBs, also alters their nest-building behavior, as they build more nests, but also causes higher hatchling mortality compared to controls (Hoogesteijn, DeVoogd, Quimby, De Caprio, & Kollias, 2005). The demonstration that exposure to sex hormones or xenoestrogens during development or as adults alters nest-building behavior in adults exemplifies the concept that hormones have both organizational and activational effects on behavior (Adkins-Regan, 2007). Available data support the general conclusion that the hormones that stimulate courtship and sexual behavior in

183

birds also stimulate nest building. The hormonal adjustments that may underlie species-specific variations in how the sexes divide or share nest-building duties remain to be determined. As with most aspects of hormones and complex behaviors, it is probable that a particular milieu of hormones is required to potentiate the display of the behavior, whereas the fine details of that behavior are determined by underlying genetic and epigenetic effects in each species.

3. INCUBATION Direct transfer of body heat from parents’ skin to eggs to warm the embryos to temperatures between about 34 and 38 C is the predominant pattern of incubation in birds (Webb, 1987). The megapodes are one well-known exception. In this family, heat for development can be derived from solar or geothermal sources or from the heat of decomposition of organic matter (Jones et al., 1995; Sinclair, 2001). In many species, such as Australian brush turkey (Alectura lathami) and mallee fowl (Leipoa ocellata), the females lay their eggs in highly elaborate mound structures built by the males. The mounds are tended for many months of the year, generally by the males, to maintain mound gas composition and egg temperatures within acceptable ranges, although these ranges are generally greater (lower temperatures, higher CO2, lower O2) than those that most bird eggs experience (Seymour, D. Vleck, & C. Vleck, 1986; Seymour, D. Vleck, C. Vleck, & Booth, 1987). The energy expended to regulate egg temperature in these mound builders is far higher than would be required for conventional incubation (Frith, 1956), and the uneven temperature distribution in the mounds can affect sex ratios of the hatchlings because of a sex-biased temperature sensitivity of the embryos (Goth & Booth, 2005). These features are probably among the reasons that this mode of parental care has not evolved in other groups (Goth, 2008). It would be useful to understand the hormonal basis of mound tending in this group because it is clearly a highly derived form of parental behavior. Incubation is influenced by a combination of hormonal and other physiological signals, environmental inputs from the eggs or nest (Hall, 1987a; Evans, 1990), and social cues such as presence or absence of a mate (Vowles & Lea, 1986; Be´de´carrats, Gue´mene´, & Richard-Yris, 1997). Previous breeding experience seems to increase an individual’s levels of, or responsiveness to, hormonal and environmental signals for incubation and/or chick rearing (Wang & Buntin, 1999; Angelier, Weimerskirch, Dano, & Chastel, 2007; Christensen & Vleck, 2008).

3.1. Costs of Incubation and Parental Attentiveness The metabolic cost of warming eggs and maintaining them at the incubation temperature has been estimated or measured

184

in a number of species of bird (reviewed in Williams, 1996; Tinbergen & Williams, 2002). Metabolic rate in incubating birds is increased over nonincubating birds when ambient temperatures are below the birds’ thermal neutral zones. For birds that intermittently leave the nest and then return to a cold nest, the cost to rewarm the eggs can be substantial, particularly for large clutches. A major cost to an incubating bird, however, is often not energy expended in incubation, but the loss of foraging time, because the incubator’s time is required at the nest (Hainsworth & Voos, 2002). In biparental species in which both members of a pair incubate, the egg may be covered nearly 100% of the time, improving the conditions experienced by the embryo (Kosztolanyi, Szekely, & Cuthill, 2003) while distributing the time and energy cost to both parents (Reid, Monaghan, & Ruxton, 2002). When only one member of the pair incubates for long periods of time, and if that bird is not fed on the nest by the mate, the incubating bird must either fast, requiring large fat stores (Criscuolo, Gabrielsen, Gendner, & Le Maho, 2002; Vleck & Vleck, 2002), or must leave the nest to obtain food and water, leaving the eggs exposed to cooling, or sometimes overheating in warm, sunny environments (Vleck, 1981) as well as to predators (Wilson, Martin, & Hannon, 2007). The ecological and evolutionary factors that influence the patterns of incubation attentiveness have received considerable attention because they represent a natural case of parenteoffspring conflict, reflecting a life-history tradeoff between reproduction and self-maintenance (Martin, 2002). Little is known of the hormonal influences on nest attentiveness patterns per se, although the increase in attentiveness during early incubation is correlated with a rise in PRL in some species (see Section 3.6). We do know that, in some species, long incubation bouts and loss of body mass are associated with increases in corticosterone (CORT) and decreases in PRL, and are probably associated with the drive to refeed and desertion of the nest or chicks (Yorio & Boersma, 1994; Groscolas & Robin, 2001; Vleck & Vleck, 2002; Groscolas, Lacroix, & Robin, 2008). In king penguins (Aptenodytes patagonicus), adults that abandon their young have higher CORT levels than those who abandon their eggs (Groscolas et al., 2008) (Figure 7.1). Artificially elevating CORT in incubating, fasting common eiders (Somateria mollissima) does not cause these ducks to desert their nests as long as energy reserves are at normal levels, even though their PRL levels fall (Criscuolo et al., 2005). These observations suggest that a decision to abandon the nest is likely to be modulated by the estimated costs or benefits of alternate behavioral responses, and is not strictly controlled by some fixed threshold in CORT level.

3.2. Behavioral PatternsdRoles of the Sexes Different modes of parental care in birds have recently been reviewed (Cockburn, 2006). Biparental incubation

Hormones and Reproduction of Vertebrates

FIGURE 7.1 Plasma levels of corticosterone (CORT) and prolactin (PRL) at different stages of incubation and chick brooding in free-living king penguins. Within incubation, values not sharing the same superscript differ significantly; within brooding, asterisks denote significant differences between birds tending their chicks and those abandoning their chicks. BI, beginning of incubation; CA, chick abandonment; D12, day 12 of incubation; EA, egg abandonment; EBS, end of brooding shift; R, relief by partner at end of incubation shift. Values are means standard error of the mean (SEM). Reproduced from Groscolas, Lacroix, and Robin (2008).

behavior, in which both members of a pair incubate, is common, occurring in over 80% of bird species. Males alone incubate and care for young in about 1% of species, distributed across 12 families. This mode predominates in ratites and four clades within the waders (Charadrii). Females alone care for eggs and young in about 8% of species and in 40 different avian families. This pattern is particularly common in hummingbirds, manakins, birds of paradise, and bowerbirds, among others, and is found in about 30e45% of ducks and pheasants and their allies. Cooperative breeding is inferred to occur in about 9% of avian species. In cooperative breeders, nonbreeding individuals help rear the young of others and sometimes spend considerable effort feeding the incubating female as well (Williams & Hale, 2008). In many passerines, the male feeds the incubating female, which helps compensate her for missed foraging opportunities and metabolic costs. In some doubleclutching species such as mountain plovers (Charadrius

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

montanus), there is sequential polyandry and a division of labor between successive clutches; the males incubate the first clutch without input from the female and the female leaves this nest, lays another clutch, and proceeds to incubate the second clutch without input from the male (Blomqvist, Wallander, & Andersson, 2001). The evolution of predominantly male parental care has been related to precocial chicks and a small clutch size (Emlen & Oring, 1977) with high assurance of paternity by the male (Delahanty, Fleischer, Colwell, & Oring, 1998). There are exceptions to this pattern, however, such as in black coucals (Centropus grillii), a member of the Cuculiformes, in which young are altricial and clutch size is relatively large (Andersson, 1995). The evolution of female-only care has also been attributed to several selective pressures including precocial, nidifugous young, which require little posthatching care and a tropical frugivorous or nectivorous lifestyle in which food can be very abundant but patchy (Cockburn, 2006).

3.3. Brood-patch Formation The brood patch or incubation patch is formed when the skin on the ventral surface becomes defeathered, edematous, and vascularized, facilitating heat transfer from the incubating bird to the clutch of eggs. It begins to form before egg laying in some passerines that have been studied, but during egg laying in Galliformes (Jones, 1971). Not all birds form brood patches; they are absent in pelicans, gannets, and boobies, which may transfer heat to the egg using their foot web (Lorme´e, Jouventin, Lacroix, Lallemand, & Chastel, 2000). There is considerable variation in the structure of the brood patch among speciesdsometimes a single patch develops; in other species multiple patches develop, often corresponding to the modal clutch size (Lea & Klandorf, 2002). The emperor penguin (Aptenodytes forsteri) does not have a brood patch and males incubate the single egg between a flap of skin and their foot web (Williams, 1995), whereas other penguin species have a brood patch (Handrich, 1989; St. Clair, 1992). When both sexes incubate, they generally both develop a brood patch. When only the female incubates, the brood patch usually develops only in that sex (Jones, 1971). In some species the male develops a brood patch but does not incubate, and in other species the male incubates but does not have a well-developed brood patch (Zann & Rossetto, 1991; Lea & Klandorf, 2002). The latter may only be possible in warm climates where the gradient that the parent must maintain between the egg and environment is small. Delay in full development of the brood patch may delay the onset of full incubation (bringing the eggs to the final incubation temperature) for several days, even though the adult is attending the eggs (Wiebe & Bortolotti, 1993;

185

Wiebe, Wiehn, & Korpimaki, 1998). The presence of eggs, however, can also influence brood-patch formation. In yellow-eyed penguins (Megadyptes antipodes), placing an artificial egg in the nest stimulates brood-patch development. The resulting brood patch is wider and the birds achieve a higher egg temperature when they begin incubation compared to control birds incubating only their own eggs (Massaro, Davis, & Davidson, 2006). Sensory input from the brood patch affects incubation behavior by stimulating PRL secretion in many species (see Section 3.8), and incubation behavior and PRL levels are, in turn, thought to control ovulation and clutch size through their antigonadal effects. If the presence of the egg also stimulates brood patch development, this complex interplay ensures an orderly and timely progression through the reproductive program, which is tied to the production and presence of the eggs and is orchestrated through hormonal control (Sockman, Sharp, & Schwabl, 2006). Endocrine control of brood-patch formation has been studied in several species (reviewed in Lea & Klandorf, 2002). Early workers concluded that induction of broodpatch formation and broody behavior in many species can be achieved only under the influence of PRL accompanied by a priming action of the sex steroids, estrogens and P4 in females, and androgens in males (Jones, 1971; Hutchison, 1975a). Recent work has reinforced these generalities. In ovariectomized female turkeys (Meleagris gallopavo), a well-developed brood patch forms after treatment with E2, P4, and ovine PRL (El Halawani, Silsby, Rozenboim, & Pitts, 1986). In bantam hens, the development of the brood patch closely follows the increase in PRL (Lea et al., 1981), which is also true for ruffed grouse (Bonasa umbellus) (Etches, Garbutt, & Middleton, 1979) and Harris’ hawks (Parabuteo unicinctus) (Vleck, Mays, Dawson, & Goldsmith, 1991). Elevated PRL early in the breeding season, when T is also elevated, may contribute to brood-patch development and incubation behavior in male blue-headed vireos (Vireo solitarius), whereas male red-eyed vireos (Vireo olivaceus) have lower PRL and do not develop a brood patch or incubate (Van Roo, Ketterson, & Sharp, 2003). Both male and female white ibis (Eudocimus albus) develop brood patches during incubation following elevation of sex steroids, but PRL was not measured in this study (Heath, Frederick, Edwards, & Guillette, 2003). Evidence suggests that androgens synergize with PRL in brood-patch formation in males, but experimentally elevating androgens in females appears to block brood-patch formation in darkeyed juncos (Junco hyemalis) (Clotfelter et al., 2004). The importance of hormones in controlling broodpatch formation is reinforced by observations that its formation can be induced even in birds that do not incubate. For example, exogenous estrogens and PRL can induce brood-patch formation in male house sparrows (Passer domesticus) even though they do not normally incubate

186

(Selander & Yang, 1966). In Wilson’s phalaropes (Phalaropus tricolor) and red-necked phalaropes (Phalaropus lobatus), in which only the male incubates, a brood patch can be induced in either sex, but under the influence of androgens plus PRL, rather than estrogens plus PRL (Johns & Pfeiffer, 1963). In contrast, steroids and PRL do not induce brood-patch formation in brown-headed cowbirds (Molothrus ater), an obligate brood parasite that does not incubate its own eggs, suggesting loss of sensitivity to hormone induction in this species (Selander, 1960).

3.4. Laying, Incubation, and Asynchronous Hatching Female birds ovulate yolked oocytes one at a time, and subsequent deposition of the albumin and eggshell within the oviduct requires many hours. Thus, birds lay single eggs sequentially at daily or longer intervals. Although the length of the interval can vary with female nutritional state (Dhondt, Eykerman, & Huble, 1983; Wiebe & Martin, 1995), maternal reserves normally affect egg size and number more than laying interval (Nager, 2006). The multiday interval required to produce a clutch of multiple eggs means that individual eggs experience significantly different histories. Position in laying sequence can affect egg viability via thermal effects on development before incubation starts (Haftorn, 1988; Ardia, Cooper, & Dhondt, 2006) or variation in risk of infection (Cook, Beissinger, Toranzos, Rodriguez, & Arendt, 2005). Such differences may affect both the developmental program of individual eggs and adults’ choices of strategy in when to initiate incubation (Stoleson, 1999; Cook, Beissinger, Toranzos, Rodriguez, & Arendt, 2003). If birds begin incubation prior to clutch completion, the eggs generally hatch asynchronously and the hatchlings within the nest are of different ages. In the case of precocial chicks that leave the nest soon after hatching (i.e., nidifugous species), this forces the parent(s) to make a decision regarding whether to keep incubating later-laid eggs or to leave the nest and accompany the hatchlings (Brunning, 1974). Whether the chicks are altricial or precocial, earlier-hatched chicks are larger and more developed and have a competitive advantage over laterhatched chicks. When parents are unable to successfully raise all the chicks, the youngest are usually the ones to fail; this phenomenon is called brood reduction. Brood reduction presumably permits large clutches to be reared in good years but ensures survival of at least some chicks even in lean years. The laying of large clutches, commencement of incubation before the clutch is complete, asynchronous hatching, and brood reduction are common forms of bet-hedging that help to increase fitness of birds in temporally variable environments. The diversity in avian incubation strategies requires a corresponding

Hormones and Reproduction of Vertebrates

diversity in modulation of control of incubation behavior, and has fostered considerable comparative study of the hormonal control of incubation.

3.5. Hormonal Control of Incubation The neural and hormonal basis of incubation behavior has been studied extensively in a few domesticated species, including chickens, turkeys, and ring doves (Buntin, 1996). Much of that work focuses on the hypothalamusepituitary unit and the pituitary secretion of PRL. Work on incubation in free-living birds has focused on correlations between plasma levels of PRL and incubation behavior and how these vary with social system, ecology, and life-history traits. Prolactin levels invariably increase during incubation within birds, including passerines (Dawson & Goldsmith, 1982; Hiatt, Goldsmith, & Farner, 1987; Wingfield, Ronchi, Goldsmith, & Marler, 1989; Wingfield & Goldsmith, 1990; Silverin, 1991; Seiler, Gahr, Goldsmith, & Guettinger, 1992; Brown & Vleck, 1998), woodpeckers (Khan, McNabb, Walters, & Sharp, 2001), shore birds (Oring, Fivizzani, & El Halawani, 1986; Gratto-Trevor, Oring, Fivizzani, El Halawani, & Cooke, 1990), ducks (Criscuolo et al., 2005), raptors (Vleck et al., 1991; Sockman, Schwabl, & Sharp, 2000), penguins (Vleck, Bucher, Reed, & Kristmundsdottir, 1999; Setiawan et al., 2006; Massaro, Setiawan, & Davis, 2007), and various seabirds (Lorme´e et al., 2000; Chastel & Lorme´e, 2002; Angelier, Shaffer, Weimerskirch, & Chastel, 2006; Angelier et al., 2007b), supporting the hypotheses that PRL and incubation behavior are functionally linked, and that this linkage is ancestral, dating prior to the origin of modern birds.

3.6. Initiation and Maintenance of Incubation In most species, full-blown incubation behavior does not begin with the first egg laid. In mallards (Anas platyrhynchos), females spend increasing numbers of short bouts in a nest box over the course of laying 10 eggs, and at the end of clutch formation there is a sudden increase in nest occupation (Hall, 1987a). Prolactin levels increase more than five-fold during the last 20% of the laying phase, as nest attentiveness more than doubles (Hall, 1991). Progesterone levels, but not E2, are falling at this time. As a rise in PRL usually occurs simultaneously with the onset of egg incubation, it is tempting to suggest cause and effect. The pattern of PRL rise does not, however, always match that of incubation. A PRL rise may occur abruptly at the time of egg laying and incubation or may rise more slowly and peak during midincubation. For example, columbiforms differ from other species in that PRL levels are not typically elevated until incubation is well-established. In these species, synergistic action of E2 and P4 is necessary to initiate incubation (Cheng & Silver,

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

1975), although PRL may be important in maintaining incubation behavior (reviewed in Buntin, 1996). The relation between PRL and incubation behavior is further complicated by the observation that incubation itself can trigger PRL secretion (see Section 3.8). Direct evidence for PRL involvement in parental behavior comes from experiments that alter PRL levels (reviewed in Vleck, 2001). Ring doves separated from their nests but given exogenous PRL maintain nest attachment for up to 10 days and resume incubation given the opportunity, whereas controls do not (Janik & Buntin, 1985; Lehrman, 1996). Thus, PRL certainly contributes to the maintenance of incubation behavior in doves. Ovine PRL from implanted osmotic pumps increases incubation behavior about 2.5-fold relative to controls in captive, laying American kestrels (Falco sparverius) (Sockman et al., 2000). Pharmacological and immunological treatments that block PRL secretion will limit broody behavior in chickens and turkeys (Sharp, 1997). Inhibition of serotonin biosynthesis or vasoactive intestinal peptide (VIP), both hypothalamic neural agents involved in the release of pituitary PRL, reduces circulating PRL levels and prevents the expression of incubation behavior in turkey hens (Rozenboim et al., 2004). Experimental manipulation of PRL in free-living birds would be extremely useful in furthering our understanding of the role of PRL in incubation behavior. Although elevated PRL titer is highly correlated with incubation behavior, it may not always be necessary. In chickens, PRL levels drop in broody females deprived of access to their nest, but, if nest deprivation lasts less than a few days, they resume incubation as soon as they are returned to their nests (Leboucher, Richard-Yris, Chadwick, & Guemene, 1996). Prolactin levels quickly return to predeprivation levels (Leboucher et al., 1996), but incubation behavior resumes before PRL levels rise (El Halawani, Burke, & Dennison, 1980; Zadworny, Walton, & Etches, 1985; Lea & Sharp, 1989). After three days of nest deprivation about 70% of domestic chickens resume nesting behavior, but individual behavior is not correlated with individual PRL levels (Richard-Yris et al., 1998a). Such behavioral effects have been attributed to a ‘carry-over’ effect of previous PRL elevation that may have primed the behavioral display (Buntin, 1996). Such carry-over might result if the PRL threshold at which incubation is initiated is higher than the threshold at which the behavior is abandoned, and might function to rescue an interrupted reproductive effort. There are often differences in PRL profiles between males and females, even when both members of the pair incubate. Levels of PRL are usually higher in females than in males, whether or not the male participates in incubation (Dawson & Goldsmith, 1982; Hiatt et al., 1987; Wingfield & Goldsmith, 1990; Lorme´e et al., 2000; C. Vleck, Ross,

187

D. Vleck, & Bucher, 2000; Angelier, Moe, Weimerskirch, & Chastel, 2007). In Ade´lie penguins (Pygoscelis adeliae), males and females share about equally in incubation, but PRL is slightly higher in females than in males (Vleck et al., 2000) (Figure 7.2). In contrast, male and female semipalmated sandpipers (Calidris pusilla) and zebra finches also share equally in incubation, but PRL levels do not differ between the sexes (Gratto-Trevor et al., 1990; Christensen & Vleck, 2008). Male mallard ducks do not incubate; their PRL levels are slightly elevated at this point in the breeding cycle but remain well below those of females (Goldsmith & Williams, 1980). In Mexican jays (Aphelocoma ultramarina), peak PRL levels are only about 20% higher in females than in males (Brown & Vleck, 1998), although the males do not incubate but rather feed the incubating females, who seldom leave the nest. This raises the question of whether elevated PRL levels in males might drive such indirect parental contributions in other species. Species in which the male incubates exclusively or considerably more than the female have higher PRL levels in males than in females (Oring et al., 1986; Oring, Fivizzani, Colwell, & El Halawani, 1988; Gratto-Trevor et al., 1990; Eens & Pinxten, 2000). If onset of incubation is brought about by an increase in PRL, which has been shown to be antigonadotropic in at least some birds, then clutch size may be determined by the same hormonal milieu that initiates incubation (Sockman et al., 2006). In American kestrels, PRL levels during the laying phase are higher in females that lay smaller clutches than those that lay larger clutches, although PRL treatment does not affect clutch size (Sockman et al., 2000). Progesterone levels as well as PRL may be involved in clutch-size limitation. Domestic canaries treated with P4 after the onset of nest building show an inhibition of

FIGURE 7.2 Plasma prolactin (PRL) levels in male and female Ade´lie penguins during the reproductive season. Data are plotted relative to the day the first of two eggs is laid. Values are means standard error (SE). Reproduced from Vleck, Bucher, Reed, and Kristmundsdottir (1999).

188

copulation solicitation and a decrease in clutch size (Leboucher, Beguin, Lacroix, & Kreutzer, 2000). Additional measurement and experimental manipulation of PRL levels could shed additional light on the relationship between PRL and parental behavior. The onset of incubation has been studied in eight species of prairienesting ducks by tracking the rise in temperature of artificial eggs in the nest (Loos & Rohwer, 2004). Incubation behavior develops gradually in all of these species, and the females that lay smaller clutches increase their nest attentiveness more rapidly than conspecifics that lay larger clutches. In canaries the percentage of time spent in the nest rises with number of days after onset of laying, and the initiation of incubation (defined as 50% of time spent in the nest) can vary from zero to four days after the initiation of laying (Sockman & Schwabl, 1999). Both are cases in which measurement or manipulation of PRL would be informative.

3.7. Steroid Effects on Incubation Studies in domesticated species indicate that induction of incubation behavior by exogenous PRL may require interaction with ovarian steroids as well (Buntin, 1996). Ovariectomized turkey hens pretreated with E2 and then given exogenous P4 express interest in nest boxes, but PRL administration is required for full incubation behavior to be expressed. Once incubation is fully established and endogenous PRL levels are elevated, no exogenous steroids are needed for sustained incubation (El Halawani et al., 1986). Certainly, sex steroids in free-living species are elevated during courtship and gamete formation prior to the parental phase, so their presence may be necessary to facilitate the behavioral response to PRL, just as has been suggested for the development of the brood patch. The drop in gonadal steroid concentrations after egg production in many species (e.g., Lorme´e et al., 2000) suggests sex steroids are not involved in incubation maintenance. Indeed, in domesticated species, gonad removal or steroid inactivation does not disrupt incubation that has already been established (Zadworny & Etches, 1987; Ramesh, Proudman, & Kuenzel, 1995; Lea, Richard-Yris, & Sharp, 1996; Youngren et al., 2002; Al Kahtane, Chaiseha, & El Halawani, 2003). Pharmacological inactivation of steroidinduced (or -dependent) behavior could be used in freeliving birds to extend these observations to other taxa. What is known is that elevating T will decrease parental behavior in many species (see Section 5).

3.8. Regulation of Prolactin (PRL) Secretion The main physiological signal for PRL release in birds is VIP (Lea & Vowles, 1986; Pitts et al., 1994; Maney, Schoech, Sharp, & Wingfield, 1999; Vleck & Patrick,

Hormones and Reproduction of Vertebrates

1999; Kulick, Chaiseha, Kang, Rozenboim, & El Halawani, 2005; Christensen & Vleck, 2008), which increases PRL transcription and release in lactotropes of the anterior pituitary. Dopamine plays a dual regulatory role, being inhibitory at low doses through antagonizing VIP but stimulatory at high doses (Youngren et al., 2002; Al Kahtane et al., 2003). This control system is activated by photoperiod in many species in which PRL levels rise following exposure to long day lengths in preparation for breeding (Chaiseha, Tong, Youngren, & El Halawani, 1998). There is considerable evidence for a feedback relationship between incubation behavior and PRL secretion in many speciesdthe act of incubation increases PRL titers and thus maintains incubation. In domestic chickens, turkeys, and mallard ducks, continuous tactile input from the eggs is required to maintain elevated PRL and broodiness (El Halawani et al., 1980; Hall, 1987a; Sharp, Macanamee, Sterling, Lea, & Pedersen, 1988). Prolactin levels drop rapidly after egg loss in cape gannets (Morus capensis) (Hall, 1986) and red-footed boobies (Sula sula) (Chastel & Lorme´e, 2002). In galliforms and anseriforms, the effect of incubation on PRL is known to be mediated by contact between the eggs or chicks and the brood patch (Opel & Proudman, 1988; Richard-Yris et al., 1998a). When the brood patch is anesthetized or denervated, PRL levels fall and incubation behavior decreases, even when the eggs are still present in the nest (Hall, 1987a; Book, Millam, Guinan, & Kitchell, 1991). Brood-patch denervation in turkey hens decreases PRL levels compared to surgical controls and decreases the time they spend in nest boxes. These birds also do not become broody and have higher eggproduction rates than controls (Book et al., 1991). Not all species, however, display a tight relation between continuous brood-patch stimulation, elevated PRL secretion, and incubation behavior. In many species, particularly seabirds, in which both members of the pair incubate, plasma PRL remains high even when birds are away from their nests for hours to weeks, and the birds return to the nest to incubate even if they have not had recent tactile input from the eggs (Hector & Goldsmith, 1985; Hall, 1986; Lea, Vowles, & Dick, 1986; Garcia, Jouventin, & Mauget, 1996; Jouventin & Mauget, 1996; Lorme´e et al., 2000; Vleck et al., 2000). In the emperor penguin, females leave the colony after egg laying and males incubate while the females forage. Yet, two months later, when they finally return to feed and brood their newly hatched chicks, the females’ PRL levels are higher than when they left (Lorme´e, Jouventin, Chastel, & Mauget, 1999). In incubating chickens, turkeys, and ring doves, experimental exposure to tactile and vocal input from chicks decreases PRL secretion and disrupts incubation behavior (Lea et al., 1986; Opel & Proudman, 1988;

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

Leboucher, Richard-Yris, William, & Chadwick, 1990; Richard-Yris et al., 1998b). A similar ‘experiment’ occurs in nature when eggs of brood parasites hatch before the natural eggs in the parasitized nest. In yellow warblers (Dendroica petechia), however, the presence of a brownheaded cowbird chick does not alter female nest attentiveness patterns (McMaster & Sealy, 1999). In free-living species, eggs and chicks can be switched between nests to artificially extend or terminate the incubation period. If such manipulation affects PRL levels, it would suggest that sensory input is important in controlling changes in PRL secretion. In pied flycatchers (Ficedula hypoleuca), PRL levels of incubating adults decline at hatching for normal or shortened incubation periods, and decline at the normal hatching time even if incubation is lengthened (Silverin & Goldsmith, 1984). In breeding albatrosses (Hector & Goldsmith, 1985) and Ade´lie penguins (Vleck et al., 2000) in which the incubation period has been altered by the investigator, PRL levels remain high from the beginning of incubation until chicks are no longer attended by their parents. In Wilson’s phalaropes and common eiders, however, delaying hatching lengthens the period when circulating PRL is elevated in incubating adults, and, in phalaropes, shortening incubation time before eggs hatch has the opposite effect (Oring et al., 1988; Criscuolo, Chastel, Gabrielsen, Lacroix, & Le Maho, 2002). Oring et al. (1988) suggested that, in species in which the natural incubation period is variable, as it is in Wilson’s phalaropes, the drop in PRL secretion that normally occurs at hatching should be cued by the hatching event. Conversely, endogenous control of PRL secretion, independent of hatching events, should be adaptive in species with little variation in incubation period, such as the pied flycatcher, because this would decrease the time a bird would waste incubating nonviable eggs. In species such as albatross and penguins, in which PRL levels are relatively independent of the bird’s exposure to nest and eggs, PRL levels may be determined by an endogenous schedule or by other external cues such as day length (Wingfield & Goldsmith, 1990; Silverin & Goldsmith, 1997). Such a pattern may result from a late-season tradeoff between parental selfmaintenance and further chick investment (Moreno, Barbosa, Potti, & Merino, 1997). Ade´lie penguins, e.g., must remain ashore and cannot forage or feed chicks while they molt. As the molt must be completed prior to winter and formation of sea ice, adults cannot prolong parental care past a critical date, and pairs that breed late in the season may have to abandon their chicks at a relatively young age (Vleck et al., 2000).

3.9. Renesting and Responses to Nest Failure Natural or experimentally induced egg or nest loss can also be used to investigate the interaction between PRL and

189

incubation. Prolactin levels decrease dramatically in many species within 24 to 48 hours of nest loss or egg removal (Etches et al., 1979; El Halawani et al., 1980; Goldsmith, Burke, & Prosser, 1984; Ramsey, Goldsmith, & Silver, 1985; Hall, 1986; 1987b; Sharp et al., 1988; Lea & Sharp, 1989; Leboucher et al., 1996; Richard-Yris et al., 1998a). In red-footed boobies that lose their egg, PRL falls within 12 hours but remains above baseline, whereas in birds that desert their nest PRL levels can be at baseline in six hours (Chastel & Lorme´e, 2002), perhaps because a drop in PRL is a prerequisite to desertion. A tight feedback loop between sensory input from eggs or chicks should be adaptive in species that can renest after premature loss of eggs or chicks, because PRL secretion after nest loss might hinder the rise in gonadotropins and sex steroids necessary for initiation of another reproductive cycle (Sharp, Dawson, & Lea, 1998). However, PRL in the multiple-brooding song sparrow (Melospiza melodia) does not decline between nesting bouts or following nest failure (Wingfield & Goldsmith, 1990). In many highlatitude seabirds, plasma PRL does not change rapidly after nest loss (Garcia et al., 1996; Jouventin & Mauget, 1996; Vleck et al., 2000; Chastel, Lacroix, Weimerskirch, & Gabrielsen, 2005), presumably the result of selection to maintain a hormone milieu conducive to promoting return of ocean-foraging birds to the colony to care for eggs and chicks during the extended nesting season. Ade´lie penguins will incubate infertile eggs for nearly four weeks past the normal hatch date (Vleck et al., 2000). In emperor penguins, PRL remains elevated up to three months after nest failure (Lorme´e et al., 1999). Continued PRL secretion after nest loss in such species may account for their propensity to remain in the nesting colony and to attempt to steal and incubate the eggs or chicks of other birds (Fowler, Wingfield, Boersma, & Sosa, 1994; Angelier, Barbraud, Lorme´e, Prud’homme, & Chastel, 2006).

4. CARE OF YOUNG 4.1. The AltricialePrecocial Spectrum Altricial hatchlings must be brooded until they can thermoregulate as well as feed themselves, while precocial hatchlings may require relatively little parental care beyond protection from predators and instruction in how to forage. Parental brooding of chicks for a few days after hatching may be necessary, however, even in precocial species such as ducks (Dzus & Clark, 1997). In the most precocial chicks, those of megapodes, hatchlings are totally independent of the parents and may even be able to fly within a few days (Goth, 2002). They can also suffer very high mortality, possibly due to lack of parental attention (Goth & Vogel, 2002).

190

Hormones and Reproduction of Vertebrates

4.2. Hormonal Correlates of Posthatching Parental Behavior Brooding and other posthatching care in birds appear to be regulated by the same hormonal mechanisms (primarily PRL) as incubation behavior. After hatching, parental PRL level and parental care are highly correlated, though that correlation is less strong than for incubation behavior because of the greater variability in both relevant behaviors and pertinent inputs, including signals from the chicks themselves. In species with precocial and relatively independent young, PRL levels may decline rapidly after the chicks hatch. A drop in PRL levels can be induced in incubating turkey hens by placing newly hatched poults in their cages (Opel & Proudman, 1988). Prolactin levels fall, although not to baseline, in bar-headed geese (Anser indicus) right after the eggs hatch, even though the females brood the young (Dittami, 1981). In common eiders, PRL drops about 50% at hatching, but remains above prelaying levels in both parenting females and those that have recently lost their young (Criscuolo et al., 2002a). Prolactin decreases rapidly at the end of incubation in mallard hens (Hall, 1987a). However, Boos, Zimmer, Carriere, Robin, and Petit (2007) found a strong positive relationship between PRL level and parental care in mallards until the henebrood bond was disrupted about six weeks after hatching (Figure 7.3). At this point, PRL may have fallen below a critical threshold as the chicks matured and became independent. Prolactin levels may decline more slowly in species with semiprecocial and altricial young, presumably because parental brooding of nonthermoregulating chicks is required for chick survival, just as it is for embryo survival (Buntin, 1996). Prolactin levels often begin to decline only after the chicks achieve thermal independence and no longer require constant brooding (Goldsmith, 1991; Schoech, Mumme, & Wingfield, 1996b) or after fledging (Seiler et al., 1992). In Wilson’s phalaropes, males are responsible for all postlaying parental care, and their PRL levels decline after chicks hatch, returning to baseline after about nine days, when the chicks are nearly thermally independent (Oring et al., 1988). Prolactin levels decline after the eggs hatch in Harris’ hawk parents, but PRL levels of helpers at the nest increase at the same time (Vleck et al., 1991). Groups of cooperatively breeding Mexican jays have from one to five asynchronous nests over a threemonth breeding season, and essentially all members of the group feed incubating females and care for the young. Prolactin levels in all group members remain elevated for many weeks after the start of incubation, and do not decline after the first nest hatches (Brown & Vleck, 1998). Seabirds that feed offshore, such as king penguins, Ade´lie penguins, red-tailed tropic birds (Phaeton rubricauda), and three Diomedea albatross species, do not care

FIGURE 7.3 Changes in (a) an index of parental care behavior and (b) associated plasma prolactin (PRL) in female mallard ducks tending their hatchlings. Values are means standard error (SE). Reproduced from Boos, Zimmer, Carriere, Robin, and Petit (2007).

for multiple nests within a season, but, like Mexican jays, their PRL levels remain high long after eggs hatch (Figure 7.2) (Hector & Goldsmith, 1985; Cherel, Mauget, Lacroix, & Gilles, 1994; Lorme´e et al., 2000; Vleck et al., 2000). In contrast, PRL declines to near baseline in masked (Sula dactylatra) and red-footed boobies shortly after their young hatch (Lorme´e et al., 2000). Although chicks depend on parental feeding long after hatching in all of these species, maintenance of high PRL may be necessary to prompt offshore-feeding parents to return to the colony and feed the young, even without recent stimulation by begging chicks. In onshore-feeding boobies, feeding behavior may be stimulated by frequent exposure to begging chicks and triggered by neural rather than hormonal control. Even when altricial chicks have fledged and are no longer fed by the adults, they may remain in close association with them. Postfledging parental behaviors can be

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

191

quite elaborate. In pied babblers (Turdoides bicolor), a cooperatively breeding species, adults use a special call to attract recently fledged birds to an abundant food source, but these same adults act aggressively towards other adults who respond to the call (Radford & Ridley, 2006). Common guillemot (Uria aalge) chicks leave the nesting colony when they are only about one-quarter adult size and swim out to sea accompanied by a parent, usually the male. The adult guides the offspring through high-predation-risk coastal areas, often for several hundred kilometers, into the open sea in search of prey (Camphuysen, 2002). Interestingly, the adult undergoes a complete molt and becomes flightless at the same time that it is accompanying its stillflightless offspring. Hormonal control of these and other postfledging behaviors has not been investigated, in large part because parent birds and their offspring are more difficult to track and sample after fledging. Experimental manipulation of PRL levels demonstrates the importance of PRL to many parental behaviors in chick care. Parental behavior in ring doves includes regurgitation feeding, defensive behavior, and crouching in the nest. These behaviors can be induced in nonbreeding females by exposure to hungry chicks, and exogenous PRL increases the incidence of this behavior, particularly in birds that have previously raised young (Wang & Buntin, 1999). Thus, PRL, experience, and signals from chicks all contribute to the display of parental behavior. Free-living female willow ptarmigan (Lagopus lagopus) receiving supplemental PRL display more intense defense of chicks compared to controls, and chick survival is also increased (Pedersen, 1989). In emperor penguins, failed breeders often attempt to kidnap and assume care of chicks of other birds. This behavior is at least partly suppressed by bromocriptine, a drug that inhibits PRL secretion (Angelier et al., 2006a).

Hnasko, Zuzick, Valentine, & Scammell, 1996; Schoech et al., 1996b). In common eiders, there is no correlation between adult PRL and clutch size, which varies naturally between two and six eggs, so feedback between egg contact and PRL secretion is apparently not tightly tied to the strength of the feedback signal (Criscuolo et al., 2002a). Prolactin levels in incubating male Wilson’s phalaropes are higher in controls than in birds with clutches artificially reduced by one or two eggs, although this was not found in a drought year, when PRL levels were low in all birds. Prolactin is also lower, however, when clutch size is artificially augmented, and both experimental groups are more likely to abandon incubation than control males (Delahanty, Oring, Fivizzani, & El Halawani, 1997). The authors suggested that birds may recognize the lower fitness potential of an altered clutch and that lowered PRL level is an adaptive endocrine response to reduce their behavioral effort. Adult body condition in Gould’s petrels (Pterodroma leucopter) is positively correlated with PRL in males during incubation and also with chick mass after hatching, so elevated PRL may promote greater parental behavior in parents of good body condition (O’Dwyer, Buttemer, Priddel, & Downing, 2006). Ross’s geese (Chen rossii) and wandering albatross (Diomedea exulans) in good condition have higher PRL levels than those in poor condition (Weimerskirch, 1995; Jonsson, Afton, Alisauskas, Bluhm, & El Halawani, 2006), and correlation between body condition and PRL has been suggested to explain variation in incubation behavior in common eiders (Criscuolo et al., 2006). Until we can experimentally eliminate covariance between body condition and PRL level, however, it is difficult to be confident that variation in parental effort between individuals results from differences in PRL levels.

4.3. Prolactin (PRL) Level and Parental Effort

4.4. ParenteChick Interactions

Parental effort can be quite variable in birds and hence in its effects on parent condition. Triglyceride levels and presumably energy reserves in male burrowing parrots (Cyanoliseus patagonus) decrease as the number of chicks increases (Masello & Quillfeldt, 2004). As parental effort must generally vary with clutch or brood size, it is reasonable to ask whether PRL or other hormones fine-tune the level of parental effort. Adult feeding behavior is certainly influenced by hungry chicks (Nunez-de la Mora, Drummond, & Wingfield, 1996; Kitaysky, Kitaiskaia, Piatt, & Wingfield, 2003), but whether adjustments in PRL mediate this response is not clear. Intensity of parental care is not tightly correlated with individual variation in PRL titer in most species that have been examined (Silverin & Goldsmith, 1984; Janik & Buntin, 1985; Ketterson, Nolan, Wolf, & Goldsmith, 1990; Vleck et al., 1991; Buntin,

Near the time of hatching, embryos can begin to vocalize as they fill their lungs from the air cell. This vocalization can affect the development of siblings within the nest, causing the last-laid eggs to speed up development and decrease hatching asynchrony (Vince, 1979). Eggs of glaucouswinged gulls (Larus glaucenscens) incubated in contact with each other will hatch relatively synchronously compared to eggs that are not in contact (Schwagmeyer, Mock, Lamey, & Becher, 1991), which will modify the amount of time for which the parent must incubate. After pipping, chicks in American white pelican (Pelecanus erythrorhynchos) eggs increase their rate of calling when they are cooled, and subsequently they are incubated at a higher temperature than unpipped eggs, suggesting that embryo vocalizations influence adult behavior (Evans, 1990). Vocalizations of embryos late in development may

192

be responsible for the increase in PRL seen at the end of incubation in common eiders (Criscuolo et al., 2002a). Maternal deposition of steroids in yolk is known to affect behavior of chicks after hatching, including begging (Groothuis & Schwabl, 2008), and begging behavior in chicks elicits more feeding by parents in most species. Female collared flycatchers (Ficedula albicollis) increase the deposition of yolk T in their eggs when they are mated with younger males, who tend to invest less in paternal behavior compared to older males (Michl, Torok, Peczely, Garamszegi, & Schwabl, 2005). This may be a compensatory tactic of the female if higher yolk T allocation increases nestling begging, which in turn elicits more male feeding, although this has not yet been demonstrated in this species.

5. TESTOSTERONE (T) AND MALE PARENTAL BEHAVIOR Male birds that contribute to parental care often have elevated levels of T during courtship and mating stages, similar to species in which males do not show parental care; however, in the former, T levels usually decrease dramatically when eggs are laid and the males enter the parental phase of reproduction (e.g. Lynn, Hayward, BenowitzFredericks, & Wingfield, 2002). In Ade´lie penguins, males take the first long bout of incubation on the eggs, and, as incubation begins, T decreases to less than 2% of the level in the courtship phase (Vleck et al., 1999). In yellow-eyed penguins (Megadyptes antipodes) this drop can even be stimulated by an artificial egg in the nest (Massaro et al., 2007). This pattern of change in T matches a prediction of the ‘challenge hypothesis,’ which relates patterns of T secretion to mating systems (Wingfield, Hegner, Dufty, & Ball, 1990). That prediction follows from the observation that moderate levels of T stimulate gonadal development and courtship behavior, while higher levels enhance aggressive behavior. When aggressive responses following challenges to territorial ownership or mate access are important, T levels should be high and increase rapidly in response to challenge. When contributing parental care has a greater impact on fitness, and if aggression interferes with such care, T levels should drop and be less sensitive to challenge when birds enter the parental phase. Androgen supplementation is known to disrupt or decrease parental behavior in many free-living species (Silverin, 1980; Hegner & Wingfield, 1987; Oring, Fivizzani, & El Halawani, 1989; Ketterson et al., 1992; Clotfelter, Chandler, Nolan, & Ketterson, 2007). Testosterone does not necessarily block the display of parental behavior, but rather seems to increase the likelihood that birds will engage in other behaviors (e.g. courtship or territorial defense) at the expense of parental behavior. In contrast, T-implanted male

Hormones and Reproduction of Vertebrates

great tits (Parus major) do not decrease chick provisioning behavior but they do display more aggressive behaviors, although, as the authors point out, the elevation of T in this study was not very great (Van Duyse, Pinxten, & Eens, 2002). Administration of GnRH elevates T in individual dark-eyed juncos and decreases parental effort (McGlothlin, Jawor, & Ketterson, 2007). The behavioral effect of T supplementation in male azure-winged magpies (Cyanopica cyanus) depends on whether the birds are breeders or helpers in this cooperatively breeding species (De la Cruz, Solis, Valencia, Chastel, & Sorci, 2003). Breeders reduce paternal care when T is elevated, but helpers respond by increasing care given to young. Male blue-headed vireos develop a brood patch, incubate, and have relatively low T and high PRL throughout the reproductive cycle compared to congeneric red-eyed vireos, which do not incubate and have elevated T early in the season (Figure 7.4). In both species, males do feed the young and by this stage T has fallen and PRL has risen in the red-eyed vireo as well (Van Roo et al., 2003). Experimental elevation of T in incubating blue-headed vireos decreases their contributions to incubation and nestling care but increases their singing behavior (Van Roo, 2004). In European starlings (Sturnus vulgaris), some males are monogamous and show extensive incubation and chickfeeding behavior, whereas others are polygynous and do not incubate extensively. The proportion of time males spend incubating in this species decreases as T increases (Pinxten, De Ridder, Arckens, Darras, & Eens, 2007). Manipulation of T in male chestnut-collared longspurs (Calcarius ornatus) reduces nest sentry behavior during incubation but has no effect on brooding or feeding behavior after hatching, suggesting that longspurs may lose sensitivity to T when chicks are present (Lynn et al., 2002).

FIGURE 7.4 Plasma testosterone (T) (solid lines) and prolactin (PRL) (dashed lines) across reproductive stages in males of two vireos (species) that differ in paternal behavior. Blue-headed (BH) vireos participate in incubation and feed their young, and red-eyed (RE) vireos do not incubate, although they do feed their young. Values are means standard error of the mean (SEM). Reproduced from Van Roo, Ketterson, and Sharp (2003).

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

The peak values of T found in males and females are correlated across species, perhaps because directional selection for elevated T in males elevates the level in the females as well (Møller, Garamszegi, Gil, HurtrezBouss’es, & Eens, 2005). Although T does appear to limit parental behavior in male birds, the results are not clear in females. Female dark-eyed juncos with experimentally elevated T show incubation and nest defense behavior similar to control females (Clotfelter et al., 2004). In a recent review, Lynn (2008) concludes that in the majority of species studied there is ample evidence for a T-mediated tradeoff between sexual or territorial behavior and parental care. She suggests that, in some species where paternal care is particularly important, not only do T levels drop below courtship levels in the nestling phase, when male parental care is critical, but also males may become insensitive to the disruptive effects of exogenous T. As we increase knowledge of hormonal changes and behavior from a wide variety of taxa living under different ecological and social conditions, additional insights into mechanisms are likely to emerge.

6. EFFECTS OF ENVIRONMENTAL STRESS ON PARENTAL BEHAVIORdROLES OF CORTICOSTERONE (CORT) AND PROLACTIN (PRL) Care of eggs and young diverts time and energy from selfmaintenance. When environmental conditions are stressful and birds are time- or energy-limited, they need to make decisions as to whether to continue with a reproductive effort, reduce their parental effort, or abandon their eggs or chicks in hope of surviving until better times return. The hormones CORT and PRL are implicated in the behavioral responses of breeding birds to stress. Activation of the hypothalamicepituitaryeadrenal (HPA) axis and resultant adrenal CORT secretion is the major hormonal mechanism used to deal with stress (see Chapter 5, this volume). Corticosterone secretion enhances survival through a series of events including redirecting behavior and mobilizing energy reserves (Wingfield et al., 1998; Landys, Ramenofsky, & Wingfield, 2006). For example, CORT implants in the chicks of black-legged kittiwakes increase their begging behavior, while CORT implants in the parents cause them to increase foraging at the expense of chick guarding (Kitaysky, Wingfield, & Piatt, 2001). Elevated CORT can also inhibit the HPG axis and reproduction (Etches, Williams, & Rzasa, 1984), but, at high latitudes or elevations where breeding seasons are short, it may be advantageous to suppress this glucocorticoid response because there is no time for a second reproductive effort; i.e., the fitness cost of a reproductive failure may be greater than the potential benefit in terms of

193

survival (Wingfield & Hunt, 2002). In dusky flycatchers (Empidonax oberholseri), e.g., baseline and stress-induced CORT levels decline at the onset of incubation (Pereyra & Wingfield, 2003), which the authors attribute to an adaptive modulation of the adrenal stress response in an unpredictable (high-elevation) environment. The relative adaptive value of suppressing a stress response that could interfere with parental behavior should increase late in a reproductive cycle, because the costs of completing the reproductive cycle should decrease and any window of opportunity for restarting the cycle should be closing. Male yellow warblers breeding in the arctic show a reduced stress response when they are feeding chicks compared to during incubation, and females show a suppressed response during both incubation and feeding stages (Wilson & Holberton, 2004). Such a strategy presumably acts to maximize current reproductive effort at the risk of decreased survival (Wingfield & Sapolsky, 2003), and would be most likely to evolve in species in which adult survivorship is low. Not surprisingly, attenuation of the stress response during parental care is far from universal, particularly in long-lived species with high future reproductive potential. In blacklegged kittiwakes (Rissa tridactyla), baseline CORT and the CORT stress response do not seem to vary systematically with reproductive stage, but reflect local variation in food availability (Shultz & Kitaysky, 2008). Prolactin levels also respond to stress, which is of interest because of PRL’s strong effects on parental behavior. Stress tends to decrease PRL levels in birds (Maney et al., 1999; Chastel et al., 2005; Angelier et al., 2007a). Corticosterone and PRL typically have opposing effects on parental behavior and CORT can directly affect PRL secretion rates. In black-legged kittiwakes that are feeding chicks, CORT implants cause a short-term (twoday) decrease in PRL of about 30%, reducing both nest attendance and breeding success (Angelier, ClementChastel, Welcker, Gabrielsen, & Chastel, 2009). In general, we know very little about the relative importance to behavioral changes of stress-induced changes in PRL and CORT, or how breeding stage may affect responses of the two hormones to stress. Black-legged kittiwakes show reduced plasma PRL levels following a standardized capture/restraint stress protocol, which also elevates CORT. Prolactin levels drop about 10% in birds feeding chicks, but about 40% in failed breeders. Corticosterone is elevated equally by the restraint (about six-fold) in both groups (Chastel et al., 2005). The authors suggest that, in the face of elevated CORT, which should increase adult foraging and reduce nest attentiveness, the attenuation of the PRL response to stress in the breeding birds as opposed to the failed breeders helps to maintain parental effort in the former. Prolactin and CORT can have pervasive effects on parental behavior and resulting large effects on fitness. Age

194

and experience can modify these actions. Stress increases CORT and decreases PRL levels in incubating snow petrels (Pagodroma nivea), and egg neglect increases as PRL levels fall. The CORT response does not vary with age, but the PRL response does. Older birds maintain PRL levels during stress better than younger birds, which may account for the increase in reproductive success with age in snow petrels (Angelier et al., 2007a). In another long-lived species, the black-browed albatross (Thallasarche melanophris), the very oldest birds have the highest baseline CORT and lowest PRL levels and also the lowest probability of fledging young, so changes in hormonal signaling are probably associated with reproductive senescence (Angelier et al., 2007b). Environmental stressors impact both CORT and PRL levels, but either or both of these responses can be modulated. Independent changes in CORT and PRL response to stress may increase the ability of birds to reproduce in a range of environments (see Angelier & Chastel, 2009) and to adjust their strategy with age and reproductive value. Our understanding of variation in life-history strategies will be greatly enhanced as we learn more about how these two hormonal systems interact to influence parental behavior in birds.

7. SPECIAL CASES OF PARENTAL BEHAVIOR 7.1. Obligate Brood Parasites Obligate brood parasites lay eggs and exhibit no parental behavior past egg laying. Conspecific nest parasitism also occurs when females lay some of their eggs in another’s nest, but in this case these birds do display normal parental behavior as well. This behavior is common in some duck species (Dugger & Blums, 2001). The question of why obligate brood parasites show no parental behavior other than locating an acceptable host nest is of interest. One obligate brood parasite, the brown-headed cowbird, displays a seasonal rise in plasma PRL (Dufty, Goldsmith, & Wingfield, 1987). This suggests that sensitivity to PRL’s effects on the urge to incubate can be decreased and the behavior eliminated, possibly by decreasing PRLbinding activity within the brain (Ball, Dufty, Goldsmith, & Buntin, 1988). Parasitic chicks of brown-headed cowbirds display more vigorous begging behavior than their nestmates, presumably to induce their adoptive parents to feed them preferentially (Hosoi & Rothstein, 2000). Maternally deposited yolk hormones can influence the behavior of the chicks (increase their begging behavior), which can then influence parental feeding behavior (Mu¨ller, Lessells, Korsten, & Von Engelhardt, 2007), so it would seem adaptive for yolk androgens to be higher in eggs of parasitic species than in their hosts. This prediction was tested in the brown-headed cowbird, but yolk T concentrations were not consistently higher than in the hosts’ eggs, although

Hormones and Reproduction of Vertebrates

cowbird chicks possibly have greater sensitivity to androgens (Hauber & Pilz, 2003). Eggs of the parasitic common cuckoo (Cuculus canorus) have similar yolk T concentrations (albeit larger absolute yolks) compared to those in the eggs of their hosts, despite more vigorous begging behavior in the cuckoo chicks than in the host chicks (Torok, Moskat, Michl, & Peczely, 2004).

7.2. Helpers at the Nest Over 800 species of birds (about 9% of the total number of species) in a variety of families show cooperative breeding, in which nonbreeding individuals help to raise the young of breeders to whom they may or may not be closely related (Cockburn, 2006). The evolution of such alloparental behavior has received much attention because of the presumed fitness costs to birds that expend time or energy to feed the incubating female or care for young that are not their offspring (Brown, 1987; Stacey & Koenig, 1990; Koenig & Dickinson, 2004). Analysis of kin selection suggests that, in many species, helpers increase their fitness by helping to raise close relatives (Hamilton, 1964). In other cases, indirect benefits can be assigned to helpers, such as the ability to stay within a productive territory rather than disperse, to inherit a breeding position within the breeding unit, or to obtain practice in parental duties (Mumme, 1997). The alloparental care, usually in the form of feeding nestlings, provided by such helpers may increase fledging success (Simon, Pratt, Berlin, & Kowalsky, 2001) or relieve the reproductive burden on the breeders (Grimes & Logan, 2001; Radford, 2004), enhancing parent survival. Such could be the case in species such as the laughing kookaburra (Daceo novaeguineae), where helpers do not alter provisioning rate to the nestlings because each individual in a group reduces its parental effort as group size increases (Legge, 2000). The hormonal basis for helping at the nest has been studied in a number of bird species (reviewed in Schoech, Reynolds, & Boughton, 2004). One important question concerns whether or not the helpers are reproductively competent. In pied kingfishers (Ceryle rudis), unrelated male helpers have T levels equivalent to those of breeding males, but related male helpers do not (Reyer, Dittami, & Hall, 1986). Adult male helpers in several other species also have elevated T during the breeding season (Mays, Vleck, & Dawson, 1991; Schmidt, Bradshaw, & Follett, 1991; Schoech, Mumme, & Wingfield, 1996a; Vleck & Brown, 1999; Khan et al., 2001). In contrast, helper males in bell miners (Manorina melanophrys), white-browed sparrowweavers (Plocepasser mahali), and superb fairy-wrens (Malurus cyaneus) have lower T and smaller testes than breeding males. Similarly, helper female sparrow-weavers have smaller ovaries than breeding females (Wingfield, Hegner, & Lewis, 1991; Poiani & Fletcher, 1994; Peters,

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

Astheimer, & Cockburn, 2001), and helper females in Harris’ hawks have lower E2 levels than do breeding females (Mays et al., 1991). Steroid profiles of helpers appear to reflect the likelihood that, if an individual had an opportunity to breed, it could quickly achieve breeding status. Another question raised by helping behavior is what physiological mechanisms promote such alloparental behavior. In Mexican jays, helpers at the nest have elevated PRL levels (compared to winter levels) even before they are exposed to begging young, suggesting that it is not just the sight of begging young that elevates PRL in helpers. Both breeder and helper Mexican jays have levels of PRL that are about twice those of breeders in the closely related and sympatric scrub jay (Aphelocoma californica), measured in the same assay. Scrub jays do not show helping behavior, and elevated PRL in the Mexican jay may have evolved because it promoted helping behavior (Brown & Vleck, 1998). Similar elevation of PRL of helpers has been reported in red-cockaded woodpeckers (Picoides borealis) (Khan et al., 2001), Florida scrub jays (Aphelocoma coerulescens) (Schoech et al., 1996b), and Harris’ hawks (Vleck et al., 1991). Although helping behavior has evolved independently multiple times in birds, in each of the studied cases the mechanism involves elevation of PRL production.

7.3. Effects of Domestication on Hormonal and Behavioral Patterns The neural and hormonal basis of parental behavior has been studied extensively in a few domesticated species, including chickens, turkeys, domesticated ring doves (Buntin, 1996), and Japanese quail (Coturnix japonica) (Mills, Crawford, Domjan, & Maure, 1997), although the behavior of the ancestral free-living forms is often poorly known. Domesticated species have often experienced selection in captivity for a promiscuous mating system, rapid maturation, high egg production, reduced seasonality, and reduced parental behavior (broodiness). However, extreme artificial selection to increase rates of egg production and limit broody behavior has had limited success. Both traits are likely to involve interaction of multiple genes, which also affect other determinants of reproduction and fitness. Another commercially attractive approach is targeted interference with endocrine signaling. One goal of poultry endocrinology has been to understand how broodiness of chickens can be hormonally inhibited in order to increase egg production (Sharp, 1997). Pharmacological and immunological treatments that block PRL secretion can be used to limit broody behavior in chickens and turkeys. Reduction of PRL activity via inhibition of the avian PRL-releasing hormone, VIP, reduces incubation behavior in chickens, and the effect can be prevented by simultaneous injection of PRL (Sharp, Sterling, Talbot, &

195

Huskisson, 1989). In ring doves, this treatment reduces PRL levels but not incubation behavior (Lea, Talbot, & Sharp, 1991). Immunization against their own PRL decreases its activity and reduces incubation behavior in turkey hens (Crisostomo, Guemene, Garreau-Mills, Morvan, & Zadworny, 1998) and in bantam hens (March, Sharp, Wilson, & Sang, 1994). Pharmacological treatments, however, are logistically challenging and expensive in commercial applications, and a recent approach to selecting for decreased broodiness in chickens has been to examine polymorphisms in the genes for PRL, the PRL receptor, and VIP and their effects on behavior (Jiang, Xu, Zhang, & Yang, 2005; Zhou et al., 2008). These studies have led to the identification of specific gene sequences that could be used as markers in selection experiments against broodiness. It seems only a matter of time until a deeper understanding of how to enhance desired traits and decrease others will be achieved based on understanding the genes controlling hormones and behavior in birds.

8. FUTURE RESEARCH The general patterns by which hormones affect parental behaviors are well-understood in birds, but much remains to be discovered about the extent and importance of variations in those patterns. At the cellular and molecular level, understanding of the mechanisms by which hormones affect behavior or how the two reinforce each other is in its infancy (Ball & Balthazart, 2008). For example, courtship and nest-building behavior in male ring doves elevates GnRH gene expression in the preoptic area of the brain, which presumably further stimulates behavior through pituitary and gonadal hormones (Mantei et al., 2008). Prolactin in ring doves increases neuropeptide Y gene expression, which in turn stimulates hyperphagia (Ramakrishnan et al., 2007), an adaptive response in this species, which must produce crop milk to feed its young. At the whole-organism level, much remains to be learned about integration among different endocrine systems and their coordination with the environment. The relationship between the HPA stress axis and PRL and their impact on parental care under stressful conditions is an active area of research (Angelier & Chastel, 2009), as are the mechanisms by which T and PRL secretion coordinate the tradeoff between sexual or aggressive behaviors and parental behaviors in different species (Lynn, 2008). We are beginning to learn more about how endocrine control is related to individual differences in reproductive behavior (Ball & Balthazart, 2008). Male European starlings may or may not participate in incubation (Reid et al., 2002). Male assistance decreases incubation periods and increases hatching success, but such males also produce less well-insulated nests and are less likely to mate with multiple females, which suggests fitness tradeoffs in male

196

Hormones and Reproduction of Vertebrates

parental behavior in this species. Knowledge of whether and how variation in endocrine control affects individual variation in behavior will be necessary if we are to fully understand the evolution of behavior (Kempenaers, Peters, & Foerster, 2008). Between-species comparisons in order to study hormonal control of behavior have routinely been carried out with two or just a few species (Hector & Goldsmith, 1985; Brown & Vleck, 1998; Van Roo et al., 2003), and such comparative studies would be much stronger if carried out with more species and placed within a phylogenetic context. The appearance of such comparative studies on hormonal control systems is beginning (Garamszegi, Eens, HurtrezBousses, & Møller, 2005; Møller et al., 2005; Schwabl, Palacios, & Martin, 2007; Bokony, Garamszegi, Hirschenhauser, & Liker, 2008). Such comparative studies require sufficient data to provide robust results and assurance that the methods and data are comparable between studies. Prolactin is found in all vertebrate species examined and is associated with a wide range of physiological responses including osmoregulation, growth, metamorphosis, and immune function, as well as parental care in a number of vertebrates (Norris, 2007). Prolactin is the most important hormone controlling parental behavior in birds, yet birds show an amazing array of behaviors in taking care of their eggs and young. The evolution of this diversity has not altered or replaced the central role of PRL, but evolution has acted to adjust control of PRL secretion, changes in interaction with other hormones, and probably receptor and signal transduction mechanisms as well. Birds provide a powerful system for identifying alternative pathways for modulating hormonal control of behavior and for understanding the functional consequences of such modulations.

ABBREVIATIONS CORT E2 GnRH HPA HPG LH P4 P450aro PCB T VIP

Corticosterone Estradiol Gonadotropin-releasing hormone Hypothalamicepituitaryeadrenal Hypothalamicepituitaryegonadal Luteinizing hormone Progesterone Aromatase Polychlorinated biphenyl Testosterone Vasoactive intestinal peptide

REFERENCES Adkins-Regan, E. (2007). Hormones and the development of sex differences in behavior. Journal of Ornithology, 148, S17eS26. Al Kahtane, A., Chaiseha, Y., & El Halawani, M. (2003). Dopaminergic regulation of avian prolactin gene transcription. Journal of Molecular Endocrinology, 31, 185e196.

Andersson, M. (1995). Evolution of reversed sex-roles, sexual size dimorphism, and mating system In coucals (Centropodidae, Aves). Biological Journal of the Linnean Society, 54, 173e181. Angelier, F., Barbraud, C., Lorme´e, H., Prud’homme, F., & Chastel, O. (2006a). Kidnapping of chicks in emperor penguins: a hormonal byproduct? Journal of Experimental Biology, 209, 1413e1420. Angelier, F., & Chastel, O. (2009). Stress, prolactin and parental investment in birds: a review. General and Comparative Endocrinology, 163, 142e148. Angelier, F., Clement-Chastel, C., Welcker, J., Gabrielsen, G. W., & Chastel, O. (2009). How does corticosterone affect parental behaviour and reproductive success? A study of prolactin in black-legged kittiwakes. Functional Ecology, 23, 784e793. Angelier, F., Moe, B., Weimerskirch, H., & Chastel, O. (2007a). Agespecific reproductive success in a long-lived bird; do older parents resist stress better? Journal of Animal Ecology, 76, 1181e1191. Angelier, F., Shaffer, S. A., Weimerskirch, H., & Chastel, O. (2006b). Effect of age, breeding experience and senescence on corticosterone and prolactin levels in a long-lived seabird: the wandering albatross. General and Comparative Endocrinology, 149, 1e9. Angelier, F., Weimerskirch, H., Dano, S., & Chastel, O. (2007b). Age, experience and reproductive performance in a long-lived bird: a hormonal perspective. Behavioral Ecology and Sociobiology, 61, 611e621. Ardia, D. R., Cooper, C. B., & Dhondt, A. A. (2006). Warm temperatures lead to early onset of incubation, shorter incubation periods and greater hatching asynchrony in tree swallows Tachycineta bicolor at the extremes of their range. Journal of Avian Biology, 37, 137e142. Ball, G. F., & Balthazart, J. (2008). Individual variation and the endocrine regulation of behaviour and physiology in birds: a cellular/molecular perspective. Philosophical Transactions of the Royal Society BBiological Sciences, 363, 169e1710. Ball, G. F., & Ketterson, E. D. (2008). Sex differences in the response to environmental cues regulating seasonal reproduction in birds. Philosophical Transactions of the Royal Society of London B Biological Sciences, 363, 231e246. Ball, G. F., Dufty, A. M., Goldsmith, A. R., & Buntin, J. D. (1988). Autoradiographic localization of brain prolactin receptors in a parental and non-parental songbird species. Society for Neuroscience Abstracts, 14, 88. Blomqvist, D., Wallander, J., & Andersson, M. (2001). Successive clutches and parental roles in waders: the importance of timing in multiple clutch systems. Biological Journal of the Linnean Society, 74, 549e555. Bokony, V., Garamszegi, L. Z., Hirschenhauser, K., & Liker, A. (2008). Testosterone and melanin-based black plumage coloration: a comparative study. Behavioral Ecology and Sociobiology, 62, 1229e1238. Book, C. M., Millam, J. R., Guinan, M. J., & Kitchell, R. L. (1991). Brood patch innervation and its role in the onset of incubation in the turkey hen. Physiology and Behavior, 50, 281e285. Boos, M., Zimmer, C., Carriere, A., Robin, J. P., & Petit, O. (2007). Posthatching parental care behaviour and hormonal status in a precocial bird. Behavioural Processes, 76, 206e214. Borgia, G., & Wingfield, J. C. (1991). Hormonal correlates of bower decoration and sexual display in the satin bowerbird (Ptilonrhynchus violaceus). Condor, 93, 935e942.

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

Brown, J. L. (1987). Helping and Communal Breeding in Birds: Ecology and Evolution. Princeton, NJ: Princeton University Press. Brown, J. L., & Vleck, C. M. (1998). Prolactin and helping in birds: has natural selection strengthened helping behavior? Behavioral Ecology, 9, 541e545. Brunning, D. F. (1974). Social structure and reproductive behavior in the greater rhea. Living Bird, 1974, 251e294. Buntin, J. D. (1996). Neural and hormonal control of parental behavior in birds. Advances in the Study of Behavior, 25, 161e213. Buntin, J. D., Hnasko, R. M., Zuzick, P. H., Valentine, D. L., & Scammell, J. G. (1996). Changes in bioactive prolactin-like activity in plasma and its relationship to incubation behavior in breeding ring doves. General and Comparative Endocrinology, 102, 221e232. Be´de´carrats, G., Gue´mene´, D., & Richard-Yris, M. A. (1997). Effects of environmental and social factors on incubation behavior, endocrinological parameters, and production traits in turkey hens (Meleagris gallopavo). Poultry Science, 76, 1307e1314. Camphuysen, K. (2002). Post-fledging dispersal of common guillemots Uria aalge guarding chicks in the North Sea: the effect of predator presence and prey availability at sea. Ardea, 90, 103e119. Chaiseha, Y., Tong, Z., Youngren, O. M., & El Halawani, M. E. (1998). Transcriptional changes in hypothalamic vasoactive intestinal peptide during a photo-induced reproductive cycle in the turkey. Journal of Molecular Endocrinology, 21, 267e275. Chastel, O., & Lorme´e, H. (2002). Patterns of prolactin secretion in relation to incubation failure in a tropical seabird, the red-footed booby. Condor, 104, 873e876. Chastel, O., Lacroix, A., Weimerskirch, H., & Gabrielsen, G. W. (2005). Modulation of prolactin but not corticosterone responses to stress in relation to parental effort in a long-lived bird. Hormones and Behavior, 47, 459e466. Cheng, M.-F., & Silver, R. (1975). Estrogen-progesterone regulation of nest building and incubation behavior in ovariectomized ring doves (Streptopelia risoria). Journal of Comparative Physiology and Psychology, 88, 256e263. Cherel, Y., Mauget, R., Lacroix, A., & Gilles, J. (1994). Seasonal and fasting-related changes in circulating gonadal steroids and prolactin in king penguins, Aptenodytes patagonicus. Physiological Zoology, 76, 1154e1173. Christensen, D., & Vleck, C. M. (2008). Prolactin release and response to vasoactive intestinal peptide in an opportunistic breeder, the zebra finch (Taeniopygia guttata). General and Comparative Endocrinology, 157, 91e98. Clotfelter, E. D., Chandler, C. R., Nolan, V. J., & Ketterson, E. D. (2007). The influence of exogenous testosterone on the dynamics of nestling provisioning in dark-eyed juncos. Ethology, 113, 18e25. Clotfelter, E. D., O’Neal, D. M., Gaudioso, J. M., Casto, J. M., ParkerRenga, I. M., Snajdr, E. A., et al. (2004). Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution? Hormones and Behavior, 46, 171e178. Cockburn, A. (2006). Prevalence of different modes of parental care in birds. Proceedings of the Royal Society Biological Sciences Series B, 273, 1375e1383. Collias, N. E., & Collias, E. C. (1984). Nest Building and Bird Behavior. Princeton, NJ: Princeton University Press. Cook, M. I., Beissinger, S. R., Toranzos, G. A., Rodriguez, R. A., & Arendt, W. J. (2003). Trans-shell infection by pathogenic micro-

197

organisms reduces the shelf life of non-incubated bird’s eggs: a constraint on the onset of incubation? Proceedings of the Royal Society Biological Sciences Series B, 270, 2233e2240. Cook, M. I., Beissinger, S. R., Toranzos, G. A., Rodriguez, R. A., & Arendt, W. J. (2005). Microbial infection affects egg viability and incubation behavior in a tropical passerine. Behavioral Ecology, 16, 30e36. Criscuolo, F., Bertile, F., Durant, J. M., Raclot, T., Gabrielsen, G. W., Massemin, S., et al. (2006). Body mass and clutch size may modulate prolactin and corticosterone levels in eiders. Physiological and Biochemical Zoology, 79, 514e521. Criscuolo, F., Chastel, O., Bertile, F., Gabrielsen, G. W., Le Maho, Y., & Raclot, T. (2005). Corticosterone alone does not trigger a short term behavioural shift in incubating female common eiders Somateria mollissima, but does modify long term reproductive success. Journal of Avian Biology, 36, 306e312. Criscuolo, F., Chastel, O., Gabrielsen, G. W., Lacroix, A., & Le Maho, Y. (2002a). Factors affecting plasma concentrations of prolactin in the common eider Somateria mollissima. General and Comparative Endocrinology, 125, 399e409. Criscuolo, F., Gabrielsen, J. P., Gendner, J. P., & Le Maho, Y. (2002b). Body mass regulation during incubation in female common eiders Somateria mollissima. Journal of Avian Biology, 33, 83e88. Crisostomo, S., Guemene, D., Garreau-Mills, M., Morvan, C., & Zadworny, D. (1998). Prevention of incubation behavior expression in turkey hens by active immunization against prolactin. Theriogenology, 50, 675e690. Crook, J. H., & Butterfield, P. A. (1968). Effects of testosterone propionate and luteinizing hormone on agonistic and nest building behaviour of Quelea quelea. Animal Behaviour, 16, 370e390. Dawson, A., & Goldsmith, A. R. (1982). Prolactin and gonadotropin secretion in wild starlings Sturnus vulgaris during the annual cycle and in relation to nesting incubation and rearing young. General and Comparative Endocrinology, 48, 213e221. De la Cruz, C., Solis, E., Valencia, J., Chastel, O., & Sorci, G. (2003). Testosterone and helping behavior in the azure-winged magpie (Cyanopica cyanus): natural covariation and an experimental test. Behavioral Ecology and Sociobiology, 55, 103e111. Delahanty, D. J., Fleischer, R. C., Colwell, M. A., & Oring, L. (1998). Sex-role reversal and the absence of extra-pair fertilization in the Wilson’s phalaropes. Animal Behaviour, 55, 995e1002. Delahanty, D. J., Oring, L. W., Fivizzani, A. J., & El Halawani, M. E. (1997). Circulating prolactin of incubating male Wilson’s phalaropes corresponds to clutch size and environmental stress. Condor, 99, 397e405. Dhondt, A. A., Eykerman, R., & Huble, J. (1983). Laying interruptions in tits Parus spp. Ibis, 125, 30e376. Dittami, J. (1981). Seasonal changes in the behavior and plasma titers of various hormones in barheaded geese, Anser indicus. Zeitshrift fu¨r Tierpsychologie, 55, 289e324. Dufty, A. M., Jr., Goldsmith, A. R., & Wingfield, J. C. (1987). Prolactin secretion in a brood parasite: the brown-headed cowbird, Molothrus ater. Journal of Zoology (London), 212, 669e675. Dugger, B. D., & Blums, P. (2001). Effect of conspecific brood parasitism on host fitness for tufted duck and common pochard. Auk, 118, 717e726. Dzus, E. H., & Clark, R. G. (1997). Brood size manipulation in mallard ducks: effects on duckling survival and brooding efficiency. Ecoscience, 4, 437e445.

198

Eens, M., & Pinxten, R. (2000). Sex-role reversal in vertebrates: behavioural and endocrinological accounts. Behavioural Processes, 51, 135e147. El Halawani, M. E., Burke, W. H., & Dennison, P. T. (1980). Effects of nest-deprivation on serum prolactin level in nesting female turkeys. Biology of Reproduction, 23, 118e123. El Halawani, M. E., Silsby, J. L., Rozenboim, I., & Pitts, G. R. (1986). Hormonal induction of incubation in ovariectomized female turkeys (Meleagris gallopavo). Biology of Reproduction, 35, 59e67. Emlen, S., & Oring, L. (1977). Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215e223. Etches, R. J., Garbutt, A., & Middleton, A. L. (1979). Plasma concentrations of prolactin during egg laying and incubation in the ruffed grouse (Bonasa umbellus). Canadian Journal of Zoology, 57, 1624e1627. Etches, R. J., Williams, J. B., & Rzasa, J. (1984). Effects of corticosterone and dietary changes in the hen on ovarian function, plasma LH and steroids and the response to exogenous LH-RH. Journal of Reproductive Fertility, 70, 121e130. Evans, M. R., & Goldsmith, A. R. (2000). Male wrens with large testes breed early. Animal Behaviour, 60, 101e105. Evans, R. M. (1990). Vocal regulation of temperature by avian embryos: a lab study with pipped eggs of the American white pelican. Animal Behaviour, 40, 969e979. Fowler, G. S., Wingfield, J. C., Boersma, P. D., & Sosa, R. A. (1994). Reproductive endocrinology and weight change in relation to reproductive success in the Magellanic penguin (Spheniscus magellanicus). General and Comparative Endocrinology, 94, 305e315. Frith, H. J. (1956). Breeding habits in the family Megapodiidae. Ibis, 98, 620e640. Garamszegi, L. Z., Eens, M., Hurtrez-Bousses, S., & Møller, A. P. (2005). Testosterone, testes size, and mating success in birds: a comparative study. Hormones and Behavior, 47, 389e409. Garcia, V., Jouventin, P., & Mauget, R. (1996). Parental care and the prolactin secretion pattern in the king penguin: an endogenously timed mechanism? Hormones and Behavior, 30, 259e265. Goldsmith, A. R. (1991). Prolactin and avian reproductive strategies. Acta Congressus Internationalis Ornithologici XX, 4, 2063e2071. Goldsmith, A. R., & Williams, D. M. (1980). Incubation in mallards (Anas platyrhynchos): changes in plasma levels of prolactin and luteinizing hormone. Journal of Endocrinology, 86, 371e380. Goldsmith, A. R., Burke, S., & Prosser, J. M. (1984). Inverse changes in plasma prolactin and luteinizing hormone concentrations in female canaries after disruption and reinitiation of incubation. Journal of Endocrinology, 103, 251e256. Goth, A. (2002). Behaviour of Australian brush-turkey (Alectura lathami, Galliformes: Megapodiidae) chicks following underground hatching. Journal fu¨r Ornithologie, 143, 477e488. Goth, A. (2008). Incubation temperatures and sex ratios in Australian brush-turkey (Alectura lathami) mounds. Austral Ecology, 32, 378e385. Goth, A., & Booth, D. T. (2005). Temperature-dependent sex ratio in a bird. Biology Letters, 1, 31e33. Goth, A., & Vogel, U. (2002). Chick survival in the megapode Alectura lathami (Australian brush-turkey). Wildlife Research, 29, 503e511. Gratto-Trevor, C. L., Oring, L. W., Fivizzani, A. J., El Halawani, M. E., & Cooke, F. (1990). The role of prolactin in parental care in a monogamous and a polyandrous shorebird. Auk, 107, 718e729.

Hormones and Reproduction of Vertebrates

Grimes, J., & Logan, C. (2001). Nest attendants in parakeet auklets. Zoo Biology, 20, 271e277. Groothuis, T. G. G., & Schwabl, H. (2008). Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Philosophical Transactions of the Royal Society of London B Biological Sciences, 363, 1647e1661. Groscolas, R., & Robin, J.-P. (2001). Long-term fasting and re-feeding in penguins. Comparative Biochemistry and Physiology Part A. Molecular and Integrative Physiology, 128A, 645e655. Groscolas, R., Lacroix, A., & Robin, J.-P. (2008). Spontaneous egg or chick abandonment in energy-depleted king penguins: a role for corticosterone and prolactin? Hormones and Behavior, 53, 51e60. Haftorn, S. (1988). Incubating female passerines do not let the egg temperature fall below the ‘physiological zero temperature’ during their absences from the nest. Ornis Scandinavica, 19, 97e110. Hainsworth, F. R., & Voos, M. A. (2002). Intermittent incubation: predictions and tests for time and heat allocations. In D. C. Deeming (Ed.), Avian Incubation (pp. 223e237). Oxford, UK: Oxford University Press. Hall, M. R. (1986). Plasma concentrations of prolactin during the breeding cycle in the cape gannet (Sula capensis): a foot incubator. General and Comparative Endocrinology, 64, 112e121. Hall, M. R. (1987a). External stimuli affecting incubation behavior and prolactin secretion in the duck Anas platyrhynchos. Hormones and Behavior, 21, 269e287. Hall, M. R. (1987b). Nesting success in mallards after partial clutch loss by predators. Journal of Wildlife Management, 51, 530e533. Hall, M. R. (1991). Endocrinological and behavioral changes associated with the onset of incubation in the duck. Physiology and Behavior, 50, 311e316. Hamilton, W. D. (1964). The genetical evolution of social behavior II. Journal of Theoretical Biology, 7, 17e52. Handrich, Y. (1989). Incubation water loss in King penguin egg. II. Does the brood patch interfere with eggshell conductance? Physiological Zoology, 62, 119e132. Hauber, M. E., & Pilz, K. M. (2003). Yolk testosterone levels are not consistently higher in the eggs of obligate brood parasites than their hosts. American Midland Naturalist, 149, 354e362. Hector, J. A. L., & Goldsmith, A. R. (1985). The role of prolactin during incubation: comparative studies of three Diomedea albatrosses. General and Comparative Endocrinology, 60, 236e243. Heath, J. A., Frederick, P. C., Edwards, T. M., & Guillette, L. J. (2003). Reproductive physiology of free-living white ibises (Eudocimus albus) in the Florida Everglades. General and Comparative Endocrinology, 133, 118e131. Hegner, R., & Wingfield, J. (1987). Effects of experimental manipulation of testosterone levels on parental investment and breeding success in male house sparrows. Auk, 104, 462e469. Hiatt, E., Goldsmith, A. R., & Farner, D. (1987). Plasma levels of prolactin and gonadotropins during the reproductive cycle of whitecrowned sparrows (Zonotrichia leucophrys). Auk, 104, 208e217. Hinde, R. A., Steel, E., & Follet, B. K. (1974). Effect of photoperiod on oestrogen-induced nest-building in ovariectomized or refractory female canaries (Serinus canarius). Journal of Reproduction and Fertility, 40, 383e399. Hoogesteijn, A. L., DeVoogd, T. J., Quimby, F. W., De Caprio, T., & Kollias, G. V. (2005). Reproductive impairment in zebra finches (Taeniopygia guttata). Environmental Toxicology and Chemistry, 24, 219e223.

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

Hosoi, S. A., & Rothstein, S. I. (2000). Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Animal Behaviour, 59, 823e840. Hutchison, R. E. (1975a). Effects of ovarian steroids and prolactin on the sequential development of nesting behavior in female budgerigars. Journal of Endocrinology, 67, 29e39. Hutchison, R. E. (1975b). Effects of ovarian steroids and prolactin on the sequential development of nesting behavior in female budgerigars. Journal of Endocrinology, 67, 29e39. Immelmann, K., & Sossinka, R. (1986). Parental behaviour in birds. In W. Sluckin, & M. Herbert (Eds.), Parental Behaviour (pp. 8e43). Oxford, UK: Basil Blackwell. Janik, D. S., & Buntin, J. D. (1985). Behavioral and physiological effects of prolactin in incubating ring doves. Journal of Endocrinology, 105, 201e210. Jiang, R. S., Xu, G. Y., Zhang, X. Q., & Yang, N. (2005). Association of polymorphisms for prolactin and prolactin receptor genes with broody traits in chickens. Poultry Science, 84, 839e845. Johns, J. E., & Pfeiffer, E. W. (1963). Testosterone-induced incubation patches of phalarope birds. Science, 140, 1225e1225. Jones, D. N., Dekker, R. W. R. J., & Roselaar, C. S. (1995). The Megapodes. Oxford, UK: Oxford University Press. Jones, R. E. (1971). The incubation patch of birds. Biological Review, 46, 315e339. Jonsson, J. E., Afton, A. D., Alisauskas, R. T., Bluhm, C. K., & El Halawani, M. E. (2006). Ecological and physiological factors affecting brood patch area and prolactin levels in arctic nesting geese. Auk, 123, 405e418. Jouventin, P., & Mauget, R. (1996). The endocrine basis of the reproductive cycle in the king penguin (Aptenodytes patagonicus). Journal of Zoology (London), 238, 665e678. Kempenaers, B., Peters, A., & Foerster, K. (2008). Sources of individual variation in plasma testosterone levels. Philosophical Transactions of the Royal Society of London B Biological Sciences, 363, 1711e1723. Ketterson, E. D., Nolan, V. J., Wolf, L., & Goldsmith, A. R. (1990). Effect of sex, stage of reproduction, season and mate removal on prolactin in dark-eyed juncos. Condor, 92, 922e930. Ketterson, E. D., Nolan, V. J., Wolf, L., & Ziegenfus, C. (1992). Testosterone and avian life histories: effects of experimentally elevated testosterone on behavior and correlates of fitness in the darkeyed junco (Junco hyemalis). American Naturalist, 140, 980e999. Khan, M. Z., McNabb, F. M. A., Walters, J. R., & Sharp, P. J. (2001). Patterns of testosterone and prolactin concentrations and reproductive behavior of helpers and breeders in the cooperatively breeding redcockaded woodpecker (Picoides borealis). Hormones and Behavior, 40, 1e13. Kitaysky, A. S., Kitaiskaia, E. V., Piatt, J. F., & Wingfield, J. C. (2003). Benefits and costs of increased levels of corticosterone in seabird chicks. Hormones and Behavior, 43, 140e149. Kitaysky, A. S., Wingfield, J. C., & Piatt, J. F. (2001). Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behavioral Ecology, 12, 619e625. Koenig, W. D., & Dickinson, J. L. (2004). Ecology and Evolution of Cooperative Breeding in Birds. Cambridge, UK: Cambridge University Press. Kosztolanyi, A., Szekely, T., & Cuthill, I. C. (2003). Why do both parents incubate in the Kentish plover? Ethology, 109, 645e658. Kulick, R. S., Chaiseha, Y., Kang, S. W., Rozenboim, I., & El Halawani, M. E. (2005). The relative importance of vasoactive

199

intestinal peptide and peptide histidine isoleucine as physiological regulators of prolactin in the domestic turkey. General and Comparative Endocrinology, 142, 267e273. Landys, M. M., Ramenofsky, M., & Wingfield, J. C. (2006). Actions of glucocorticods at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. General and Comparative Endocrinology, 148, 132e149. Lea, R. W., & Klandorf, H. (2002). The brood patch. In D. C. Deeming (Ed.), Avian Incubation (pp. 100e118). Oxford, UK: Oxford University Press. Lea, R. W., & Sharp, P. J. (1989). Concentrations of plasma prolactin and luteinizing hormone following nest deprivation and renesting in ring doves (Streptopelia risoria). Hormones and Behavior, 23, 279e289. Lea, R. W., & Vowles, D. M. (1986). Vasoactive intestinal polypeptide stimulates prolactin release in-vivo in the ring dove (Streptopelia risoria). Experientia, 42, 420e422. Lea, R. W., Dods, A. S. M., Sharp, P. J., & Chadwick, A. (1981). The possible role of prolactin in the regulation of nesting behavior and the secretion of luteinizing hormone in broody bantams. Journal of Endocrinology, 91, 89e98. Lea, R. W., Richard-Yris, M. A., & Sharp, P. J. (1996). The effect of ovariectomy on concentrations of plasma prolactin and LH and parental behavior in the domestic fowl. General and Comparative Endocrinology, 101, 115e121. Lea, R. W., Talbot, R. T., & Sharp, P. J. (1991). Passive immunization against chicken vasoactive intestinal polypeptide suppresses plasma prolactin and crop sac development in incubating ring doves. Hormones and Behavior, 25, 283e294. Lea, R. W., Vowles, D. M., & Dick, H. R. (1986). Factors affecting prolactin secretion during the breeding cycle of the ring dove (Streptopelia risoria) and its possible role in incubation. Journal of Endocrinology, 110, 447e458. Leboucher, G., Beguin, N., Lacroix, A., & Kreutzer, M. (2000). Progesterone inhibits female courtship behavior in domestic canaries (Serinus canaria). Hormones and Behavior, 38, 123e129. Leboucher, G., Richard-Yris, M.-A., Chadwick, A., & Guemene, D. (1996). Influence of nest deprivation on behaviour, hormonal concentrations and on the ability to resume incubation in domestic hens (Gallus domesticus). Ethology, 102, 660e671. Leboucher, G., Richard-Yris, M. A., William, J., & Chadwick, A. (1990). Incubation and maternal behavior in domestic hens: influence of the presence of chicks on circulating luteinizing hormone, prolactin, and estradiol and on behavior. British Poultry Science, 31, 851e862. Legge, S. (2000). The effect of helpers on reproductive success in the laughing kookaburra. Journal Animal Ecology, 69, 714e724. Lehrman, D. S. (1996). Interaction between internal and external environments in the regulation of the reproductive cycle of the ring dove (Reprinted from: Sex and Behavior F.A. Beach, (Ed.) (pp. 344-80). Wiley, New York, 1965). In (L.D. Houck and L.C. Drikamer, Eds.) Foundations of Animal Behavior: Classic papers with Commentaries (pp. 440e465). Chicago: Chicago University Press. Loos, E. R., & Rohwer, F. C. (2004). Laying-stage nest attendance and onset of incubation in prairie nesting ducks. Auk, 121, 587e599. Lorme´e, H., Jouventin, P., Chastel, O., & Mauget, R. (1999). Endocrine correlates of parental care in an Antarctic winter breeding seabird, the emperor penguin, Aptenodytes forsteri. Hormones and Behavior, 35, 9e17.

200

Lorme´e, H., Jouventin, P., Lacroix, A., Lallemand, J., & Chastel, O. (2000). Reproductive endocrinology of tropical seabirds: sexspecific patterns in LH, steroids, and prolactin secretion in relation to parental care. General and Comparative Endocrinology, 117, 413e426. Lynn, S. E. (2008). Behavioral insensitivity to testosterone: why and how does testosterone alter paternal and aggressive behavior in some avian species but not others? General and Comparative Endocrinology, 157, 233e240. Lynn, S. E., Hayward, L. S., Benowitz-Fredericks, Z. M., & Wingfield, J. C. (2002). Behavioural insensitivity to supplementary testosterone during the parental phase in the chestnut-collared longspur, Calcarius ornatus. Animal Behaviour, 63, 795e803. Maney, D. L., Schoech, S. J., Sharp, P. J., & Wingfield, J. C. (1999). Effects of vasoactive intestinal peptide on plasma prolactin in passerines. General and Comparative Endocrinology, 113, 323e330. Mantei, K. E., Ramakrishnan, S., Sharp, P. J., & Buntin, J. D. (2008). Courtship interactions stimulate rapid changes in GnRH synthesis in male ring doves. Hormones and Behavior, 54, 669e675. March, J. B., Sharp, P. J., Wilson, P. W., & Sang, H. M. (1994). Effect of active immunization against recombinant-derived chicken prolactin fusion protein on the onset of broodiness and photoinduced egg laying in bantam hens. Journal of Reproduction and Fertility, 101, 227e233. Martin, T. E. (2002). A new view of avian life-history evolution tested on an incubation paradox. Proceedings of the Royal Society Of London Series B-Biological Sciences, 269, 309e316. Martinez-Vargas, M. C. (1974). The induction of nest-building in the ring dove (Streptopelia risoria): hormonal and social factors. Behaviour, 50, 123e151. Masello, J. F., & Quillfeldt, P. (2004). Are haematological parameters related to body condition, ornamentation and breeding success in wild burrowing parrots Cyanoliseus patagonus? Journal of Avian Biology, 35, 445e454. Massaro, M., Davis, L. S., & Davidson, R. S. (2006). Plasticity of brood patch development and its influence on incubation periods in the yellow-eyed penguin Megadyptes antipodes: an experimental approach. Journal of Avian Biology, 37, 497e506. Massaro, M., Setiawan, A. N., & Davis, L. S. (2007). Effects of artificial eggs on prolactin secretion, steroid levels, brood patch development, incubation onset and clutch size in the yellow-eyed penguin (Megadyptes antipodes). General and Comparative Endocrinology, 151, 220e229. Mays, N. A., Vleck, C. M., & Dawson, J. (1991). Plasma luteinizing hormone, steroid hormones, behavioral role, and nest stage in cooperatively breeding Harris’ hawks (Parabuteo unicinctus). Auk, 108, 619e637. McCarty, J. P., & Secord, A. L. (1999). Nest-building behavior in PCBcontaminated tree swallows. Auk, 116, 55e63. McGlothlin, J. W., Jawor, J. M., & Ketterson, E. D. (2007). Natural variation in a testosterone-mediated trade-off between mating effort and parental effort. American Naturalist, 170, 864e875. McMaster, D. G., & Sealy, S. G. (1999). Do brown-headed cowbird hatchlings alter adult yellow warbler behavior during the hatching period? Journal of Field Ornithology, 70, 365e373. Michl, G., Torok, J., Peczely, P., Garamszegi, L. Z., & Schwabl, H. (2005). Female collared flycatchers adjust yolk testosterone to male age, but not to attractiveness. Behavioral Ecology, 16, 383e388.

Hormones and Reproduction of Vertebrates

Mills, A. D., Crawford, M. L., Domjan, M., & Maure, J. M. (1997). The behavior of the Japanese or domestic quail Coturnix japonica. Neuroscience & Biobehavioral Reviews, 261e281. Moreno, J., Barbosa, A., Potti, J., & Merino, S. (1997). The effects of hatching date and parental quality on chick growth and creching age in the chinstrap penguin (Pygoscelis antarctica): a field experiment. Auk, 114, 47e54. Mumme, R. L. (1997). A bird’s-eye view of mammalian cooperative breeding. In S. N. G., & J. A. French (Eds.), Cooperative Breeding in Mammals (pp. 364e388). Cambridge, UK: Cambridge University Press. Møller, A. P., Garamszegi, L. Z., Gil, D., Hurtrez-Bousse’s, S., & Eens, M. (2005). Correlated evolution of male and female testosterone profiles in birds and its consequences. Behavioral Ecology and Sociobiology, 58, 534e544. Mu¨ller, W., Lessells, M., Korsten, P., & Von Engelhardt, N. (2007). Manipulative signals in family conflict? On the function of maternal yolk hormones in birds. American Naturalist, 169, E84eE96. Nager, R. D. (2006). The challenges of making egg. Ardea, 94, 323e346. Nice, N. N. (1962). Development of behavior in precocial birds. Transactions of the Linnean Society, New York, 8, 1e211. Norris, D. O. (2007). Vertebrate Endocrinology. San Diego, CA: Elsevier Academic Press. Nunez-de la Mora, A., Drummond, H., & Wingfield, J. C. (1996). Hormonal correlates of dominance and starvation-induced aggression in chicks of the blue-footed booby. Ethology, 102, 748e761. O’Dwyer, T. W., Buttemer, W. A., Priddel, D. M., & Downing, J. A. (2006). Prolactin, body condition and the cost of good parenting: an interyear study in a long-lived seabird, Gould’s petrel (Pterodroma leucoptera). Functional Ecology, 20, 806e811. Opel, H., & Proudman, J. A. (1988). Effects of poults on plasma concentrations of prolactin in turkey hens incubating without eggs or a nest. British Poultry Science, 29, 791e800. Oring, L., Fivizzani, A., & El Halawani, M. E. (1986). Changes in plasma prolactin associated with laying and hatch in the spotted sandpiper. Auk, 103, 820e822. Oring, L., Fivizzani, A. J., & El Halawani, M. E. (1989). Testosteroneinduced inhibition of incubation in the spotted sandpiper (Actitus macularia). Hormones and Behavior, 23, 412e423. Oring, L. W., Fivizzani, A. J., Colwell, M. A., & El Halawani, M. E. (1988). Hormonal changes associated with natural and manipulated incubation in the sex-role reversed Wilson’s phalarope. General and Comparative Endocrinology, 72, 247e256. Pedersen, H. C. (1989). Effects of exogenous prolactin on parental behaviour in free-living female willow ptarmigan Lagopus l. lagopus. Animal Behaviour, 38, 926e934. Pereyra, M. E., & Wingfield, J. C. (2003). Changes in plasma corticosterone and adrenocortical response to stress during the breeding cycle in high altitude flycatchers. General and Comparative Endocrinology, 130, 222e231. Peters, A., Astheimer, L. B., & Cockburn, A. (2001). The annual testosterone profile in cooperatively breeding superb fairy-wrens, Malurus cyaneus, reflects their extreme infidelity. Behavioral Ecology and Sociobiology, 50, 519e527. Pinxten, R., De Ridder, E., Arckens, L., Darras, V. M., & Eens, M. (2007). Plasma testosterone levels of male Europe starlings (Sturnus vulgaris) during the breeding cycle and in relation to song and paternal care. Behaviour, 144, 393e410.

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

Pitts, G. R., Youngren, O. M., Silsby, J. L., Foster, L. K., Foster, D. N., Rozenboim, I., et al. (1994). Role of vasoactive intestinal peptide in the control of prolactin-induced turkey incubation behaviour. I. Acute infusion of vasoactive intestinal peptide. Biology of Reproduction, 50, 1344e1349. Poiani, A., & Fletcher, T. (1994). Plasma levels of androgens and gonadal development of breeders and helpers in the bell miner (Manorina melanophrys). Behavioral Ecology and Sociobiology, 34, 31e41. Radford, A. N. (2004). Incubation feeding by helpers influences female nest attendance in the green woodhoopoe, Phoeniculus purpureus. Behavioral Ecology and Sociobiology, 55, 583e588. Radford, A. N., & Ridley, A. R. (2006). Recruitment calling: a novel form of extended parental care in an altricial species. Current Biology, 16, 1700e1704. Ramakrishnan, S., Strader, A. D., Wimpee, B., Chen, P., Smith, M. S., & Buntin, J. D. (2007). Evidence for increased neuropeptide Y synthesis in mediobasal hypothalamus in relation to parental hyperphagia and gonadal activation in breeding ring doves. Journal of Neuroendocrinology, 19, 163e171. Ramesh, R., Proudman, J. A., & Kuenzel, W. J. (1995). Changes in pituitary somatotrophs and lactotrophs associated with ovarian regression in the turkey hen (Meleagris gallopavo). Comparative Biochemistry and Physiology C Pharmacology Toxicology and Endocrinology, 112, 327e334. Ramsey, S. M., Goldsmith, A. R., & Silver, R. (1985). Stimulus requirements for prolactin and LH secretion in incubating ring doves. General and Comparative Endocrinology, 59, 246e256. Reid, J. M., Monaghan, P., & Ruxton, G. D. (2002). Males matter: the occurrence and consequences of male incubation in starlings (Sturnus vulgarus). Behavioral Ecology and Sociobiology, 51, 255e261. Reyer, H. U., Dittami, J., & Hall, M. (1986). Avian helpers at the nest: are they psychologically castrated? Ethology, 71, 216e228. Richard-Yris, M. A., Guemene, D., Lea, R. W., Sharp, P. J., Bedecarrats, G., Foraste, M., et al. (1998a). Behaviour and hormone concentrations in nest deprived and renesting hens. British Poultry Science, 39, 309e317. Richard-Yris, M. A., Sharp, P. J., Wauters, A. M., Guemene, D., Richard, J. P., & Foraste, M. (1998b). Influence of stimuli from chicks on behavior and concentrations of plasma prolactin and luteinizing hormone in incubating hens. Hormones and Behavior, 33, 139e148. Rochester, J. R., Heiblum, R., Rozenboim, I., & Millam, J. R. (2008). Post-hatch oral estrogen exposure reduces oviduct and egg mass and alters nest-building behavior in adult zebra finches (Taeniopygia guttata). Physiology & Behavior, 95, 370e380. Rozenboim, I., Mobarky, N., Heiblum, R., Chaiseha, Y., Kang, S. W., Biran, I., et al. (2004). The role of prolactin in reproductive failure associated with heat stress in the domestic turkey. Biology of Reproduction, 71, 1208e1213. Schmidt, L., Bradshaw, S., & Follett, B. (1991). Plasma levels of luteinizing hormone and androgens in relation to age and breeding status among cooperatively breeding Australian magpies (Gymnorhina tibicen Latham). General and Comparative Endocrinology, 83, 48e55. Schoech, S. J., Mumme, R. L., & Wingfield, J. C. (1996a). Delayed breeding in the cooperatively breeding Florida scrub-jay (Aphelocoma coerulescens): inhibition or the absence of stimulation? Behavioral Ecology and Sociobiology, 39, 77e90.

201

Schoech, S. J., Mumme, R. L., & Wingfield, J. C. (1996b). Prolactin and helping behaviour in the cooperatively breeding Florida scrub-jay, Aphelocoma c. coerulescens. Animal Behaviour, 52, 445e456. Schoech, S. J., Reynolds, S. J., & Boughton, R. K. (2004). Endocrinology. In W. D. Koenig, & J. L. Dickenson (Eds.), Ecology and evolution of cooperative breeding in birds. Cambridge, UK: Cambridge University Press. Schwabl, H., Palacios, M. G., & Martin, T. E. (2007). Selection for rapid embryo development correlates with embryo exposure to maternal androgens among passerine birds. American Naturalist, 170, 196e206. Schwagmeyer, P. L., Mock, D. W., Lamey, T. C., & Becher, M. D. (1991). Effects of sibling contact on hatch timing in an asynchronously hatching bird. Animal Behaviour, 41, 887e894. Seiler, H. W., Gahr, M., Goldsmith, A. R., & Guettinger, H.-R. (1992). Prolactin and gonadal steroids during the reproductive cycle of the Bengalese finch (Lonchura striata var. domestica, Estrildidae), a nonseasonal breeder with biparental care. General and Comparative Endocrinology, 88, 83e90. Selander, R. K. (1960). Failure of estrogen and prolactin treatment to induce brood patch formation in brown-headed cowbirds. Condor, 62, 65. Selander, R. K., & Yang, S. Y. (1966). The incubation patch of the house sparrow, Passer domesticus Linnaeus. General and Comparative Endocrinology, 6, 325e333. Setiawan, A. N., Davis, L. S., Darby, J. T., Lokman, P. M., Young, G., Blackberry, M. A., et al. (2006). Hormonal correlates of parental behavior in yellow-eyed penguins (Megadyptes antipodes). Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology, 145, 357e362. Seymour, R. S., Vleck, D., & Vleck, C. M. (1986). Gas exchange in the incubation mounds of megapode birds. Journal of Comparative Physiology B, 156, 773e782. Seymour, R. S., Vleck, D., Vleck, C. M., & Booth, D. T. (1987). Water relations of buried eggs of mound building birds. Journal of Comparative Physiology B, 157, 413e422. Sharp, P. J. (1997). Immunological control of broodiness. World’s Poultry Science, 53, 23e31. Sharp, P. J., Dawson, A., & Lea, R. W. (1998). Control of luteinizing hormone and prolactin secretion in birds. Comparative Biochemistry and Physiology C Pharmacology Toxicology and Endocrinology, 119, 275e282. Sharp, P. J., Macanamee, M. C., Sterling, R. J., Lea, R. W., & Pedersen, H. C. (1988). Relationships between prolactin LH and broody behavior in bantam hens. Journal of Endocrinology, 118, 279e286. Sharp, P. J., Sterling, R. J., Talbot, R. T., & Huskisson, N. S. (1989). The role of hypothalamic vasoactive intestinal polypeptide in the maintenance of prolactin secretion in incubating bantam hens: observations using passive immunization, radioimmunoassay and immunohistochemistry. Journal of Endocrinology, 122, 5e13. Shultz, M. T., & Kitaysky, A. S. (2008). Spatial and temporal dynamics of corticosterone and corticosterone binding globulin are driven by environmental heterogeneity. General and Comparative Endocrinology, 155, 717e728. Silverin, B. (1980). Effects of long-acting testosterone treatment on freeliving pied flycatchers, Ficedula hypoleuca, during the breeding period. Animal Behaviour, 28, 906e912. Silverin, B. (1991). Annual changes in plasma levels of LH and prolactin in free-living female great tits (Parus major). General and Comparative Endocrinology, 83, 425e431.

202

Silverin, B., & Goldsmith, A. (1984). The effects of modifying incubation on prolactin secretion in free-living pied flycatchers. General and Comparative Endocrinology, 55, 239e244. Silverin, B., & Goldsmith, A. (1997). Natural and photoperiodically induced changes in plasma prolactin levels in male great tits. General and Comparative Endocrinology, 105, 145e154. Simon, J. C., Pratt, T. K., Berlin, K. E., & Kowalsky, J. R. (2001). Reproductive ecology and demography of the Akohekohe. Condor, 103, 736e745. Sinclair, J. R. (2001). Temperature regulation in mounds of three sympatric species of megapode (Aves: Megapodiidae) in Papua New Guinea: testing the ‘Seymour Model’. Australian Journal Of Zoology, 49, 675e694. Sockman, K. W., & Schwabl, H. (1999). Daily estradiol and progesterone levels relative to laying and onset of incubation in canaries. General and Comparative Endocrinology, 114, 257e268. Sockman, K. W., Schwabl, H., & Sharp, P. J. (2000). The role of prolactin in the regulation of clutch size and onset of incubation behavior in the American kestrel. Hormones and Behavior, 38, 168e176. Sockman, K. W., Sharp, P. J., & Schwabl, H. (2006). Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition. Biological Reviews, 81, 629e666. St. Clair, C. C. (1992). Incubation behaviour, brood patch formation and obligate brood reduction in Fiordland crested penguins. Behavioral Ecology and Sociobiology, 31, 409e416. Stacey, P. B., & Koenig, W. D. (1990). Cooperative Breeding in Birds, Long Term Studies of Ecology and Behaviour. Cambridge, UK: Cambridge University Press. Starck, J. M., & Ricklefs, R. E. (1998). Avian Growth and Development: Evolution within the Altricial-Precocial Spectrum. Oxford, UK: Oxford University Press. Steel, E., & Hinde, R. A. (1972). Influence of photoperiod on oestrogenic induction of nest-building in canaries. Journal of Endocrinology, 55, 265e278. Stoleson, S. H. (1999). The importance of the early onset of incubation for the maintenance of egg viability. In N. J. Adams, & R. H. Slotow (Eds.), Proceedings of the 22nd International Ornithological Congress, Durban. Johannesburg, South Africa: BirdLife South Africa. Tinbergen, J. M., & Williams, J. B. (2002). Energetics of incubation. In D. C. Deeming (Ed.), Avian Incubation (pp. 298e313). Oxford, UK: Oxford University Press. Torok, J., Moskat, C., Michl, G., & Peczely, P. (2004). Common cuckoos (Cuculus canorus) lay eggs with larger yolk but not more testosterone than their great reed warbler (Acrocephalus arundinaceus) hosts. Ethology Ecology and Evolution, 16, 271e277. Van Duyse, E., Pinxten, R., & Eens, M. (2002). Effects of testosterone on song, aggression, and nestling feeding behavior in male great tits, Parus major. Hormones and Behavior, 41, 178e186. Van Roo, B. L. (2004). Exogenous testosterone inhibits several forms of male parental behavior and stimulates song in a monogamous songbird: the blue-headed vireo (Vireo solitarius). Hormones and Behavior, 46, 678e683. Van Roo, B. L., Ketterson, E. D., & Sharp, P. J. (2003). Testosterone and prolactin in two songbirds that differ in paternal care: the blue-headed vireo and the red-eyed vireo. Hormones and Behavior, 44, 435e441.

Hormones and Reproduction of Vertebrates

Vince, M. A. (1979). Effects of accelerating stimulation on different indices of development in Japanese quail embryos. Journal of Experimental Zoology, 208, 201e212. Vleck, C. M. (1981). Hummingbird incubation: female attentiveness and egg temperature. Oecologia, 51, 199e205. Vleck, C. M. (2001). Hormonal control of incubation behaviour. In C. Deeming (Ed.), Avian Incubation: Behaviour, Environment and Evolution (pp. 54e62). Oxford, UK: Oxford University Press. Vleck, C. M., & Brown, J. L. (1999). Testosterone and social and reproductive behaviour in Aphelocoma jays. Animal Behaviour, 56, 943e951. Vleck, C. M., & Patrick, D. L. (1999). Effects of vasoactive intestinal peptide on prolactin secretion in three species of passerine birds. General and Comparative Endocrinology, 113, 146e154. Vleck, C. M., & Vleck, D. (2002). Physiological condition and reproductive consequences in Ade´lie penguins. Integrative and Comparative Biology, 42, 76e83. Vleck, C. M., Bucher, T. L., Reed, W. L., & Kristmundsdottir, A. Y. (1999). Changes in reproductive hormones and body mass through the reproductive cycle in the Ade´lie penguin (Pygoscelis adeliae), with associated data on courting-only individuals. In N. J. Adams, & R. H. Slotow (Eds.), Proceedings of the 22nd International Ornithological Congress, Durban (pp. 1210e1223). Johannesburg, South Africa: BirdLife South Africa. Vleck, C. M., Mays, N. A., Dawson, J. W., & Goldsmith, A. R. (1991). Hormonal correlates of parental and helping behavior in cooperatively breeding Harris’ hawks Parabuteo unicinctus. Auk, 108, 638e648. Vleck, C. M., Ross, L. L., Vleck, D., & Bucher, T. L. (2000). Prolactin and parental behavior in Ade´lie penguins: Effects of absence from nest, incubation length, and nest failure. Hormones and Behavior, 38, 149e158. Vowles, D. M., & Lea, R. W. (1986). External factors affecting the duration of broody behavior in the ring dove (Streptopelia risoria). Hormones and Behavior, 20, 249e262. Wang, Q., & Buntin, J. D. (1999). The roles of stimuli from young, previous breeding experience, and prolactin in regulating parental behavior in ring doves (Streptopelia risoria). Hormones and Behavior, 35, 241e253. Webb, D. R. (1987). Thermal tolerance of avian embryos: a review. Condor, 89, 874e898. Weimerskirch, H. (1995). Regulation of foraging trips and incubation routine in male and female wandering albatrosses. Oecologia, 102, 37e43. Wiebe, K. L., & Bortolotti, G. R. (1993). Brood patches of American kestrels: an ecological evolutionary perspective. Ornis Scandinavica, 24, 197e204. Wiebe, K. L., & Martin, K. (1995). Ecological and physiological effects on egg lying intervals in ptarmigan. Condor, 97, 708e7171. Wiebe, K. L., Wiehn, J., & Korpimaki, E. (1998). The onset of incubation in birds: can females control hatching patterns? Animal Behaviour, 55, 1043e1052. Williams, D. A., & Hale, A. M. (2008). Investment in nesting activities and patterns of extra- and within-group genetic paternity in a cooperatively breeding bird. Condor, 110, 13e23. Williams, J. B. (1996). Energetics of avian incubation. In C. Carey (Ed.), Avian Energetics and Nutritional Ecology (pp. 375e416). New York, NY: Chapman and Hall. Williams, T. D. (1995). The Penguins: Spheniscidae. New York, NY: Oxford University Press.

Chapter | 7

Hormones and Regulation of Parental Behavior in Birds

Wilson, C. M., & Holberton, R. L. (2004). Individual risk versus immediate reproductive success: a basis for latitudinal differences in the adrenocortical response to stress in yellow warblers (Dendroica petechia). Auk, 121, 1238e1249. Wilson, S., Martin, K., & Hannon, S. J. (2007). Nest survival patterns in willow ptarmigan: influence of time, nesting stage, and female characteristics. Condor, 109, 377e388. Wingfield, J., Hegner, R., & Lewis, D. (1991). Circulating levels of luteinizing hormone and steroid hormones in relation to social status in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. Journal of Zoology, 225, 43e58. Wingfield, J. C., & Farner, D. S. (1993). In D. S. Farner, J. R. King, & K. C. Parkes (Eds.), Avian Biology. Endocrinology of reproduction in wild species, Vol. IX (pp. 163e327). New York, NY: Academic Press. Wingfield, J. C., & Goldsmith, A. R. (1990). Plasma levels of prolactin and gonadal steroids in relation to multiple-brooding and renesting in free-living populations of the song sparrow, Melospiza melodia. Hormones and Behavior, 24, 89e103. Wingfield, J. C., & Hunt, K. E. (2002). Arctic spring: hormoneebehavior interactions in a severe environment. Comparative Biochemistry and Physiology Part B. Biochemistry and Molecular Biology, 132B, 275e286. Wingfield, J. C., & Sapolsky, R. M. (2003). Reproduction and resistance to stress: when and how? Journal of Neuroendocrinology, 15, 711e724. Wingfield, J., Hegner, R., Dufty, A. J., & Ball, G. (1990). The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. American Naturalist, 136, 829e846.

203

Wingfield, J. C., Maney, D. L., Breuner, C. W., Jacobs, J. D., Lynn, S., Ramenofsky, M., et al. (1998). Ecological bases of hormonee behavior interactions: the “emergency life history stage”. American Zoologist, 38, 191e206. Wingfield, J. C., Ronchi, E., Goldsmith, A. R., & Marler, C. (1989). Interactions of sex steroid hormones and prolactin in male and female song sparrows, Melospiza melodia. Physiological Zoology, 62, 11e24. Yorio, P., & Boersma, P. D. (1994). Causes of nest desertion during incubation in the Magellanic penguins (Spheniscus magellanicus). Condor, 96, 1076e1083. Youngren, O., Chaiseha, Y., Al-Zailaie, K., Whiting, S., Kang, S. W., & El Halawani, M. (2002). Regulation of prolactin secretion by dopamine at the level of the hypothalamus in the turkey. Neuroendocrinology, 75, 185e192. Zadworny, D., & Etches, R. J. (1987). Effects of ovariectomy or force feeding on the plasma concentrations of prolactin and luteinizing hormone in incubating turkey hens. Biology of Reproduction, 36, 81e88. Zadworny, D., Walton, J. S., & Etches, R. J. (1985). Effect of feed and water deprivation or force-feeding on plasma prolactin concentration in turkey hens. Biology of Reproduction, 32, 241e247. Zann, R., & Rossetto, M. (1991). Zebra finch incubation: brood patch, egg temperature and thermal properties of the nest. Emu, 91, 107e120. Zhou, M., Lei, M., Rao, Y., Nie, Q., Zeng, H., Xia, M., et al. (2008). Polymorphisms of vasoactive intestinal peptide receptor-1 gene and their genetic effects on broodiness in chickens. Poultry Science, 87, 893e903.

Chapter 8

Hormones in Migration and Reproductive Cycles of Birds Marilyn Ramenofsky University of California, Davis, CA, USA

SUMMARY The life-history stages of the annual cycles of birds are varied and complex, yet what all have in common is that the timing and duration of each stage are closely tied to environmental conditions. In a predictable environment, exogenous cues provide reliable and consistent information that regulates the onset, progression, and termination of the stages that help to synchronize the activities of the organism with both current and long-term conditions, and to maximize fitness. This discussion takes a finite state machine approach to the studies of the migration and breeding stages of the annual cycle, and the endocrine mechanisms, where known, of the migratory and sedentary races of the white-crowned sparrow (Zonotrichia leucophrys). A comparative approach illustrates how closely related subspecies have diverged in their life histories to capitalize on local conditions that support migratory patterns and reproductive success while providing a fuller understanding of the lifecycles of birds in general.

1. INTRODUCTION The life-history stages of the annual cycles of birds are varied and complex, and in most cases not completely understood. What all have in common, however, is that the timing and duration of each stage are closely tied to environmental conditions. In a predictable environment, exogenous cues provide reliable and consistent information that serves to regulate the onset and progression of the stages that help to synchronize the activities of the organism with both current and long-term conditions. By contrast, complete reliance on external cues in an unpredictable environment can have disastrous results. In this chapter, the discussion will focus on how the environmental cues in a predictable environment affect the life histories of closely related species. Specifically, the approach taken is to focus on migration and breeding stages of the annual cycle and the endocrine mechanisms, where known, of a number of north temperate species including both migratory and Hormones and Reproduction of Vertebrates, Volume 4dBirds Copyright Ó 2011 Elsevier Inc. All rights reserved.

sedentary populations, with particular attention given to the Pacific races of white-crowned sparrows (Zonotrichia leucophrys). This comparative approach illustrates how closely related subspecies have diverged in their life histories in order to capitalize on local conditions that support migratory patterns and reproductive success.

2. LIFE HISTORY AND ECOLOGY OF THE SUBSPECIES OF THE WHITE-CROWNED SPARROW (ZONOTRICHIA LEUCOPHRYS) Historically, Z. leucophrys is thought to have arisen from the ancestral species, the rufous-collared sparrow (Zonotrichia capensis). This polytypic species possesses at least 20 taxonomic forms and ranges from Central Mexico to Cape Horn (King, 1974). In the western USA, leucophrys diverged further into multiple subspecies as a result of glaciations during the Pleistocene Epoch, producing secluded refugia promoting allopatric speciation (Rand, 1948; Mayr, 1963; Selander, 1965; Avise & Walker, 1998). Environmental barriers resulted in the evolution of four subspecies that range in migratory tendencies from long distance (Z. l. gambelii, oriantha), moderate (pugetensis), to resident (nuttalii) species (Blanchard 1941; 1942; Banks, 1964; Selander, 1965; Zink, 1982; Zink, Dittman, & Rootes, 1991; Zinc & Blackwell, 1996). The breeding ranges of these subspecies are distinct with a modicum of overlap. Z. l. gambelii and oriantha are strongly migratory, with gambelii breeding from the northern US border into the arctic of Alaska and Canada and overwintering from the continental USA into northern Mexico (Blanchard, 1941; Cortopassi & Mewaldt, 1965). Divisions within Z. l. gambelii are based on reproductive behavior, endocrinology, and geographic locations of breeding populations as outlined in the work of Wingfield and Farner (1978a; 1978b), Wingfield et al. (1999); Moore, Perfito, Wada, Sperry, and Wingfield (2002); Morton (2002); Wingfield 205

206

and Hunt (2002). The tundra white-crowned sparrow breeds north of the Brooks Range in Alaska, covering latitude 68 N and longitude 149 W. The taiga population breeds in the central interior of Alaska (latitude 64 N, longitude 147 W). The mountain white-crowned sparrow (Z. l. oriantha) breeds at higher elevations of the Sierra, southern Cascade, and Rocky Mountains, extending from the southwestern USA into southern Canada and covering a latitude of 44 N and longitude of 110 W (Morton, 1992). Birds overwinter in northern Baja, California, and Mexico. Z. l. pugetensis (the Puget Sound race) is considered a transitional migratory stage that has historically bred along the coast from northern California to southwestern British Columbia (latitude 47 N, longitude 122 W) and is currently moving eastward into ecologically disturbed areas of the Cascade range (Addis, Davis, Bonier, Miner, & Wingfield, in press). The wintering range extends from southern California to the Oregon boarder. Not all populations migrate but, among those that do, records indicate a maximum distance covered of 650 km (Blanchard, 1941; Banks, 1964). Z. l. nuttalli, the sedentary race, is confined to the Pacific coast from Santa Barbara to Humboldt counties (latitude 38 N, longitude 122 W). At its northern extent, Z. l. nuttalli overlaps with breeding Z.l. pugetensis (Blanchard, 1941).

3. HYPOTHALAMICePITUITARY CONTROL OF HORMONES IN THE REPRODUCTIVE CYCLES OF MALE AND FEMALE BIRDS Organisms synchronize the events of the annual cycle with environmental signals. Environmental information is perceived and transduced by the neuroendocrine system, which affects the timing of breeding (Figure 8.1). The vernal increase in daylength stimulates neuroendocrine pathways, leading to production and secretion of gonadotropin-releasing hormone (GnRH) and gonadotropininhibiting hormone (GnIH), both of which influence secretion of the gonadotropins (GTHs) luteinizing hormone (LH) and follicle-stimulating hormone (FSH). In males, LH induces production of testosterone (T) by the Leydig Cells in the interstitium of the testis. Follicle-stimulating hormone induces growth and development of the seminiferous tubules of the testis as well as stimulating steroidogenesis and the production of androgen-binding protein, all of which promote and sustain spermatogenesis. In the ovary, LH and FSH enhance folliculogenesis as well as steroidogenesis of estradiol and progesterone and production of protein hormones and growth factors. As the follicle matures, the release of progesterone promotes development of the oviduct and estradiol enhances breeding behavior. Rapidly rising progesterone has positive feedback on GnRH release and induces the LH surge that culminates in

Hormones and Reproduction of Vertebrates

FIGURE 8.1 Sagittal schematic of the passerine brain, anterior pituitary, and gonads. External stimuli are perceived by the sensory systems and reach brain regions to evoke a neuroendocrine response. Hatched lines depict the hypothalamus, containing the third ventricle (filled structure). Neuroendocrine pathways of gonadotropin-releasing hormone (GnRH) and gonadotropin-inhibiting hormone (GnIH) reach the anterior pituitary (stippled oval structure), each influencing the secretion of gonadotropins (luteinizing hormone (LH) and follicle-stimulating hormone (FSH)), which in turn affect the development and endocrine secretion of the gonads (ovaries and testes). Gonadal steroids exert both positive and negative feedback on the hypothalamus and the pituitary, regulating gonadotropin (GTH) secretion.

ovulation of the ova and oviposition of the egg. In both males and females, steroids secreted into the peripheral circulation feed back on the pituitary and hypothalamus to regulate secretion of GTHs.

4. ANNUAL CYCLES OF MIGRATORY AND SEDENTARY WHITE-CROWNED SPARROWS The annual cycle of an adult organism is made up of a temporal sequence of life-history stages that includes migration and breeding. Each stage can be subdivided further; e.g., within a species there exist a fixed number of stages, each with its associated substages. This means that there is a finite number of states that a species will experience in a given year, described as a ‘finite state machine’ (Wingfield & Jacobs, 1999; Jacobs & Wingfield, 2000; Ramenofsky & Wingfield, 2007). The number of states, or finite state diversity, has marked implications for studying endocrine control mechanisms while representing a classic tradeoff between the number of states and flexibility. For example, a higher number of stages provides greater tolerance for varied environmental conditions but, with the increased number, there is a loss of flexibility in terms of timing as the duration of each stage is restricted. By contrast, lower finite state diversity indicates a reduced ability to accommodate

Chapter | 8

207

Hormones in Migration and Reproductive Cycles of Birds

a wide range of environmental conditions, pointing out a tradeoff between greater flexibility in the timing of a given stage and reduced capacity to withstand a broad spectrum of environments (Jacobs & Wingfield, 2000). The number of states varies across species and populations as well as within species and across age and sex classes. For example, life-history stages for two subspecies of the white-crowned sparrow, the long-distance migrant Z. l. gambelii and the sedentary Z. l. nuttalli, are illustrated in Figure 8.2. As noted above, the number of stages expressed by Z. l. gambelii outnumbers those of Z. l. nuttalli. On an annual basis, migratory species travel between distinct geographic locations, in general one for breeding and the other for nonbreeding (wintering), each offering seasonal resources that increase the overall fitness of an individual. By contrast, sedentary species remain within the area or habitat in which they were hatched throughout their entire lifespan, as local resources are sufficient to supply their annual needs. To accommodate the demands of travel, migrants display additional stages in their annual program of activities: autumn and vernal migration and prenuptial molt. Thus, it is evident that the additional stages leave migratory species with less time for breeding and, hence, less flexibility within the annual cycle (Table 8.1). Greater state diversity, however, provides migrants with a larger potential for withstanding a broad range of environmental conditions, in contrast to those with more limited state diversity. The depiction of life-history stages in the light of finite state machine theory has helped to identify the critical time points for elucidating endocrine control mechanisms specific to a particular stage, species, condition, etc.

FIGURE 8.2 Sequence of the life-history stages of the annual cycle of two subspecies of white-crowned sparrow: the long distance race (Zonotrichia leucophrys gambelii) and the sedentary race (Z. l. nuttalli). Each stage is depicted by a trapezoid figure that is comprised of three phases: development (left-pointing triangle of trapezoid), mature capability (rectangle of the trapezoid), and termination (right-pointing triangle of trapezoid).

TABLE 8.1 Finite state divisions of life-history stages Hierarchical order Description

Examples

Stages

Total number expressed throughout the annual cycle

Gambelii: six stages; Nuttalli: three stages

Phases

Three progressive divisions of each stage

Development; mature expression; termination

Substages

The distinct behavioral and physiological states that make up each phase of the life-history stage

Migration: (n); breeding: (n)

5. APPLYING FINITE STATE MACHINE THEORY TO MIGRATION AND BREEDING Each stage of the annual cycle progresses through three phases, the first being a developmental component that encompasses the activation of molecular and physiological systems that transform an individual from an immature condition into one that is fully developed and prepared to express the behaviors and physiology characteristic of the life-history stage; this is the mature capability phase. The final phase is termination, in which the developed characteristics subside, making way for the onset and development of the subsequent life-history stage (Jacobs & Wingfield, 2000; Ramenofsky & Wingfield, 2007). Each phase is divided into sequential and unique categories called substages. In the annual cycle of an organism there is a fixed number of life-history stages and their substages, which means that there is a finite number of states, hence the name ‘finite state machine’ (Wingfield & Jacobs, 1999). Progress through the substages is always in a forward direction, but a certain number of substages may cycle repeatedly until completion of the phase (Figures 8.3 and 8.4). For migratory stages, these are cycles of fueling and flight as migrants travel to their destination. In the breeding stage, pairs may repeat nesting efforts to raise more than one brood, or renest should the initial nest or young be lost to a predator or other disruptive event(s). In addition, certain ecological or temporal constraints may result in some species overlapping portions of two life-history stages; i.e., mature capability of one stage and developmental portion of the subsequent stage. Although it is not energetically feasible to overlap the mature capability of both stages, it is possible for species to overlap the mature capability or the termination phase of one life-history stage with the developmental phase of the next stage, particularly in species confronting severe time and energy constraints. This

208

FIGURE 8.3 Diagram of the three phases of vernal and autumn migration life-history stages in birds. Phases of migration are outlined in the three larger boxes: (1) the developmental phase (enclosed by a solid line), (2) the mature capability phase (enclosed by a dotted line), and (3) the termination phase (enclosed by a double line). Substages are defined in smaller boxes outlined with a single line: substages enclosed in the developmental phase are changes in gene expression, morphology, and physiology; during the mature capability phase, birds initiate processes of fueling and flight cycles, which may repeat multiple times until the destination is reached (revolving arrows); the termination phase begins with arrival biology as the destination is approached, but final completion is not attained until conditions are optimal for either breeding or overwintering.

overlap is described as a ‘super state’ and requires finer tuning to variable environmental conditions. Under certain circumstance, however, it may be possible to overlap mature capability of two life-history stages if energy sources are sufficient to support both. Usually it is not possible to simultaneously trigger the onset of two mutually exclusive life-history stages, such as migration and breeding. Both require a great deal of energy and one is highly mobile whereas the other is restricted in movement. It is possible to overlap the mature capability phases of both, but only one is fully activated while the other is not, as seen in cases with the overlap of breeding and molt in the red crossbill (Loxia curvirostra) (Cornelius, 2009).

6. TIMING MIGRATION AND BREEDING CYCLES When considering biological systems, nearly all organisms live in environments where conditions fluctuate. These

Hormones and Reproduction of Vertebrates

FIGURE 8.4 Diagram of the three phases of the breeding life-history stage. Phases of breeding are outlined in the three larger boxes: (1) the developmental phase (enclosed by a solid line), (2) the mature capability phase (enclosed by a dotted line), and (3) the termination phase (enclosed by a double line). Substages are defined in smaller boxes outlined with a single line: increase in daylength induces changes in gene expression of neural peptides, gonadal development, and behavior, which culminate in sexual maturity; expression of diverse physiological and behavioral substages of the mature capability phase proceeds sequentially and may have repeating cycles (revolving arrows) for multiple-brooded species; the termination of breeding begins with onset of photorefractoriness, molt, and finally territory breakdown.

changes can be classified into two categories: predictable and unpredictable. Predictable seasonal changes include photoperiod, temperature, rainfall, and food abundance, to name only a few. These factors provide information that allows organisms to anticipate future events and thus time activities in synchrony with seasonal fluctuations (Wingfield, 2008b). Unpredictable changes generally occur without warning, leaving little opportunity to do anything other than respond (Wingfield & Romero, 2001). Responses to the unpredictable involve the hypothalamicepituitaryeadrenal (HPA) axis and are associated with the emergency life-history stage (Wingfield & Ramenofsky, 1999; Wingfield & Romero, 2001). The focus in this chapter will primarily be on the predictable changes.

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

To maintain synchrony with predictable fluctuations, organisms alter their physiological and behavioral states, which helps to maximize survival at different times of the year (Piersma, 1998). This alternation of states is described as ‘phenotypic flexibility’, as many physiological processes change as the organism progresses through a stage. Such changes include perception of environmental information or cues, and neuroendocrine, endocrine, and physiological responses. For example, the seasonal increase in daylength is perceived by the organism and initiates development of two life-history stages: vernal migration and breeding, each with its attendant physiological and behavioral changes. As the season progresses, daylengths commensurate with those that initiated the cycle are no longer perceived to be stimulatory, as many organisms enter a state of photorefractoriness that is followed by postnuptial molt and autumn migration. In other words, a set of environmental conditions instigates endocrine and behavioral responses at one time but not another. These changes can be summarized in a temporal sequence of life-history stages with an overall benefit that maximizes fitness (Piersma, 1998; Wingfield, 2004).

6.1. Environmental Factors Influencing Migration and Breeding Cycles Environmental cues synchronize the onset, progression, and termination of life-history stages throughout the annual cycle. This coordination ensures that life-history events coincide with conditions that can support them. For example, the timing of breeding should occur at a time when food is most abundant and available to feed young (Baker, 1938; Perrins, 1970; Wingfield, 2008b). Both food abundance and weather are considered to be ultimate factors that select individuals that breed when conditions are optimal. If this coordination is accurate, organisms breed successfully and enhance fitness. However, ultimate factors do not provide immediate or predictive information. To allow sufficient time for adequate preparationdi.e., development of biochemical and physiological systemsd organisms must use reliable cues in the environment that provide predictive information, which organisms must be able to perceive and respond to. This involves perception by the central nervous system (CNS), which affects a neuroendocrine response resulting in the transduction of the environmental signals to the production and secretion of endocrine signals that regulate specific alterations of behavioral, morphological, and physiological systems. These cues are many and diverse but can be organized into the following general categories (Wingfield & Farner, 1993). Initial predictive information includes permanent and reliable cues that possess both proximate (immediate) and predictive (long-term) value. The annual change in

209

daylength or photoperiod provides immediate and seasonal information, to which the hypothalamicepituitarye gonadal (HPG) axis responds. It can act directly as a driver or as a zeitgeber (time giver) to entrain endogenous rhythms, and serves as a trigger for the developmental phase of migration and breeding stages, and ultimately their termination. Local predictive or supplementary cues provide immediate information about the current conditions and affect the rate of change by promoting or slowing the progress of the life-history stage. Local cues can include predator density, temperature, rainfall, and food availability, to name just a few. Taken together, the initial predictive cues allow individuals to anticipate a future time when conditions will be favorable for breeding. For example, migrants overwintering in locations distant from breeding sites must rely on proximate cues to initiate both spring migration and the preliminary stages of ovarian and testicular growth, in order to arrive at the breeding grounds in a state near-ready to commence breeding (Bauchinger, Van’t Hof, & Biebach, 2007; Bauchinger, Van’t Hof, & Biebach, 2009). Under optimal conditions, testicular growth from a regressed state requires nearly a month, and, if migrants were to delay until arrival at the breeding grounds to initiate gonadal development, particularly at high latitudes and altitudes, there would simply be insufficient time to complete the breeding cycle. This is less of a problem for sedentary species as the local conditions are relevant to current and future events once the onset of breeding has been initiated by the initial predictive cues. Regulation of termination phase in all species remains poorly understood, however.

6.2. Photoperiodic Responsiveness and Patterns of Migration and Breeding Among the north temperate species, a bewildering array of patterns of migration and breeding exists. The initial predictive cue for most north temperate species is daylength (Lofts & Murton, 1968; Ball & Hahn, 1997; Hahn, Boswell, Wingfield, & Ball, 1997; Dawson, King, Bentley, & Ball, 2001; Hau, 2001; Coppack & Pulido, 2004; MacDougall-Shackleton & Hahn, 2007; Hahn & MacDougall-Shackleton, 2008). In their seminal paper, Lofts and Murton (1968) suggested that the manner by which organisms perceive and respond to daylength relates to distinct patterns of migration and breeding observed across a variety of avian species. For example, species and population differences are based on the degree of sensitivity to daylength, which influences the onset and termination of breeding. Species with low thresholds are those that perceive and respond to shorter photophasesdi.e., earlier in spring, before the vernal equinoxdwhereas those with high thresholds require long daylengths to induce a HPG

210

response, leading to development of the spring migratory and breeding life-history stages. Distinct thresholds of photosensitivities also influence the termination phase or photorefractoriness, when the HPG axis completely shuts down, inhibiting further breeding even under daylengths that were once stimulatory. This is followed by postnuptial molt and development of the autumnal migratory stage. Lofts and Murton (1968) presented six models (AeF) explaining how migratory and breeding patterns relate to the photoperiods experienced throughout the annual cycle; these are discussed in detail below. Recent studies have expanded the ideas of Lofts and Murton (1968) by illustrating how environmental conditions influence the effects of photoperiod on the regulation of the onset and termination of breeding. For example, nonphotoperiodic cues affected photoinduced testicular growth, plasma levels of LH, and nest-building and egglaying behavior of blue tits (Parus caeruleus) (Caro, Lambrechts, Balthazart, & Perret, 2007; Silverin et al., 2008). Further, gonadal development and breeding in red crossbills can occur during winter months if food supply is plentiful (Hahn & MacDougall-Shackleton, 2008). Finally, termination of breeding was delayed in male song sparrows (Melospiza melodia) when exposed to the solicitations of an estrogen-implanted female at the end of the breeding season (Runfeldt & Wingfield, 1985). Hahn and MacDougall-Shackelton (2008) have incorporated these findings into the Loft and Murton (1968) models and describe the system in terms of responses to multiple cuesda cue response system. As intriguing as these ideas are, the mechanisms involved are not well understood. Whether one cue assumes precedence over another depending upon timing of exposure remains uncertain, but taking these ideas at face value expands our appreciation of the possibilities of how organisms synchronize their breeding efforts to a variety of environmental conditions. In combination, it is the cue response system that has contributed to the diverse lifecycles of many north temperate species. What is not known is the origin of such diversity. It is likely the repeated ice ages that led to multiple invasions into and retreats from the higher latitudes of populations, promoting the diversity of mechanisms for variable cue responses. Such diversity may have provided the selective advantages allowing certain populations to exploit seasonal areas on a more permanent basis, leading to differential reproductive success. Hypotheses concerning the evolution of migratory populations are central to a basic understanding of migration. Whether colonization arose from an ancestral sedentary populationdallowing further expansion into more recently available habitatsdor the appearance of sedentary populations from migratory ancestors are major issues in this field. Discussions assessing the physiological mechanisms and molecular genetics of sedentary and migratory populations may offer critical clues regarding the evolution

Hormones and Reproduction of Vertebrates

of migratory patterns (Williams & Webb, 1996; Bell, 2000; Bearhop et al., 2005). As a topic, the evolution of migration is one of great interest and debate (Bell, 2000; Coppack & Pulido, 2004; Salewski & Bruderer, 2007) but is beyond the scope of this chapter.

6.3. Six Models Proposed by Lofts and Murton (1968) To integrate the cue response system with the earlier ideas of Lofts and Murton (1968), the six models will be reviewed in this section, with particular attention given to the subspecies of Z. leucophrys. Type A species possess a low threshold for increased daylength and initiate development of the HPG axis followed by migration and breeding early in the season. Tolerance for long-day conditions is low and breeding is curtailed probably due to a decline in available food and/or other critical resources. Refractoriness sets in prior to the summer solstice (12 hours of light (L) : 12 hours of dark (D)) and remains in place well into the fall. Exposure to short daylengths breaks refractoriness, and development proceeds once the photoperiod starts to increase. The prime type A example is the European starling (Sturnis vulgaris), with migratory populations in Europe and sedentary species in the UK. The gonadal cycles of the two populations differ. Testicular recrudescence is initiated in February, with the first meiotic divisions and spermatozoa apparent in March. Continental migratory populations were delayed by one month (Bullough, 1942). Testes of the migrants regressed to a greater extent than those of the sedentary population. Bullough (1942) attributes these distinctions in timing to the different life histories of these populations. Despite the disparities, starlings are restricted to a single brood followed by a long refractory period, which ensures that breeding is not activated under persistent long-day conditions (Figure 8.5(a)). Type B species have low thresholds for increased daylength and initiate gonadal activity and breeding early in the season. Tolerance for long-day conditions is high and breeding is sustained until refractoriness sets in, after the summer solstice. The exposure to short daylengths breaks refractoriness and development proceeds with the increase in photoperiod early in the season. The sedentary whitecrowned sparrow (Z. l. nuttalli) and some populations of Z. l. pugetensis are typical of this pattern. Birds remain territorial for the majority of the year. With the extended breeding season, birds have multiple broods, concluding in midsummer, followed by a postnuptial molt and wintering stage (Figure 8.5(b)). Type C includes migratory species that breed from moderate to high latitudes but winter near the equator, where daylength is approximately 12L : 12D. Initiation of the migratory stage may be influenced by a circannual

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

211

FIGURE 8.5 Examples of distinct breeding seasons (black-filled figures) of three north temperate species in relation to seasonal changes in daylength (photoperiod). Hours of daylight are indicated on the Y axis and are illustrated with a solid line. Months of the year are listed on the X axis. Patterns are influenced by a cue response system with testicular development (dotted line) in males initiated by photosensitivity to a critical daylength (indicated by arrow) and curtailed by the onset of photorefractoriness, which persists for a variable length of time under short daylengths (cross-hatched horizontal bar). Modified from Lofts and Murton (1968): (a) European starling (Sturnus vulgaris) refers to model A in the text; (b) Nuttall’s white-crowned sparrow (Zonotrichia leucophrys nuttalli) refers to model B in the text; (c) Gambel’s white-crowned sparrow (Z. l. gambelii) refers to model D.

rhythm, but progression to breeding requires relatively long photoperiods to which birds are exposed en route. Once on the breeding grounds, rapid development of refractoriness terminates breeding in time for molt and preparations for autumn migration. A prolonged refractory period is required to inhibit premature development of breeding on the equatorial wintering grounds. Examples may include numerous shorebirds such as the red knot (Calidris canutus) (Cade´e, Piersma, & Daan, 1996) and equatorial passerines such as the African stonechat (Saxicola torquata axillaries) (Ditami & Gwinner, 1985). Type D species have a high tolerance for increased daylength and initiate gonadal activity during the spring equinox. Being migratory species, expression of the mature capability phase of reproduction is delayed until birds reach the breeding grounds. Tolerance for long photoperiods is low, necessitating a short breeding period of two months or less, and photorefractoriness sets in around the time of the summer solstice and lasts for an extended period until it is broken by the short photoperiods of autumn. The longdistance race of the white-crowned sparrow (Z. l. gambelii) represents this pattern. Wintering in locations distant from breeding grounds, the photoperiodic cue reliably initiates migratory activity and subsequent development of gonads such that birds are able to start breeding once the habitat is reached and local environmental conditions are conducive. Birds are restricted to a single brood because arctic summers are short and food supply later in the season is unreliable. Photorefractoriness heralds the conclusion of breeding with first postnuptial molt followed by autumnal migration (Figure 8.5(c)). Type E includes transequatorial migrants that breed at relatively high latitudes and overwinter as far south as northern Argentina. Thus, birds never experience photophases that drop below 12 hours. It is likely that the initial predictive factor regulating development of the HPG axis is a circannual oscillator that possesses a strong threshold for a long photophase to initiate and subsequently terminate breeding as well as to break refractoriness. Examples of

this include the bobolink (Dolichonyx oryzivorus) (Engels, 1962), Siberian and European stonechats (Saxicola torquata rubicola, Saxicola torquata maura) (Helm, Schwabl, & Gwinner, 2009), and great knots (Calidris tenuirostris) (Piersma, Brugge, Spaans, & Battley, 2008). Type F examples lack the type of refractory period described above and are able to respond to photostimulation throughout the year. Such species demonstrate reproductive schedules that are symmetric about the spring solstice and are found within the Columbiformes and Galliformes (Nichols, Goldsmith, & Dawson, 1988). For example, relative photorefractoriness has been identified in Japanese quail (Coturnix coturnix japonica); this state is dependent upon the photoperiodic regimen to which the animal was previously exposed (Robinson & Follett, 1982). In addition, recent studies have identified relative photorefractoriness in rufous-winged sparrows (Aimophila carpalis), a Sonoran Desert specialist that initiates the developmental phase of breeding with spring photoperiods but arrests the mature capability phase until the onset of the summer monsoon season (Small et al., 2008). Given the present focus on north temperate species, three of the six models presented by Lofts and Murton (1968) are relevant to this discussion, namely types B (Figure 8.5(a)), C (Figure 8.5(b)), and D (Figure 8.5(c)). Using this comparative approach will prove instrumental in explaining how environmental conditions influence migration and breeding cycles.

6.4. Photoinduction: Cue Responses The developmental phases of vernal migration and breeding are initiated by increasing daylength (Farner, 1955; Farner & Follett, 1979; Schwabl & Farner, 1989a; 1989b), endogenous circannual rhythms (Evans, 1970; Gwinner, 1985; Holberton & Able, 1992; Berthold, 1996), or a combination of both (Wingfield, Schwabl, & Mattocks, 1990; Ramenofsky & Wingfield, 2007). For white-crowned sparrows, induction includes the biochemical and

212

molecular processes that lead to the expression of metabolic enzymes and hormones, increased appetite (hyperphagia), fattening, hypertrophy of flight muscles, and increased red cell proliferation (erythropoiesis) (Mattocks, 1976; Morton, 2002). Such functions culminate in achievement of the second phased‘migratory disposition’ or ‘mature capability’din which the behavior and physiology associated with cycles of fueling and flight are expressed (Wingfield et al, 1999; Ramenofsky & Wingfield, 2006; 2007) (Figure 8.3). The developmental phase of breeding also follows photoinduction, but the timing in relation to migration is delayed (Figure 8.4). These responses include molecular and physiological processes that result in transmission of GnRH and GnIH from cell bodies in the hypothalamus to the nerve terminals in the median eminence (ME) (Dawson et al., 2001; Tsutsui et al., 2009; see also Chapter 1, this volume) (Figure 8.1). Peptides are secreted into the ME and reach the anterior pituitary via the hypothalamicehypophysial portal system. Recent evidence has identified the thyroid hormone triiodothyronine (T3) as a regulator of GnRH release (Yoshimura, 2006; Nakao, Ono, & Yoshimura, 2008). Gonadotropin-releasing hormone and GnIH bind to the gonadotrope cells in the anterior pituitary, where they influence secretion of the GTHs FSH and LH. Both GTHs affect gonadal growth and development, and the secretion of gonadal hormones (estrogens, androgens, and progestins) that affect secondary sexual characteristics, accessory sexual organs, and reproductive behavior, all contributing to sexual maturity or the mature capability phase of breeding.

6.5. Regulation of the Developmental Phases of Migratory and Breeding Stages Development of the spring migratory and breeding stages is contingent upon increasing daylength in Z. l. gambelii (Stetson & Erickson, 1972; Mattocks, 1976; Wingfield, Schwabl, Schwabl-Benzinger, Goldsmith, & Farner, 1988; Hegner, Dufty, & Ball, 1990; Berthold, 1996; Wingfield & Silverin, 2009), golden-crowned sparrows (Zonotrichi atricapilla) (Morton & Mewaldt, 1962; King & Farner, 1963), white-throated sparrows (Zonotrichi albicollis) (Wolfson, 1958; Weise, 1967), dark-eyed juncos (Junco hyemalis) (Rowan, 1925; Wolfson, 1952; Deviche, 1995), red-headed buntings (Emberiza bruniceps) (Thapliyal, Lal, Pati, & Gupta, 1983), and bramblings (Fringilla montifringilla) (Lofts & Marshall, 1961). Although it is obvious that the gonads play a prominent role in breeding, their activity in relation to migration is less well known. Cue responses to long days activate specific photoreceptors and neuroendocrine pathways; one pathway directs migratory functions of hyperphagia and fattening. Flight-muscle

Hormones and Reproduction of Vertebrates

hypertrophy and oriented migratory flight or migratory restlessness are included in this list but their regulation is poorly understood. The other response pathway regulates the developmental phase of the breeding stage.

6.6. Morphological Evidence for Separate Control Systems for Migration and Breeding Separation of the neuroendocrine events regulating migration and breeding has been suggested in the literature but generally overlooked. Electrolytic lesions of distinct locations in the hypothalamus of white-throated sparrows (Z. albicollis) (Kuenzel & Helms, 1967; 1970) and whitecrowned sparrows (Stetson, 1971; Stetson & Erickson, 1972; Yokoyama, 1976a; 1976b) showed separate pathways controlling migratory fattening from migratory restlessness and gonadal activity. Neuropeptides produced in specific ganglia in distinct regions of the hypothalamus are released from nerve terminals in the ME into the hypothalamicehypophysial portal system, which serves the anterior pituitary (pars distalis) (Figure 8.6). The portal system of the white-crowned sparrow is divided into anterior and posterior networks, highlighting the site-specific or ‘point-to-point’ control the hypothalamus exerts over the pars distalis. Evidence for this includes studies involving electrocauterization of hypothalamic regions. Destruction of the anterior portion of the ME did not affect photoinduced fattening, gonadal development, or Zugunruhe (migratory restlessness), whereas disruption of either the posterior portion or entire ME eradicated all three (Stetson & Erickson, 1972; Yokoyama, 1976a; 1976b). Lesions of the basal infundibular nucleus (IFN) located in the ventral reaches of the hypothalamus disrupted testicular growth and migratory restlessness but birds showed variable degrees of migratory fattening (Yokoyama, 1976a; 1976b). Results from these studies pinpoint the IFN and posterior ME as potential neurosecretory components regulating the photoperiodic induction of both migratory and breeding activities. Recently, evidence suggesting separate neuroendocrine pathways leading to the posterior ME has been presented. Immunocytological studies identified avian GnRH-I (also known as chicken GnRH-I (cGnRH-I)), the neuropeptide regulating gonadal activity in birds, in cell bodies of the preoptic nucleus and septal regions of the hypothalamus, with fibers extending through the IFN and into the ME in white-crowned sparrows (Meddle, Bush, Sharp, Millar, & Wingfield, 2006) and European starlings (Parry, Goldsmith, Millar, & Glennie, 1997). Neurons coexpressing neuropeptide Y (NPY) and agouti-related protein mRNA coursing through the infundibulum of Japanese quail have been associated with compensatory hyperphagia (Boswell, Li, & Takeuchi, 2002). Considered together, these results suggest that the neuroendocrine

Chapter | 8

213

Hormones in Migration and Reproductive Cycles of Birds

FIGURE 8.6 Schematic diagram of the hypothalamusehypophysial system in the whitecrowned sparrow (Zonotrichia leucophrys gambelii), illustrating the anterior (AME) and posterior median eminence (PME). Three crosssectional images of the hypothalamus are presented, each containing successive views of the third ventricle and tracts of the neurosecretory axons traveling posteriorly through the infundibulum: I, anterior; II, medial; III, posterior sections of the basal hypothalamus. For functional considerations it is important to note that in Z. l. gambelii the cephalic (Ce) and caudal (Ca) lobes of the pars distalis (PD) are supplied by independent bundles of portal vessels. The capillaries leading to these vessels are in point-topoint contact with the endings of distinct divisions of hypothalamic tracts. CHO, optic chiasma; IS, infundibular stalk; NI, basal infundibular nucleus with clusters of different types of neurons coursing through; NL, neural lobe (posterior pituitary ¼ pars nervosa); PD, pars distalis; PT, pars tuberalis. Reproduced from Oksche and Farner (1974), with permission of Springer Science and Business Media.

pathway directing hyperphagia and fattening that reaches the posterior ME probably circumvents the IFN, thus separating the two pathways. Granted, the electrocautery methods described above may have not been as precise as the modern techniques of molecular neurochemistry; however, the results are compelling and highlight the importance of future research into regulation of the migratory and breeding stages by the CNS.

7. THE VERNAL MIGRATORY STAGE 7.1. The Developmental Phase Hyperphagia leading to fattening is of critical importance to migrants, as lipid is a main fuel because of its biochemical properties of high energetic density and low water content (Blem, 1980; Ramenofsky, 1990). As early as February, the increasing daylength activates androgen secretion, resulting in moderate and temporary peaks of T and 5a-dihydrotestosterone (DHT) in both sexes of whitecrowned sparrows and dark-eyed juncos (Wingfield & Farner, 1980; Ramenofsky, Savard, & Greenwood, 1999). Androgens secreted at this time may act to organize the feeding centers possibly located in the infundibular hypothalamus (Boswell et al., 2002; Boswell, 2005). The subsequent exposure to the critical daylength has stimulatory effects, activating the previously organized hypothalamic neurons. Suggested mechanisms by which this occurs

involve NPY, peptide YY (PYY), avian pancreatic peptide, and prolactin (PRL) (Meier & Farner, 1964; Yokoyama, 1976a; Kuenzel, Douglass, & Davidson, 1987; Denbow, Duke, & Chaplin, 1988; Kuentzel & McMurtry, 1988; Boswell et al., 1995; Richardson et al., 1995; Boswell, Millam, & Dunn, 1998; Denbow, 1999) and expression of insulin receptor gene in Japanese quail (C. c. japonica) (Anraku et al., 2007) while reducing sensitivity in the hypothalamus to the anorexigenic peptide cholecystokinin (CCK) (Boswell et al., 1995; Richardson et. al., 1995). As much work remains to be completed on this topic, it is clear that secretion of androgens has organizing effects on subsequent phases of the vernal migratory stage. Specific components of this system have been studied in depth, but the way in which these fit together and are coordinated to influence vernal as well as autumn migration remains obscure. Thus, a review of specific components of the system is provided in the hope of encouraging future research in these areas.

7.1.1. Hyperphagia and fattening Hyperphagia promotes fattening by processes involving increased ingestion, uptake of carbohydrate and fats across the gut, synthesis, and storage (Ramenofsky, 1990; Klasing, 1998; Ramenofsky et al., 1999). Fats or triacylglycerols (also known as triglycerides) are taken in via the diet as well as synthesized during lipogenesis or the de-novo

214

synthesis of nonesterified fatty acids from an acetate precursor. This occurs primarily in the liver in birds and results from the combination of malonyl coenzyme A (malonyl-CoA) and acetyl coenzyme A (acetyl-CoA) and Nicotinamide adedine dinucleotide phosphate (NADPH) in the presence of malic enzyme and fatty acid synthase (FAS). The activities of both enzymes relate to ingestion: increased activity is observed in domesticated chicks and ducklings fed normal mash diets, but low activity is observed under conditions of starvation (Goodridge, 1973; Goodridge, Jenik, McDevitt, Morns, & Winberry, 1984). Endocrine regulation of feeding and fattening in migrants is not well understood, but studies of domesticated species provide insight. Corticosterone (CORT) administration increases fat deposition in conjunction with elevated levels of insulin, insulin-like growth factor-1 (IGF-1), glucose, triglyceride, free fatty acids (FFAs), low-density lipoprotein, adipose tissue lipoprotein lipase (ALPL), and insulin resistance in broiler chickens (Yuan, Lin, Jiang, Jiao, & Song, 2008). Insulin and IGF-1 increase levels of T3, which, in conjunction with cyclic-3’,5’-adenosine monophosphate (cAMP), is thought to play a major role in the regulation of transcription of the malic enzyme gene in relation to feeding regimes. Corticosterone has a permissive role, affecting responsiveness of the malic enzyme gene to T3 (Goodridge et al., 1991). During autumn migration, birds have been documented feeding on fruits with high carbohydrate and fat content, which contributes to fattening (Bairlein, 1991; Bairlein & Gwinner, 1994; Parrish, 1997; McWilliams, Guglielmo, Pierce, & Klaassen, 2004). Such foodstuffs promote lipogenesis, whereas a protein-rich diet supports muscle anabolism, which can inhibit fat deposition (Rosebrough & McMurtry, 1993; Klasing, 1998). At first glance muscle hypertrophy and lipogenesis may appear to be opposing events, yet preparation for migration requires both power and fuel; this highlights that more work is needed in order to decipher the timing and endocrine mechanisms involved. Once synthesized, fatty acids may be incorporated into triglycerides and stored as fat. Fat deposition is expedited by the activity of ALPL, located in the endothelial lining of the capillary beds. Adipose tissue lipoprotein lipase hydrolyzes the ester bonds of the triglyceride, releasing fatty acids and glycerol to be absorbed by adipose tissue, resynthesized as triacylglycerols, and stored. Insulin promotes ALPL activity in the adipocytes of domestic fowl (Borron, Jensen, McCartney, & Britton, 1978; Borron, Jensen, McCartney, & Britton, 1979), and correlations of plasma insulin and ALPL have been identified in whitecrowned sparrows (Ramenofsky & Boswell, 1994). Further, periods of refeeding following bouts of migratory activity were associated with elevations of ALPL in captive dark-eyed juncos (Ramenofsky et al., 1999). In addition, plasma insulin was correlated with food intake and

Hormones and Reproduction of Vertebrates

increased body mass and plasma triglycerides in garden warblers (Sylvia borin) during autumnal migratory fattening (Totzke, Hu¨binger, & Bairlein, 1997).

7.1.2. Carbohydrates and lipids Studies focusing on peripheral effects have shown that manipulation of glucose levels via injections of either insulin or glucagon have no appreciable effect on food intake in short-day white-crowned sparrows (Boswell, Lehman, & Ramenofsky, 1997). These findings confirmed results presented for chickens indicating that birds may lack glucostatic regulation for feeding (Smith & BrightTaylor, 1974; Braun & Sweazea, 2008). However, increasing the circulating levels of FFAs inhibited food intake, suggesting that circulating levels of lipids may play an integral role in regulating food intake (Boswell et al., 1995). Further, studies on birds focusing on the migratory stages are needed.

7.1.3. The enigmatic roles of the pancreatic hormones: insulin and glucagon For most vertebrates insulin tightly regulates plasma glucose, but in birds these effects appear to be more complicated. Plasma levels of glucose are notoriously elevated in birds, exceeding those observed in mammals of similar mass (Braun & Sweazea, 2008). In general, insulin regulates plasma glucose by uptake via membranebound proteins, glucose transporters (GLUTs), and sodiumeglucose cotransporters (SGLTs) (Uldry & Thorens, 2004; Braun & Sweazea, 2008). Yet, in birds, the presence and identity of these proteins vary across tissues, as do their binding affinities for glucose (Braun & Sweazea, 2008). In the limited number of avian species studied, expression of both types of transporter is upregulated in the intestine and kidney, thus contributing to the elevated plasma glycemic levels. Further, expression of GLUT1 and -3 is elevated in the brains of chicks, broiler chickens, and house sparrows (Passer domesticus) over measurements in other target tissues including the skeletal muscle of the mourning dove (Zenaida macroura) (Kono, Nishida, Seki, Sato, & Akiba, 2005; Sweazea & Braun, 2006). Such findings emphasize the reliance of the CNS on glucose metabolism and offer a possible explanation for the requirement of sustained and elevated glycemic levels in birds (Sweazea & Braun, 2006). By contrast, administration of glucagon resulted in increased levels of glucose through enhanced glycogenolysis of liver glycogen (Hazelwood, 1973). However, other than glucose requirements for the CNS, glucose metabolism is not a major pathway for support of long-distance flight, and further consideration of these issues in terms of migratory life histories is needed.

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

7.1.4. Role of the gonad Evidence for the effect of the gonad on hyperphagia and fattening have been found from studies in a number of passerine species. Gonadectomy in males and females prior to the winter solstice erases the initial androgen signal in white-crowned sparrows (Stetson & Erickson, 1972; Mattocks, 1976; Wingfield et al., 1990; Schwabl & Farner, 1989a; 1989b). Consequently, birds do not fatten, although they do demonstrate limited migratory restlessness, suggesting that motor activity may be independent of the feedingefattening loop (Yokoyama, 1976a; 1976b; Ramenofsky et al., 1999; Landys, Ramenofsky, Guglielmo, & Wingfield, 2004). Replacement of androgens in castrates induces fattening in white-crowned sparrows (Mattocks, 1976) and golden-crowned sparrows (Morton & Mewaldt, 1962) but the effect is delayed in relation to controls. By contrast, male white-crowned sparrows castrated in the fall fatten normally for the subsequent autumn migration, pointing to a lack of influence of the testis at this time (Mattocks, 1976; Wingfield et al., 1990). Studies investigating the hypothalamicepituitaryethyroid (HPT) axis implicate a role for thyroid hormones in the association between gonadal activity and fattening (Figure 8.7). In the redheaded bunting (Emberiza bruniceps), injections of thyroid hormones and specifically T3 have been associated with migratory fattening and nocturnal restlessness (Pant & Chandola-Sakalani, 1993). The increased feeding, in conjunction with lipogenic enzymes, affects fattening and elevated body mass in preparation for spring migration

FIGURE 8.7 The hypothalamicepituitaryethyroid (HPT) axis in birds. The hypothalamic releasing peptide, thyrotropin-releasing factor (TRF), stimulates the secretion of thyroid-stimulating hormone (thyrotropin) (TSH) from the pituitary thyrotropes. In addition, the hypothalamic peptide corticotropin-releasing factor (CRF) also stimulates the secretion of TSH from the pituitary thyrotropes. Thyrotropin-releasing factor acts on thyroid follicle cells to increase secretion of the thyroid hormones triiodothyronine (T3) and thyroxine (T4). CNS, central nervous system.

215

(Blem, 1980; Ramenofsky, 1990; Ramenofsky et al., 1999; Egeler, Williams, & Guglielmo, 2000).

7.1.5. Prolactin (PRL) The effect of PRL on appetite may well be localized in the CNS. Specific binding sites of PRL have been identified in several regions of the hypothalamus, including the suprachiasmatic nucleus (SCN), ventromedial nucleus (VMN), paraventricular nucleus (PVN), lateral hypothalamus (LT), and tuberal hypothalamus in the brain of the ring dove (Streptopelia risoria) (Buntin & Tesch, 1985; Fechner & Buntin, 1989). Microinjections of PRL into specific hypothalamic sites have been shown to increase food intake in incubating ring doves (S. risoria) (Hnasko & Buntin, 1993). The roles of PRL and neural peptides in the regulation of migratory hyperphagia remain in question. It is possible that central levels of PRL or sensitivity of PRL receptors may be altered with photostimulation or by androgens, as suggested by Boswell, Dunn, and Corr (1999). Other systems may be at work as well, as hyperphagia is thought to be regulated by the visceral forebrain system, which balances the parasympathetic and sympathetic activities of the autonomic nervous system (ANS) in birds (Kuenzel, Beck, & Teruyama, 1999). Relationships between the ANS and PRL are not known. Prolactin also may directly effect tissues by stimulating hepatic lipogenesis, as observed in the in-vitro studies of domestic pigeons, Columba livia (Goodridge & Ball, 1967). Administration of PRL enhances fattening in a number of migratory passerines (Meier & Farner, 1964; Yokoyama, 1976a; Vleck & Wingfield, 1980). Such findings led to the hypothesis that circulating levels of PRL in conjunction with gonadal steroids induce migratory fattening. However, supporting evidence for this is lacking in white-crowned sparrows and dark-eyed juncos (Schwabl et al., 1988; Holberton, Boswell, & Hunter, 2008). Both studies showed an elevation of PRL within 14 to 16 days of photostimulation. However, the peak of PRL was not coincident with the onset of fattening in either study. The point of confusion stems from the fact that pituitary secretion of PRL is regulated by photoperiodic influence on the hypothalamus. Long daylengths induce the production of vasoactive intestinal peptide (VIP), the stimulatory neuropeptide for the production and secretion of PRL, by the lactotropes within the anterior pituitary (Figure 8.8). The rate of rise of PRL lags behind fattening and GTH induction, with peak levels achieved long after the onset of premigratory hyperphagia. This peak seems to co-occur with refractoriness and onset of postnuptial molt in starlings (Dawson & Sharp, 1998; Dawson, 2006). By contrast, inhibition of PRL is instigated by short daylengths and the neuropeptide dopamine, which inhibits VIP activation of

216

Hormones and Reproduction of Vertebrates

stages, possibly including migration. These suggestions hearken back to the findings that plasma lipids, namely FFAs, influence food intake in short-day white-crowned sparrows (Boswell et al., 1995). However, concern has been raised over the existence of the avian leptin gene regarding whether it truly has a function in birds (Sharp, Dunn, Waddington, & Boswell, 2008). Until these issues are resolved, the jury is out as to the role played by this hormone during migration.

7.1.7. Ghrelin

FIGURE 8.8 Central regulation of prolactin (PRL) secretion in birds. The hypothalamic releasing peptide, vasoactive intestinal peptide (VIP), promotes (solid line arrow) secretion of PRL from the pituitary lactotropes. Dopamine inhibits (dotted line arrow) PRL release from the pituitary lactotropes. CNS, central nervous system.

pituitary lactotropes (Youngren, Chaiseha, & El Halawani, 1998; Dawson et al., 2001).

7.1.6. Leptin In conjunction with hyperphagia and fattening, maintenance of lipid stores is vital throughout the migratory period. Although the regulatory mechanisms of this anabolic condition are not well understood in birds, the large polypeptide hormone leptin may hold great promise in tackling this complex issue. In mammals, adipose tissue produces leptin, a product of the ob gene; the ob gene regulates adiposity and the management of energy (Friedman, 2002). Administration of recombinant chicken leptin to caged great tits (Parus major) resulted in a rapid depression of food intake that was reversed within 30 min (Lo¨hmus, Sundstro¨m, El Halawani, & Silverin, 2003). Synthesis of leptin has been identified in the liver and adipose tissues of dunlin (Calidris alpina), with elevated levels found in fed vs. food-restricted birds (Kochan, Karbowksa, & Meissner, 2006). Recently, plasma levels of leptin-like immunoreactivity have been found to be elevated in females during the autumn as well as during the egg-laying and clutch-completion phases of breeding in female European starlings (Sturnus vulgaris) (Kordonowy, McMurtry, & Williams, 2010). Otherwise, no relationships were identified between the hormone and either mass or body condition. Together, this wide spread of results may suggest that leptin plays an important role in regulating adiposity and food intake in birds at various life-history

This 28-amino-acid peptide is synthesized in the gut as well as in the hypothalamus of mammals. Ghrelin is reported to be a growth hormone (GH)-releasing factor in chickens and mammals, which may make it a candidate for the regulation of lipid metabolism, growth, and development (Baudet & Harvey, 2003). In rats, both intraperitoneal (IP) and intracerebroventricular (ICV) injections of ghrelin increased food intake. This effect is most apparent during fasting, with ghrelin acting on the NPY/agouti-related peptide (AGRP) neurons in the arcuate nucleus (Nakazato et al., 2001). In quail, plasma ghrelin has been found to be elevated in fasted birds but levels dropped with feeding. The results obtained with injections were less clear cut; at low concentrations, IP injections enhanced feeding but at greater dosages both IP and ICV injections decreased feeding. Other studies in which ghrelin was administered reported that food intake in neonatal chicks was inhibited (Furuse et al., 2001). Although presently controversial, these results suggest that ghrelin could serve as a candidate for regulating feeding during migration, particularly when birds are lean, as they would be at the end of a migratory bout.

7.1.8. Corticosterone (CORT) Corticosterone (CORT), the major adrenal glucocorticoid in birds, plays an instrumental role in behavioral and metabolic processes during migration (Wingfield et al., 1990; Landys, Ramenofsky, & Wingfield, 2006; Holberton et al., 2008; Ramenofsky, Moffat, Guglielmo, & Bentley, 2008). However, to fully comprehend the functions of this glucocorticoid, it is helpful to view the hypothalamice pituitary regulation of CORT secretion (Figure 8.9) and to consider its actions at multiple physiological states or hormone levels (McEwen & Wingfield, 2003; Wingfield, 2004; Landys et al., 2006; Holberton et al., 2008). Level A is the undisturbed state, at which the basal level of CORT supports basic requirements for life such as maintaining hypothalamic feedback mechanisms and providing glucose to target tissues. Level B represents the levels that fluctuate in response to predictable and diel changes as well as seasonal adjustments for migration, breeding, wintering,

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

217

mechanisms at the level of the hypothalamus take over and the plasma CORT declines. Should the stressor persist and the condition become chronic, CORT levels return to level C, as the negative feedback mechanisms are overwhelmed and function declines (Wingfield & Sapolsky, 2003).

7.1.9. Hormone action of corticosterone (CORT)

FIGURE 8.9 Central regulation of corticosterone (CORT) secretion in birds. The hypothalamus regulates pituitary secretion of a variety of peptides and proteins that are cleaved from the prohormone proopiomelanocortin (POMC). Hypothalamic corticotropin-releasing factor (CRF) directs cleavage of corticotropin (ACTH) from POMC. Additional hypothalamic peptides, arginine vasotocin and mesotocin, regulate cleavage of other biologically active fragments from the POMC molecule, including endorphin and a-melanotropin (a-MSH). These have various effects on behavior, development, and metabolism. Corticotropin acts on the cortical tissue of the adrenal gland to stimulate the enzymatically directed synthesis of glucocorticoids, which in birds is primarily CORT. CNS, central nervous system.

and molt. Level C includes the titers induced by an acute and unpredictable stressor, such as capture and handling, that activates the hypothalamusepituitaryeadrenal (HPA) axis, resulting in an elevation of plasma CORT (Figure 8.9). These levels exceed level B and call into play alternative behavioral and physiological strategiesdan emergency life-history stagedthat promote survival functions in order to cope with the immediate stressor (Wingfield & Ramenofsky, 1999; Wingfield & Romero, 2001; Wingfield & Sapolsky, 2003). Many of these functions are catabolic; one promotes the breakdown of skeletal muscle protein, which for birds includes flight and heart muscle, for the production of glucose via gluconeogenesis. Many studies investigating the patterns of plasma CORT have elucidated both baseline and stress-induced levels during most of the life-history stages of birds (Wingfield & Ramenofsky, 1999; Wingfield & Romero, 2001; Wingfield & Sapolsky, 2003). Baseline levels are obtained by collecting blood within the first three minutes following capture; this provides an estimate of the predisturbance blood titers, as the HPA axis is thought to require at least that amount of time before secretion of CORT is elevated (but see L. Romero & R. Romero, 2002; Romero & Reed, 2005). After three minutes, plasma CORT rises to level C (stress-induced) and remains so for approximately 60 minutes, after which feedback

Corticosterone has specific effects on behavior and physiology at each of three levels and affects changes through one of four receptors, the high-affinity mineralocorticoid receptor (MR), the low-affinity glucocorticoid receptor (GR), the nongenomic membrane receptor (mGR), and a plasma-binding globulin, CORT-binding globulin (CBG) (Breuner & Orchinik, 2000; Breuner et al., 2003; Landys et al., 2006; see also Chapter 5, this volume). The specificity, affinity, and capacity of these proteins exert major effects on the hormonal action of CORT. In a study aiming to determine whether ecological factors influence the activities of CORT receptors, Breuner et al. (2003) compared Z. l. pugetensis, Z. l. oriantha, and Z. l. gambelii, representing a spectrum of migratory and breeding strategies. The binding capacity of CBG was highest in Z. l. gambelii but the values of the low-affinity GR-like receptor were decreased in the brain and liver. Together these results suggest a reduced response to stress during periods of inclement weather in the arctic, where breeding opportunities for Z. l. gambelii are restricted by a short breeding season. Modulation of the stress response is affected by the reduction of free circulating levels of CORT, owing to the elevated capacity of CBG in plasma and the reduction of free circulating levels of steroid, thought to be the biologically active form that enters target tissues. In addition, behavioral responsiveness or increased insensitivity to the hormone signal results from the smaller number of GR-like receptors in the brain and liver. Thus, receptor activity can have an impact on hormone action and appears to be influenced by environmental factors. Endogenous levels of glucocorticoids cycle in a diel pattern, with peaks of baseline CORT occurring prior to the onset of daytime activities that include feeding (Breuner, Wingfield, & Romero, 1999). This has led to the idea that increased levels of CORT induce feeding. However, administration of CORT to intact birds does not enhance food intake in dark-eyed juncos (Gray, Yarian, & Ramenofsky, 1990), mountain chickadees (Poecile gambeli) (Saldanha, Schlinger, & Clayton, 2000), white-crowned sparrows (Astheimer, Buttemer, & Wingfield, 1992), and domestic fowl (Gallus domesticus) (Simon, 1989). Administration of dexamethasone, a glucocorticoid agonist, had no effect on food intake during the onset of

218

the vernal migratory stage in dark-eyed juncos (Holberton, Wilson, Hunter, Cash, & Sims, 2007). However, interfering with GR via the use of the receptor antagonist RU486 decreased feeding in captive white-crowned sparrows during the spring stage (Landys et al., 2004a). Further, it is unlikely that binding of the GR (the low-affinity receptor) occurs during the wintering stage, when plasma levels of CORT are low, since disruption of the GR receptor had no effect on feeding at this time in white-crowned sparrows (Landys et al., 2004a). Thus, CORT plays a permissive role in regulating food intake at a threshold of level B, since supplementation of steroids or use of agonists does not enhance feeding (Landys et al., 2004a). It certainly is possible that other receptors are involved during the stages of migration. As a permissive agent, CORT affects many metabolic processes in conjunction with insulin, IGF-1, glucagon, and T3 (Simon, 1989; Goodridge et al., 1991; Landys et al., 2006; Remage-Healey & Romero, 2001), and, given the dramatic cycles of anabolism and catabolism that occur during migratory stages, it is highly likely that such hormones play critical roles.

7.1.10. Flight-muscle hypertrophy The increase in flight-muscle size occurs in conjunction with increased body mass and fat deposition to accommodate the power and fuel requirements for extended flight (Baggott, 1975; Marsh, 1984; Lundgren & Kiessling, 1985; Driedzic, Crowe, Hicklin, & Sephton, 1993; Piersma & Gill, 1998; Bauchinger & Biebach, 2001; Ramenofsky & Wingfield, 2007). Muscle hypertrophy was thought to occur primarily as a training effect, with the gain in mass and increased flight activity occurring prior to departure. However, studies that restricted movement of red knots during the developmental phase of both vernal and autumn migration questioned this premise (Dietz, Piersma, & Dekinger, 1999). Similarly, flight-muscle hypertrophy of eared and great-crested grebes (Podiceps nigricollis, Podiceps cristatus) were not associated with increased load or exercise (Piersma, 1988; Gaunt, Hikada, Jehl, & Fenbert, 1990). Thus, the mechanisms regulating flight-muscle hypertrophy remain enigmatic. The flight-muscle complex, pectoralis major and minor, is responsible for depressing the wing during flight and represents nearly 25e30% of fresh body weight (Goldspink, 1962; Lundgren & Kiessling, 1985; Davidson & Evans, 1988). Composition of the flight muscle of a number of long-distance migrants includes a predominance of fast-twitch oxidative-glycolytic fibers (Lundgren & Kiessling, 1985). The cross-sectional area of the individual fibers of long-distance migrants was found to be smaller than either the partial or nonmigratory species, while showing greater capillary densities. This distinction indicates shorter distances for diffusion of oxygen and metabolite delivery to the muscles, which

Hormones and Reproduction of Vertebrates

would increase the aerobic capacity of muscles supporting long-distance flight (Lundgren & Kiessling 1985). However, there are species differences in terms of the components of the muscle that enlarge. Davidson and Evans (1988) reported in Calidris shorebirds that flightmuscle hypertrophy prior to migration was the result of an increase in myofibril mass and mitochondria. After migration, the fibrillar mass decreased but the mitochondrial component remained intact to accommodate aerobic demands of the breeding stage. Muscle hypertrophy correlated with fattening in the gray catbird (Dumetella carolinensis) as birds prepared for fall migration (Marsh, 1984). Changes were attributed to the increased crosssectional area of the muscle fibers. Thus, in terms of hypertrophy of muscular components, a wide variety of adaptations are apparent across migratory species. In addition to hypertrophy of the contractile components, lipid content, which provides fatty acids for oxidative metabolism to fuel flight, fluctuates. Lipid within the muscle fibers increases in concert with adiposity in juvenile willow warblers (Phylloscopus trochilus) preparing for autumn migration (Baggott, 1975). Marsh (1984) reported in gray catbirds that, as birds fattened for fall migration, the lipid content of muscle increased accordingly. Studies of the eared grebe at a molting site in autumn indicate a sequelae of events that starts with a period of plentiful food resources, during which birds molt while mass and adiposity are elevated (Gaunt et al., 1990). But once the food source declines, the mass of the birds drops and deposition of intracellular lipid within the flight muscles begins. Within a matter of weeks, muscle hypertrophy occurs and birds depart for wintering grounds further south. Such sequential steps suggest site-specific regulation, but the hormonal mechanisms implementing these seasonal changes are poorly understood. Flight-muscle hypertrophy and lipid deposition may have additional advantages for migrants. Increased muscle mass supports more rapid contraction of fibers and promotes shivering thermogenesis and thermal tolerance for low ambient temperatures, which migrants might experience en route (Marsh, 1981; Dawson, Yacoe, & Marsh, 1983; Lundgren & Keissling, 1988; Morton, 2002; Swanson & Liknes, 2006). As dramatic as these morphological and biochemical changes are, relatively little is known of either the endocrine mechanisms regulating, or the precise timing of, muscle hypertrophy in migrants. Nevertheless, it may be important to distinguish between the power (contractile components) and fuel deposition (lipid) in muscle as separate processes with distinct endocrine regulatory mechanisms. Clues for such mechanisms may be drawn from a variety of sources. Studies on the growth and development of flight muscles in young barnacle geese (Branta leucopsis) have shown that rapid development and aerobic

Chapter | 8

219

Hormones in Migration and Reproductive Cycles of Birds

capacity are associated positively with plasma levels of thyroid hormones (Bishop, Butler, El Haj, & Egginton, 1998). Treatment with thyroid hormones enhanced expression of the thyroid hormone receptor TR-b0 mRNA in the pectoralis muscle of domestic ducklings (Anas platyrhynchos) (Bishop, McCabe, Gittoes, & Butler, 2000). The suggestion that thyroid hormones may play major roles during the developmental phase of spring migration has gained credence, since plasma levels of thyroxine (T4) increase with photostimulation and reach a peak within 10 days of exposure to 20L : 4D in white-crowned sparrows (Wingfield, Breuner, & Jacobs, 1997). Further, clues from the mammalian literature indicate that injections of recombinant IGF-1, insulin, and dexamethasone enhance Ca2þ-dependent calcineurin signaling pathways, supporting skeletal muscle hypertrophy (Semsarian et al., 1999). Taken together, it is clear that the endocrine regulation of muscle hypertrophy during the developmental phases of both vernal and autumnal migration deserves further investigation.

7.1.11. Erythropoiesis Erythropoiesis, the synthesis of red blood cells with increased hematocrit, is noted during migration; however, the timing and endocrine mechanisms involved are unclear. This process enhances oxygen-carrying capacity for prolonged flight and the requisite mobilization of fuel reserves. Specifically, measures of hematocrit are elevated in both male and female mountain white-crowned sparrows upon arrival at the breeding grounds in spring and at the time of departure in autumn (Morton, 2002) (Table 8.2). Hematocrit levels show seasonal increases during both the vernal and autumn stages of migration in Z. l. gambelii but not in the short-distance migrant, Z. l. pugetensis. In addition, increased hematocrit has been identified in bar-tailed godwits during the month-long stopover in spring

migration, particularly in high-quality individuals (Piersma, Everaarts, & Jukema, 1996). Sources of red blood cells include the spleen and bone marrow in adult birds (John, 1994), and there is the expectation that spleen size and activity, at least, would increase during the developmental phase of migration. Studies investigating morphological changes in the spleen in migrants have found varied results, partly due to the problems of sampling birds at the opportune sites (which include wintering, stopover, and breeding grounds) (Oakeson, 1953; 1956; Fa¨nge & Silverin, 1985). The most promising data achieved thus for have been obtained from garden warblers (S. borin) sampled prior to and during spring migration (Bauchinger & Biebach, 2005; Bauchinger, Wohlmann, & Biebach, 2005). These results showed an increased spleen size during the developmental phase and early stages of spring migration over samples collected following the first leg of the flight across the Sahara. Such results suggest that erythropoiesis is a preparatory step during the developmental phase of migration; however, seasonal and species comparisons remain controversial. The regulatory mechanisms of erythropoiesis are not well understood, but, in the nonmigratory spotted munia (Lonchura punctulata), increased production of erythropoietin in the kidney was enhanced with administration of T and T4 (Thapliyal, Pati, & Gupta, 1982). Testosterone is known to enhance both erythropoiesis and hematocrit in domestic fowl (Herrick, Lockhart, Martin, & Nusser, 1955) but had little effect on female white-crowned sparrows (Kern, DeGraw, & King, 1972). More recently, immunoreactive erythropoietin was measured in the plasma of Japanese quail; the results suggested that the kidney may be a source of this hormone (Wickramasinghe, Shiels, & Wickramasinghe, 1994). In summary, application of new molecular techniques and more extensive sampling are needed in order to clarify the endocrine mechanisms regulating erythropoiesis.

TABLE 8.2 Seasonal measures of hematocrit in adult male and female white-crowned sparrows Stages Races of Zonotrichia leucophrys*

Winter

Vernal migration

Breeding

Molt

Autumn migration

gambelii female

51.8 0.7

56.2 1.2

47.9 1.2

47.5 1.6

51.6 1.3

gambelii male

51.6 1.1

57.0 2.5

51.5 1.2

46.6 1.1

50.9 2.0

pugetensis male

50.9 1.1

51.5 2.5

48.9 1.6

45.2 3.0

51.2 0.8

oriantha female

e

57.0 2.5

53.0 0.4

50.0 0.6

54.5 0.4

oriantha male

e

59.0 1.5

54.0 0.2

49.0 0.6

55.0 1.0

e, No data available. *Data for Z. l. gambelii from Wingfield and Farner (1980) and for Z l. oriantha from Morton (2002).

220

7.2. The Mature Capability Phase 7.2.1. Fueling and flight cycles Upon completion of the developmental phase, birds enter the mature capability phase and express the behaviors and physiology that typify migratory disposition as they ready for departure. Throughout much of the year, birds exhibit periodic bouts of specific behaviors and physiology on a daily basis. For diurnal species, most of the intense activity occurs during the daylight hours, with rest at night. This pattern changes dramatically during migration, however, as birds alternate between periods of daytime fueling and rest and nocturnal flight. Long-distance, shortbout migrants such as the white-crowned sparrow demonstrate daily cycles of fueling and flying. In captive whitecrowned sparrows, 24-hour cycles of behavior and activity have been identified during autumn and vernal migratory stages (Agatsuma & Ramenofsky, 2006). During both stages, birds show daytime feeding followed by a period of absolute quiescence just prior to onset of night and active migratory restlessness. Studies investigating the circadian control of these daily components have found that daytime behavior appears to be under the control of an endogenous circadian rhythm but that nocturnal flight activity or migratory restlessness is initiated by the dark conditions of night (Coverdill, Bentley, & Ramenofsky, 2008). In fact, when exposed to prolonged dark conditions during the spring stage, the birds express migratory restlessness for 48 hours nonstop (Coverdill et al., 2008). This led to the suggestion that a circadian oscillator may regulate behavioral components of spring migration and that the dark conditions that promote migratory restlessness may mask the underlying rhythm.

7.2.2. Melatonin (MEL) Daily rhythms of activity are associated with the diel secretion of melatonin (MEL), the indolamine hormone produced by the pineal gland and other tissues, and a major component of the circadian system (Cassone & Menaker, 1984; Gwinner, Hau, & Heigle, 1997). Melatonin secretion is elevated during the dark phase but basal during the day in diurnal or day-active species. For a number of nocturnal migrants, MEL levels are reduced during the night phase, when birds actively express migratory restlessness (Fusani & Gwinner, 2004). In experimental studies in which levels of migratory restlessness are dampened by manipulating food availability (Beibach, 1985; Gwinner, Schwabl, & Schwabl-Benzinger, 1988), MEL levels are increased (Fusani & Gwinner, 2004). Further, when comparing migratory and nonmigratory forms of black-capped warblers (Sylvia atricapilla), nonmigrants had higher levels of nocturnal MEL than did migrants (Fusani & Gwinner, 2001). These results suggest that MEL is related

Hormones and Reproduction of Vertebrates

to low-level activity during the dark phase. A causal relationship between activity and MEL is not known, however, in Lapland longspurs (Calcarius lapponicus) breeding at high latitudes under nearly constant light conditions, peak levels of night-time MEL fell below samples collected during the winter stage, when birds roosted quietly at night (Hau, Romero, Brawn, & Van’t Hof, 2002). It is possible that nocturnal illumination was not low enough during the arctic summer to stimulate sufficient MEL secretion or that the levels relate directly to activity. Regardless, it is apparent that MEL plays a role in regulating diel cycles of activity in birds; its relationship with migratory behavior remains to be discerned.

7.2.3. Corticosterone (CORT) In addition to the effects discussed previously, CORT plays important roles during the flight or catabolic cycles of migration. Field studies of bar-tailed godwits (Limosa lapponica) throughout stopover en route to the breeding grounds have provided almost complete pictures of plasma levels of CORT throughout the substages of vernal migration (Ramenofsky, Piersma, & Jukema, 1995; LandysCiannelli, Ramenofsky, Piersma, Jukema, & Wingfield, 2002). Baseline levels were elevated as lean birds landed at the conclusion of the first leg of the migratory flight, which covered 4500 km. Throughout the month-long period of refueling, baseline levels of CORT declined, but rose precipitously as birds reached peak mass and prepared to depart for the second leg of the flight, to the breeding grounds some 4500 km away. Stress-induced levels of CORT increased at least three-fold in birds at arrival at the stopover as well as during refueling, indicating that baseline levels are lower than those associated with the acute and unpredictable stress of capture. Other long-distance migrants show peaks of CORT in relation to flight phase. Red-eyed vireos (Vireo olivaceus) have been studied during autumn migration at stopover sites along the Gulf Coast of the southeastern USA. Birds departing from the coast and heading for the Amazon basin showed elevations of baseline CORT (Lo¨hmus et al., 2003). Further, as red-knots (Calidris c. islandica) arrived at the breeding grounds in the Canadian arctic following longdistance flight across the Atlantic Ocean, baseline levels of CORT were elevated, but they dropped precipitously once birds had settled into breeding (Reneerkens, Morrison, Ramenofsky, Piersma, & Wingfield, 2002). These studies suggest that CORT measured within level B may have at least two roles during the flight substage of migration: (1) in a preemptive manner to mobilize stored fuels that will be needed and/or to prepare for the unpredictable conditions that might be encountered during flight and (2) in response to flight itself, to sustain the availability of fuel for target tissues including flight muscles, heart, brain, etc.

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

7.2.4. Captive studies and corticosterone (CORT) In support of the field studies, experiments with captive white-crowned sparrows have identified diel patterns of CORT, with elevated levels of baseline CORT occurring when birds express nocturnal migratory restlessness over the daytime levels when they feed and rest (Landys, Wingfield, & Ramenofsky, 2004; Ramenofsky et al., 2008). Investigations into the regulatory control of migratory restlessness in captive white-crowned sparrows found that exposure to persistent night conditions (dim light of < 1 Lux) resulted in continuous expression of migratory restlessness (Coverdill et al., 2008). Using this paradigm, it was possible to test the correlation of expression of migratory restlessness and baseline CORT. After extending migratory restlessness for 2, 24, and 48 hours, plasma CORT remained elevated over the subjective daytime samples, when birds feed and rest (Ramenofsky et al., 2008). Stress-induced samples measured 30 minutes postcapture revealed levels two- to three-fold higher than baseline values, indicating that, like free-living migrants, captive birds will respond rapidly to an acute stressor. Despite the increased energy demands associated with migratory flight, these results support earlier findings that migration itself does not constitute a stress but is a predictable stage within the life history of migrants for which birds prepare. Though more field and captive studies are needed, these results suggest that CORT may play a critical role as a metabolic regulator of energy flow during migratory flight.

7.2.5. The migration modulation hypothesis Corticosterone appears to be involved in both fueling and flight cycles; it plays a permissive role in hyperphagia and fattening and is involved with the flight phase. At first glance it may seem enigmatic to have one steroid involved in both anabolic and catabolic activities, particularly in light of the fueling/flight cycles. One explanation for this apparent puzzle is the migration modulation hypothesis, which contends that during migration birds maintain moderately elevated levels of CORT to promote hyperphagia and fattening during periods of fueling (Holberton, Parrish, & Wingfield, 1996; Long & Holberton, 2004). However, if a bird is exposed to a stressor and the resulting titers rise to level C, this may contribute to extensive catabolism of flight muscles for gluconeogenesis, which could impair flight. To avoid this condition, the adrenocortical response to stressors is suppressed. Support for this hypothesis is drawn from a series of studies on autumn migrants. Lean gray catbirds in the postnuptial molt stage were compared with individuals of the same species that had completed the developmental phase and had fattened

221

in preparation for departure (Holberton et al., 1996). Migratory birds had very high baseline levels of CORT and did not respond to capture stress with further elevations, whereas the molting birds had lower baseline levels and responded to capture stress with increased levels of CORT. Further, a cohort of migratory yellow-rumped warblers (Dendroica coronata) captured at a stopover site during autumn migration had elevated and stable plasma levels of both baseline and stress-induced CORT (Holberton et al., 1996). Comparing individual hermit thrushes (Catharus guttatus) in different energetic states during autumn migration, Long and Holberton (2004) found that lean birds tended to have higher baseline levels of CORT without an adrenocortical response to capture in comparison with birds with greater fuel stores. These results led to the suggestion that energetic state may influence baseline levels of CORT and stress sensitivity in migrants. By contrast, other studies on both autumn and vernal migrants have found little support for the hypothesis. Romero, Ramenofsky, and Wingfield (1997) identified lower baseline levels in autumn migrants in comparison with those garnered during the vernal stage. Both migratory stages responded to capture with an adrenocortical response, though the stress-induced levels in autumn birds fell below those of spring. Although no seasonal distinction was observed, male and female western sandpipers (Calidris mauri) showed a marked response to capture stress (O’Reilly & Wingfield, 1995). Schwabl, Bairlein, and Gwinner (1991) reported a low baseline value for CORT followed by increased levels in response to capture during autumn migration in garden warblers. Two studies on semipalmated sandpipers (Calidris pusilla) sampled at the Delaware Bay stopover site identified a stress response during spring and autumn migration (Tsipoura, Scanes, & Burger, 1999; Mizrahi, Holberton, & Gauthreaux, 2001). Body condition of birds varied by year as well as throughout the stopover period. Estimation of fat mass calculated from published allometric equations was negatively correlated with plasma levels of GH, indicating variations in lipolysis or the catabolism of fat stores across individuals and migratory stages (Tsipoura et al., 1999). Yearly variation in sensitivity to capture stress was identified and associated with potential fluctuations in the abundance of the primary food source (egg masses of the horseshoe crab (Limulus polyphemus)) (Mizrahi et al., 2001). Recent studies have tested these assumption in birds with distinct migratory strategies. The flammulated owl (Otus flammeolus), a long-distance, neotropical migrant, relies on large deposits of fat and flight-muscle mass to fuel flight. The northern saw-whet owl (Aegolius acadius), a short-distance nomad, stores little fat and has smaller muscle mass, and relies on available resources to support flight (Hamilton, 2002). Despite the differences in

222

migratory strategies and energetic states, the baseline levels of CORT sampled during autumn migration were identical. Further, the adrenocortical response to capture stress was likewise similar and robust. Another example is a population of partially migratory blue tits (Cyanistes caeruleus) in southern Sweden (Nilsson & Sandell, 2009). Migrants of the population showed levels of CORT at capture elevated over those of resident birds, but both groups showed a marked stress response. Given these reports, it appears that there is great variation across species, seasons, and fueling periods in terms of the sensitivity of the adrenocortical response to capture. Yet, for the majority of species studied, the adrenocortical response to stress remains intact during the migratory stages. The thread running through all of these studies is the question of whether lean birds (birds in poor energetic condition) possess elevated levels of baseline CORT in order to promote foraging and fattening during migration. The baseline levels of CORT of both gray catbirds and yellow rumped warblers did not relate to fat stores (Holberton et al., 1996). Rather, plasma levels of CORT remained elevated throughout the migratory period, when birds experienced rapid changes in fat deposits. Likewise, no correlation was identified in autumn-migrating whitecrowned sparrows (Romero et al., 1997). Throughout the month-long stopover in the Wadden Sea, bar-tailed godwits experience dramatic changes in mass, and baseline levels of CORT are lowest during the period of refueling and elevated when fueling ceases at departure. A similar pattern of peak baseline CORT was observed in a captive group of red knots, which express the seasonally appropriate preparation for spring migration in spite of being unable to leave the confines of their cages. Baseline levels of CORT reach a peak at the pinnacle of heightened mass (Piersma, Reneerkens, & Ramenofsky, 2000). It is possible that the captive studies that track individuals throughout the period of mass gain suggest that, as the levels of CORT rise during the feeding and fattening substage, they offer support for its influential role. However, studies that administer CORT at various stages to a variety of species have found variable results on food intake (see Section 7.1.9). Thus, we are left with the suggestion made earlier that CORT plays a permissive role in conjunction with other hormones; this emphasizes the need for further investigations, with a focus on the specific phases of both migratory stages. Finally, blood samples collected from a variety of songbirds during the autumnal crossing of the Alps showed low baseline levels of CORT in all but one lean and emaciated pied flycatcher (Ficedula hypoleuca) (Gwinner et al., 1992). These results suggest that the increase in CORT is related to exhaustion of the fuel (lipid and fat) depots, as this individual appears to have experienced an elevation of allostatic load (Wingfield, 2004). Results of this nature

Hormones and Reproduction of Vertebrates

certainly point to the conclusion that CORT is instrumental in regulating energy storage and mobilization during the fueling and flight cycles of migration; however, they also suggest that an overriding hypothesis such as the migration modulation hypothesis is inadequate when applied to the vast number of adaptations for this life history across the broad spectrum of species.

7.2.6. Corticosterone-binding globulin (CBG) Throughout the annual cycle of many species, the baseline and stress-induced levels of CORT fluctuate as baseline levels are low during postnuptial molt and winter. With spring photoperiods, baseline levels increase throughout migration and peak on arrival at the breeding grounds (Romero et al., 1997; Deviche, Breuner, & Orchinik, 2001; Romero, 2002; Breuner et al., 2003). Thereafter, levels decrease once nesting begins (Holberton & Wingfield, 2003). For many species, these seasonal fluctuations of CORT are associated with plasma levels of androgen, which can regulate the binding capacity of CBG (Breuner & Orchink, 2000; Breuner et al., 2003). Binding capacity of CBG alters both free and bound titers of plasma CORT where the free component is thought to be the biologically active form that binds to either the membrane or intracellular receptors. Factors that influence CBG, such as androgens, food restriction, and possibly elevated allostatic load, can have major impacts on the actions of CORT during migration (Bruener & Hahn, 2003; Lynn, Breuner, & Wingfield, 2003). Curiously, seasonal differences in baseline CORT have not been reported in other migrant species, suggesting that regulation of CBG may vary with species and migratory strategy.

7.2.7. Metabolic adjustments during fueling/ flight cycles For long-distance migrants, the digestive organs and enzyme systems undergo major remodeling to promote either fueling or flight efficiency, depending upon the stage of the cycle. At stopover, birds rest and reconstitute the digestive organs and enzyme systems in order to refuel. At the conclusion of stopover, much of the digestive system again regresses to accommodate weight requirements and also to provide additional energy gained from protein catabolism via gluconeogenesis (Gaunt et al., 1990; Battley & Piersma, 1997; Schwilch, Grattarola, Spina, & Jenni, 2002; Bauchinger et al., 2005). The process by which this occurs is not well understood and probably involves apoptosis, a common means of physiological cell loss or programmed cell death in tissues (Medh & Thompson, 2000). Epithelial and stem cell turnover of the intestine is regulated by hormones as well as by paracrines secreted by the enteroendocrine and pancreatic cells. Somatostatin

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

(GHRIH) and related compounds inhibit DNA synthesis of gastrointestinal stem cells and promote degeneration of the epithelial cells of the crypts that form the villi in the intestines of mammals (Bjork, Nilsson, Hultcrantz, & Johansson, 1993; Thompson, 1998). Corticosterone promotes both cell growth and death in distinct tissues, depending upon the titer and receptor activity (Devenport, Knehans, Sunstrom, & Thomas, 1989; Distelhorst, 1997), and may play a critical role in orchestrating organ remodeling during migration. During flight, enzymatic and hormonal regulation of fuel delivery from stock depots to working tissues, including the muscle and brain, occurs. Flight muscle capacity for oxidative metabolism is enhanced by the protein-mediated transport of circulating fatty acids into the flight muscle complex (pectoralis major and minor). Elevated mRNA expression of three genes instrumental in fatty transportdfatty acid translocase (FAT/CD36), plasma membrane fatty acid-binding protein (FABPpm), and hearttype fatty acid-binding protein (H-FABP)dhas been identified in the autumn and vernal stages (over that of the wintering stage) in white-throated sparrows (McFarlan, Bonen, & Guglielmo, 2009). Further, protein expression of the plasma membrane FABP and the cytosolic H-FABP were increased, offering support for a heightened capacity for fatty acid delivery to mitochondria within the flight muscle. This, coupled with increased enzyme activity for oxidative metabolism, contributes to the overwhelming evidence that migratory birds capitalize on fatty acids as the main source of fuel supporting long distance flight (Jenni & Jenni-Eiermann, 1998; Guglielmo, Haunerland, Hochachka, & Williams, 2002; McWilliams et al., 2004; Guelgimo, Cerasale, & Eldermire, 2005; Lyons, Collazo, & Guglielmo, 2008). The degree to which many of these metabolic processes occur may be dependent upon migratory strategy, with long-distance migrants showing the most dramatic changes in comparison with short-distance migrants, but few comparative studies have been conducted. While the cycles of fueling and flight repeat numerous times depending upon the species and route covered, the patterns of fuel delivery and endocrine mechanisms involved remain to be investigated more completely.

7.3. The Termination Phase

223

many species breeding at high latitudes and altitudes may involve spatial opportunism and facultative altitudinal migration (Hahn & Morton, 1995; Hahn, Wingfield, & Mullen, 1995; Hahn, Sockman, Breuner, & Morton, 2004). Such concepts address ideas presented earlier (DeWolfe, West, & Peyton, 1973; Gauthreaux, 1982; Terrill & Able, 1988) concerning adaptations of physiology and behavior of migrants confronting severe conditions at either the breeding or wintering sites that include prevalent storms, decreased availability of food, and heightened demands for energy. Under such conditions, birds may retreat to locations where food and shelter are accessible, thus reducing the cost of subsistence. On a daily basis, they may visit the breeding territories until conditions ameliorate (Bruener & Hahn, 2003). During this time, birds remain in a mobile state and may wander further to locate optimal breeding sites. Hyperphagia maintains enhanced lipid stores to support mobile activity and provides protection against the potential of severe food limitation owing to inclement weather (Wingfield & Ramenofsky, 1999; Wingfield et al., 2004). Condition of the flight muscles at this stage is largely unknown as to whether muscle size, fatty acid uptake and metabolism are maintained or decreased. As the energetic requirements for long-distance flight have been terminated, it is likely that flight muscle may have reverted to its premigratory condition. Again, the endocrine mechanisms regulating this and other muscle sites remain unclear. Once conditions at the breeding grounds ameliorate or a suitable site for breeding is located, the vernal migratory life-history stage is terminated, flocks disband, hyperphagia wanes, and fat stores decline as birds become territorial and commence breeding.

8. THE BREEDING LIFE-HISTORY STAGE 8.1. The Developmental Phase Photoinduction initiates the developmental phase of breeding and influences termination. Progression and duration of the mature capability phase are affected by local predictive factors. Taken together, these environmental cues affect distinct cycles of breeding. The subspecies of Zonotrichia provide an illuminating array of examples for comparing the timing and duration of breeding in relation to migratory strategy and environmental parameters (Figure 8.10).

7.3.1. Arrival biology Once the breeding grounds have been reached, the fueling/ flight cycles cease and arrival behavior and physiology ensue, the nature of which is contingent upon local phenological conditions and species. This phase marks the beginning of the termination of vernal migration and is called ‘arrival biology’ (Wingfield et al., 2004), which for

8.1.1. Latitude and photoperiod When investigating the cue responses that initiate the developmental phase of breeding among the subspecies of Zonotrichia, one must take into account both the latitude and photoperiod to which the population is exposed at the time of initiation (Farner & Wilson, 1957; Farner, Follett,

224

Hormones and Reproduction of Vertebrates

FIGURE 8.10 Life cycles of five divisions of whitecrowned sparrow with distinct breeding localities that range from high- and mid-latitude migratory forms to lower latitude sedentary populations. The length of vernal migratory period increases with latitude, whereas territoriality decreases. The profile of testosterone secretion is most brief in the arctic and expands in more southerly populations. Postnuptial molt is apparent in all races but only migratory species have a prenuptial molt. Species: tundra white-crowned (Zonotrichia leucophrys gambelii), taiga (Z. l. gambelii), mountain (Z. l. oriantha), Puget Sound (Z. l. pugetensis), and Nuttall’s (Z. l. nuttalli) sparrows. See color plate section.

King, & Morton, 1966; King, Follett, Farner, & Morton, 1966; King & Mewaldt, 1981; Morton, 2002). Comparisons drawn from both Z. l. gambelii and Z. l. pugetensis at wintering latitudes of 34.4 and 46.5 N indicate that the developmental phase of testicular growth in populations wintering further south is initiated early in February, when photoperiod reaches 10.35L : 13.25D. Birds wintering further north do not begin the developmental phase until late February or early March, when the photoperiod at this latitude is 11.38L : 12.22D, which constitutes about an hour difference in timing (Blanchard & Erickson, 1949; King & Mewaldt, 1981). Following initiation, the rate of testicular growth in relation to photoperiod was slower in more southerly populations than in those of the north. The rate of gonadal growth, however, is related to the amount of exposure to daylight, which increases faster at higher latitudes; this has been termed the ‘Farner rule’ (Farner & Follett, 1966). This effectively brings birds breeding at a given latitude but wintering at diverse locations into reproductive readiness at approximately the same time.

8.1.2. Sedentary vs. migratory Zonotrichia The cue response to photophase of the sedentary Z. l. nuttalli has a lower threshold than that of the migratory subspecies and initiates the developmental phase of breeding soon after the winter solstice, when the photophase is only slightly greater than 9L (Blanchard, 1941; Mewaldt & King, 1977). Expression of mature reproductive capability can commence in early March and continues until the birds become photorefractory around July 20 (Blanchard, 1941; Mewaldt & King, 1977). Z. l. nuttalli are reported to produce three or four broods

per year (Blanchard, 1941; Mewaldt & King, 1977). By comparison, the migratory subspecies have shorter breeding stages. For example, the short-distance migrant Z. l. pugetensis breeds at lower latitudes and covers a migratory distance of approximately 650 km. Thus, the spring migratory stage is relatively short and the developmental stage of breeding can be completed two months earlier than that of the long-distance subspecies Z. l. gambelii or Z. l. oriantha. Local predictive cues, including climatic conditions and temperature, can affect the photoperiodically induced rate of gonadal development and the timing of the onset of breeding (Lewis & Farner, 1973; Wingfield et al., 1997). Nevertheless, under optimal conditions, Z. l. pugetensis can produce a maximum of three broods, in comparison with the single-brooded Z. l. gambelii or the potential two broods for Z. l. oriantha. Termination of breeding (photorefractoriness) sets in at approximately the same time for all three subspecies (mid-July) indicating a moderate threshold of photosensitivity for long photoperiods (Lofts & Murton, 1968; Hahn & MacDougall-Shackleton, 2008). Therefore, the major distinction in the timing of breeding across Zonotrichia subspecies is the photoperiodic threshold for initiating the developmental phase of breeding, though other factors include migratory strategy and the influence of local predictive factors.

8.1.3. Lifecycles of Zonotrichia It is instructive to compare the lifecycles of the five divisions of Zonotrichia, which range from high-latitude and mid-latitude migratory species to lower-latitude sedentary populations (Z. l. nuttalli). Figure 8.10 depicts features of the male life-history stages. Testosterone is

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

illustrated as it plays a major role during the breeding stage in males. This steroid has diverse functions including anabolic effects on muscle, development of secondary sexual structures, and promotion and sustainment of spermatogenesis, and it affects sexual behaviors such as territoriality, courtship, and mate defense (Balthazart, 1983; Wingfield, Lynn, & Soma, 2001; Moore et al., 2002; Goymann, 2009). For monogamous species, such as white-crowned sparrows, plasma T peaks during territorial establishment and mate guarding, after which levels decline during the parental phase as elevated levels of androgens interfere with chick rearing (Hegner & Wingfield, 1987; Silverin, 1990; Ketterson, Nolan, Wolf, & Zeigenfus, 1992; Wingfield & Hunt, 2002) and the subsequent stagedpostnuptial molt (Schleussner, Dittami, & Gwinner, 1985). This phenomenon has been termed the ‘challenge hypothesis,’ and it has helped to explain the relationship between the profiles of androgens and mating systems, a topic that extends beyond the scope of this chapter (Wingfield, Ball, Dufty, Hegner, & Ramenofsky, 1987; Wingfield et al., 1990). At lower latitudes, duration of the breeding stage is prolonged, and territoriality, mate defense, and elevated levels of T persist. The opportunity to raise multiple broods increases with a longer breeding stage. The sedentary Z. l. nuttalli presents a nearly yearlong period of territoriality. Once a male establishes a territory, he will remain on the site year-round. Quite surprisingly, the shallow levels of T appear to be sustained throughout breeding and without a clear peak. This may be due to the fact that synchrony is strongest within a pair and not across the population, which would make a peak difficult to discern. Once breeding and molt conclude, birds remain territorial but levels of T are nondetectable. Similar patterns have been observed in other sedentary species including the song sparrow (Melospiza melodia), a tropical species of bay wren (Thryothorus nigricapillus) (Levin & Wingfield, 1992), white-browed sparrow weaver (Plocepasser mahali) (Wingfield, Hegner, & Lewis, 1991); suggest alternative mechanisms for androgen control of territorial behavior. Examples of some of the alternative mechanisms are presented in two current hypotheses. The first is the ‘circulating precursor hypothesis,’ which suggests that the androgen dehydroepiandrosterone (DHEA), synthesized by the adrenal glands or the regressed testes, has no effect on male behavior. Its conversion to biologically active steroids, androstenedione, T, and estrogens in the brain may, however, affect aggressive behavior during the period of fall territoriality (Wingfield & Soma, 2002; Pradhan et al., 2010). The second, the ‘neural steroid hypothesis,’ involves androgens and estrogens synthesized locally in the brain from cholesterol in the presence of steroidogenic enzymes. It is in these sites that the neurosteroids exert effects on aggressive behavior (Tsutsui & Yamakazi, 1995;

225

Ukena et al., 1999). Current studies in the field have yielded novel and exciting results. Current studies in the field have yielded novel and exciting results (see for review: Wingfield and Silverin, 2009).

8.2. The Termination Phase 8.2.1. Photorefractoriness Termination includes the substage of photorefractoriness that is followed by postnuptial molt (Farner & Follett, 1979; Donham, Moore, & Farner, 1983; Dawson et al., 2001). The actual timing of the onset of photorefractoriness is difficult to determine but, in general, onset of molt is a visual indication that refractoriness has set in (Nicholls et al., 1988; Morton, 2002). As seen in Figure 8.10, conclusion of the breeding stage across the migratory Zonotrichia occurs at about the same time (late June to early July), but the length of the breeding season, including the parental phase, varies with latitude. This may seem somewhat perplexing given the large spread of breeding habitats, from the high arctic (68 N) to the mid-range of the Sierra Nevada in California (38 N). However, in Z. l. gambelii, photorefractoriness is established earlier in the year, during photoinduction of gonadal growth (Moore, Donham, & Farner, 1982). Once refractoriness is initiated, the rate at which it develops is contingent upon the increasing photoperiod birds experience during spring (Farner & Follett, 1966; Farner, 1985). This is one explanation given for the similar timing of refractoriness across Zonotrichia subspecies (Farner & Follett, 1966; 1979; Morton, 2002). Though this may hold true for adult birds, it cannot be applied to juveniles hatched under long photoperiods and in a state of refractoriness (Dawson & McNaughton, 1992; McNaughton, Dawson, & Goldsmith, 1992). Though refractory, European starling nestlings exposed to long photoperiods are reported to be able to perceive daylength but do not secrete GnRH until fully adult (McNaughton & Dawson, 1992). The explanation proposed by Morton (2002) for this fact is that the annual cycle of life-history stages may reflect an underlying circannual rhythm that is regulated by long and short photoperiods (Ashoff, 1980; Gwinner, 1985). Proximate factors affect the ontogenetic stages of young birds, including postfledging molt and development of autumn migration (Farner & Follett, 1966; 1979). The continued exposure to short daylengths breaks refractoriness in juvenile birds, which then enter the adult schedule of life-history stages (Morton, 2002). For other species, including the song sparrow (Wingfield, 1993), house sparrow (Dawson, 1991), white-throated sparrow (Harris & Turek, 1982), and mountain white-crowned sparrow (Morton, 1992), exposure to decreasing daylengths appears to regulate expression of photorefractoriness.

226

Hormones and Reproduction of Vertebrates

However, in transequatorial migrants such as Phylloscopus and Sylvia warblers (Gwinner, 1985; Berthold, 1996), the red knot (Piersma, 2002), and short-tailed shearwaters (Puffinus tenuirostris) (Marshall, 1959), exposure to decreasing daylengths is curtailed at the conclusion of breeding and during autumn migration. In these cases, circannual rhythms entrained by a specific photoperiod serve to regulate patterns of gonadal growth and regression. The critical test for demonstration of an endogenous rhythm relies on the removal of all exogenous cues (Dunlap, Loros, & DeCoursey, 2004). However, there are only two studies in which endogenous cycles have been demonstrated in birds held in constantly dim or light conditions; the species studied were the spotted munia (Chandola, Bhatt, & Pathak, 1973) and the dark-eyed junco (Holberton & Able, 1992). Both cases offer support for the role of circannual rhythms regulating gonadal function and may be applicable to other species as well. Nonphotic cues may also affect the timing of photorefractoriness. Food availability and temperature have been shown to influence the termination of breeding in freeliving zebra finches (Taeniopygia guttata) (Wingfield, Hahn, Wada, Astheimer, & Schoech, 1996; Wingfield, Hahn, Wada, & Schoech, 1997; Dawson, 2006; Perfito, Bentley, Zann, & Hau, 2006; Silverin et al., 2008). Further, departure from breeding grounds was delayed in male song sparrows (Runfeldt & Wingfield, 1985). Males remained on the territory when exposed to the solicitations of an estradiol-implanted female at the end of breeding, when birds were photorefractory and controls had migrated south. Curiously, the converse effect did not impress the females. A territorial male, treated with T, did not delay timing of departure from the breeding grounds for the females. Thus, it appears that the regulation of the behavior and physiology associated with refractoriness varies across a wide spectrum of both endogenous and exogenous factors.

9. THE AUTUMN MIGRATORY STAGE

8.2.2. The role of the hypothalamicepituitarye thyroid (HPT) axis

9.1.2. Hyperphagia and fattening

Thyroid hormones appear to play a prominent role in the termination phase of breeding. A series of studies focusing on the thyroid axis and reproduction in European starlings demonstrated that T4 must be present for both gonadal regression and postnuptial molt (Goldsmith & Nicholls, 1984; Nicholls et al., 1988; Dawson et al., 2001). In juvenile European starlings, thyroid hormones promote development of refractoriness (Dawson, 1989). Juvenile whitecrowned sparrows (Z. l. gambelii) revealed elevations of T4 during post-juvenile molt at the breeding grounds in central Alaska (Wingfield, Smith, & Farner, 1980). As is apparent, investigations of the HPT axis and refractoriness across the Zonotrichia subspecies and other species deserve further attention.

9.1. The Developmental Phase 9.1.1. Photoperiod and refractoriness Once molt is completed, the developmental phase of autumn migration begins with the appearance of the same preparatory events that occurred during the vernal staged hyperphagia, fattening, muscle hypertrophy, and erythropoiesis. Unlike the developmental stage of spring migration, which overlaps with breeding, the autumnal phase follows photorefractoriness and postnuptial molt, in which the ovaries and testes are regressed and circulating levels of androgens are basal (Wingfield & Farner, 1993). Further, castrated Z. l. gambelii, which failed to show hyperphagia and fattening during the vernal stage, fattened normally during the autumn, suggesting that gonadal activity is not involved and pointing to an entirely different control mechanism (King, Mewaldt, & Farner, 1960; Mattocks, 1976; Wingfield et al., 1990). It is thought that the photoinduction that regulates development of the spring stage may have delayed effects on the autumn migratory stage (King, 1963; Moore et al., 1982). Even though the mechanisms by which this occurs are not known, it is entirely possible that the timings of refractoriness and postnuptial molt somehow influence the development of the autumnal migratory stage. It is also possible that the mechanisms regulating the autumn migratory stage are similar to those of the vernal stage and involve androgens, with the major distinction being the site of hormone synthesis and action. Both the steroid precursor and the neural steroid hypotheses may be applicable to the development for the autumn migration. If this is the case, circulating levels of androgens would remain basal and avoid the costs of elevated plasma levels of androgensdnamely breeding morphologies and aggressive behavior.

Very few studies have monitored birds on the breeding grounds as they prepare for autumn migration. One exception is the long-term study of Z. l. oriantha in the Sierra mountain range in California (38 N) by Morton (2002). Birds begin to fatten and gain mass at the termination of postnuptial molt. Males reach a peak rate of mass gain of 2.3 to 2.6%, with one individual gaining at an incredible rate of 14% over a period of eight to nine days. Once maximal mass and fat loads are achieved, birds depart for wintering grounds in Baja, California. Similar findings were reported for juvenile tundra white-crowned sparrows (Z. l. gambelii) on the breeding grounds as they progressed through postjuvenile molt and fattened for autumn migration (Bonier et al., 2007). Birds in the midst of heavy molt had very low deposits of fat. Once molt subsided, the rate of

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

fattening increased, suggesting that energetic demands for the replacement of feathers, blood, and other components renewed during the molt exceed that for fuel deposition. Thus, it appears that, for populations at high latitudes and altitudes, overlapping the mature capability phase of molt and the developmental phase of autumn migration is not energetically feasible. Somewhat surprising are the measures of baseline CORT collected from the tundra white-crowned sparrows throughout molt. Levels throughout molt in lean and fat males and females remained low (F. Bonier, unpublished results). This pattern was also observed in male taiga white-crowned sparrows captured in the central interior of Alaska, as well as both male and female Z. l. pugetensis, in which plasma CORT is basal during postnuptial molt and remains low throughout departure (Wingfield & Farner, 1978a; 1978b). However, the female pattern at this time diverges from that of the male, with an elevation following postnuptial molt. The difference for this disparity is unclear; however, both sexes captured at more southerly stopover sites during autumn migration have low baseline levels, suggesting a strong difference from the spring migratory stage, when baseline levels are elevated (Wingfield & Farner, 1978a; Romero et al., 1997). Clearly, studies investigating these disparities are needed in order to determine what role CORT plays during the developmental phase of migratory hyperphagia and fattening in autumn.

9.2. The Mature Capability Phase In comparison with the vernal migratory stage, departure and movement during autumn migration are far less synchronous and intense (King, 1963; Wingfield & Farner, 1978a). Once birds leave the high arctic, the rate of passage slows as the risk of confronting foul weather diminishes and daylength decreases at a slower rate. Studies of captive Z. l. gambelii confirm the field observations as the 24-hour locomotor profiles and recorded behaviors of autumn migrants were quantitatively and qualitatively lower than records from spring birds (Ramenofsky et al., 2003; Agatsuma & Ramenofsky, 2006).

9.2.1. Navigation and juvenile birds As birds depart for wintering grounds, another distinction between the spring and autumn migratory stages becomes apparent. In spring, all birds traveling north have completed at least one leg of the journey during the previous autumn stage. In autumn, however, juveniles are making this trip for the first time. During their ‘maiden voyage’, juvenile European starlings were not able to detect navigational errors, possibly owing to the lack of the cognitive map of directions that is compiled with migratory experience

227

(Perdeck, 1967; 1974). As a test of this hypothesis, both juvenile and adult Z. l. gambelii captured at a stopover site in central Washington state (latitude 46 N, longitude 120 W) during autumn migration were displaced to Princeton, New Jersey (latitude 40 N, longitude 74 W). Upon release, the juvenile birds were unable to compensate for the eastward displacement and continued to migrate south. By contrast, the adults responded to the displacement by migrating in a westerly direction, heading toward the original migratory route (Thorup et al., 2007). These data suggest that juvenile white-crowned sparrows may lack a navigational map that would allow for detection of an unusual location as they proceed through their first autumnal migration. Orientation and navigation during migration have been associated with other complex behaviors such as food caching, which requires reliance on spatial organization and memory. Both of these are functions associated with the size and neuronal populations of the hippocampus of the brain (Pravosudov, Kitaysky, & Omanska, 2006). Studies designed to test the performance of spatial memory revealed that Z. l. gambelii were more adept than the nonmigratory Z. l. nuttalli. The relative size of the hippocampus of migrants was larger and contained more neurons in the right portion of the brain structure (Pravosudov et al., 2006). Comparisons of adult and juvenile Z. l. gambelii identified that young birds had fewer neurons in the right hippocampus than adults, a distinction not found in Z .l. nuttalli (Pravosudov et al., 2006). Another study with migrants found that adult garden warblers (S. borin) that had completed a round-trip migration from Africa to Europe and back possessed greater hippocampal volume than juveniles that had yet to migrate (Healy, Gwinner, & Krebs, 1996). These results suggest that orientation and navigation behavior is an acquired skill involving a learning experience and the development of neuronal networks within the hippocampus. It is unknown when juveniles gain competence, but it must occur sometime during the later stages of autumn migration or during the return flight in spring. Such cases emphasize the potential danger facing juveniles during the first autumnal migration, should conditions force birds off course. Records indicate that mortality is greatest for the young cohort during autumn migration. Estradiol and T have been implicated in promoting spatial learning in male and female meadow voles (Microtus pennsylvanicus) (Galea, Kavaliers, Ossenkopp, & Hampson, 1995). Such findings may suggest that gonadal steroids, which are increasing in incremental amounts at this time, may play a role in the development of a navigational map during spring migration as birds return to breeding grounds, but this is only speculation. Gagliardo, Loale`, Savini, Dell’Omo, and Bingman (2009) reported that homing pigeons (Columba livia) also

228

possess a map-like representation of familiar landmarks in the hippocampus that aids in locating home lofts. Such findings broaden the scope of mechanisms of orientation, navigation, and learning to a wider variety of highly mobile avian species. Future work in this area should prove highly fruitful.

9.3. The Termination Phase 9.3.1. Local environmental conditions As birds near their overwintering sites, the consensus of opinion among researchers is that adults generally return to areas where they spent the previous winter, whereas juveniles may be more mobile until they finally settle (Curry-Lindahl, 1981; Terrill, 1990). Upon arrival, Z. l. gambelii no longer carry large loads of fat, and muscle mass appears to be reduced to levels observed during the developmental phase (M. Ramenofsky, unpublished data). Baseline levels of CORT are low and commensurate with the values measured at the breeding grounds at departure, and at stopover sites (Romero et al., 1997). Migratory flight wanes as behavior and physiology become influenced more by local environmental conditions, perhaps in a manner similar to the termination of spring migration, although the mechanisms remain entirely unknown. The predictability of resources, climatic conditions, and social dominance each appear to have a great impact on the termination phase (Terrill & Ohmart, 1984). Should environmental conditions degrade and birds be unable to maintain positive energy balance, movements away from the area are likely. However, it is not clear that birds will enlarge stores of fat and flight muscle mass to fuel and power these facultative movements. By December, termination of autumn migration is complete, with further movement unlikely, but very little is known of this phase.

10. CONCLUSIONS The timing and duration of life-history stages of the annual cycle of birds represent evolutionary adaptations to the predictable variations of the environment. Such adaptations provide a window for studying the endocrine mechanisms that regulate the temporal patterns of each stage. In this chapter the focus has been on the migration and breeding stages of migratory and sedentary races of the Pacific white-crowned sparrows. Taking a finite state machine approach provides a means by which these varied cycles may be aligned, compared, and analyzed. In summary, environmental conditions have influenced the migratory and sedentary strategies that are mediated by the endocrine system.

Hormones and Reproduction of Vertebrates

11. FUTURE DIRECTIONS 11.1. Vernal and Autumn Migration: Similarities and Differences The alignment of and relationships between the two migration stages and other life-history stages highlights important distinctions across the stages. On the one hand, the vernal stage follows directly from prenuptial molt to breeding, with photoinduction and gonadal activity playing directive roles. Birds rely on a signal from the gonad to indicate whether the spring migratory trip is necessary. On the other hand, the autumn stage is separated from breeding by the postnuptial molt. Current photoperiod and gonadal function do not appear to be involved. Yet, for the most part, the distances and landscapes covered by the two stages are similar, as are the substages of hyperphagia, fattening, and muscle hypertrophy, as well as the flight and fueling cycles. Thus far, it appears that the mechanisms regulating the two stages are distinct, but our knowledge of the endocrine mechanisms regulating the stages is far from perfect. Many migratory species are declining at shockingly rapid rates as a result of changes in global temperatures, ecology, and resources (Friedman, 2008; Newton, 2008; Wilcove, 2008; Turner, 2009). Under such circumstances it is critical that an understanding of the environmental control of endocrine mechanisms of both autumn and vernal migration be reached (Wingfield, 2008a). Many studies of migratory populations have concentrated on one species or one phase of a particular stage as a result of the difficulties of locating and trapping migratory birds. This is helpful but does not provide a full picture. The most effective way of tackling this problem is to focus on a species and, where possible, draw comparison across closely related taxa with varying migratory tendencies. These kinds of investigation can provide valuable insights into the environmental and endocrine mechanisms regulating both stages while offering significant clues as to the evolution of the life history. Such an approach could easily pinpoint historical, current, or potential problems that contribute to a species’ decline or success.

ACKNOWLEDGEMENTS Many individuals generously gave time and thoughts to discussions covering the topics presented in the manuscript and I wish to thank them all: Rene´e Agatsuma, George Bentley, Fran Bonier, Tim Boswell, Jamie Cornelius, Alex Coverdill, Tom P. Hahn, Meta Landys, John Moffat, Zoltan Nemeth, Gang Wang, Heather Watt, and John C. Wingfield. Many ideas and some of the research presented in this chapter were supported by grant IOS#0920791 from the National Science Foundation to M.R.

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

ABBREVIATIONS AGRP ALPL cAMP CBG CCK cGnRH-I CNS CORT DHEA DHT FABPpm FAS FAT/CD36 FFA FSH GH GHRIH GLUT GnIH GnRH GR GTH H-FABP HPA HPG HPT ICV IFN IGF-1 IP LH LT ME MEL mGR MR NADPH NPY PRL PVN PYY SCN SGLT T T3 T4 TR VIP VMN

Agouti-related peptide Adipose tissue lipoprotein lipase Cyclic-3’,5’-adenosine monophosphate Corticosterone-binding globulin Cholecystokinin Chicken gonadotropin-releasing hormone-I Central nervous system Corticosterone Dehydroepiandrosterone 5a-dihydrotestosterone Plasma membrane fatty acid-binding protein Fatty acid synthase Fatty acid translocase Free fatty acid Follicle-stimulating hormone Growth hormone Somatostatin Glucose transporter Gonadotropin-inhibiting hormone Gonadotropin-releasing hormone Glucocorticoid receptor Gonadotropin Heart-type fatty acid-binding protein Hypothalamicepituitaryeadrenal Hypothalamicepituitaryegonadal Hypothalamicepituitaryethyroid Intracerebroventricular Infundibular nucleus Insulin-like growth factor-1 Intraperitoneal Luteinizing hormone Lateral hypothalamus Median eminence Melatonin Nongenomic membrane receptor Mineralocorticoid receptor Nicotinamide adenine dinucleotide phosphate Neuropeptide Y Prolactin Paraventricular nucleus Peptide YY Suprachiasmatic nucleus Sodiumeglucose cotransporter Testosterone Triiodothyronine Thyroxine Thyroid hormone receptor Vasoactive intestinal peptide Ventromedial nucleus

REFERENCES Addis, E. A., Davis, J. E., Bonier, F., Miner, B. E., Wingfield, J.C. Physiological variation is associated with range expansion in a passerine bird, (in press).

229

Agatsuma, R., & Ramenofsky, M. (2006). Migratory behaviour of captive white-crowned sparrows, Zonotrichia leucophrys gambelii, differs during autumn and spring migration. Behaviour, 143, 1219e1240. Anraku, T., Takagi, T., Nakao, N., Watanabe, M., Yasuo, S., Katou, Y., et al. (2007). Photoperiodic changes in hypothalamic insulin receptor gene expression are regulated by gonadal testosterone. Brain Res., 1163, 86e90. Ashoff, J. (1980). Biological clocks in birds. Proc. Int. Ornithol. Congr. 17th, 113e136. Astheimer, L. B., Buttemer, W. A., & Wingfield, J. C. (1992). Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scan., 23, 355e365. Avise, J. C., & Walker, D. (1998). Pleistocene phylogeographic effects of avian populations and the speciation process. Proc. R. Soc. Lond. B, 265, 457e463. Baggott, G. K. (1975). Moult, flight muscle “hypertrophy” and premigratory lipid deposition of the juvenile willow warbler, Phylloscopus trochilus. J. Zool. Lond., 175, 299e314. Bairlein, F. (1991). Body mass of garden warblers (Sylvia borin) on migration: a review of field data. Vogelwarte, 36, 48e61. Bairlein, F., & Gwinner, E. (1994). Nutrional mechanisms and temporal control of migratory energy accumulation in birds. Ann. Rev. Nutr., 14, 187e215. Baker, J. R. (1938). The evolution of breeding season. In G. B. DeBeer (Ed.), Evolution: essays on aspects of evolutionary biology (pp. 161e177). Oxford, UK: Oxford University Press. Ball, G. F., & Hahn, T. P. (1997). GnRH neuronal systems in birds and their relation to the control of seasonal reproduction. In I. S. Parhar, & Y. Sakuma (Eds.), GnRH neurons: gene to behaviour (pp. 325e342). Tokyo, Japan: Brain Shuppan Publishers. Balthazart, J. (1983). Hormonal correlates of behavior. In D. S. Farner, J. R. King, & K. S. Parkes (Eds.), Avian Biology, (Vol. 7) (pp. 221e365). New York, NY: Academic Press. Banks, R. C. (1964). Geographic variation in the white-crowned sparrow, Zonotrichia leucophrys. Uni. Calif. Publ. Zool., 70, 1e123. Battley, P. F., & Piersma, T. (1997). Body composition of lesser knots (Calidris canutus rogersi) preparing to take off on migration from northern New Zealand. Notornis, 44, 137e150. Bauchinger, U., & Biebach, H. (2001). Differential catabolism of muscle protein in garden warblers (Sylvia borin): flight and leg muscle act as a protein source during long-distance migration. J. Comp. Physiol., 171, 293e301. Bauchinger, U., & Biebach, H. (2005). Phenotypic flexibility of skeletal muscles during long-distance migration of garden warblers: muscle changes are differentially related to body mass. Ann. NY Acad. Sci., 1046, 271e281. Bauchinger, U., Van’t Hof, T., & Biebach, H. (2007). Testicular development during long-distance spring migration. Horm. Behav., 51, 295e305. Bauchinger, U., Van’t Hof, T., & Biebach, H. (2009). Food availability during migratory stop-over affects testis growth and reproductive behaviour in a migratory passerine. Horm. Behav., 55, 425e433. Bauchinger, U., Wohlmann, A., & Biebach, H. (2005). Flexible remodeling of organ size during spring migration of the garden warbler (Sylvia borin). Zoology, 108, 97e106. Baudet, M. L., & Harvey, S. (2003). Ghrelin-induced GH secretion in domestic fowl in vivo and in vitro. J. Endocrinol., 179, 97e105.

230

Bearhop, S., Fiedler, W., Furness, R. W., Votier, S. C., Waldron, S., Newton, J., et al. (2005). Assortative mating as a mechanism for rapid evolution of a migratory divide. Science, 310, 502e524. Bell, C. P. (2000). Process in the evolution of bird migration and pattern in avian ecogeography. J. Avian Biol., 31, 258e265. Berthold, P. (1996). Control of bird migration. London, UK: Chapman and Hall. Biebach, H. (1985). Sahara stopover in migratory flycatchers (Muscicapa striata); fat and food affect the time program. Experientia, 41, 695e697. Bishop, C. M., Butler, P. J., El Haj, A. J., & Egginton, S. (1998). Comparative development in captive and migratory populations of the barnacle goose. Physiol. Zool., 71, 198e207. Bishop, C. M., McCabe, C. J., Gittoes, N. J. L., & Butler, P. J. (2000). Tissue-specific regulation of thyroid hormone receptor mRNA isoforms and target gene proteins in domestic ducks. J. Endocrinol., 165, 607e615. Bjork, J., Nilsson, J., Hultcrantz, R., & Johansson, C. (1993). Growthregulatory effects of sensory neuropeptides, epidermal growth factor, insulin and somatostatin on the non-transformed intestinal epithelial cell line IEC-6 and colon cancel cell line HT 29. Scand. J. Gastroenterol., 28, 879e884. Blanchard, B. D. (1941). The white-crowned sparrow (Zonotrichia leucophrys) of the pacific seaboard: environmental and annual cycle. Univ. Calif. Publ. Zool., 46, 1e178. Blanchard, B. D. (1942). Migration in pacific coast white-crowned sparrows. Auk, 59, 47e63. Blanchard, B. D., & Erickson, M. M. (1949). The cycle of the Gambel sparrow. Univ. Calif. Publ. Zool., 47, 255e318. Blem, C. R. (1980). The energetics of migration. In S. A. Gauthreaux (Ed.), Animal migration, orientation, and navigation (pp. 175e224). London, UK: Academic Press. Bonier, F., Martin, P. R., Jensen, J. P., Butler, L. K., Ramenofsky, M., & Wingfield, J. C. (2007). Pre-migratory life history stages of juvenile arctic birds: cost, constraints and tradeoffs. Ecology, 88, 2729e2735. Borron, D. C., Jensen, L. S., McCartney, M. G., & Britton, W. M. (1978). Role of lipoprotein-lipase in regulation of lipid deposition in chickens and turkeys. Poult. Sci., 57, 1097. Borron, D. C., Jensen, L. S., McCartney, M. G., & Britton, W. M. (1979). Comparison of lipoprotein-lipase activities in chickens and turkeys. Poult. Sci., 58, 659e662. Boswell, T. (2005). Regulation of energy balance in birds by the neuroendocrine hypothalamus. J. Poultry Science, 42, 161e181. Boswell, T., Boswell, T., Richardson, R. D., Seeley, R. J., Ramenofsky, M., Wingfield, J. C., et al. (1995). Regulation of food intake by metabolic fuels in white-crowned sparrows. Am. J. Physiol., 269, R1462e1468. Boswell, T., Dunn, I. C., & Corr., S. A. (1999). Hypothalamic neuropeptide Y mRNA is increased after food restriction in growing broilers. Poult. Sci., 78, 1203e1207. Boswell, T., Lehman, T. L., & Ramenofsky, M. (1997). Effects of plasma glucose manipulations in white-crowned sparrows. Comp. Biochem. Physiol., 118A, 721e726. Boswell, T., Li., Q., & Takeuchi, S. (2002). Neurons expressing neuropeptide Y mRNA in the infundibular hypothalamus of Japanese quail are activated by fasting and co-express agouti-related protein mRNA. Mol. Brain Res., 100, 31e42.

Hormones and Reproduction of Vertebrates

Boswell, T., Millam, J. R., Li., Q., & Dunn, I. C. (1998). Cellular localization of neuropeptide Y mRNA and peptide in the brain of the Japanese quail and domestic chicken. Cell Tissue Res., 293, 31e38. Braun, E. J., & Sweazea, K. L. (2008). Glucose regulation in birds. Comp. Biochem. Physiol. B, 151, 1e9. Breuner, C. W., & Hahn, T. P. (2003). Integrating stress physiology, environmental change and behavior in free-living sparrows. Hormones and Behavior, 43, 115e123. Breuner, C. W., & Orchinik, M. (2000). Downstream from corticosterone: seasonality of binding globulins, receptors and behavior in the avian stress response. In A. Dawson, & C. M. Chaturvedi (Eds.), Avian endocrinology (pp. 1e12). New Delhi, India: Narosa Publishing. Breuner, C. W., Orchinik, M., Hahn, T. P., Meddle, S. L., Moore, I. T., Owen-Ashley, N. T., et al. (2003). Differential mechanisms for regulation of the stress response across latitudinal gradients. Am. J. Physiol. Regul. Integr. Comp. Physiol., 285, R594eR600. Breuner, C. W., Wingfield, J. C., & Romero, L. M. (1999). Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambel’s white-crowned sparrow. J. Exp. Zool., 284, 334e342. Bullough, W. S. (1942). The reproductive cycles of the British and continental races of the starling, Sturnus vulgaris l. Philosophical Transactions Royal Society London B, 231, 165e246. Buntin, J. D., & Tesch, D. (1985). Effects of intracranial prolactin administration on maintenance of incubation readiness, ingestive behavior, and gonadal condition in ring doves. Horm. Behav., 19, 188e203. Cade´e, N., Piersma, T., & Daan, S. (1996). Endogenous circannual rhythmicity in a non-passerine migrant, the knot, Calidris canutus. Ardea, 84, 75e84. Caro, S. P., Lambrechts, M. M., Balthazart, J., & Perret, P. (2007). Nonphotoperiodic factors and timing of breeding in blue tits: impact of environmental and social influences in semi-natural conditions. Behavioural Processes, 75, 1e7. Cassone, V. M., & Menaker, M. (1984). Is the avian circadian system a neuroendocrine loop? J. Exp. Zool., 232, 539e349. Chandola, A., Bhatt, D., & Pathak, V. K. (1973). Environmental manipulation of seasonal reproduction in spotted munia, Lonchura punctulata. In S.-I. Mikami, K. Homma, & M. Wada (Eds.), Avian Endocrinology: Environmental and Ecological Perspectives (pp. 229e242). Tokyo, Japan: Jap. Sci. Soc Press. Coppack, T., & Pulido, F. (2004). Photoperiodic response and the adaptability of avian life cycles to environmental change. Advan. Ecol. Res., 35, 131e150. Cornelius, J. (2009). Annual schedules, environmental cues and stress physiology in an irruptive, nomadic songbird, the red crossbill (Loxia curvirostra). Davis, Ph.D. Thesis, U. of California. Cortopassi, A. J., & Mewaldt, L. R. (1965). The circumannual distribution of white-crowned sparrows. Bird-Banding, 36, 141e169. Coverdill, A. J., Bentley, G. E., & Ramenofsky, M. (2008). Circadian and masking control of migratory restlessness in Gambel’s Whitecrowned Sparrow (Zonotrichia leucophrys gambelii). J. Biol. Rhy., 23, 59e68. Curry-Lindahl, K. (1981). Bird migration in Africa. London, UK: Academic Press. Davidson, N. C., & Evans, P. R. (1988). Prebreeding accumulation of fat and muscle protein by arctic-breeding shorebirds. Ottawa, Canada: Proc. XIX Int’l Ornithol Congr. 342e352.

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

Dawson, A. (1989). The involvement of thyroxine and daylength in the development of photorefractoriness in European Starlings. J. Exp. Zool., 249, 68e75. Dawson, A. (1991). Photoperiodic control of testicular regression and moult in male house sparrows, Passer domesticus. Ibis, 133, 312e316. Dawson, A. (2006). Control of molt in birds: association with prolactin and gonadal regression in starlings. Gen. Comp. Endocrinol., 147, 314e322. Dawson, A., & Sharp, P. J. (1998). The role of prolactin in the development of reproductive photorefractorness and postnuptial molt in the European starling (Sturnus vulgaris). Endocrinol., 139, 485e490. Dawson, A., King, V. M., Bentley, G. E., & Ball, G. R. (2001). Photoperiodic control of seasonality in birds. J Biol. Rhythms, 16, 365e380. Dawson, A., & McNaughton, F. J. (1992). Puberty in European starlings: can nestlings perceive daylength. Ornis Scand., 23, 209e213. Dawson, W. R., Yacoe, M. E., & Marsh, R. L. E. (1983). Metabolic adjustment of small passerine birds for migration and cold. Am. J. Physiol., 245, R755eR767. Denbow, D. M. (1999). Food intake regulation in birds. J. Exp. Zool., 283, 333e338. Denbow, D. M., Duke, G. E., & Chaplin, S. B. (1988). Food intake, gastric secretion, and motility as affected by avian pancreatic polypeptide administered centrally in chickens. Peptides, 9, 449e454. Devenport, L., Knehans., A., Sunstrom, A., & Thomas, T. (1989). Corticosterone’s dual metabolic actions. Life Sci., 45, 1389e1396. Deviche, P. (1995). Androgen regulation of avian premigratory hyperphagia and fattening: from eco-physiology to neuroendocrinolgy. Amer. Zool., 35, 234e245. Deviche, P., Breuner, C. W., & Orchinik, M. (2001). Testosterone, corticosterone and photoperiod interact to regulate plasma levels of binding globulin and free steroid hormone in dark-eyed Juncos, Junco hyemalis. Gen. Comp. Endocrinol., 122, 67e77. DeWolfe, B. B., West, G. C., & Peyton, L. J. (1973). The spring migration of Gambel’s sparrows through southern Yukon Territory. Condor, 75, 43e59. Dietz, M. W., Piersma, T., & Dekinga, A. (1999). Body-building without power training: endogenously regulated pectoral muscle hypertrophy in confined shorebirds. J. Exp. Biol., 202, 2831e2837. Distelhorst, C. W. (1997). Glucocorticoid-induced apoptosis. Adv. Pharmacol., 41, 247e270. Dittami, J., & Gwinner, E. (1985). Annual cycles in the African stonechat Saxicola torquata axillaries and their relationship to environmental factors. J. Zool. Lond., 207, 357e370. Donham, R. S., Moore, M. C., & Farner, D. S. (1983). Physiological basis of repeated testicular cycles on twelve-hour days (12L:12D) in whitecrowned sparrows, Zonotrichia leucophrys gambelii. Physiol. Zool., 56, 302e307. Driedzic, W. R., Crowe, H. L., Hicklin, P. W., & Sephton, D. H. (1993). Adaptations in pectoralis-muscle, heart mass, and energy-metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can. J. Zool., 71, 1602e1608. Dunlap, J. C., Loros, J. J., & DeCoursey, P. J. (2004). Chronobiology. Sunderland, MA: Sinauer Associates, Inc. Egeler, O., Williams, T. D., & Guglielmo, C. G. (2000). Modulation of lipogenic enzymes, fatty acid synthase and D9edesaturase, in relation to migration in the western sandpipler (Calidris mauri). J. Comp. Physiol. B, 170, 169e174.

231

Engels, W. L. (1962). Day-length and termination of photorefractoriness in the annual testicular cycle of the transequatorial migrant Dolichonyx (the bobolink). Biol. Bull., 123, 94e104. Evans, P. R. (1970). Timing mechanisms and the physiology of bird migration. Sci. Prog. Oxf., 58, 263e275. Fa¨nge, R., & Silverin, B. (1985). Variation of lymphoid activity in the spleen of a migratory bird, the pied flycatcher (Ficedula hypoleuca; Aves, Passeriformes). J. Morph., 184, 33e40. Farner, D. S. (1955). The annual stimulus for migration: experimental and physiologic aspects. In A. Wolfson (Ed.), Recent studies in avian biology (pp. 198e237). Urbana, IL: University of Illinois. Farner, D. S. (1985). Annual rhythms. Ann. Rev. Physiol., 47, 65e82. Farner, D. S., & Follett, B. K. (1966). Light and other environmental factors affecting avian reproduction. J. Anim. Sci., 25, 90e115. Farner, D. S., & Follett, B. K. (1979). Reproductive periodicity in birds. In E. J. W. Barrington (Ed.), Hormones and Evolution (pp. 829e872). New York, NY: Academic Press. Farner, D. S., Follett, B. K., King, J. R., & Morton, M. L. (1966). A quantitative examination of ovarian growth in the white-crowned sparrow. Biol. Bull., 130, 67e75. Farner, D. S., & Wilson, A. C. (1957). A quantitative examination of testicular growth in the white-crowned sparrow. Biol. Bull., 113, 254e267. Fechner, J. H., & Buntin, J. D. (1989). Localization of prolactin bindingsites in ring dove brain by quantitative autoradiography. Brain Res., 487, 245e254. Friedman, J. M. (2002). The function of leptin in nutrition, weight and physiology. Nutr. Rev., 60, S1eS14. Friedman, T. L. (2008). Hot, flat and crowded, why we need a green revolution and how it can renew America. Farrar, Straus and Giroux Publishing. Furuse, M., Tachibana, T., Ohgushi, A., Ando, R., Yoshimatsu, T., & Denbow, D. M. (2001). Intracerebroventricular injection of ghrelin and growth hormone releasing factor inhibits food intake in neonatal chicks. Neurosecience Letters, 301, 123e126. Fusani, L., & Gwinner, E. (2001). Reduced amplitude of melatonin secretion during migration in the blackcap warblers (Sylvia atricapilla). In H. J. T. Goos, R. K. Rastogi, H. Vaudry, & R. Pierantoni (Eds.), Perspectives in Comparative endcroinology: Unity and diversity (pp. 295e300). Bologna, Italy: Moduzzi Press. Fusani, L., & Gwinner, E. (2004). Simulation of migratory flight and stopover affects night levels of melatonin in a nocturnal migrant. Proc. R. Soc. Lond. B, 271, 205e211. Gagliardo, A., Loale`, P., Savini, M., Dell’Omo, G., & Bingman, V. P. (2009). Hippocampal-dependent familiar area map supports corrective re-orientation following navigational error during pigeon homing: a GPS-tracking study. Euro. J. Neurosci., 29, 2389e2400. Galea, L. A. M., Kavaliers, M., Ossenkopp, K.-P., & Hampson, E. (1995). Gonadal hormone levels and spatial learning performance in the Morris water maze in male and female meadow voles, Microtus pennsylvanicus. Horm. Behav., 29, 106e125. Gaunt, A. S., Hikada, R. S., Jehl, J. R., Jr., & Fenbert, L. (1990). Rapid atrophy and hypertrophy of an avian flight muscle. Auk, 107, 649e659. Gauthreaux, S. A. (1982). The ecology and evolution of avian migration systems. In D. S. Farner, J. R. King, & K. C. Parkes (Eds.), Avian Biology (pp. 93e168). Academic Press.

232

Goldsmith, A. R., & Nicholls, T. J. (1984). Thyroidectomy prevents the development of photorefractorniss and the associated rise in plasma prolactin in starlings. Gen. Comp. Endocrinol., 54, 256e263. Goldspink, G. (1962). Biochemical and physiological changes associated with postnatal development of the biceps brachii. Comp. Biochem. Physiol., 7, 157e168. Goodridge, A. G. (1973). On the relationship between fatty acid synthesis and the total activities of acetyl coenzyme A carboxylase and fatty synthetase in the liver of prenatal and early postnatal chicks. J. Biol. Chem., 248, 1932e1938. Goodridge, A. G., & Ball, E. G. (1967). The effect of prolactin on lipogenesis in pigeon adipose tissue: in vitro studies. Biochemistry, 6, 2335e2343. Goodridge, A. G., Jenik, R. A., McDevitt, M. A., Morns, S. M., & Winberry, L. K. (1984). Malic enzyme and fatty acid synthase in uropygial gland and liver of embryonic and neonatal ducklings. Tissue-specific regulation of gene expression. Arch. Biochem. Biophys., 230, 82e92. Goodridge, A. G., Fantozzi, D. A., Klautky, S. A., Ma, X.-J., Roncero, C., & Salati, L. M. (1991). Nutritional and hormonal regulation of genes for lipogeneic enzymes. Proceedings of nutrition society, 50, 115e122. Goymann, W. (2009). Social modulation of androgens in male birds. Gen. Comp. Endocrinol., 163, 149e157. Gray, J. M., Yarian, D., & Ramenofsky, M. (1990). Corticosterone, foraging behavior, and metabolism in dark-eyed juncos, Junco hyemalis. Gen. Comp. Endocrinol., 79, 375e384. Guglielmo, C. G., Cerasale, D. J., & Eldermire, C. (2005). A field validation of plasma metabolite profiling to assess refueling performance of migratory birds. Physiol. Biochem. Zool., 78, 116e125. Guglielmo, C. G., Haunerland, N. H., Hochachka, P. W., & Williams, T. D. (2002). Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in migratory shorebird. Am. J. Physiol. Regulatory Integrative Comp. Physiol., 282, R1405eR1413. Gwinner, E. (1985). Circannual rhythms in bird migration: control of temporal patterns and interaction with photoperiod. In E. Gwinner (Ed.), Bird Migration (pp. 257e268). Berlin, Germany: Springer-Verlag. Gwinner, E., Hau, M., & Heigle, S. (1997). Melatonin: generation and modulation of avian circadian rhythms. Brain Res. Bull., 44, 439e444. Gwinner, E., Schwabl, H., & Schwabl-Benzinger, I. (1988). Effects of food deprivation on migratory restlessness and diurnal activity in the garden warbler, Sylvia borin. Oecologia, 77, 321e326. Gwinner, E., Zeman, M., Schwabl-Benzinger, I., Jenni-Eiermann, S., Jenni, L., & Schwabl, H. (1992). Corticosterone levels of passerine birds during migratory flight. Naturwissenschaften, 79, 276e278. Hahn, T. P., & MacDougall-Shackleton, S. A. (2008). Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response system of birds. Phil. Trans. R. Soc. B, 363, 267e286. Hahn, T. P., & Morton, M. L. (1995). Repetitive altitudinal migrations before breeding by mountain white-crowned sparrows, Zonotichia leucophrys oriantha. Am. Zool., 35, 86A. Hahn, T. P., Boswell, T., Wingfield, J. C., & Ball, G. F. (1997). Temporal flexibility in avian reproduction: patterns and mechanisms. Curr. Ornithol., 14, 39e80. Hahn, T. P., Sockman, W., Breuner, C. W., & Morton, M. L. (2004). Facultative altitudinal movements by mountain white-crowned sparrows (Zonotrichia leucophrys oriantha) in the Sierra Nevada. Auk, 121, 1269e1281.

Hormones and Reproduction of Vertebrates

Hahn, T. P., Wingfield, J. C., & Mullen, R. (1995). Endocrine bases of spatial and temporal opportunism in arctic-breeding birds. Ameri. Zool., 35, 259e273. Hamilton, S. L. (2002). A comparative analysis of the ecology and physiology of the Flammulated Owl (Otus flammeolus) and Northern Saw-whet Owl (Aegolius acadicus). (p. 90). Moscow, ID: M.S. Thesis. University of Idaho. Harris, M. O., & Turek, F. W. (1982). Photoperiodic control of the timing of testicular regresson in white-throated sparrows. Gen. Comp. Endocrinol., 46, 124e129. Hau, M. (2001). Timing of breeding in variable environments: tropical birds as model systems. Horm. Behav., 40, 281e290. Hau, M., Romero, L. M., Brawn, J. D., & Van’t Hof, T. J. (2002). Effect of polar day on plasma profiles of melatonin, testosterone, and estradiol in high-arctic Lapland longspurs. Gen. Comp. Endocrinol, 126, 101e112. Hazelwood, R. L. (1973). The avian endocrine pancreas. Am. Zool., 13, 699e709. Healy, S. D., Gwinner, E., & Krebs., J. R. (1996). Hippocampal volume in migratory and non-migratory warblers: effects of age and experience. Behav. Brain Res., 81, 61e68. Hegner, R. E., & Wingfield, J. C. (1987). Effects of experimental manipulation of testosterone levels on parental investment and breeding success in male house sparrows. Auk, 104, 462e469. Helm, B., Schwabl, I., & Gwinner, E. (2009). Circannual basis of geographically distinct bird schedules. J. Exp. Biol., 212, 1259e 1269. Herrick, E. H., Lockhart, C. H., Martin, E. P., & Nusser, W. L. (1955). Influence of sex hormones on blood cell counts and hemoglobin levels in fowls. Trans. Kansas Acad. Sci., 57, 483e492. Hnasko, R. M., & Buntin, J. D. (1993). Functional mapping of neural sites mediating prolactin-induced hyperphagia in doves. Brain Res., 623, 257e266. Holberton, R. L., & Able, K. P. (1992). Persistence of circannual cycles in a migratory bird held on constant dim light. J. Comp. Physiol. A., 171, 477e481. Holberton, R. L., & Wingfield, J. C. (2003). Modulating the corticosterone stress response: a mechanism for balancing risk and reproductive success in arctic breeding sparrows? Auk, 120, 1140e1150. Holberton, R. L., Boswell, T., & Hunter, M. J. (2008). Circulating prolactin and corticosterone concentrations during the development of migratory condition in the dark-eyed junco, Junco hyemalis. Gen. Comp. Endocrinol., 155, 641e649. Holberton, R. L., Parrish, J. D., & Wingfield, J. C. (1996). Modulation of adrenocortical stress response in neotropical migrants during autumn migration. Auk, 113, 558e564. Holberton, R. L., Wilson, C. W., Hunter, M. J., Cash, W. B., & Sims, C. G. (2007). The role of corticosterone in supporting migratory lipogenesis in the dark-eyed junco, Junco hyemalis: a model for central and peripheral regulation. Physiol. Biochem. Zool., 80, 125e137. Jacobs, J. D., & Wingfield, J. C. (2000). Endocrine control of life-cycles: a constraint on response to the environment? Condor, 102, 25e51. Jenni, L., & Jenni-Eiermann, S. (1998). Fuel supply and metabolic constraints in migrating birds. J. Avian Biol., 29, 521e528. John, J. L. (1994). The avian spleen: a neglected organ. Q. Rev. Biol., 69, 327e351.

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

Kern, M. D., DeGraw, W. A., & King, J. R. (1972). Effects of gonadal hormones on the blood composition of white-crowned sparrows. Gen. Comp. Endocrinol., 18, 43e53. Ketterson, E. D., Nolan, V., Jr., Wolf, L., & Zeigenfus, C. (1992). Testosterone and avian life histories, effects of experimentally elevated testosterone on behavior and correlates of fitness in the darkeyed junco (Junco hyemalis). Am. Natl., 140, 980e999. King, J. R. (1963). Autumnal migratory fat deposition in the whitecrowned sparrow. Proc. XIII Intern. Ornithol. Congr., 940e949. King, J. R. (1974). Notes on geographical variation and annual cycle in Patagonian populations of rufous-collared sparrow, Zonotrichia capensis. Ibis, 116, 74e83. King, J. R., & Farner, D. S. (1963). The relationship of fat deposition to zugunrhue and migration. Condor, 65, 200e223. King, J. R., & Mewaldt, L. R. (1981). Variation of body weight in gambel’s white-crowned sparrows in winter and spring: latitudinal and photoperiodic correlates. Auk, 98, 752e764. King, J. R., Follett, B. K., Farner, D. S., & Morton, M. L. (1966). Annual gonadal cycles and pituitary gonadotropins in Zonotrichia leucophrys gambelii. Condor, 68, 476e487. King, J. R., Mewaldt, R., & Farner, D. S. (1960). The duration of postnuptial metabolic refractoriness in the white-crowned sparrow. Auk, 77, 89e92. Klasing, K. C. (1998). Comparative avian nutrition. New York, NY: CAB International. Kochan, Z., Karbowksa, J., & Meissner, W. (2006). Leptin is synthesized in the liver and adipose tissue of the dunlin (Calidris alpina). Gen. Comp. Endocrinol., 148, 336e339. Kono, T., Nishida, M., Seki, Y., Sato, K., & Akiba, Y. (2005). Characterization of glucose tranporter (GLUT) gene expression in broiler chickens. Br. Poult. Sci., 46, 510e515. Kordonowy, L. L., McMurtry, J. P., & Williams, T. D. (2010). Variation in plasma leptin-like immunoreactivity in free-living European starlings (Sturnus vulgaris). Gen. Comp. Endocrinol., 166, 47e53. Kuenzel, W. J., Beck, M. M., & Teruyama, R. (1999). Neural sites and pathways regulating food intake in birds: a comparative analysis to mammalian systems. J. Exp. Zool., 283, 348e364. Kuenzel, W. J., & Helms, C. W. (1967). Obesity produced in a migratory bird by hypothalamic lesions. BioScience, 17, 395e396. Kuenzel, W. J., & Helms, C. W. (1970). Hyperphagia, polydipsia, and other effects of hypothalamic lesions in the white-throated sparrow. Zonotrichia albicollis. Condor, 72, 66e75. Kuenzel, W. J., & McMurtry, J. (1988). Neuropeptide Y: brain localization and central effects on plasma insulin levels in chicks. Physiol. Behav., 44, 669e678. Kuenzel, W. J., Douglass, L. W., & Davidson, B. A. (1987). Robust feeding following central administration of neuropeptide Y or peptide YY in chicks, Gallus domesticus. Peptides, 8, 823e838. Landys, M. M., Wingfield, J. C., & Ramenofsky, M. (2004b). Plasma corticosterone increases during migratory restlessness in the captive white-crowned sparrow, Zonotrichia leucophrys gambelii. Horm. Behav., 46, 574e581. Landys, M., Ramenofsky, M., & Wingfield, J. C. (2006). Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen. Comp. Endocrinol., 148, 132e149.

233

Landys, M. M., Ramenofsky, M., Guglielmo, C. G., & Wingfield, J. C. (2004a). The low-affinity glucocorticoid receptor regulates feeding and lipid breakdown in the migratory Gambel’s white-crowned sparrow, Zonotrichia lecuophyrs gambelii. J. Exp. Biol., 207, 143e154. Landys-Ciannelli, M. M., Ramenofsky, M., Piersma, T., Jukema, J., Wingfield, J. C., & Castricum Ringing Group. (2002). Baseline and stress-induced plasma corticosterone during long-distance migration in the bar-tailed godwit, Limosa lapponica. Physiol. Biochem. Zool., 75, 101e110. Levin, R., & Wingfield, J. C. (1992). Control of territorial aggression in tropical birds. Ornis. Scand., 23, 284e291. Lewis, R. A., & Farner, D. S. (1973). Temperature modulation of photoperiodically induced vernal phenomena in white-crowned sparrows (Zonotrichia leucophrys). Condor, 75, 279e286. Lofts, B., & Marshall, A. J. (1961). Zugunruhe activity in castrated bramblings Fringilla montifringilla. Ibis, 103a, 189e194. Lofts, B., & Murton, R. K. (1968). Photoperiodic and physiological adaptions regulating avian breeding cycles and their ecological significance. J. Zool. (Lond.), 155, 327e294. Lo¨hmus, M., Sundstro¨m, L. F., El Halawani, M., & Silverin, B. (2003). Leptin depresses food intake in great tits (Parus major). Gen. Comp. Endocrinol., 131, 57e61. Long, J., & Holberton, R. L. (2004). Corticosterone secretion, energetic conditions, and a test of the migration modulation hypothesis in the hermit thrush (Catharus guttatus), a short-distance migrant. Auk, 121, 1094e1102. Lundgren, B. O., & Kiessling, K.-H. (1985). Seasonal variation in catabolic enzyme activities in breast muscle of some migratory birds. Oecologica, 66, 468e471. Lundgren, B. O., & Kiessling, K.-H. (1988). Catabolic enzyme activity in the pectoralis muscle of migratory and nonmigratory goldcrests, great tits, and yellowhammers. Ornis Scan., 19, 190e194. Lynn, S. E., Breuner, C. W., & Wingfield, J. C. (2003). Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Horm. Behav., 43, 150e157. Lyons, J. E., Collazo, J. A., & Guglielmo, C. G. (2008). Plasma metabolites and migration physiology of semipalmated sandpipers: refueling performance at five latitudes. Oecolgia, 155(3), 417e427. MacDougall-Shackleton, S. A., & Hahn, T. P. (2007). Adaptation and evolution of photoperiod response systems in birds. J. Ornithol., 148, S219eS224. Marsh, R. (1981). Catabolic enzyme activities in relation to premigratory fattening and muscle hypertrophy in the gray catbird (Dumetella carolinensis). J. Comp. Physiol., 141, 417e423. Marsh, R. (1984). Adaptation of the gray catbird Dumetella carolinensis to long-distance migration; flight muscle hypertrophy associated with elevated body mass. Physiol. Zool., 57, 105e117. Marshall, A. J. (1959). Internal and environmental control of breeding. Ibis, 101, 456e478. Mattocks, P. W., Jr. (1976). The role of gonadal hormones in the regulation of the premigratory fat deposition in the white-crowned sparrow, Zonotrichia leucophrys gambelii. Seattle: MS Thesis University of Washington. Mayr, E. (1963). Animal species and evolution. Cambridge, MA: Harvard University Press. McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Horm. Behav., 43, 2e15.

234

McFarlan, J. T., Bonen, A., & Guglielmo, C. G. (2009). Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J. Exp. Biol., 212, 2934e2940. McNaughton, F. J., Dawson, A., & Goldsmith, A. R. (1992). Puberty in birds: the reproductive system of starlings does not respond to short days until birds are fully grown. J. Endocrinol., 132, 411e417. McWilliams, S. R., Guglielmo, C., Pierce, B. J., & Klaassen, M. (2004). Flying, fasting and feeding in birds during migration: a nutritional and physiological ecology perspective. J. Avian Biol., 35, 377e393. Meddle, S. L., Bush, S., Sharp, P. J., Millar, R. P., & Wingfield, J. C. (2006). Hypothalamic Pro-GnRH-GAP, GnRH-I and GNRH-II during the onset of photorefractorniss in the white-crowned sparrow, Zonotrichia leucophrys gambelii. J. Neuroendocrinol., 18, 217e226. Medh, R. D., & Thompson, E. B. (2000). Hormonal regulation of physiological cell turnover and apoptosis. Cell Tiss. Res., 301, 101e124. Meier, A. H., & Farner, D. S. (1964). A possible basis for premigratory fattening in the white-crowned sparrow, ZL (Nuttall). Gen. Comp. Endocrinol., 4, 584e595. Mewaldt, L., & King, J. R. (1977). The annual cycle of white-crowned sparrows (Zonotrichia leucophrys nuttalli) in coastal California. Condor, 79, 445e455. Mizrahi, D. S., Holberton, R. L., & Gauthreaux, S. A., Jr. (2001). Patterns of corticosterone secretion in migrating semipalmated sandpipers at a major spring stopover site. Auk, 118, 79e91. Moore, I. T., Perfito, N., Wada, H., Sperry, T. S., & Wingfield, J. C. (2002). Latitudinal variation in plasma testosterone levels in birds of the genus Zonotrichia. Gen. Comp. Endocrinol., 129, 13e19. Moore, M. C., Donham, R. S., & Farner, D. S. (1982). Physiological preparation for autumnal migration in white-crowned sparrows. Condor, 84, 410e419. Morton, M. L. (1992). Control of postnuptial molt in the mountain whitecrowned sparrow: a perspective from field data. Ornis Scand., 23, 322e327. Morton, M. L. (2002). The mountain white-crowned sparrow: migration and reproduction at high altitude. Studies in Avian Biol., 24, 236. Morton, M. L., & Mewaldt, L. R. (1962). Some effects of castration on a migratory sparrow (Zonotrichia atricapilla). Physiol. Zool., 35, 237e247. Nakao, N., Ono, H., & Yoshimura, T. (2008). Thyroid hormones and seasonal reproductive neuroendocrine interactions. Reproduction, 136, 1e8. Nakazato, M., Murakami, N., Date, Y., Kojima, M., Matsuo, H., Kangawa, K., et al. (2001). A role for ghrelin in the central regulation of feeding. Nature, 409, 194e198. Newton, I. (2008). The migration ecology of birds. Oxford, UK: Academic Press. Nicholls, T. J., Goldsmith, A. R., & Dawson, A. (1988). Photorefractoriness in birds and comparison with mammals. Physiol. Rev., 68, 133e176. Nilsson, A. L. K., & Sandell, M. (2009). Stress hormone dynamicsdan adaptation to migration? Biol. Lett., 5, 480e483. O’Reilly, K. M., & Wingfield, J. C. (1995). Spring and autumn migration in arctic shorebirds: same distance, different strategies. Am. Zool., 35, 222e233. Oakeson, B. B. (1953). Cyclic changes in liver and spleen weights in migratory white-crowned sparrows. Condor, 55, 3e16. Oakeson, B. B. (1956). Liver and spleen weight cycles in non-migratory white-crowned sparrows. Condor, 58, 45e50.

Hormones and Reproduction of Vertebrates

Oksche, A., & Farner, D. S. (1974). Neurohistological studies on the hypothalamoehypophysial system of Zontorichia leucophrys gambelii (Aves, Passiformes). Ergebnisse der Anat. 48; (Fasc. 4). BerlinHeidelberg-New York: Springer. Pant, K., & Chandola-Saklani, A. (1993). A role for thyroid hormones in the development of premigratory disposition in redheaded bunting, Emberiza bruniceps. J. Comp. Physiol. B, 163, 389e394. Parrish, J. D. (1997). Patterns of frugivory and energetic condition in neararctic landbirds during autumn migration. Condor, 99, 681e697. Parry, D. M., Goldsmith, A. R., Millar, R. P., & Glennie, L. M. (1997). Immunocytochemical localization of GnRH precursor in the hypothalamus of European starlings during sexual maturation and photorefractoriness. J. Neuroendocrinol., 9, 235e243. Perdeck, A. C. (1967). Orientation of starlings after displacement to Spain. Ardea, 55, 194e202. Perdeck, A. C. (1974). An experiment on the orientation of juvenile starlings during spring migration. Ardea, 62, 190e195. Perfito, N., Bentley, G. E., Zann, R. A., & Hau, M. (2006). Endocrine and neuroendocrine regulation of reproductive timing in an opportunistic breeder. J. Ornithol., 147m (Supp. 1), E227. Perrins, C. M. (1970). The timing of birds’ breeding seasons. Ibis, 112, 242e255. Piersma, T. (1988). Breast muscle atrophy and constraints on foraging during flightless periods of wing moulting great crested grebes. Ardea, 76, 96e106. Piersma, T. (1998). Phenotypic flexibility during migration: optimization of organ size contingent on the risks and rewards of fueling and flight? J Avian Biology, 29, 511e520. Piersma, T. (2002). When a year takes 18 months: evidence for a strong circannual clock in a shorebird. Naturwissenschaften, 89, 278e279. Piersma, T., & Gill, R. E., Jr. (1998). Guts don’t fly: small digestive organs in obsess bar-tailed godwits. Condor, 96, 363e370. Piersma, T., Brugge, M., Spaans, B., & Battley, P. F. (2008). Endogenous circannual rhythmicity in body mass, molt, and plumage of great knots (Calidris tenuirostris). Auk, 125, 140e148. Piersma, T., Everaarts, J. M., & Jukema, J. (1996). Build-up of red blood cells in refuelling bar-tailed godwits in relation to individual migratory quality. Condor, 98, 363e370. Piersma, T., Reneerkens, J., & Ramenofsky, M. (2000). Baseline corticosterone peaks in shorebirds with maximal energy stores for migration: a general preparatory mechanism for rapid behavioral and metabolic transitions? Gen. Comp. Endocrinol., 120, 118e126. Pradhan, D. S., Newman, A. E. M., Wacker, D. W., Wingfield, J. C., Schlinger, B. A., & Soma, K. K. (2010). Aggressive interactions rapidly increases androgen synthesis in the brain during the nonbreeding season. Horm. Behav., 57, 381e389. Pravosudov, V. V., Kitaysky, A. S., & Omanska, A. (2006). The relationship between migratory behaviour, memory and the hippocampus: an intraspecifc comparison. Proc. R. Soc. B, 273, 2641e2649. Ramenofsky, M. (1990). Fat storage and fat metabolism in relation to migration. In E. Gwinner (Ed.), Bird Migration (pp. 214e231). Berlin, Germany: Springer-Verlag. Ramenofsky, M., & Boswell, T. (1994). Regulation of feeding cycles during migration: A possible role for insulin. Vienna, Austria: XXI Int’l Ornithological Congress. Ramenofsky, M., & Wingfield, J. C. (2006). Behavioral and physiological conflicts in migrants: the transition between migration and breeding. J. Ornithol., 147, 135e145.

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

Ramenofsky, M., & Wingfield, J. C. (2007). Regulation of migration. Bioscience, 57, 135e143. Ramenofsky, M., Piersma, T., & Jukema, J. (1995). Plasma corticosterone in bar-tailed godwits at a major stop-over site during spring migration. Condor, 97, 580e584. Ramenofsky, M., Savard, R., & Greenwood, M. R. C. (1999). Seasonal and diel transitions in physiology and behavior in migratory darkeyed juncos. Comp. Biochem. Physiol A, 122, 385e397. Ramenofsky, M., Moffat, J., Guglielmo, C. G., & Bentley, G. (2008). Corticosterone and migratory behavior of captive white-crowned sparrows. In S. Morris, & A. Vosloo (Eds.), Molecules to migration: The pressures of life (pp. 575e582). Bologna, Italy: Proceedings ICA-CPB Meeting, Maasai Mara, Kenya, Medimond Publishing Co. Ramenofsky, M., Agatsuma, R., Barga, M., Cameron, R., Harm, J., Landys, M., et al. (2003). Migratory behavior: new insights from captive studies. In P. Berhold, E. Gwinner, & E. Sonnenschein (Eds.), Avian Migration (pp. 97e112). Berlin, Germany: Springer. Rand, A. L. (1948). Glaciation, an isolating factor in speciation. Evolution, 2, 314e321. Remage-Healey, L., & Romero, L. M. (2001). Corticosterone and insulin interact to regulate glucose and triglyceride levels during stress in a bird. Am. J. Physiol., 281, R994eR1003. Reneerkens, J., Morrison, R. I. G., Ramenofsky, M., Piersma, T., & Wingfield, J. C. (2002). Baseline and stress-induced levels of corticosterone during different life cycle substages in a shorebird on the high arctic breeding grounds. Physiol. Biochem. Zool., 75, 200e208. Richardson, R. D., Boswell, T., Raffety, B. D., Seeley, R. J., Wingfield, J. C., & Woods, S. C. (1995). NPY increases food intake in white-crowned sparrows: effect in short and long photoperiods. Am. J. Physiol., 268, RI1418e1422. Robinson, J. E., & Follett, B. K. (1982). Photoperiodism in Japanese quaildthe termination of seasonal breeding by photorefractoriness. Proc. Roy. Soc. Lond. B, 215, 95e116. Romero, L. M. (2002). Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen. Comp. Endocrinol., 128, 1e24. Romero, L. M., & Reed, J. M. (2005). Collecting baseline corticosterone in the field: is under 3 min good enough? Comp. Biochem. Physiol A, 140, 73e39. Romero, L. M., & Romero, R. C. (2002). Corticosterone responses in wild birds: the importance of rapid initial sampling. Condor, 104, 129e135. Romero, L. M., Ramenofsky, M., & Wingfield, J. C. (1997). Season and migration alters the corticosterone response to capture and handling in an arctic migrant, the white-crowned sparrow (Zonotrichia leucophrys gambelii). Comp. Biochem. Physiol., 116C, 171e177. Rosebrough, R. W., & McMurtry, J. P. (1993). Energy repletion and lipidmetabolism during compensatory gain in broiler-chickens. Growth Devel. Aging, 57, 73e83. Rowan, W. (1925). Relation of light to bird migration and development changes. Nature, 115, 494e495. Runfeldt, S., & Wingfield, J. C. (1985). Experimentally prolonged sexual activity in female sparrows delays termination of reproductive activity in their untreated mates. Anim. Behav., 33, 403e410. Saldana, C. J., Schlinger, B. A., & Clayton, N. S. (2000). Rapid effects of corticosterone on cache recovery in mountain chickadees (Parus gambeli). Horm. Behav., 37, 109e115.

235

Salewski, V., & Bruderer, B. (2007). The evolution of bird migrationd a synthesis. Naturwissenschaften, 94, 268e279. Schleussner, G., Dittami, J. P., & Gwinner, E. (1985). Testosterone implants affect molt in male European starlings, Sturnus vulgaris. Physiol. Zool., 58, 597e604. Schwabl, H., & Farner, D. S. (1989a). Dependency on testosterone of photoperiodically-induced vernal fat deposition in female whitecrowned sparrows. Condor, 91, 108e112. Schwabl, H., & Farner, D. S. (1989b). Endocrine and environmental control of vernal migration in male white-crowned sparrows, Zonotrichia l. gambelii. Physiol. Zool., 62, 1e10. Schwabl, H., Bairlein, F., & Gwinner, E. (1991). Basal and stress-induced corticosterone levels of garden warblers, Sylvia borin, during migration. J. Comp. Physiol. B, 161, 576e580. Schwabl, H., Schwabl-Benzinger, I., Goldsmith, A. R., & Farner, D. S. (1988). Effects of ovariectomy on long-day premigratory fat deposition, plasma levels of luteinizing hormone and prolactin and molt in white-crowned sparrows, Zonotrichia leucophrys gambelii. Gen. Comp. Endocrinol., 71, 398e405. Schwilch, R., Grattarola, A., Spina, F., & Jenni, L. (2002). Protein loss during long-distance migratory flight in passerine birds: adaptation or constraint. J. Exp. Biol., 205, 687e695. Selander, R. K. (1965). Avian speciation in the Quaternary. In H. E. Wright, Jr., & D. G. Grey (Eds.), The Quaternary of the United States. Princeton, NJ: Princeton U. Press. Semsarian, C., Wu, M.-J., Marcinec, T., Yeoh, T., Allen, D. G., Harvey, R. P., et al. (1999). Skeletal muscle hypertrophy is mediated by a Caþþ -dependent calcineurin signalling pathway. Nature, 400, 576e581. Sharp, P. J., Dunn, I. C., Waddington, D., & Boswell, T. (2008). Chicken leptin. Gen. Comp. Endocrinol., 158, 2e4. Silverin, B. (1990). Testosterone and corticosterone and their relation to territorial and parental behavior in the pied flycatcher. In J. Balthazart (Ed.), Hormones, brain, and behavior in vertebrates. 2, (Vol. 9) (pp. 129e142). Basel, Switzerland: Karger. Silverin, B., Wingfield, J., Stokkan, K.-A., Massa, R., Ja¨rvinen, A., ˚ , et al. (2008). Ambient temperature effects on Andersson, N-A photo induced gonadal cycles and hormonal secretion patterns in great tits from three different breeding latitudes. Horm. Behav., 54, 60e68. Simon, J. (1989). Chicken as a useful species for the comprehension of insulin action. Crit. Re. Poult. Bio., 2, 121e148. Small, T. V., Sharp, P. J., Bentley, G., Millar., R. P., Mura, E., & Deviche, P. (2008). Photoperiod-independent hypothalamic regulation of luteinzing hormone secretion in a free-living Sonoran desert bird, the rufous-winged sparrow (Aimpohila carpalis). Brain Behav. Evol., 71, 127e142. Smith, C. J. V., & Bright-Taylor, B. (1974). Does a glucostatic mechanism for food intake control exist in chickens? Poult. Sci., 53, 1720e1724. Stetson, M. (1971). Neuroendocrine control of photoperiodically induced fat deposition in white-crowned sparrows. J. Exp. Zool., 176, 409e414. Stetson, M., & Erickson, J. E. (1972). Hormonal control of photoperiodically induced fat deposition in white-crowned sparrows. Gen. Comp. Endocrinol., 19, 355e362. Swanson, D. L., & Liknes, E. T. (2006). A comparative analysis of thermogenic capacity and cold tolerance in small birds. J. Exp. Biol., 209, 466e474.

236

Sweazea, K. L., & Braun, E. J. (2006). Glucose transporter (GLUT) expression in English sparrows (Passer domesticus). Comp. Biochem. Phyiol. B, 144, 263e270. Terrill, S. B. (1990). Ecophysiological aspects of movements by migrants in the wintering quarters. In E. Gwinner (Ed.), Bird Migration (pp. 130e143). Berlin, Germany: Springer-Verlag. Terrill, S. B., & Able, K. P. (1988). Bird migration terminology. Auk, 105, 205e206. Terrill, S. B., & Ohmart, R. D. (1984). Facultative extension of fall migration by yellow-rumped warblers (Dendroica coronata). Auk, 101, 427e438. Thapliyal, J. P., Lal, P., Pati, A. K., & Gupta, B. B. P. (1983). Thyroid and gonad in the oxidative metabolism, erythropoiesis, and light response of the migratory red-headed bunting, Emberiza bruniceps. Gen. Comp. Endocrinol., 512, 444e452. Thapliyal, J. P., Pati, A. K., & Gupta, B. B. P. (1982). The role of erythropoietin, testosterone, and L-thyroxine in the tissue oxygen consumption and erthrypoiesis of spotted munia, Lonchura punctuala. Gen. Comp. Endocrinol., 48, 84e88. Thompson, J. S. (1998). Somatostatin analogue predisposes enterocytes to apoptosis. J. Gasterointest. Surg., 2, 167e173. Thorup, K., Bisson, I.-A., Bowlin, M. S., Holland, R. A., Wingfield, J. C., Ramenofsky, M., et al. (2007). Evidence for a navigational map stretching across the continental U.S. in a migratory songbird. Proc. Nat. Acad. Sci., 104, 18115e18119. Totzke, U., Hu¨binger, A., & Bairlein, F. (1997). A role for pancreatic hormones in the regulation of autumnal fat deposition of the garden warbler, Sylvia borin? Gen. Comp. Endocrinol., 107, 166e171. Tsipoura, N., Scanes, C. G., & Burger, J. (1999). Corticosterone and growth hormone levels in shorebirds during spring and fall migration stopover. J. Exp. Zool., 284, 645e651. Tsutsui, K., Saigoh, E., Yin, H., Ubuka, T., Chowdhury, V. S., Osugi, T., et al. (2009). A new key neurohomorne controlling reproduction, gonadotrophin-inhibitory hormone in birds: discovery, progress and prospects. J. Neuroendocrinol., 21, 271e275. Tsutsui, K., & Yamazaki, T. (1995). Avian neurosteroids: 1. Pregnenolone biosynthesis in the quail brain. Brain Res., 678, 1e9. Turner, A. (2009). Climate change: a swallow’s eye view. Brit. Birds, 102, 3e16. Ukena, K., Honda, Y., Inai, Y., Kohchi, C., Lea, R., & Tsutsui, K. (1999). Expression and activity of 3b-hydroxysteroid dehydrogenase/6564-isomerase in different regions of the avian brain. Brain Res., 818, 536e542. Uldry, M., & Thorens, B. (2004). The SLC2 family of facilitated hexose and polyol transporters. Pflugers Arch. Eur. J. Physiol., 447, 480e489. Vleck, C. M., & Wingfield, J. C. (1980). No temporal synergism of prolactin and corticosterone influencing reproduction in whitecrowned sparrows. Am. Zool., 20, 899. Weise, G. (1967). Castration and spring migration in the white-throated sparrow. Condor, 69, 49e68. Wickramasinghe, S. N., Shiels, S., & Wickramasinghe, P. S. (1994). Immunoreactive erythropoietin in teleosts, amphibians, reptiles and birds. Ann. NY Acad. Sci., 718, 366e370. Wilcove, D. S. (2008). No way home: the decline of the world’s great animal migrations. Washington, DC: Island Press. Williams, T. C., & Webb, T. (1996). Neotropical bird migration during the ice ages: orientation and ecology. Auk, 113, 105e118.

Hormones and Reproduction of Vertebrates

Wingfield, J. C. (1993). Control of testicular cycles in the song sparrow, Melospiza melodia: interactions of photoperiod and an endogenous program? Gen. Comp. Endocrinol., 92, 388e401. Wingfield, J. C. (2004). Allostatic load and life cycles: implications for neuroendocrine mechanisms. In J. Schulkin (Ed.), Allostasis, homeostasis and the cost of physiological adaptations (pp. 302e342). Cambridge, UK: Cambridge University Press. Wingfield, J. C. (2008a). Comparative endocrinology, environment and global change. Gen. Comp. Endocrinol., 157, 207e216. Wingfield, J. C. (2008b). Organization of vertebrate annual cycles; implications for control mechanisms. Phil. Trans. R. Soc. B, 363, 425e441. Wingfield, J. C., & Farner, D. S. (1978a). The annual cycle of plasma irLH and steroids hormones in feral populations of the white-crowned sparrow, Zonotrichia leucophrys gambelii. Biol. Reprod., 19, 1046e1056. Wingfield, J. C., & Farner, D. S. (1978b). The endocrinology of a natural breeding population of the white-crowned sparrow (Zonotrichia leucophrys pugetensis). Physiol. Zool., 51, 188e205. Wingfield, J. C., & Farner, D. S. (1980). Control of seasonal reproduction in temperate-zoned birds. Prog. Repro. Biol., 5, 62e101. Wingfield, J. C., & Farner, D. S. (1993). Endocrinology of reproduction in wild species. In D. S. Farner, J. R. King, & K. C. Parkes (Eds.), Avian Biology, vol 9 (pp. 164e327). Wingfield, J. C., & Hunt, K. E. (2002). Arctic spring: hormoneebehavior interactions in a severe environment. Comp. Biochem. Physiol., B132, 275e286. Wingfield, J. C., & Jacobs, J. D. (1999). The interplay of innate and experiental factors regulating the life history cycle of birds. In N. Adams, & R. Slotow (Eds.), Proceedings of the 22nd International Ornithological Congress (pp. 2417e2443). Johannesburg, South Africa: Bird Life of South Africa. Wingfield, J. C., & Ramenofsky, M. (1999). Hormones and behavioral ecology of stress. In P. H. E. Balm (Ed.), Stress Phyisology of Animals (pp. 1e51). Sheffield, UK: Sheffield University Press. Wingfield, J. C., & Romero, L. M. (2001). Adrenocortical responses to stress and their modulation in free-living vertebrates. In B. S. McEwen (Ed.), Handbook of physiology, section 7, The endocrine system, volume 4: Coping with the Environment: Neural and endocrine mechanisms (pp. 211e236). Oxford, UK: Oxford University Press. Wingfield, J. C., & Sapolsky, R. M. (2003). Reproduction and resistance to stress: when and how? J. Neuroendocrinol., 15, 711e724. Wingfield, J. C., & Silverin, B. (2009). Ecophysiological studies of hormoneebehavior relations in birds. In D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach, & R. T. Rubin (Eds.) (2nd ed.).Hormones, Brain and Behavior, Vol. 2 (pp. 817e854) New York, NY: Academic Press. Wingfield, J. C., & Soma, K. K. (2002). Spring and autumn territoriality: same behavior, different mechanisms? Integrat. Comp. Biol., 42, 11e20. Wingfield, J. C., Breuner, C. W., & Jacobs, J. (1997). Corticosterone and behavioral responses to unpredictable events. In S. Harvey, & R. J. Etches (Eds.), Perspectives in Avian Endocrinology (pp. 267e278). Bristol, UK: Journal of Endocrinology Press. Wingfield, J. C., Hegner, R. E., & Lewis, D. (1991). Circulating levels of luteinizing hormone and steroid hormones in relation to social status

Chapter | 8

Hormones in Migration and Reproductive Cycles of Birds

in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. J. Zool. Lond., 225, 43e58. Wingfield, J. C., Lynn, S., & Soma, K. K. (2001). Avoiding the ‘costs’ of testosterone: ecological bases of hormoneebehavior interactions. Brain Behav. Evol., 57, 239e251. Wingfield, J. C., Schwabl, H., & Mattocks, P. W., Jr. (1990). Endocrine mechanisms of migration. In E. Gwinner (Ed.), Bird Migration (pp. 232e256). Berlin, Germany: Springer-Verlag. Wingfield, J. C., Smith, J. P., & Farner, D. S. (1980). Changes in plasma levels of luteinizing hormone, steroid, and thyroid hormones during the postfledgling development of white-crowned sparrows, Zonotrichia leucophyrs. Gen. Comp. Endocrinol., 41, 372e377. Wingfield, J. C., Hahn, T. P., Wada, M., & Schoech, S. J. (1997). Effects of day length and temperature on gonadal development, body mass, and fat depots in white-crowned sparrows, Zonotrichia leucophrys pugetensis. Gen. Comp. Endocrinol., 107, 44e62. Wingfield, J. C., Hegner, R. E., Dufty, A. M., Jr., & Ball, G. F. (1990). The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist, 136, 829e846. Wingfield, J. C., Hahn, T. P., Wada, M., Astheimer, L. B., & Schoech, S. (1996). Interrelationship of day length and temperature on the control of gonadal development, body mass, and fat score in white-crowned sparrows, Zonotrichia leucophrys gambelii. Gen. Comp. Endocrinol., 101, 242e255. Wingfield, J. C., Hahn, T. P., Wada, M., Astheimer, L. B., & Schoech, S. (1997). Effects of day length and temperature on gonadal development, body mass, and fat depots in white-crowned sparows, Zonotrichia leucophrys gambelii. Gen. Comp. Endocrinol., 107, 44e62. Wingfield, J. C., Ball, G. F., Dufty, A. M., Jr., Hegner, R. E., & Ramenofsky, M. (1987). Testosterone and aggression in birds: Tests of the ‘challenge hypothesis’. American Scientist, 75, 602e608. Wingfield, J. C., Jacobs, J. D., Tramontin, A. D., Perfito, N., Meddle, S., Maney, D. L., et al. (1999). Toward an ecological basis of hormonee behavior interactions in reproduction of birds. In K. Wallen, & J. Schneider (Eds.), Reproduction in Context (pp. 85e128). Cambridge, MA: M.I.T. Press.

237

Wingfield, J. C., Owen-Ashley, N. T., Benowitz-Fredericks, Z. M., Lynn, S. E., Hahn, T. P., Wada, H., et al. (2004). Arctic spring: the arrival biology of migrant birds. Acta Zool. Sinica, 50, 948e960. Wolfson, A. (1952). The occurrence and regulation of the refractory period in the gonadal and fat cycles of the junco. J. Exp. Zool., 121, 311e325. Wolfson, A. (1958). Regulation of refractory period in the photoperiodic responses of the white-throated sparrow. J. Exp. Zool., 139, 349e379. Yokoyama, K. (1976a). Hypothalamic and hormonal control of photoperiodically induced vernal functions in the white-crowned sparrow, Zonotrichia leucophrys gambelii. I. The effects of hypothalamic lesions and exogenous hormones. Cell Tissue Res., 174, 391e416. Yokoyama, K. (1976b). Hypothalamic and hormonal control of photoperiodically induced vernal functions in the white-crowned sparrow, Zonotrichia leucophrys gambelii. II. The effects of hypothalamic implantation of testosterone proprionate. Cell Tissue Res., 176, 91e108. Yoshimura, T. (2006). Molecular mechanisms of the photoperiodic response of gonads in birds and mammals. Comp. Biochem. Physiol. A, 144, 345e350. Youngren, O. M., Chaiseha, Y., & El Halawani, M. E. (1998). Regulation of prolactin secretion by dopamine and vasoactive intestinal peptide at the level of the pituitary in the turkey. Neuroendocrinology, 68, 319e325. Yuan, L., Lin, H., Jiang, K. J., Jiao, H. C., & Song, Z. G. (2008). Corticosterone administration and high-energy feed results in enhanced fat accumulation and insulin resistance in broiler chickens. Brit. Poult. Sci., 49, 487e495. Zink, R. M. (1982). Patterns of genic and morphologic variation among sparrows in the genera Zontotrichia, Melospiza, Junco and Passerella. Auk, 99, 632e649. Zink, R. M., & Blackwell, R. C. (1996). Patterns of allozyme, mitochondrial DNA, and morphometric variation in four sparrow genera. Auk, 113, 59e67. Zink, R. M., Dittman, D. L., & Rootes, W. L. (1991). Mitochondrial DNA variation and the phylogeny of Zonotrichia. Auk, 108, 578e584.

Chapter 9

Endocrine Disruption of Reproduction in Birds Mary Ann Ottinger*, Karen Dean, Moira McKernan and Michael J. Quinn, Jr. University of Maryland, College Park, MD, USA, y American Bird Conservancy, Washington, DC, USA, ** US Army Center for Health Promotion and Preventive Medicine, Aberdeen Proving Ground, MD, USA *

SUMMARY Endocrine-disrupting chemicals (EDCs), which mimic endogenous hormones, are creating an emerging issue for avian species. These chemicals include pesticides, herbicides, endocrine-active phytochemicals (EAPs), industrial products, and byproducts of technology that have structural and functional properties that enable them to interact with physiological systems, including the reproductive, thyroid, metabolic, and immune axes. Characterizing the effects of these varied EDCs and establishing reliable indices of exposure that relate to potential risk to avian populations is challenging. The complexity of assessing EDC effects in birds is exacerbated by unique aspects of avian biology including sexual differentiation, lifetime reproductive strategies, migration with varied exposure, mechanisms of actions, and diverse lifespans of birds. Further, exposure is often to a mixture of chemicals with differential species sensitivity at various stages of the lifecycle. It is critical to understand the bioavailability of these compounds in the environment. This chapter considers these issues, including probable mechanisms of action, affected species, lifetime sensitivity to exposure, and potential impacts on avian populations.

1. INTRODUCTION The widespread use of chemicals for agriculture, industry, medicine, recreation and residential purposes has dramatically increased the chemical exposure of vertebrates. Moreover, our understanding of the potential impacts of environmental chemicals that have endocrinedisrupting effects has greatly increased since our last review of this area (Figure 9.1) (Ottinger & Vom Saal, 2001). Information regarding potential adverse effects on wildlife is becoming available as data emerge regarding unexpected coincident effects of these chemicals on biological systems. Many of these chemicals, especially certain pesticides, herbicides, and endocrine-active phytochemicals (EAPs) (see Vajda & Norris, 2005), have demonstrated

Hormones and Reproduction of Vertebrates, Volume 4dBirds Copyright Ó 2011 Elsevier Inc. All rights reserved.

biological actions on the endocrine system with subsequent effects on reproductive, thyroidal, metabolic, and immunological functions in vertebrates. These endocrine-disrupting chemicals (EDCs) act on hormone-sensitive neural systems, organs, and tissues, often with deleterious toxicological effects that ultimately affect individual fitness and health as a result of damage at the genetic, molecular, cellular, and system levels. There has been increased attention given to short- and long-term effects of early exposure to EDCs, especially in terms of lifetime impacts. Finally, it is essential that a multidisciplinary approach be used to ascertain the potential effects of EDCs in birds because this is a multifaceted problem involving chemistry, biochemistry, industrial engineering, neurobiology, genetics, environmental sciences, and a host of other disciplines. Investigations of EDCs have been conducted in a variety of animal models, including invertebrates, amphibians, reptiles, fishes, birds, and mammals. Understanding the effects of EDCs requires an understanding of the roles of hormones at specific stages in the animal lifecycle, with special consideration of stages at which animals are sensitive to exposure to these chemicals. While all vertebrate classes occupy a range of ecological niches that predispose them to particular levels and types of exposure, birds are amongst some of the most challenging for study. Not only do they have a wide range of feeding strategies, reproductive patterns, and longevity, but many species are migratory and traverse continents twice per year. One aspect of avian life history that can influence the degree or pattern of EDC effects is the extent of prehatch development. Precocial species, such as quail, appear to be most sensitive to EDC effects during embryonic development. Conversely, passerines and other altricial birds may remain moderately responsive to the effects of EDCs throughout their lifetime due to the plasticity of the song system and other associated neural systems. Several avian model species have been routinely used for toxicological 239

240

testing including domestic chickens (Gallus gallus) and mallard ducks (Anas platyrhynchos). Although the Japanese quail (Coturnix japonica) is a laboratory species, its reproductive strategy is similar to that of many free-ranging species. Avian laboratory models for altricial birds include finches, and most of the other information on passerines has been collected in field studies. As such, the varied reproductive strategies of birds present a challenge as we identify reliable indices of exposure to EDCs and risk assessment models for avian populations.

2. IMPACTS OF ENDOCRINE-DISRUPTING CHEMICALS (EDCs) There is a large body of literature in ecotoxicology; the reader is referred to many excellent texts (see Hoffman, Rattner, Burton, & Cairns, 2003). More recently, EDCs have emerged as a potential issue for birds and mammals alike. The effects of EDCs can be subtle, and generally exposure occurs at nonlethal doses for domestic species, wildlife, and humans, with the exception of occupational exposure or industrial accidents. This is generally true, except for the rare cases in which spills or accidents have resulted in high levels of exposure; EDC exposures in field birds often have been assumed to be innocuous. Presently, it is estimated that there are thousands of environmental chemicals that have been introduced into the environment since the 1930s. The sheer number of these potential EDCs has made rapid screening of possible problem chemicals essential. Some EDCs are highly persistent industrial products, e.g., polychlorinated biphenyls (PCBs) and organochlorine pesticides, which can persist for decades or centuries; flame retardants; and other chemicals produced for specific purposes and that may have endocrine-disrupting effects. Interestingly, some natural EDCs, including phytoestrogens produced by plants, provide key environmental signals that synchronize reproduction in rodent populations (Berger, Negus, & Rowsemitt, 1987). However, these ‘natural’ exposures have occurred gradually over time with rodents and other species, providing the opportunity to adapt and adjust to changing levels in their diets. Conversely, the rapid appearance of environmental chemicals and the changing panorama of exposures to wildlife make it imperative to understand the long-term impacts of these endocrine-active compounds, which are also termed endocrine-active phytochemicals (EAPs), on individuals and populations. The capacity of EDCs to bioaccumulate within the food chain, coincident with the lipophilic nature of many of these compounds, means that top predators, such as fisheating birds and raptors, are potentially exposed to very high concentrations (National Research Council (NRC),

Hormones and Reproduction of Vertebrates

1999). The tendency toward high lipid solubility and persistence in the body fat further exacerbates potential adverse effects. This means that avian females will deposit some of their body burden into each egg as they produce the lipid components of yolk (Ottinger et al., 2005). This deposition into an egg parallels the chemical deposition into the fetus or neonate by a mammalian female via the umbilicus and during lactation. Thus, the avian embryo and young birds also are exposed to EDCs and/or their bioactive metabolites. The adverse health effects of exposure to EDCs during embryonic development, a particularly vulnerable stage of the vertebrate lifecycle, appear to be universally deleterious across vertebrates. One of the first recognized fetal effects of EDCs was associated with diethylstilbestrol (DES) treatments given to pregnant women, which resulted in adverse health effects in their children, particularly daughters, often emerging many years later (Bern, 1992a; 1992b). Developmental EDC exposure of any kind, whether from drugs used in therapy or inadvertently from environmental chemicals, has the potential to produce longlasting abnormalities in the organization of multiple endocrine and physiological systems, resulting later in functional impairment of these systems at the time of activation. In other words, although critical exposure to estrogenic chemicals may occur in the embryo, the consequences of such exposure often have delayed impacts (Gray & Kelce, 1996; Colborn, Vom Saal, & Soto, 1993; Gray, Ostby, Wolf, Lambright, & Kelce, 1998; Vom Saal & Timms, 1999). The effect of embryonic DES exposure demonstrated that estrogenic chemicals can profoundly disturb the differentiation of estrogen target organs (see Colborn et al., 1993). More recent data on androgen- and thyroid-active compounds have revealed similar deleterious potential for long-term impacts from these compounds via different mechanisms of action (Custer et al., 1999; Chen, Sible, & McNabb, 2008; Zoeller, 2008). Understanding the varied consequences of EDC exposure will inform outcomes of exposure unique to EDCs, especially regarding developmental exposures, potential delayed effects, and possibly disease. Therefore, it is critical to consider both long-term effects of early exposure and more ephemeral effects of short-term adult exposures. Potential effects of EDCs on mammals, birds, and other taxa have been documented in many ways, including epidemiological studies, controlled laboratory studies, and wildlife surveys (NRC, 1999). Initial evidence was primarily taken from observations of deleterious effects on fertility, sperm production, and reproductive system cancers, especially those associated with exposure to the insecticide dichlorodiphenyltrichloroethane (DDT) (Bern, 1992; Colborn & Clement, 1992; Colborn et al., 1993; Kavlock et al., 1996; Longnecker,

Chapter | 9

241

Endocrine Disruption of Reproduction in Birds

Rogan, & Lucier, 1997). A negative impact of EDC exposure at the level of the ecosystem is evidenced in a number of wildlife species (Fox, Gilman, Peakall, & Anderka, 1978; Fox, 1992; Colborn et al., 1993; Fry, 1995; Grasman, Scanlon, & Fox, 1998; Grasman & Fox, 2001). These studies all suggest that developmental stages of the lifecycle are particularly vulnerable to EDCs (Colborn et al., 1993; Kavlock et al., 1996). Many other types of deleterious effect have been reported to occur as a result of developmental exposure to EDCs separately and in combination with other contaminants; impacts include reproductive impairment, reduced fertility and hatchability, decreased survival of offspring, and neurobehavioral effects in wildlife (Bosveld & Van den Berg, 1994; Conley et al., 1997; Bishop, Mahony, Trudeau, & Pettit, 1999; Crews, Willingham, & Skipper, 2000; Guillette et al., 2000; Golden, Rattner, McGowan, Parsons, & Ottinger, 2003). Recent evidence also raises the distinct potential of transgenerational effects of EDCs, even with exposure only to the parent generation (Anway & Skinner, 2008). Development of male and female reproductive systems, as well as of neural systems, appear to be sensitive to the effects of a variety of EDCs with different modes of toxicity (Colborn et al., 1993; Vom Saal, 1995; Jacobson & Jacobson, 1996; Schantz, 1996; Cheek, Vonier, Oberdorster, Burow, & McLachlan, 1998; Colborn, Smolen, & Rolland, 1998; Tilson & Kodavanti, 1998). Therefore, it is important to understand the potential and extent of EDC effects so that the consequences of exposure may be scientifically evaluated using appropriate analytical tools (Fairbrother et al., 1998).

GENOTYPE

+

ENVIRONMENT

=

3. MODES OF EXPOSURE IN BIRDS A primary mode of exposure to exogenous steroids or environmental chemicals in birds is via maternal deposition into yolk (Adkins-Regan, Ottinger, & Park, 1995; Ottinger et al., 2005). Interestingly, there is significant maternal deposition across a range of EDCs and contaminants, with the distribution of the toxicant in the egg being dependent on the chemical characteristics of the compound (Lin, Wu, Abdelnabi, Ottinger, & Guisti, 2004; Ottinger et al., 2005; McKernan, Rattner, Hale, & Ottinger, 2007). As may be seen in Figure 9.1, Japanese quail hens fed the pesticide methoxychlor (MXC) had increasing MXC concentrations in yolk over the exposure period; yolk MXC decreased over time following cessation of exposure (Ottinger et al., 2005). Enzymes in the yolk or albumin metabolize some of the EDCs to produce metabolites, which in some cases have greater biological potency. This potential route of exposure is supported by a study in which Japanese quail hens were given 17b-estradiol (E2) implants (Adkins-Regan et al., 1995). Assay of plasma samples showed increased circulating E2 levels, with either daily E2 injections or with a silastic implant containing crystalline E2. Eggs produced by treated females had significantly elevated E2 concentrations in their yolks compared to eggs of control females. These data provide evidence for maternal transfer of steroid hormones to the offspring via the yolk (Adkins-Regan et al., 1995). Similarly, other lipophilic compounds, including the soy phytoestrogens, also can be transferred from the hen into the egg, and more specifically the yolk (Lin et al., 2004).

PHENOTYPE

(EDC at sub-lethal or low dose)

Individuals affected by: in-ovo exposure changes to parental DNA

Affects the responses of individuals to changes in:

Individuals affected throughout lifetime by interaction of genotype and environment

patterns of rainfall and temperature food availability parasites/disease load Intra- and inter-specific competition predation

Potential Endpoints: DNA damage DNA methylation

Potential Endpoints:

Behavioral Ecology endpoints Habitat availability Parental behavior Measures of fitness Health and life span

molecular physiological anatomical biochemical ecological/behavioral

FIGURE 9.1 Schematic of EDC effects on biological mechanisms and associated outcomes for the organism.

242

Hormones and Reproduction of Vertebrates

The EDCs absorbed into eggs may accumulate in females via the diet or transdermally. Laboratory studies often have used dietary treatment as a means of EDC exposure. Additionally, EDCs may be injected into eggs via the air cell or by direct injection into the yolk or albumin (Ottinger et al., 2001b; 2005; Quinn, McKernan, Lavoie, & Ottinger, 2007). Effect of vehicles, timing of treatment, and egg position all have effects on embryonic development (McKernan et al., 2007). These studies, as well as data collected in our laboratory and those of others, clearly demonstrate species differences in sensitivity, even to the vehicles. However, laboratory studies do not generally replicate the sporadic exposure experienced by wild birds or the changing cocktail of chemicals in the environment. We have attempted to portray the potential effects of different exposure patterns on reproduction in a hypothetical population of migratory birds in Figure 9.3. If we assume that an optimal lifetime reproductive output would occur in an optimal environment (excellent conditions and food availability, and minimal disease and climate challenge) and with consistent return of birds from migration, we have a characteristic pattern, with young birds achieving maximal reproductive potential and remaining at

that level of productivity until an age-related decline begins at two years of age. With intermittent exposure to EDCs, we suggest that there would be diminished reproductive success and that this would be exacerbated by increasing constant exposures, especially when coupled with harsh environmental challenges. Realistically, if an individual has lifelong immunosuppression or other impairments, the stress of migration will impact the return rate of the migrating population further and delay the return to reproduction following migration (see Chapters 5 and 8, this volume). If this were the case, there might be a steeper than predicted decline and greater impairment in the reproductive capability as well as a shorter reproductive lifespan and fewer aging individuals.

3.1. Avian Models Birds that historically have been the subject of the United States Environmental Protection Agency (USEPA) test guidelines as representative models for toxicological testing include eastern bobwhite quail (Colinus viginianus) and mallard ducks. The rationale for these model species is that they are indigenous to North America and are thereby

MXC gel capsules (50 mg/day) 2750

a MXC bolus

2500

a

2250

Methoxychlor (ppb)

2000

a

1750 1500

b

1250

Day -2 -1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

n 4 2 4 5 4 3 2 3 3 4 1 3 2 2 2 2 2 2

b 1000

bcf

750

bce

500

cd

250 0

d -2

de -1

df 0

de

d 1

2

3

4

5

6

7

8

9

10

de

d

de

de

de

11

12

13

14

15

Day of Experiment

parental exposure

embryonic exposure

FIGURE 9.2 Exposure in birds occurs via maternal transfer. Reproduced from Ottinger et al. (2004). See color plate section.

Chapter | 9

243

Endocrine Disruption of Reproduction in Birds

representative of effects in wild birds. The development of testing paradigms in response to the Endocrine Disruption Screening and Testing Committee (EDSTAC) Final Report (EDSTAC, 1998) includes avian tests in the second tier of testing for potential effects of suspected EDCs. Japanese quail, chickens, mallard ducks, and possibly an altricial model such as the zebra finch (Taeniopygia guttata) have emerged as avian models of choice, with the Japanese quail being an optimal avian model for multigenerational testing. Further, it is clear that EDC effects go beyond the hypothalamicepituitaryegonadal (HPG) axis; EDCs also exert adverse effects on the thyroid, adrenal, and metabolic endocrine axes as well as impacting on immune function. Candidate measurement endpoints for detection of endocrine disruption in birds are deformities, lethality, organ weights and/or morphology, neural and/or neuroendocrine changes, endocrine impairment, delayed maturation, impaired immune functions, impaired thyroid function, and accelerated aging.

4. CHALLENGES IN ASSESSING ENDOCRINE-DISRUPTING CHEMICAL (EDC) EFFECTS IN BIRDS The great diversity in lifespans, reproductive strategies, and adaptations in avian species make it difficult to have a common method or even a common avian model for assessing the varied effects of EDCs and their mechanisms of action in birds (Ottinger & Vom Saal, 2002; Panzica et al., 2007). Additionally, precocial and altricial species differ in the timing of exposure and responses to EDCs throughout their lifecycles (Adkins-Regan, Abdelnabi, Mobarak, & Ottinger, 1990; Ottinger et al., 2002; Iwaniuk et al., 2006; Markman et al., 2008). To add to the confusion, it is becoming increasingly clear that there are speciesspecific differences in sensitivity that may be the result of responsiveness of detoxification systems and even subtle molecular differences in some receptors to certain classes of EDCs (Igushi, Watanabe, & Katsu, 2007). These factors, as well as variation in exposures to single or, more often, mixtures of EDCs and other environmental challenges, make it both difficult and vital to assess the lifetime consequences of EDCs in avian species under controlled laboratory conditions and field studies, in order to provide sound data for risk assessment.

4.1. Consideration of the Lifecycle of Endocrine-disrupting Chemicals (EDCs) A key consideration in ascertaining the effects of potential EDCs is determination of the chemical form of the compound to which exposure occurs. This is dictated by a variety of factors, including the halflife of the specific

compound, biological activity of the parent compound and its metabolites, and modes of exposure. For wildlife, ecological risk assessment includes factoring in the potential impact of a compound or mixture (Hooper, Pettigrew, & Sayler, 1990). This includes the fate of chemicals and the ‘lifecycle’ of these compounds after release into the environment (for reviews see Johnson et al., 2005; Munoz & Panero, 2006; Valle, Panero, & Shor, 2007; New York Academy of Sciences Harbor Consortium, 2008). It is clear from these reviews that biologists and toxicologists attempting to understand the potential consequences of exposure in birds must consider the physicoechemical properties of environmental contaminants.

5. DISCERNING THE EFFECTS OF DIFFERENT CLASSES OF ENDOCRINEDISRUPTING CHEMICALS (EDCs) There have been several general approaches to gaining an understanding of EDC impacts in avian species. In field birds, most of the published literature has resulted from focus on exposures related to known release or documented high levels of suspected EDCs in areas of concern (Fox, 1992; Nichols, Daniel, Moore, Edwards, & Pote, 1997; McCarty & Secord, 1999; Fairbrother, 2000; Rattner et al., 2000). Earlier observations included consideration of a range of contaminants, and, more recently, EDCs have been recognized in general according to their activity and potential mechanism of interaction with the estrogen, androgen, or thyroid endocrine axes (Shore, 1993; Ankley et al., 1997; NRC, 1999; Rattner et al., 2000; Ottinger & Vom Saal, 2002; Panzica et al., 2007; Zoeller, 2008). Accordingly, designs of initial screens have utilized these chemical and biological characteristics for the purpose of rapid initial identification of potential EDCs (EDSTAC, 1998; Zacharewski, 1998). Subsequent characterization in a battery of in-life test paradigms then afford the more precise ability to assess potential risks associated with exposure at selected life stages. As described below, the vulnerability of birds varies with reproductive strategy, developmental characteristics, habitat and migration, and life-history.

6. LIFECYCLE AND SPECIES DIFFERENCES IN THE TIMING OF VULNERABILITY TO ENDOCRINE-DISRUPTING CHEMICALS (EDCs) There is a series of ‘sensitive periods’ during development when one observes the formation of the various physiological systems, many of which occur in tandem. For example, establishment of the HPG axis involves migration of gonadotropin-releasing hormone-I (GnRH-I) cells from

244

the olfactory lobe to the lateral septal region within the hypothalamus (Gao, Abou-Nasr, & Norgren, 1996; Norgren, 1996). These cells begin to function as part of the HPG axis midway through embryonic development (Li, AlstonMills, & Ottinger, 1991; Li, Tamarkin, Levantine, & Ottinger, 1994; Ottinger & Abdelnabi, 1997). In mammals, there is evidence of direct effects of EDCs on GnRH neurons (Gore, 2002; Gore, Wu, Oung, Lee, & Woller, 2002; Bisenius, Veeramachaneni, Sammonds, & Tobet, 2006; Gore, 2008). Data from birds support a similar potential for deleterious effects of EDCs on the avian GnRH-I system (Ottinger et al., 2001b; Panzica et al., 2007; Ottinger et al., 2009). Specific EDCs have the capability of exerting short- and long-term impacts on the GnRH system. However, the extent and nature of the functional consequences associated with exposures are likely to vary with the timing of exposure and sensitivity of that species to the EDC. If an EDC alters the GnRH-I system, there are potentially effects on the functioning of the reproductive axis. This might be expressed in delays or changes in the normal sequence of sexual maturation, as shown in Figure 9.3 (for more details see Ottinger & Brinkley, 1978; 1979a; 1979b).

6.1. Sexual Differentiation in Birds In contrast to mammals, the female avian is the heterogametic sex: ZW (female) vs. ZZ (male). As such, it appears that the steroid environment required for sexual differentiation, especially for sex differences in reproductive behavior, is largely the opposite of mammals in that E2 exposure is required for demasculinization or feminization of the female. However, as will be discussed in Section 6.4, birds appear to depend on exposure to both T and E2 (each within a defined range) to provide the appropriate signal for sexual differentiation of both endocrine and behavioral responses. Within both mammals and birds, developmental events that are mediated by endogenous steroids also define the developmental stages likely to be most affected by EDCs.

6.2. Discerning Effects in Altricial Birds as Compared to Precocial Birds Birds with altricial chicks, such as robins or sparrows, may have greater lifelong neuroplasticity associated with sexual differentiation and subsequent seasonal changes in the song control nuclei and other associated steroidsensitive neural areas (Wade & Arnold, 2004). As such, they may remain more vulnerable to the reproductive and behavioral effects of EDCs throughout their lifetime. Altricial birds differ from precocial birds in being less mature at hatch and having a more complex song system that is steroid-responsive and sexually dimorphic. The

Hormones and Reproduction of Vertebrates

FIGURE 9.3 The impact of exposure pattern on field birds. See color plate section.

neural basis of the song-control system is sexually differentiated under both steroidal and nonsteroidal modulation (Arnold, 1996; Vanson, Arnold, & Schlinger, 1996; Balthazart & Adkins-Regan, 2002; Wade & Arnold, 2004). Although steroid hormone patterns during late embryonic and early posthatch development in which plasma testosterone (T), 5a-dihydrotestosterone (5a-DHT), and E2 levels follow similar patterns in male and female zebra finch (Adkins-Regan et al., 1995), it is the differential metabolism of these steroids that provides the biologically active products essential for sexual differentiation of neural centers (Adkins-Regan, 1990; Arnold, Wade, Grisham, Jacobs, & Campagnoni, 1996; Freking, Nazairians, & Schlinger, 2000; for review see Balthazart & Adkins-Regan, 2002). Thus, timing and level of exposure are key determinants in the impact of EDC exposure. As altricial birds appear to have lifetime vulnerability to endocrine disruption via effects on the steroid-sensitive song system, it is critical to have an altricial model species. Several songbird species have been extensively studied in order to understand the modulation of the song-control system, and overlay of effects of EDCs in these species would provide valuable information. A few laboratory studies have addressed specific effects of selected EDCs in altricial species (Gee, Craig-Veit, & Millam, 2004; Hoogesteiin, DeVoogd, Quimby, De Caprio, & Kollias, 2005); most of the data are from field observations (Hoffman, 1990; McCarty & Secord, 1999; Iwaniuk et al., 2006; Markman et al., 2008). A few studies have attempted hormone or EDC treatment of birds in the field and these studies provide additional insight into the effects of these compounds. Both altricial and precocial species show long-term effects from EDCs from embryonic exposure;

Chapter | 9

245

Endocrine Disruption of Reproduction in Birds

FIGURE 9.4 Overview of development with birth and movement of gonadotropin-releasing hormone-I (GnRH-I) cells; role of steroid hormones and maturation-related increase in hormones with initiation of gonadal function and reproductive behavior. E2, 17b-estradiol; GnRH, gonadotropin-releasing hormone; HPG, hypothalamicepituitaryegonadal. Reproduced from Ottinger and Brinkley (1979). See color plate section.

FIGURE 9.5 The effects of dietary methoxychlor (MXC) on sexual maturation.

Effects of Dietary Methoxychlor on Sexual Maturation % of F1 females with functional ovaries

% of F2 males with developed testes at seven weeks of age 100 X = 9.36, < 0.05

80 60 40 20 0

10/10

3/7

4/6

Control

Low

High

100 90 80 70 60 50 40 30 20 10 0

Control X 2= 9.29,

Weight (g)

F2 testes weight in males at seven weeks 4.5 4 3.5 3 2.5 2 1.5 1 0.5 0

Ancova F (2, 13) = 8.03, p < 0.05 (adjusted least square means)

Control Low

High

6/6 6/6

10/12 10/12 Low

5/13 High

p < 0.05

% of F2 adult females with mature ovaries 100 90 80 70 60 50 40 30 20 10 0

X 2 = 6.69, p < 0.05

5/7

0/5

Control

Low

however, the intensity and duration of the effect may differ with the ontogenetic characteristics of the species.

6.3. Discerning Effects in Precocial Birds Precocial birds such as Japanese quail, bobwhite quail, and mallard ducks are well developed at hatch and have

6/10 High

a relatively limited period of time during which gonadal steroids exert their effects on sexual differentiation. As part of achieving greater maturity at the time of hatch, precocial species have been the primary models for toxicological testing because generally they exhibit earlier development and organization of the central nervous system (CNS). By the time of hatch or shortly thereafter, these birds have

246

undergone sexual differentiation of reproductive endocrine and behavioral responses. Exposure of precocious species to exogenous steroids is effective only for a finite period of time during development; i.e., during sexual differentiation in ovo. Therefore, different reproductive and developmental strategies of precocial and altricial birds pertain to the stage of the lifecycle most vulnerable to EDCs, and precocial birds, such as Japanese quail, appear to be more affected by EDC exposure as embryos. In Japanese quail, gonadal steroids produced by both the gonads and adrenal glands play a critical role in differentiation of endocrine and neuroendocrine systems. There appear to be two phases in the differentiation of the reproductive system as a whole entity: gonadal differentiation early in embryonic development and later sexual differentiation of the hypothalamus. Females generally have higher relative levels of plasma E2 compared to androgens; males have the opposite pattern (Ottinger & Bakst, 1981; Abdelnabi, Bakst, Woods, & Ottinger, 2000; Ottinger, Pitts, & Abdelnabi, 2001a). If embryos are treated with exogenous T or E2 before embryonic day 12, males exhibit impaired courtship and mating behavior as adults, whereas treatment after embryonic day 12 has little effect (Adkins, 1979; Ottinger & Abdelnabi, 1997; Ottinger et al., 2001b; Ottinger & Vom Saal, 2002). Embryonic EDC exposure may provide additional steroid-like activity, impacting sexual differentiation and, more specifically, neural systems that control many endocrine and behavioral components of reproduction.

6.4. Steroid- and Endocrine-disrupting Chemical (EDC)-sensitive Neural Centers and the Hypothalamicepituitaryegonadal (HPG) Axis in Japanese Quail The preoptic lateral septal (POLS) region of the brain primarily regulates reproductive behaviors and endocrine functions in Japanese quail (Watson & Adkins Regan, 1989a; 1989b; Panzica, Garcia-Ojeda, Viglietti-Panzica, Thompson, & Ottinger, 1996; Panzica, Garcia-Ojeda, Viglietti-Panzica, Aste, & Ottinger, 1997; Balthazart & Adkins-Regan, 2002). Accordingly, studies have focused on the neural systems contained in this area as well as the hypothalamic regions that regulate endocrine aspects of the reproductive axis and the role of steroid hormones at all stages of the lifecycle (Ottinger, 1998). In addition, the preoptic-septal region (POA-SL) also contains many of the GnRH-I cell bodies and these cells project their axons to the median eminence (ME) of the neurohypophysis, making this region critical in the regulation of both endocrine and behavioral components of reproduction (Li, Paciotti, Tamarkin, & Ottinger, 1994a; Millam et al., 1998; Ottinger, 1998). The aromatase enzyme (P450aro) is

Hormones and Reproduction of Vertebrates

required to metabolize T to E2 in the POA-SL and is strongly sexually dimorphic late in embryonic development and in adults, with males having higher levels (Foidart, Harada, & Balthazart, 1994; Aste et al., 1996; Hutchison et al., 1997; Panzica et al., 1997; Balthazart & AdkinsRegan, 2002). Aromatase enzyme is also sexually dimorphic in the embryonic gonads, with high levels in the ovary compared to the very low activity in the testes (Elbrecht & Smith, 1996; Shimada, Yoshida, & Saito, 1996). In addition to 5a-DHT, produced by the 5a-reductase enzyme, there are higher brain levels of 5b-reductase, which produces the corollary biologically inactive metabolite 5b-DHT, in embryonic Japanese quail in both males and females (Balthazart & Ottinger, 1984). This conversion may limit the amount of active metabolites (E2 and 5aDHT) to which the male embryo brain is exposed, thereby preventing behavioral demasculinization from metabolized T. The presence of estrogenic EDCs may alter the process of sexual differentiation because it is the relative exposure to androgens and E2 that appears to be a key component of sexual differentiation of both behavioral circuits and endocrine responses in both males and females. Several other neural systems are also sexually dimorphic, making them potentially vulnerable to EDCs during sexual differentiation. The GnRH-I system is central to the functioning of the reproductive axis; it is also a sexually dimorphic system in birds, with a higher number of GnRHI cells in the adult male hypothalamus and concomitantly higher GnRH-I concentrations compared to adult females (Li et al., 1994a; 1994b; Ottinger et al., 2004; 2009b). This sexual dimorphism is also observed in the hatchling and could provide an excellent bioindicator of exposure to endocrine-active compounds during development. The GnRH-I system is regulated by neurotransmitters and neuropeptides and the dynamics of the HPG axis change during aging (Ottinger, Thompson, Viglietti-Panzica, & Panzica, 1997; Panzica et al., 1996; Ottinger, 2007; see also Chapter 1, this volume). A neuropeptide system that is sexually dimorphic and responsive to steroids is the arginine vasotocin (AVT) system; it is also affected by exposure to EDCs (Panzica et al., 1996; 2007). A further interesting association is the close proximity of vasotocinergic neurons to GnRH-I perikarya in the septal region (Panzica et al., unpublished data). In addition, a sexual dimorphism has been observed in the number of apparent connections between AVT-containing neurons and GnRH-I neurons, with a higher number of contacts in males (GnRHeAVT: F1,4 ¼ 10.5; p ¼ 0.03; male: 32 4; female: 11 2) and also in the number of GnRH-I cells (F1,4 ¼ 12.4; p ¼ 0.02; male: 259 106; female: 129 53) (Panzica et al., 2007; Ottinger, Panzica, Viglietti-Panzica, Thompson, and Dean, unpublished data). The combination of the strong sexual dimorphism in the GnRH-I system in the quail and dimorphic

Chapter | 9

247

Endocrine Disruption of Reproduction in Birds

neuroregulatory systems provides multiple potential targets that may be impacted by EDC exposure, especially during periods of sexual differentiation or seasonal changes in the reproductive axis. Finally, early effects of EDC exposure may exert more subtle long-term effects that ultimately may diminish lifetime individual reproductive success and even have population-level effects. The effects of exogenous steroid hormones on sexual differentiation provide some insights into the potential effects of EDCs that may not be quite as potent as the native steroid hormones. Administration of gonadal steroids to Japanese quail embryos alters anatomical, neuroendocrine, and behavioral components of reproduction when they become adults (Adkins, 1979; Adkins-Regan et al., 1990; 1995; Halldin, Berg, Brandt, & Brunstrom, 1999; Ottinger et al., 2005). By embryonic day 12 (E12), administration of exogenous E2 resulted in sex differences in later male or female behavior and impacted on behavioral control areas in the POLS (Adkins-Regan et al., 1990a; 1990b; 1995; Aste et al., 1996; Ottinger & Vom Saal, 2002). Interference with steroid action by embryonic treatment with the P450aro inhibitor fadrozole or the antiestrogen tamoxifen on E12 reduced later expression of sexual behavior (Adkins, 1979; Rissman, Ascenzi, Johnson, & AdkinsRegan, 1984; Panzica et al., 1996). As discussed earlier, the timing of the steroid exposure is critical; males treated with steroids between E1 and E12 do not show any courtship or mating behavior, whereas steroid exposures after E12 have little or no effect on sexual behavior in adult males. Interestingly, the cloacal gland, which is an androgen-responsive accessory sex structure, remains responsive to circulating androgens in all groups, indicating that the behavioral impairment is not due to a total lack of responsiveness to steroid hormone but rather is likely to involve a hypothalamic neural mechanism. However, there is increasing evidence of specific effects on key regions of the hypothalamus that permanently alter endocrine and behavioral responses during ontogeny and in the adult. Examples of this type of mechanism of action have been observed (Ottinger et al., 2005; 2009). Embryonic exposure to E2 or androgens greatly affects sexual differentiation of the reproductive tract in females, whereas adult exposure is ineffective (Adkins-Regan, 1990; Ottinger & Abdelnabi, 1997). Early steroid exposure or treatment with fadrozole or tamoxifen also altered gonadal development, producing defeminization of the ovary and accessory structures and altering the expression of 17ahydroxylase (P450c17) and P450aro in the gonads and brain (Gildersleeve et al., 1985; Elbrecht & Smith, 1992; Stoll et al., 1993; Perrin, Stacey, Burgess, & Mittwoch, 1995; Shimada et al., 1996; Nishikimi et al., 2000; Ottinger, Bohannon, McKernan, Abdelnabi, & Rossellil, unpublished data). In summary, gonadal steroids, specifically E2 and T, are key players in the sequence of events leading to sexual

differentiation. In Japanese quail, steroid exposure by E12 organizes sexually dimorphic behavioral responses. However, less is known about the organizational effects of embryonic steroid exposure on sexually dimorphic neurotransmitter and neuropeptide systems. There is increasing evidence for more global effects of early exposure to endocrine-active compounds on reproductive and metabolic endocrine function. As steroid hormones play a critical role in appropriate sexual differentiation and maturation, exposure to exogenous hormonally active substances is likely to have both short- and long-term consequences on reproductive function in the adult. Finally, for birds, reproductive fitness measures include fertility, hatching success, and offspring viability, with supporting endocrine and neuroendocrine measures providing a predictive index of impact associated with impaired behavioral and functional outcomes from early EDC exposure. These measures could provide very sensitive indicators to be used as windows into assessing risk for avian populations.

7. MAJOR EFFECTS OF ENDOCRINEDISRUPTING CHEMICALS (EDCs) IN AVIAN SPECIES 7.1. Observations in Wild Populations Wild birds are exposed to a myriad of compounds and contaminants, and their exposures may drastically vary between breeding grounds and wintering grounds. However, these compounds, which include EDCs, have many differing mechanisms of action. Certain herbicides, insecticides, fungicides, and other chemicals, in addition to their overt toxicity at high doses, have been recognized for their potentials as EDCs (Short & Colborn, 1999). Suspected EDCs include as MXC, industrially produced compounds such as PCB-126 (3, 30 , 4, 40 , 5-pentachlorobiphenyl), plant phytoestrogens, the DDT metabolite dichlorodiphenyldichloroethylene (DDE), and the synthetic androgen trenbolone acetate. Although many of these compounds were produced for specific applications, their presence in the environment has resulted in unpredicted effects in wildlife. For example, MXC replaced DDT in use as an insecticide because of the latter’s toxicity and eggshell-thinning effects in birds. However, as will be discussed in Section 7.3.1, MXC also has endocrine-disrupting effects. Contaminant-associated changes in normal growth, behavior, and reproduction, along with population impacts, have been reported for wild birds (Fox, 1978; Kubiak et al., 1989; Hoffman, 1990; Fox, 1992; Colborn et al., 1993; Rattner et al., 1993; Ankley et al., 1997; Crews et al., 2000; Fairbrother, 2000). Contaminant exposure is associated with altered embryonic development, especially in precocial species (Fox et al., 1978; Van den Berg et al., 1994; Fry,

248

1995; Brunstrom, Axelsson, & Halldin, 2003). Initial effects of estrogenic EDCs in birds were observed in the eggshell thinning associated with o,p’-DDT exposure (reviewed by Ankley et al., 1997; Cheek et al., 1998). There were also persistent effects of contaminants in bald eagles (Anthony, 1993). Dichlorodiphenyltrichloroethane and its metabolites are lipid-soluble compounds, stored in organ lipids. The main component of DDT, p, p’ - DDT, has little androgenic or estrogenic activity. However, o, p’ - DDT, which makes up less than 15% of the mixture in manufacturing, is estrogenic. This is in contrast to the potent androgen receptor antagonistic activity of the DDT metabolite, DDE. Both o, p’ - DDT and DDE are persistent in the environment. Environmental contaminants, including white phosphorous, perchlorate, and DDE, act as EDCs in several species of bird (Bosveld & Van den Berg, 1994; Brandt, Berg, Halldin, & Brunstro¨m, 1998; McCarty & Secord, 1999; Vann, Sparling, & Ottinger, 2000). Dioxin exposure was associated with altered symmetry in major brain areas in great blue herons (Ardea herodias) (Henshel et al., 1995). Similarly, exposure to the insecticide methyl parathion resulted in reduced reproductive success in northern bobwhite quail (C. virginianus) associated with reduced eggshell weight (Bennett, Bentley, Shiroyama, & Bennett, 1990). However, dietary tests must take into account palatability issues, as the effect of another insecticide, methamidophos, on northern bobwhite quail was primarily a result of induced anorexia (Stromborg, 1986). Fish-eating birds exposed to biomagnified concentrations of some contaminants display the Great Lakes embryo mortality, edema, and deformity syndrome, which leads to morphological abnormalities and long-term effects in adult birds (Giesy, Ludwig, & Tillitt, 1994; Henshel et al., 1995; Grasman et al., 1998; Grasman & Fox, 2001). As more data become available on EDC effects, the targets and mechanisms of action of classes of EDCs will become clearer, making it possible to assess potential impact on wildlife populations (Mineau, Boersma, & Collins, 1994; Mineau et al., 2001; Rattner et al., 2000). Assessment of risk to field populations is difficult due to the presence of mixtures of chemicals, however (Barron, Galbraith, & Beltman, 1995), complicating assessment of the risks to wildlife populations (Kortenkamp, 2007). Screening assays, which assess potential EDC activity based on chemical interaction in vitro with steroid receptor expression systems, are useful for determining potential biological activity (Shelby et al., 1996; Murk, 1997; Cheek et al., 1998; Gray et al., 1998; Crews et al., 2000). Future techniques for assessment of EDCs will rely on conserved mechanisms and will likely take advantage of screening microarray technology and other such molecular techniques to detect potential damage to wildlife and ascertain risk to avian populations.

Hormones and Reproduction of Vertebrates

7.2. Laboratory Studies in Birds As there are up to 80 000 suspected EDCs already in the environment, clearly it is impossible to test each individually for even one type of endocrine-disrupting activity. Laboratory studies necessarily have underpinned the interpretation of observations on wild birds because the effects of known EDC treatments can be determined for selected compounds. The EDC is usually delivered by egg injection to study embryonic effects, or via the diet to understand the effects on maturing or adult birds. Laboratory studies have often used E2 or another strong estrogen as a positive control for comparisons with the compound under study. Consequently, chemicals such as PCB-126 and 2,3,7,8-tetrachlorodibenzodioxin (TCDD) (the most potent of the dioxins) have been well characterized according to their toxicity and physiological impacts as estrogen-active EDCs (Hatano & Hatano, 1994; Barron et al., 1995; Elliott, Kennedy, & Lorenzen, 1997; Murk et al., 1997; Alonso et al., 1998). In the laboratory, the avian egg has provided a basis for evaluation of the implications of the deposition of contaminants in wild birds (Rattner et al., 1993; Berg, Halldin, Brunstrom, & Brandt, 1998; Berg, Halldin, Fridolfsson, Brandt, & Brunstrom, 1999). Moreover, administration of an EDC directly to the avian embryo provides exposure to a known dose of the chemical and allows for determination of long-term effects on endocrine and behavioral responses as the chicks mature (Brandt et al., 1998; Halldin et al., 1999; Halldin, Axelsson, & Brunstrom, 2005). As a result of the ability to isolate embryonic development from later maternal or other environmental influences, eggs have been used extensively in toxicology studies (Hoffman, 1990; Wehler, Brunstrom, Rannug, & Bergman, 1990; Y. Hatano & A. Hatano, 1994). Studies have examined gonadal morphology in response to EDC exposure (Berg et al., 1998). Embryonic exposure to the synthetic estrogens DES and ethinylestradiol is associated with the formation of an ovotestis or feminization of the testis and accessory structures in a dose-related index of estrogenicity (Rissman et al., 1984; Perrin et al., 1995; Berg et al., 1999). Tamoxifen, used to interfere with E2 action, alters early gonadal steroidogenesis (Scheib, Mignot, & Guichard, 1984). In-ovo exposure to organophosphorus and carbamate compounds also disrupt development of neuroendocrine regulatory mechanisms, later impairing reproduction (Rattner & Ottinger, 1984; Rattner et al., 1993). Some endpoints previously used in assessing toxicity show promise in evaluating EDC activity. These include cytochrome P450 1A activity in chicken hepatocytes and apolipoprotein-II mRNA production by the liver in response to estrogenic chemicals (Ronis, Ingelman-Sundberg, & Badger, 1994; Elliott et al., 1997; Andersson, Van der Burght, Van den Berg, & Tysklind, 2000). Similarly, the presence of

Chapter | 9

249

Endocrine Disruption of Reproduction in Birds

the yolk protein precursor vitellogenin (Vtg) and ER estrogen receptor assays has been the subject of extensive studies as indices of EDC exposure across species (Zacharewski, 1998). As mentioned in Section 6.4, embryonic measures of enzymatic activation, gonadal morphology, steroid hormone levels, and specific neurotransmitters and neuropeptides can provide useful indices of EDC exposure. Effects of EDC exposure in parental generations may result in reduced plasma steroid concentrations, both in the parents and in the offspring in mammals and birds (Ottinger et al., 2009a). Similarly, the timing of sexual maturation may be a more sensitive measure of EDC exposure than egg production or fertility as these parameters were unaffected by dioxin treatment of chickens (Alonso et al., 1998). Several types of behavioral endpoint should be assessed as well, because behavioral responses may prove to be reliable indicators of EDC exposure at critical stages in development. For example, motor tests in young chicks, such as those used in determining fearfulness and early social behaviors, may be excellent indicators of neuromotor or other behavioral consequences that involve neurotransmitter systems (Panzica et al., 2007; Ottinger et al., 2009a). In addition, these types of test may provide an indication of neurotoxicities, even those that may be expressed in behavioral or reproductive function (Varghese, Bursian, Tobias, & Tanaka, 1995; Ottinger et al., 2005). Exposure to E2 during midembryonic development greatly diminishes male sexual behavior and reproductive success in adults (Ottinger & Abdelnabi, 1997; Ottinger et al., unpublished). Similar results have been observed in northern bobwhite quail and also in mammals, indicating that this effect may be common across species and even phyla (Lien, Cain, & Beasom, 1987; Csaba et al., 1993). Other estrogenic chemicals also impair sexual behavior, providing evidence that testing courtship

and mating behavior in embryonically exposed male Japanese quail would offer a reliable indicator of estrogenic EDC exposure (Halldin et al., 1999).

7.3. Estrogen-active Compounds 7.3.1. Methoxychlor (MXC) The organochlorine pesticide MXC is used on fruits, vegetables, trees, home gardens, forage crops, and livestock, with the highest use occurring in the northwest and eastern seaboard states of the USA (Fry, 1995; Ottinger et al., 2002). In Japanese quail, females readily deposit MXC into the egg yolk. Exposure of Japanese quail embryos to 1.5 or 3.0 mg/egg MXC resulted in a significant increase in GnRH-I in female hatchlings and a significant decrease of GnRH-I in female adults (Ottinger et al., 2004). Adult males hatched from eggs exposed to 1.5 or 3.0 mg/ egg MXC showed reduced male sexual behavior (Figure 9.5); exposure to 5 mg/egg MXC completely inhibited adult male sexual behavior (Ottinger et al., 2001b; Eroshenko, Amstislavsky, Schwabel, & Ingermann, 2002). We performed a multigenerational study to examine the effects of low-level dietary exposure of adult females to 0, 0.5, 5 and 10 parts per million (ppm) MXC (Ottinger et al., 2005). These levels of dietary MXC did not significantly diminish egg production or reproductive performance; however, sexual maturation was delayed in both males and females hatched from eggs of exposed mothers (Table 9.1). These data provide evidence that, even at low dietary levels, EDCs that might be considered relatively innocuous with respect to lethality may have long-term consequences for reproductive functions of offspring and hence a negative impact on fitness.

TABLE 9.1 Measurement endpoints indicative of endocrine disruption Measurement

Interpretation of observed effect

Relevant for field birds? Conserved across species?

Lethality

Relative effects on inidividuals

At high exposures

Yes, species differences

Deformities

Impact viability and longevity

Yes if birds are found

Yes, species differences

Organ weights and morphology

Impaired physiology

Yes if birds are found

Yes, organ and system specific

Neural/neuroendocrine effects

Reduced fitness and altered behavior

Yes

Yes

Endocrine impairment

Reduced function and impaired fitness Variable

Yes, survivor effect?

Delayed maturation

Reduced fitness

Yes

Yes

Impaired immune and thyroid system function

Reduced fitness/survival

Yes

Yes

Parental, reproductive, and migratory behavior

Reduced fitness/survival

Yes

Yes

Accelerated aging

Reduced fitness/survival

Yes

Yes

250

7.3.2. 3, 30 , 4, 40 , 5-Pentachlorobiphenyl -126 (PCB-126), other polychlorinated biphenyls (PCBs), and dioxins Polychlorinated biphenyls, originally designed and produced to be heat-resistant when used as a lubricant, occur in a number of forms. Data are available on the forms of PCBs and their distribution in the environment (Beyer & Biziuk, 2009). Polychlorinated biphenyls were banned in the USA because of their potent effects on reproduction and offspring viability in numerous taxa (Giesy et al., 1994; Barron et al., 1995). There are more than 200 possible PCB congeners that have found their way into the environment (NRC, 1999). As a result of their chemical structures, these congeners may have estrogenic, androgenic, and/or thyroid-active properties (Zoeller, 2008). Therefore, it is difficult to assess their potential risk to populations. For example, endogenous thyroxine and E2 levels were reduced in American kestrels (Falco sparverius) exposed to PCBs (Quinn, French, McNabb, & Ottinger, 2002). In the ecosystem, PCBs bioconcentrate along the food chain; PCBs partition into fatty tissues, accumulating over time (Hooper et al., 1990; Ness, Schantz, & Hansen, 1994). Effects in birds include impaired reproductive success in tree swallows (Tachycineta bicolor) exposed to PCBs (Bishop et al., 1999; Custer et al., 1999). Coplanar PCBs bind to the arylhydrocarbon receptor (AhR) and there is clear evidence of species differences in responses associated with receptor activation (Ness et al., 1994; Karchner et al., 2005; Head, Hahn, & Kennedy, 2008). Hydroxylation of coplanar PCBs decreases their toxicity: hydroxylated metabolites of 3,3’,4, 4’-tetrachlorobiphenyl (PCB-77) injected into chicken (white leghorn) eggs showed lower affinity for the AhR and were less acutely toxic than the parent compound (Wehler et al., 1990). Ortho-substituted PCBs have estrogenic activity (Korach et al., 1988). Additionally, a number of PCBs also affect courtship and nesting behavior, effectively causing a delay in the onset of reproductive activity (Tori & Peterle, 1983), stunted development, and impaired hatching success (Kubiak et al., 1989; Becker, Schuhmann, & Koepff, 1993). A great deal of data has utilized PCB-126 as the standard against which the biological activity of other PCBs is measured. The biological activity of PCBs includes both estrogen- and thyroid-disrupting properties. Most of the data regarding PCB-126 focuses on its toxicological effects, with more recent consideration of its endocrinedisrupting actions. Behavioral impacts (Tori & Peterle, 1983) as well as effects on cardiac, hepatic, thyroid, and reproductive functions have been documented (Grasman et al., 1998; Guillette et al., 2000; McNabb & Fox, 2003; Fisher, Bortolotti, Fernie, Bird, & Smith, 2006; Halldin et al., 2005). A number of studies have examined the

Hormones and Reproduction of Vertebrates

lethality of a variety of PCBs, including PCB-126 (Custer et al., 1999; T. Custer, C. Custer, & Hines, 2002). Additionally, circulating androgens were reduced in adult chickens that received Aroclor 1254, suggesting impacts on gonadal function (Zhang, Fang, Liu, Xia, & Qiao, 2002). Both PCBs and the dioxin TCDD have immunotoxic effects in birds (Grasman & Fox, 2001), including effects on the development of the bursa of Fabricius, a unique primary component of the immune system of birds. The bursa of Fabricius is extremely sensitive to androgen exposure. During embryonic development, the bursa is sensitive to androgen exposure, which inhibits development. Conversely, the bursa is relatively larger in the female and remains active throughout adulthood in Japanese quail, where it serves as a lymphoid organ for humoral immunity (Glick, 1991; Guellati et al., 1991). Polychlorinated biphenyl-126 caused decreases in bursa weight and in the numbers of developing B lymphocytes in the bursas of chicken embryos (Fox & Grasman, 1999). Dioxins and PCBs also have been linked to thymic atrophy and suppression of mitogen-induced proliferation, mixed lymphocyte responses, cell-mediated cytotoxicity, and humoral responses (Grasman & Fox, 2001).

7.3.3. Endocrine-active phytochemicals (phytoestrogens) Benign effects of naturally occurring plant phytoestrogens have been observed, particularly in rodent populations, in which changing phytoestrogen levels modulate reproductive functions (Berger et al., 1987). The primary biologically active isoflavone in soybeans and certain other plants is genistein, which is approximately 1000 less active than E2, based on in-vitro screens that utilize cell systems with E2 receptors (Setchell, 1998; Lin et al., 2004). However, when taken in through the diet, the hen readily transfers genistein and genistin (the 7-O-b-D-glycoside of genistein) into the yolk (Lin et al., 2004). Laboratory studies showed that genistein injected into the egg at E3 in Japanese quail resulted in impaired male sexual behavior and was associated with reduced immunostaining for AVT in the hypothalamus of adult males hatched from these eggs (Panzica et al., 2007), suggesting a direct effect on sexual differentiation. Genistein acts primarily on the estrogen receptor-b (ERb) (Kostelac et al., 2003), and there is a higher density of ERb transcripts in areas that modulate male sexual behavior. Other studies in embryonic quail brain have showed that ERb is expressed developmentally earlier than ERa (Axelsson et al., 2007). Estrogen receptorb mRNA was detected on E9 and E17, whereas expression of ERa mRNA was detected only on E17. Perhaps ERb is responsible for mediating the effects of estrogens on sexual differentiation of the avian brain.

Chapter | 9

251

Endocrine Disruption of Reproduction in Birds

7.4. Anti-androgenic Endocrine-disrupting Chemicals (EDCs) In Japanese quail, the two main metabolites of DDT are DDE (31%), and 2,2-bis(4-chlorophernyl)-acetic acid (DDA) (35%), with DDE being more chemically stable and biologically persistent (French & Jeffries, 1969; Ahmed & Walker, 1979). Japanese quail embryos exposed to p,p0 DDE (20 and 40 mg/egg) had significantly increased bursal weight, consistent with the antiandrogenic effects of this compound. However, sections of bursal tissue from p,p0 DDE-treated birds had lesions and abnormalities not observed in control birds. Moreover, females showed delayed sexual maturation, and males treated with 40 mg/ egg showed impaired mating behavior as adults (Quinn et al., 2008). Other measures of reproductive and immune functions also were altered in the p,p0 -DDE-treated birds. These effects would impact individual fitness and potentially affect wild avian populations if exposure occurred in a critical number of individuals.

7.5. Androgenic Endocrine-disrupting Chemicals (EDCs) Trenbolone acetate (TbA) (17b-acetoxyestra-4,9,11-triene3-one) is a synthetic androgen used in production agriculture; the bioactive metabolites of TbA are trenbolone-17b and trenbolone-17a (Quinn et al., 2007). Trenbolone and other synthetic and natural steroid hormones released from human and animal wastes have been measured in rivers and streams, sometimes at levels that exert endocrine-disrupting effects on aquatic species (Orlando et al., 2004). In Japanese quail, embryonic exposure to TbA has deleterious effects for hatchlings that persist as the birds mature (Quinn et al., 2007). Effects occur in both reproductive (delayed sexual maturation and impaired male mating behavior in adults) and immune (reduced hatchling bursa index) measures (Quinn et al., 2007). One of the most interesting effects was observed in young chicks subjected to a ‘runway test’, in which the chick would rejoin other chicks. In this test, the isolated chick typically uses an alarm/separation call to locate other chicks, orients on the other chicks, and then runs to rejoin them. Chicks treated with TbA exhibited a dose-related impairment in their calling behavior; loss of this behavior could be a serious problem for birds in the wild (Quinn & Ottinger, unpublished data).

7.5.1. Vinclozolin Vinclozolin is a fungicide used in agricultural practices. It is considered to be relatively safe but appears to have primarily an antiandrogenic action, depending on the purity of the chemical (for review see Ottinger & Vom Saal,

2002). Embryonic exposure to vinclozolin does not affect plasma androgen levels or relative testes weights. Vinclozolin does not alter either the relative pattern in or concentrations of GnRH-I concentrations in females. In addition, there is a typical pattern in these concentrations, with higher concentrations in the POA-SL region as compared to the ME. Typically, males show the opposite pattern in that POA-SL concentrations of GnRH-I are relatively lower than those in the ME (Li et al., 1994). However, treated males show significant differences as hatchlings, but these disappear in adults. As adults, vinclozolin-treated males also show more female-typical patterns in the distribution of the peptide, in that GnRH-I concentrations are relatively higher in the POA-SL region than in the ME. This suggests that GnRH-I is produced but is perhaps less available for release in the ME in vinclozolin-treated males. These data also suggest feminization in the pattern of production and release of GnRH-I in treated males. Subtle behavioral effects were observed in treated males that did not improve in mating performance over three days of successive mating tests compared to control males that showed an increased number of mounting attempts and successful matings (McKernan et al., 2001). This suggests that there may be a subtle impairment of sexual behavior with vinclozolin exposure, in terms of both the appetitive and the consummatory components of mating behavior. Therefore, vinclozolin should be further examined for nonlethal, yet subtle, consequences on endocrine and behavioral components of reproduction, which could impact wild populations. Males are more affected by vinclozolin than females, supporting the hypothesis that relative exposure to endogenous androgens and E2 are the signals driving sexual differentiation of endocrine and behavioral components of reproduction.

7.6. Thyroid-disrupting Compounds Most studies investigating the effects of EDCs on the thyroid system in birds have focused on plumage development. Onset of molt, sequence of molt, pigment deposition (carotenoid and melanoid), and overall feather structure (e.g., barbules) are mediated by the thyroid system and can be altered by administration of exogenous thyroid hormones (Payne, 1972; Kuenzel, 2003; Quinn, French, McNabb, & Ottinger, 2005). Feathers play important roles in many aspects of a bird’s survival and reproductive fitness, including thermoregulation, flight, and communication of mate quality and age. Plumage colors and patterns are often the major secondary sexual characteristics that are used for sexual selection. Birds with brighter plumage are most often healthier and better able to contribute to a pair’s reproductive efforts than those with dull plumage. Thyroid-active contaminants that alter any

252

aspect of plumage production may, therefore, have the potential to alter a bird’s survival or reproductive output. There are a number of EDCs that have been associated with thyroid effects; a few of these will be considered below. Polychlorinated biphenyls have been used as a model class of chemicals for environmental contaminants that may alter aspects of avian coloration via disruption of the thyroid system. Individual PCB congeners and mixtures disrupt thyroid action in a number of avian species (Fowles, Fairbrother, Trust, & Kerkvliet, 1997; Gould, Cooper, & Scanes, 1999; Quinn et al., 2002). Female tree swallows from PCB-contaminated areas along the Hudson River have been observed to have more adult blue-green coloring than the dull brown coloration that is characteristic of subadults of that species (McCarty & Secord, 2000). Bortolotti, Fernie, and Smits (2003) showed that oral exposure to a 1 : 1 : 1 mixture of Aroclors (PCB mixtures) 1254, 1248, and 1260 disrupted soft-part coloration (ceres and lores) and plasma carotenoid levels in American kestrels during the breeding season. The males that were exposed to the PCB mixtures not only were duller in color than controls but also exhibited a higher number of sexual behaviors than controls during courtship. In the same study, Bortolotti, Smits, and Bird (2003) found decreases in noncarotenoid pigmentation of irides in older male kestrels. Despite causing significant decreases in circulating thyroxine (T4) levels in American kestrels, Aroclor 1242 failed to cause any effects on coloration, patterns, molt timing or sequence, or reflectance in the visible and ultraviolet light spectrums in oral exposure levels up to 60 ppm (Quinn et al., 2002). This may be due to variability in the determination of coloration as to timing or dose of exposure, genetic control over coloration, and the actual classes of pigments involved in different mechanisms of coloration. One of the main difficulties with assessing overall mechanisms of action and predicting effects of environmental contaminants that are thyroid-active is that many of these chemicals do not solely target the thyroid system. Many of the PCB molecules and mixtures that have been used in recent studies contain PCB molecules that are estrogen- as well as thyroid-active. Steroid hormones also have been shown to greatly affect plumage development and coloration (Owens & Short, 1995). Additionally, it has been suggested that plumage manipulations in some species appear to be more resistant to hormonal treatments (Ralph, 1969), specifically those species that are sexually dimorphic all year round rather than just seasonally (Owens & Short, 1995). Since thyroid hormones are important in the modulation of the immune system, as suggested by correlations between plumage brightness and immunocompetence, thyroid-active chemicals may disrupt normal lymphoid development or function. Bortolotti et al. (2003a) suggest

Hormones and Reproduction of Vertebrates

that decreases in carotenoid levels from contaminants may cause reductions in the ability to scavenge free radicals and the amount of antioxidants deposited in eggs. Many studies have shown that suppression of the thyroid system also suppresses humoral and cell-mediated responses in birds and mammals (reviewed in Klecha et al., 2006). Information concerning the effects of thyroid hormones on the development of the immune system is practically absent in avian species, and unclear from studies using mammalian species. Although thyroid hormones are necessary for normal B-cell development, their role in thymopoiesis remains uncertain. Future studies may reveal more about the relationships among the thyroid and immune systems and plumage development, which will enable better understanding of the effects of thyroid-active chemicals on these systems.

7.7. Polybrominated Diphenyl Ethers (PBDEs) and Potential Thyroid Disruption Polybrominated diphenyl ethers (PBDEs) are a chemical class of fire retardants most commonly used in polymers, textiles, electronics, and other materials. As PBDEs are physically combined (i.e., not covalently bound) with the product matrix, they may migrate out of that matrix over time. Polybrominated diphenyl ethers bioaccumulate in aquatic and terrestrial food chains, and biomagnify in predators due to consumption of contaminated prey. Monitoring studies indicate that PBDE concentrations are increasing in the environment. Notably, a retrospective study of archived herring gull eggs (Larus argentatus) from the Great Lakes demonstrated that PBDE concentration increased by one and a half orders of magnitude during 1981e2000, with a concentration doubling time of between 2.6 and 3.1 years (Gauthier et al., 2008) and, as recently reported, concentrations of these congeners in gull eggs have leveled off (Gauthier, Hebert, Weseloh, & Letcher, 2008). Remarkably, there are few toxicological data on the possible effects of PBDEs on wildlife, especially for avian species. Intermediate-duration oral studies in animals indicate that, similar to acute toxicity studies, the liver and thyroid are the primary targets of repeated exposures to technical mixtures of deca-, penta-, and octa-BDEs (Darnerud, 2003). Effects include enlargement and histological alterations in both organs and altered serum thyroid hormone levels, specifically decreased serum T4. This response may be related to the structural similarity between PBDEs and thyroid hormones. As a result of this structural similarity, PBDEs are believed to bind competitively to thyroid hormone-transporting proteins, thereby disrupting the normal transport of T4 to target tissues (Marsh, Bergman, Bladh, Gillner, & Jakobsson, 1998).

Chapter | 9

Endocrine Disruption of Reproduction in Birds

There are emerging data on the effects of PBDEs in avian species. This class of compounds has become ubiquitous in the environment due to their efficacy as flame retardants; these chemicals are also persistent in the environment. Only a few dosing studies in birds have examined developmental and reproductive effects of environmentally relevant concentrations of PBDEs (Fernie et al. 2005a; 2005b; 2006; 2008). In these studies, American kestrels exposed in ovo and via diet were larger, gained weight more quickly, and ate more food compared to their unexposed counterparts. Fledgling kestrels exposed to PBDEs had lower T4, plasma retinol, hepatic retinol, and retinyl palmitate concentrations, all of which are indicative of metabolic function. Polybrominated diphenyl ether exposure also induced hepatic oxidative stress, but did not affect hatching or fledging success. Exposure to PBDEs did not affect triiodothyronine (T3) concentrations or thyroid-gland structure. Bursal and spleen somatic indices were smaller in PBDE-exposed birds and these birds exhibited a reduced antibody response and a greater phytohemagglutinin (PHA) skin response, which is mediated by T-cell-mediated immunity. This study indicates that environmentally relevant concentrations of PBDEs may induce sublethal effects on growth, immune function, and thyroid hormone and vitamin A concentrations in wild birds. Changes in reproductive behavior (e.g., fewer bonding behaviors, less copulation, and less time spent in nest box) occur in reproductively active adult American kestrels fed a commercial penta-BDE formulation. McKernan, Rattner, Hale, and Ottinger (2009) evaluated survival, pipping, and hatching success as well as sublethal biochemical, endocrine, and histological endpoints in chicken, mallard duck, and American kestrel hatchlings following in-ovo exposure to environmentally relevant concentrations of PBDEs. These concentrations of PBDEs induced ethoxyresorufinO-dealkylase activity, and reduced the size and number of follicles in the bursa of Fabricius in chicken hatchlings, but not in other species. Pipping and hatching success decreased in American kestrels receiving 10 and 20 mg PBDE-71/g egg, but these endpoints were unaffected in chickens and mallard ducks. Glandular T4 concentrations were unaffected at all doses in all species. The lowest observable effect level on pipping and hatching success was 1.8 mg total PBDEs/g egg, which approaches concentrations detected in the eggs of free-ranging birds. As some PBDE congeners are still increasing in the environment, the embryotoxic effects observed following PBDE administration at very low doses are a cause for concern. Compared to circulating concentrations of T4 and T3 or thyroid weight, glandular T4 content is a more sensitive indicator of decreased thyroid function in studies of perchlorate and PCB toxicity in birds (McNabb & Fox,

253

2003; McNabb, Jang, & Larsen, 2004; McNabb, Larsen, & Pooler, 2004). Toxic effects of PBDEs on thyroid function are incompletely known. In laboratory studies in mice and rats, PBDE exposure decreases plasma T4 concentrations (Fowles, Fairbrother, Baecher-Steppan, & Kerkvliet, 1994; Hallgren, Sinjari, Hakansson, & Darnerud, 2001; Zhou, Ross, De Vito, & Crofton, 2001), may alter plasma transport of T4 through competitive binding mechanisms (Hallgren & Darnerud, 2002), and induces enzymatic degradation of thyroid hormones through induction of hepatic T4-glucuronidation activity (Zhou et al., 2001; Richardson et al., 2008). Fernie et al. (2005b) suggested that PBDE exposure results in slightly lower plasma T4 concentrations in American kestrels, although no alterations in thyroid histology were observed. The detection of high concentrations of PBDEs in wild birds and eggs indicates that further work on the potential effects of PBDEs on the thyroid system is warranted.

8. OTHER CONSIDERATIONS: EFFECTS OF ENDOCRINE-DISRUPTING CHEMICALS (EDCs) ON IMMUNE FUNCTION AND STRESS RESPONSES It is clear that the roles of steroid hormones in the differentiation of sexually dimorphic endocrine, neuroendocrine, and behavioral responses vary in precocial and altricial birds. However, in both precocial and altricial birds, the pre- and perihatch steroid hormones impact the development of key components of the immune system. Neuroendocrine and immune systems interact, possibly via gonadal steroid receptors on bursal epithelial cells and glucocorticoid receptors on bursal B cells (Sullivan & Wira, 1979; Marsh & Scanes, 1994). Sex differences in immune responses have been observed across birds and other mammals (Zuk, 1990). In general, females tend to be more resistant to infection, have a greater ability to reject skin grafts, and are more efficient in antibody production in response to antigen challenges than males (Novotny et al., 1983). Higher levels of androgens in males appear to be immunosuppressive, whereas estrogens enhance immune responses in females (Novotny et al., 1983). Higher levels of androgens also reduce liver production of plasma proteins that bind corticosterone (CORT), resulting in higher concentrations of circulating unbound corticosteroids and resultant alterations in immune functions. Corticosteroids directly affect the immune system of all vertebrates by altering cytokine production and decreasing T-cell production. A primary function of the hypothalamicepituitaryeadrenal (HPA) axis is the stress response. As such, one of its primary functions is to respond to

254

immediate threats to survival. In doing so, more glucose and amino acids are released into the circulation to provide energy to muscles. In contrast, all ‘nonessential’ systems are suppressed, including reproduction and immune function. Species with chronically elevated stress levels, as might occur with EDC exposure, are likely to suffer from allostatic load (McEwen & Wingfield, 2003), whereby an altered stress state results in greater energy expenditure than intake and frequently is followed by pathophysiology (see Chapter 5, this volume for additional discussion of stress and reproduction). Tree swallow nestlings and adult females exposed to PCBs (Franceshini, Custer, Custer, Reed, & Romero, 2008) showed a marked reduction in their stress response. Circulating levels of CORT for adult females showed an inverse-U dose-response, such that those exposed to the highest PCB concentrations had lower circulating CORT concentrations that those exposed to midrange PCB concentrations. Nestling CORT concentrations, however, were correlated positively with PCB exposure. On examination of the nestling stress response itself, through a dexamethasone (a synthetic glucocorticoid) suppression test followed by a corticotropin (ACTH) challenge, it was found that PCB-exposed nestlings are incapable of mounting a full stress response.. Tree swallow and eastern bluebird nestlings exposed to pesticides and persistent p,p’DDE showed differing stress responses (Mayne, Martin, Bishop, & Boermans, 2004). Following a 10-minute restraint stress, tree swallows from exposed areas had higher corticosteroid levels, whereas in bluebirds this response was reduced with exposure. Tree swallow nestlings exposed to polychlorinated dibenzofuran (PCDF) had plasma CORT concentrations correlated positively with PCDF exposure and exhibited an altered stress response (Martinovic et al., 2003).

9. CONCLUSIONS Discernment of the consequences of early exposure to EDCs and their primary mechanisms of action has significance for wild and domestic birds. There are conserved mechanisms found across classes of vertebrates and these effects point to similarities in the target tissues and modes of action. A hallmark of EDC action is the sublethal impairment of functional components of physiological systems, including reproductive, immune, and stress response. All these physiological systems interact and ultimately can impact the fitness of the organism. As the actions of EDCs are complex and varied across vertebrates, focused studies using current tools are critical in order to understand mechanisms of action and potential short- and long-term impacts. Once these mechanisms have been characterized, comparisons across species and classes of vertebrate will reveal the bases of

Hormones and Reproduction of Vertebrates

differential sensitivities and life stages that may be more vulnerable.

ACKNOWLEDGEMENTS This work has been supported by EPA grant numbers R826134010 (Star Grant) and R-82877801; Battelle contract for EPA-EDSTAC validation studies, NRI #92-37203 and NSF #9817024; MAES, University of Maryland, College Park; and the Fish and Wildlife Service. The authors also appreciate our wonderful collaborators and students, who have made these studies possible, including Ashley Barton, Kasen Whitehouse, Barnett Rattner, Mark Jaber, Joanne Beavers, Sara Pollack, Brandon Sitzmann, Kara Duffy, Anna Schlappal, Marci Strauss, Kimya Davani, and Krisztina Larson.

ABBREVIATIONS 5a-DHT ACTH AhR AVT CNS CORT DDA DDD DDE DDT DES E E2 EAP EDC EDSTAC EPA ERb GnRH-I HPA HPG ME MXC P450aro P450C17 PBDE PCB PCB-77 PCDF PHA POA-SL POLS ppm T T3 T4 TbA TCDD Vtg

5a-dihydrotestosterone Corticotropin Arylhydrocarbon receptor Arginine vasotocin Central nervous system Corticosterone 2,2-bis(4-chlorophernyl)-acetic acid Dichlorodiphenyldichloroethane Dichlorodiphenyldichloroethylene Dichlorodiphenyltrichloroethane Diethylstilbestrol Embryonic day 17b-estradiol Endocrine-active phytochemical Endocrine-disrupting chemical Endocrine Disruptor Screening and Testing Advisory Committee Environmental Protection Agency Estrogen receptor-b Gonadotropin-releasing hormone-I Hypothalamicepituitaryeadrenal Hypothalamicepituitaryegonadal Median eminence Methoxychlor Aromatase enzyme 17a-hydroxylase Polybrominated diphenyl ether Polychlorinated biphenyl 3,3’,4, 4’-tetrachlorobiphenyl Polychlorinated dibenzofurans Phytohemagglutinin Preoptic-septal region Preoptic lateral septal Parts per million Testosterone Triiodothyronine Thyroxine Trenbolone acetate 2,3,7,8-tetrachlorodibenzodioxin Vitellogenin

Chapter | 9

Endocrine Disruption of Reproduction in Birds

REFERENCES Abdelnabi, M. A., Bakst, M. R., Woods, J. E., & Ottinger, M. A. (2000). Plasma 17 b estradiol levels and ovarian interstitial cell structure in embryonic Japanese quail. Poultry Sci., 79, 564e567. Adkins, E. K. (1979). Effect of embryonic treatment with estradiol or testosterone on sexual differentiation of the quail brain. Neuroendocrinology, 29, 178e185. Adkins-Regan, E., Abdelnabi, M., Mobarak, M., & Ottinger, M. A. (1990a). Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata). Gen. Comp. Endocrinol., 78, 93e109. Adkins-Regan, E., Abdelnabi, M., Mobarak, M., & Ottinger, M. A. (1990b). Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata). Gen. Comp. Endocrinol., 78(1), 93e109. Adkins-Regan, E. K., Ottinger, M. A., & Park, J. (1995). Maternal transfer of estradiol to egg yolks alters sexual differentiation of avian offspring. J. Exp. Zool., 271, 466e470. Ahmed, M. M., & Walker, C. H. (1979). The metabolism of DDT in vivo by the Japanese quail (Coturnix coturnix japonica). Pesticide Biochem. Physiol., 10(1), 40e48. Alonso, K. R., Peden-Adams, M. M., Liu, J. Y., Charbonneau, C., Henshel, D., & Dickerson, R. L. (1998). Effects of in-ovo exposure to 2,3,7,8-TCDD on F1 generation adult chickens (Gallus gallus). Chemosphere, 37, 1873e1883. Andersson, P. L., Van der Burght, A. S. A. M., Van den Berg, M., & Tysklind, M. (2000). Multivariate modeling of polychlorinated biphenyl-induced CYP1A activity in hepatocytes from three different species: ranking scales and species differences. Environ. Toxicol. Chem., 19(5), 1454e1463. Ankley, G., Mihaich, E., Stahl, R., Tillitt, D., Colborn, T., McMaster, S., et al. (1997). Overview of a workshop on screening methods for detecting potential (anti-) estrogenic/androgenic chemicals in wildlife. Environ. Toxicol. Chem., 17(1), 68e87. Anthony, R. G. (1993). Environmental contaminants in bald eagles in the Columbia River estuary. J. Wildlife Mngmt., 57(1), 10e19. Anway, M. D., & Skinner, M. K. (2008). Epigenetic programming of the germ line: effects of endocrine disruptors on the development of transgenerational disease. Reprod. Biomed. Online, 16(1), 23e25. Arnold, A. P., Wade, J., Grisham, W., Jacobs, E. C., & Campagnoni, A. T. (1996). Sexual differentiation of the brain in songbirds. Dev. Neurosci., 18, 124e136. Aste, N., Panzica, G. C., Aimar, P., Viglietti-Panzica, C., Foidart, N., & Balthazart, J. (1996). Morphometric studies demonstrate that aromataseimmunoreactive cells are the main target of androgens and estrogens in the quail medial preoptic nucleus. Exper. Brain Res., 101, 241e252. Axelsson, J., Mattsson, A., Brunstrom, B., & Halldin, K. (2007). Expression of estrogen receptor-alpha and -beta mRNA in the brain of Japanese quail embryos. Develop. Neurobiol., 67(13), 1742e1750. Balthazart, J., & Adkins-Regan, E. (2002). Sexual differentiation of brain and behavior in birds. In D. Pfaff, A. Arnold, A. Etgen, & R. Rubin (Eds.), Hormones and Behavior in Higher Vertebrates, Vol 4 (pp. 223e302). Academic Press. Balthazart, J., & Ottinger, M. A. (1984). 5ß-reductase activity in the brain and cloacal gland of male and female embryos in the Japanese quail (Coturnix coturnix japonica). J. Endocrinol., 102, 77e81. Barron, M. G., Galbraith, H., & Beltman, D. (1995). Comparative reproductive and developmental toxicology of PCBs in birds. Comp. Biochem. Physiol., 112C, 1e14.

255

Becker, P. H., Schuhmann, S., & Koepff, C. (1993). Hatching failure in common terns (Sterna hirundo) in relation to environmental chemicals. Environ. Pollut., 79, 207e213. Bennett, R. S., Bentley, R., Shiroyama, T., & Bennett, J. K. (1990). Effects of the duration and timing of dietary methyl parathion exposure on bobwhite reproduction. Environ. Toxicol. Chem., 7, 1473e1480. Berg, C., Halldin, K., Brunstrom, B., & Brandt, I. (1998). Methods for studying xenoestrogenic effects in birds. Tox. Lett., 102-103, 671e676. Berg, C., Halldin, K., Fridolfsson, A.-K., Brandt, I., & Brunstrom, B. (1999). The avian egg as a test system for endocrine disrupters: effects of dietylstilbestrol and ethynylestradiol on sex organ development. Science Total Environ., 233, 57e66. Berger, P. J., Negus, N. C., & Rowsemitt, C. N. (1987). Effect of 6-methoxybenzoxazolinone on sex ratio and breeding performance in Microtus montanus. Biol. Reprod., 36, 255e260. Bern, H. A. (1992a). Diethylstilbesrol (DES) syndrome: Present status of animal and human studies in Hormonal Carcinogenesis: Proceedings of the first International Symposium. In J. J. Li, S. Nandi, & S. A. Li (Eds.) New York, NY: Springer-Verlag. Bern, H. A. (1992b). The fragile fetus. Chemically Induced Alterations in Sexual and Functional Development: The Wildlife/Human Connection. In T. Colborn, & Clement, C. Princeton (Eds.). (pp. 9e16). Princeton Scientific Publishing. Beyer, A., & Biziuk, M. (2009). Environmental fate and global distribution of polychlorinated biphenyls. Rev. Environ. Contam. Toxicol., 201, 137e158. Bisenius, E. S., Veeramachaneni, D. N., Sammonds, G. E., & Tobet, S. (2006). Sex differences and the development of the rabbit brain: effects of vinclozolin. Biol. Reprod., 75(3), 469e476. Bishop, C. A., Mahony, N. A., Trudeau, S., & Pettit, K. E. (1999). Reproductive success and biochemical effects in tree swallows (Tachycineta bicolor) exposed to chlorinated hydrocarbon contaminants in wetlands of the great lakes and St. Lawrence River Basin, USA and Canada. Environ. Toxicol. Chem., 18, 263e271. Bortolotti, G. R., Fernie, K. J., & Smits, J. E. (2003a). Carotenoid concentration and coloration of American Kestrels (Falco sparverius) disrupted by experiments exposure to PCBs. Funct. Ecol., 17, 651e657. Bortolotti, G. R., Smits, J. E., & Bird, D. M. (2003b). Iris colour of American kestrels varies with age, sex, and exposure to PCBs. Biochem. Physiolog. Zool., 76, 99e104. Bosveld, A. T. C., & Van den Berg, M. (1994). Effects of polychlorinated biphenyls, dibenzo-p-dioxins and dibenzofurans on fish-eating birds. Environ. Rev., 2, 147e166. Brandt., I., Berg., C., Halldin., K., & Brunstro¨m., B. (1998). Developmental and reproductive toxicity of persistent environmental pollutants. Archives Toxicol., Suppl., 20, 111e119. Brunstrom, B., Axelsson, J., & Halldin, K. (2003). Effects of endocrine modulators on sex differentiation in birds. Ecotoxicology, 12(1-4), 287e295. Cheek, A. O., Vonier, P. M., Oberdorster, E., Burow, B. C., & McLachlan, J. A. (1998). Environmental signaling: a biological context for endocrine disruption. Environ. Health Perspect., 106(Suppl 1), 5e10. Chen, Y., Sible, J. C., & McNabb, F. M. (2008). Effects of maternal exposure to ammonium perchlorate on thyroid function and the expression of thyroid-responsive genes in Japanese quail. Gen. Comp. Endocrinol., 159(2-3), 196e207.

256

Colborn, T., & Clement, C. (1992). Chemically induced alterations in sexual and functional development: The wildlife/human connection.. In Adv Modern Environ Tox 21 Princeton, NJ: Princeton Scientific Publishing Co., Inc. Colborn, T., Vom Saal, F. S., & Soto, A. M. (1993). Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health Perspect., 101(5), 378e384. Colborn, T., Smolen, M. J., & Rolland, R. (1998). Environmental neurotoxic effects: the search for new protocols in functional teratology. Toxicol. Industr. Health, 14(1-2), 9e23. Conley, A. J., Elf, P., Corbin, C. J., Dubowsky, S., Fivizzani, A., & Lang, J. W. (1997). Yolk steroids decline during sexual differentiation in the alligator. Gen. Comp. Endocrinol., 107, 191e200. Crews, D., Willingham, E., & Skipper, J. K. (2000). Endocrine disruptors: present issues, future directions. Quart. Rev. Biol., 75(3), 243e260. Csaba, G., Karabeivos, C., & Dallo, J. (1993). Fetal and neonatal action of a polycyclic hydrocarbon (benzpyrene) or a synthetic steroid hormone (allylestrenol) as reflected by the sexual behaviour of adult rats. J. Devel. Physiol., 19(2), 67e70. Custer, T. W., Custer, C. M., Hines, R. K., Gutreuter, S., Stromborg, K. L., Allen, P. D., et al. (1999). Organochlorine contaminants and reproductive success of double-crested cormorants from Green Bay, Wisconsin, USA. Environ. Toxicol. Chem., 18(6), 1209e1217. Custer, T. W., Custer, C. M., & Hines, R. K. (2002). Dixoins and congener-specific polychlorinated biphenyls in three avian species from the Wisconsin River, Wisconsin. Environ. Poll., 119, 1e11. Darnerud, P. O. (2003). Toxic effects of brominated flame retardants in man and in wildlife. Environ. Internl., 29, 841e853. Elbrecht, A., & Smith, R. G. (1992). Aromatase enzyme activity and sex determination in chickens. Science, 255, 467. Elliott, J. E., Kennedy, S. W., & Lorenzen, A. (1997). Comparative toxicity of polychlorinated biphenyls to Japanese quail (Coturnix c. japonica) and American kestrels. J. Tox. Environ. Health, 51, 57e75. EDSTAC, Endocrine Disruptor Screening and Testing Advisory Committee (EDSTAC) Final Report. Environmental Protection Agency, 1998, Washington, DC, USA. http://www.epa.gov/endo/ pubs/edspoverview/finalrpt.htm Eroschenko, V. P., Amstislavsky, S. Y., Schwabel, H., & Ingermann, R. L. (2002). Altered behaviors in male mice, male quail, and salamander larvae following early exposures to the estrogenic pesticide methoxychlor. Neurotox. Teratol., 24(1), 29e36. Fairbrother, A. (2000). Comparative aspects of estrogen functions and measurements in oviparous and vivparous vertebrates. Human Ecologic. Risk Assess., 6(1), 73e102. Fairbrother, A., Landis, W. G., Dominquez, S., Shiroyama, T., Buchholz, P., Roze, M. J., et al. (1998). A novel nonmetric multivariate approach to the evaluation of biomarkers in terrestrial field studies. Ecotoxicology, 7, 1e10. Fernie, K. J., Mayne, G., Shutt, L. J., Pekarick, C., Grasman, K. A., Letcher, R. J., et al. (2005a). Evidence of immunomodulation in nestling American kestrels (Falco sparverius) exposed to environmentally relevant PBDEs. Environ. Poll., 138, 485e493. Fernie, K. J., Shutt, J. L., Letcher, R. J., Ritchie, J. I., Sullivan, K., & Bird, D. M. (2008). Changes in reproductive courtship behaviors of adult American kestrels (Falco sparverius) exposed to environmentally relevant levels of the polybrominated diphenyl ether mixture, DE-71. Toxicol. Sci., 102, 171e178.

Hormones and Reproduction of Vertebrates

Fernie, K. J., Shutt, L. J., Mayne, G., Hoffman, D. J., Letcher, R. J., Droullard, K. G., et al. (2005b). Exposure to polybrominated diphenyl ethers (PBDEs): changes in thyroid, vitamin A, glutathione homeostasis, and oxidative stress in American kestrels (Falco sparverius). Tox. Sci., 88, 375e383. Fernie, K. J., Shutt, L. J., Ritchie, J. L., Letcher, R. J., Droullard, K. G., & Bird, D. M. (2006). Changes in the growth, but not the survival, of American kestrels (Falco sparverious) exposed to environmentally relevant polybrominated diphenyl ethers. J. Tox. Environ. Health, 69, 1541e1554. Fisher, S. A., Bortolotti, G. R., Fernie, K. J., Bird, D. M., & Smits, J. E. (2006). Behavioral variation and its consequences during incubation for American kestrels exposed to polychlorinated biphenyls. Ecotox. Environ. Saf., 63(2), 226e235. Foidart, A., Harada, N., & Balthazart, J. (1994). Effects of steroidal and non steroidal aromatase inhibitors on sexual behavior and aromatased immunoreactive cells. Brain Res., 657, 105e123. Fowles, J. R., Fairbrother, A., Baecher-Steppan, L., & Kerkvliet, N. I. (1994). Immunologic and endocrine effects of the flame-retardant pentabromodiphenyl ether (DE-71) in C57BL/6J mice. Toxicology, 86, 49e61. Fowles, J. R., Fairbrother, A., Trust, K. A., & Kerkvliet, N. I. (1997). Effects of aroclor 1254 on the thyroid gland, immune function, and hepatic cytochrome P450 activity in mallards. Environ. Res., 75, 119e129. Fox, G. A. (1992). Epidemiological and pathobiological evidence of contaminant-induced alterations in sexual development in free-living wildlife. In T. Colborn, & C. Clement (Eds.), Chemically-induced alterations in sexual and functional development: the wildlife / human connection (pp. 147e158). Princeton, NJ: Princeton Scientific Publishing Co., Inc. Fox, G. A., Gilman, A. P., Peakall, D. B., & Anderka, F. W. (1978). Behavioral abnormalities of nesting Lake Ontario herring gulls. J. Wildl. Mngmt., 42(3), 477e483. Franseschini, M. D., Custer, C. M., Custer, T. W., Reed, J. M., & Romero, L. M. (2008). Corticosterone stress response in tree swallows nesting near polychlorinated biphenyl- and dioxin-contaminated rivers. Environ. Toxicol. Chem., 27. 2326-2311. Freking, F., Nazairians, T., & Schlinger, B. A. (2000). The expression of the sex steroid-synthesizing enzymes CYP11A1, 3-HSD, CYP17, and CYP19 in gonads and adrenals of adult and developing zebra finches. Gen. Comp. Endocrinol., 119, 140e151. French, M. C., & Jeffries, D. J. (1969). Degradation and disappearance of ortho, para, isomer of technical DDT in living and dead avian tissues. Science, 165, 914e916. Fry, M. (1995). Reproductive effects in birds exposed to pesticides and industrial chemicals. Environ. Health Perspect, 103(Suppl. 7), 165e171. Gao, C., Abou-Nasr, R., & Norgren, R. B., Jr. (1996). Subpopulations of migrating neurons express different levels of LHRH in quail and chick embryos. Dev. Brain Res., 91, 237e244. Gauthier, L., Hebert, C. E., Weseloh, D. V. C., & Letcher, R. J. (2008). Dramatic changes in the temporal trends of polybrominated diphenyl ethers (PBDEs) in herring gull eggs from the Laurentian Great Lakes: 1982e2006. Environ. Sci. Technol., 42, 1524e1530. Gee, J. M., Craig-Veit, C. B., & Millam, J. R. (2004). Posthatch methoxychlor exposure adversely affects reproduction of adult zebra finches, Taeniopygla guttata. Bull. Environ. Contam. Toxicol., 73(4), 607e612. Giesy, J. P., Ludwig, J. P., & Tillitt, D. E. (1994). Deformities in birds of the Great Lakes region. Environ. Sci. Technol., 28(3), 128.

Chapter | 9

Endocrine Disruption of Reproduction in Birds

Gildersleeve, R. P., Tilson, H. A., & Mitchell, C. L. (1985). Injection of diethylstilbestrol on the first day of incubation affects morphology of sex glands and reproductive behavior of Japanese quail. Teratology, 31(1), 101e109. Glick, B. (1991). Historical perspective: the bursa of Fabricius and its influence on B-cell development, past and present. Vet. Immunol. Immunopathol., 30(1), 3e12. Golden, N. H., Rattner, B. A., McGowan, P. C., Parsons, K. C., & Ottinger, M. A. (2003). Concentrations of metals in feathers and blood of nestling black-crowned night-herons (Nycticorax nycticorax) in Chesapeake and Delaware Bays. Bull. Environ. Contam. Toxicol., 70(2), 385e393. Gore, A. C. (2002). Organochlorine pesticides directly regulate gonadotropin-releasing hormone gene expression and biosynthesis in the GT1-7 hypothalamic cell line. Mol. Cell. Endocrinol., 192(1-2), 157e170. Gore, A. C. (2008). Neuroendocrine systems as targets for environmental endocrine disrupting chemicals. Fertil. Steril., 89(2 suppl), e103ee108. Gore, A. C., Wu, T. J., Oung, T., Lee, J. B., & Woller, M. J. (2002). A novel mechanism for endocrine-disrupting effects of polychlorinated biphenyls: direct effects on gonadotropin-releasing hormone neurons. Neuroendocrinol., 14(10), 814e823. Grasman, K. A., & Fox, G. A. (2001). Associations between altered immune function and organochlorine contamination in young Caspian terns (Sterna caspia) from Lake Huron, 1997e1999. Ecotoxicology, 10, 101e114. Grasman, K. A., Scanlon, P. F., & Fox, G. A. (1998). Reproductive and physiological effects of environmental contaminants in fish-eating birds of the Great Lakes: a review of historical trends. Environ. Monitor. Assess., 53(1), 117e145. Gray, L. E., Jr., & Kelce, W. R. (1996). Latent effects of pesticides and toxic substances on sexual differentiation of rodents. Toxicol. Ind. Health, 12(3-4), 515e531. Gray, L. E., Jr., Ostby, J., Wolf, C., Lambright, C., & Kelce, W. (1998). The value of mechanistic studies in laboratory animals for the prediction of reproductive effects in wildlife: Endocrine effects on mammalian sexual differentiation. Environ. Toxicol. Chem., 17, 109e118. Guellati, M., Ramade, F., Le Nguyen, D., Ibos, F., & Bayle, J. D. (1991). Effects of early embryonic bursectomy and opotheapic substitution on the functional development of the adrenocorticotropic axis. J. Devel. Physiol., 15(6), 357e363. Guillette, L. J., Crain, D. A., Gunderson, M. P., Kools, S. A. E., Milnes, M. R., Orlando, E. F., et al. (2000). Alligators and endocrine disrupting contaminants: a current perspective. Amer. Zool., 40, 438e452. Gould, J. C., Cooper, K. R., & Scanes, C. G. (1999). Effects of polychlorinated biphenyls on thyroid hormones and liver type I monodeiodinase in the chick embryo. Ecotoxicol. Environ. Saf., 43, 195e203. Halldin, K., Axelsson, J., & Brunstrom, B. (2005). Effects of endocrine modulators on sexual differentiation and reproductive function in male Japanese quail. Brain Res. Bull., 65(3), 211e218. Halldin, K., Berg, C., Brandt, I., & Brunstrom, B. (1999). Sexual behavior in Japanese quail as a test end point for endocrine disruption: effects of in-ovo exposure to ethinylestradiol and diethylstilbestrol. Environ. Health Perspect., 107(11), 861e866.

257

Hallgren, S., & Darnerud, P. O. (2002). Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and chlorinated paraffins (CPs) in ratsdtesting interactions and mechanisms for thyroid hormone effects. Toxicology, 177, 227e243. Hallgren, S., Sinjari, T., Hakansson, H., & Darnerud, P. O. (2001). Effects of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) on thyroid hormone and vitamin A levels in rats and mice. Arch. Toxicol., 75, 200e208. Hatano, Y., & Hatano, A. (1994). Influence of polychlorinated biphenyls on the growth of chicken embryos. J. Toxicol. Environ. Health, 42, 357. Head, J. A., Hahn, M. E., & Kennedy, S. W. (2008). Key amino acids in the aryl hydrocarbon receptor predict dioxin sensitivity in avian species. Environ. Sci. Technol., 1(42), 7535e7541. Henshel, D. S., Martin, J. W., Norstrom, R., Whitehead, P., Steeves, J. D., & Cheng, K. M. (1995). Morphometric abnormalities in brains of great blue heron hatchlings exposed in the wild to PCDDs. Environ. Health Perspect., 103(4), 61e66. Hoffman, D. J. (1990). Embryotoxicity and teratogenicity of environmental contaminants to bird eggs. Rev. Environ. Contam. Toxicol., 115, 39. Hoffman, D. J., Rattner, A., Burton, G. A., Jr., & Cairns, J., Jr. (2003). Handbook of Ecotoxicology. CRC Press. Hoogesteiin, A. L., DeVoogd, T. J., Quimby, F. W., De Caprio, T., & Kollias, G. V. (2005). Reproductive impairment in zebra finches (Taeniopygia guttata). Environ. Toxicol. Chem., 24(1), 219e223. Hooper, S. W., Pettigrew, C. A., & Sayler, G. S. (1990). Ecological fate, effects and prospects for the elimination of environmental polychlorinated biphenyls (PCBs). Environ. Toxicol. Chem., 9, 655. Hutchison, J. B., Beyer, C., Hutchison, R. E., & Wozniak, A. (1997). Sex difference in the regulation of embryonic brain aromatase. J. Steroid Biochem. Molec. Biol., 61(3-6), 315e322. Hutchison, J. B., Schumacher, M., & Hutchison, R. E. (1990). Developmental sex differences in brain aromatase activity are related to androgen level. Dev. Brain Res., 57, 198e205. Igushi, T., Watanabe, H., & Katsu, Y. (2007). Toxicogenomics and ecotoxicogenomics for studying endocrine disruption and basic biology. Gen. Comp. Endocrinol., 153(1-3), 25e29. Iwaniuk, A. N., Koperski, D. T., Cheng, K. M., Elliott, J. E., Smith, L. K., Wilson, L. K., et al. (2006). The effects of environmental exposure to DDT on the brain of a songbird: changes in structures associated with mating and song. Behav. Brain Res., 173(1), 1e10. Jacobson, J. L., & Jacobson, S. W. (1996). Prospective, longitudinal assessment of developmental neurotoxicity. Devel. Health Perspect., 104(Suppl 2), 275e283. Johnson, M. S., Ruppert, W. H., Taylor, Packer, B., Watts, K., Byrd, E. F. C., Hurley, M. M., et al. (2005). Toxicological Study No. 87-XE-03N3e05 Assessing the potential environmental consequences of a new energetic metarial: A phased approach. U.S. Army Center for Health Promotion and Preventive Medicine publication; approved for public release and unlimited distribution. Karchner, S. I., Franks, D. G., Kennedy, S. W., & Hahn, M. E. (2006). The molecular basis for differential dioxin sensitivity in birds: role of the aryl hydrocarbon receptor. Proc. Natl. Acad. Sci. USA., 103(16), 6252e6257. Kavlock, R. J., Daston, G. P., DeRosa, C., Fenner-Crisp, P., Gray, L. E., Kaatari, S., et al. (1996). Research needs for the risk assessment of health and environmental effects of endocrine disruptors: a report of the U.S. EPA-sponsored workshop. Environ. Health Perspect., 104 (Suppl 4), 715e740.

258

Klecha, A. J., Genaro, A. M., Gorelik, G., Barreiro Arcos, M. L., Silberman, D. M., Schuman, M., et al. (2006). Integrative study of hypothalamusepituitaryethyroideimmune system interaction: thyroid hormone-mediated modulation of lymphocyte activity through the protein kinase C signaling pathway. J. Endocrinol., 189, 45e55. Korach, K. S., Sarver, P., Cahe, K., McLachlan, J. A., & McKinney, J. D. (1988). Estrogen receptor-binding activity of polychlorinated hydroxybiphenyls: conformationally restricted structural probes. Molec. Pharmacol., 33(1), 120e126. Kortenkamp, A. (2007). Ten years of mixing cocktails: a review of combination effects of endocrine disrupting chemicals. Environ. Health Perspect., 115(suppl 1), 98e105. Kubiak, T. J., Harris, H. J., Smith, L. M., Schwartz, T. R., Stalling, D. L., Trick, J. A., et al. (1989). Microcontaminants and reproductive impairment of the Forster’s tern on Green Bay, Lake Michigand1983. Arch. Environ. Contamin. Toxicol., 18, 706e727. Kuenzel, W. J. (2003). Neurobiology of molt in avian species. Poult. Sci., 82, 981e991. Li, Q., Alston-Mills, B., & Ottinger., M. A. (1991). Avian LHRH during embryonic development: measurement by competitive ELISA with a monoclonal antibody. Gen. Comp. Endocrinol., 82, 444e450. Li, Q., Paciotti, G. F., Tamarkin, L., & Ottinger, M. A. (1994a). LHRH I release from hypothalamic slices measured by specific EIA. Gen. Comp. Endocrinol., 95, 13e24. Li, Q., Tamarkin, L., Levantine, P., & Ottinger, M. A. (1994b). Estradiol and androgen modulate chicken luteinizing hormone-releasing hormone-I release in vitro. Biol. Reprod., 51, 896e903. Lin, F., Wu J Abdelnabi, M. A., Ottinger, M. A., & Guisti, M. M. (2004). Effects of dose and glycosylation on the transfer of genistein into the eggs of Japanese quail (Coturnix japonica). J. Agric. Food Chem., 52, 2397e2403. Lien, R. J., Cain, J. R., & Beasom, S. L. (1987). Effects of dietary and parenteral estrogens on bobwhite reproduction. Poultry Sci., 66, 154e161. Longnecker, M. P., Rogan, W. J., & Lucier, G. (1997). The human health effects of DDT (dichlorodiphenyltrichloroethane) and PCBs (polychlorinated biphenyls) and an overview of organochlorines in public health. Ann. Rev. Public Health, 18, 211e244. Markman, S., Leitner, S., Catchpole, C., Burnsley, S., Miller, C. T., Pascoe, D., et al. (2008). Pollutants increase song complexity and the volume of the brain area HVC in a songbird. PloS ONE, 3(20), e1674. Marsh, G., Bergman, A., Bladh, L. G., Gillner, M., & Jakobsson, E. (1998). Synthesis of p-hydroxybromodiphenyl ethers and binding to the thyroid receptor. Organohalogen Compounds, 37, 305e308. Martinovic, B., Lean, D., Bishop, C., Birmingham., E., Secord, A., & Jock, K. (2003). Health of tree swallow (Tachycineta bicolor) nestlings exposed to chlorinated hydrocarbons in the St. Lawrence River Basin. Part II. Basal and stress plasma corticosteron concentrations. J. Toxicol. Environ. Health A, 66, 2015e2029. Mayne, G. J., Martin, P. A., Bishop, C. A., & Boermans, H. J. (2004). Stress and immune response of nestling tree swallows (Tachycinete bicolor) and eastern bluebirds (Sialia sialis) exposed to non-persistent pesticides and p, p’-dichlorodiphenyldichloroethylene in apple orchards of southern Ontario, Canada. Environ. Toxicol. Chem., 23, 2930e2940. McCarty, J. P., & Secord, A. L. (1999). Reproductive ecology of tree swallows (Tachycineta bicolor) with high levels of polychlorinated biphenyl contamination. Environ. Toxicol. Chem., 18(7), 1433e1439.

Hormones and Reproduction of Vertebrates

McCarty, J. P., & Secord, A. L. (2000). Possible effects of PCB contamination on female color and reproductive success in Hudson River tree swallows. Auk, 117, 987e995. McEwen, B. S., & Wingfield, J. C. (2000). The concept of allostasis in biology and biomedicine. Horm. Behav., 43, 2e15. McKernan, S., Henry, P. F. P., & Ottinger, M. A. (2001). Impact of vinclozolin exposure on Japanese quail reproduction. Environ. Toxicol. Chem., 20(11), 2487e2493. McKernan, M. A., Rattner, B. A., Hale, R. C., & Ottinger, M. A. (2007). Egg incubation position affects toxicity of air cell administered polychlorinated biphenyl 126 (3, 30 , 4, 40 , 5-pentachlorobiphenyl) in chicken (Gallus gallus) embryos. Environ. Toxicol. Chem., 26(12), 2724e2727. McKernan, M. A., Rattner, B. A., Hale, R. C., & Ottinger, M. A. (2009). Toxicity of polybrominated diphenyl ethers (DE-71) in developing chicken (Gallus gallus), mallard (Anas platyrhynchos), and American kestrel (Falco sparverius) embryos and hatchlings. Environ Toxicol Chem. in press. McNabb, F. M. A., & Fox, G. A. (2003). Avian thyroid development in chemically contaminated environments: is there evidence of alterations in thyroid function and development? Evolut. Dev., 5, 76e82. McNabb, F. M. A., Jang, D. A., & Larsen, C. T. (2004a). Does thyroid function in developing birds adapt to sustained ammonium perchlorate exposure? Toxicol. Sci., 82, 106e113. McNabb, F. M. A., Larsen, C. T., & Pooler, P. S. (2004b). Ammonium perchlorate effects on thyroid function and growth in bobwhite quail chicks. Environ. Toxicol. Chem., 23, 997e1003. Millam, J. R., Ottinger., M. A., Craig-Viet, C., Fan, Y., Chaiseha, Y., & El Halawani, M. E. (1998). Multiple forms of GnRH are released from perifused medial basal hypothalamic/preoptic area (MBH/POA) explants in birds. Gen. Comp. Endocrinol., 111, 95e101. Mineau, P., Baril, A., Collins, B. T., Duffe, J., Joerman, G., & Luttik, R. (2001). Pesticide acute toxicity reference values for birds. Rev. Environ. Contam. Toxicol., 170, 13e74. Mineau, P., Boersma, D. C., & Collins, B. (1994). An analysis of avian reproduction studies submitted for pesticide registration. Ecotoxicol. Environ. Safety, 29, 304e329. Munoz, G. R., & Panero, M. A. (2006). Pollution prevention and management strategies for dioxins in the New York/New Jersey harbor. New York, NY: New York Academy of Sciences. Murk, A. J., Leonards, P. E. G., Bulder, A. S., Jones, A. S., Rozemiejer, M. J. C., Denison, M. S., et al. (1997). The calux (chemical-activated luciferase expression) assay adapted and validated for measuring TCDD equivalents in blood plasma. Environ. Toxicol. Chem., 16, 1583e1589. Ness, D. K., Schantz, S. L., & Hansen, L. G. (1994). PCB congeners in the rat brain: selective accumulation and lack of regionalization. J. Toxicol. Environ. Health, 43(4), 453e468. New York Academy of Sciences Harbor Consortium. (2008). Safe harbor: bringing people and science together to improve the New York/New Jersey harbor. New York, NY: New York Academy of Sciences. Nichols, D. J., Daniel, T. C., Moore, P. A., Jr., Edwards, D. R., & Pote, D. H. (1997). Runoff of estrogen hormone 17 b-estradiol from poultry litter applied to pasture. J. Environ. Quality., 26, 1002e1006. Nishikimi, H., Kansaku, N., Saito, N., Usami, M., Ohno, Y., & Shimada, K. (2000). Sex differentiation and mRNA expression of P450c17, P450arom and AMH in gonads of the chicken. Molec. Reprod. Dev., 55, 20e30.

Chapter | 9

Endocrine Disruption of Reproduction in Birds

Norgren, R. B., Jr. (1996). Development of LHRH neurons in the avian embryo. Poultry Avian Biol. Rev., 7(2/3), 163e182. Norstrom, R. J., Simon, M., Moisey, J., Wakeford, B., & Weseloh, D. V. (2002). Geographical distribution (2000) and temporal trends (1981e2000) of brominated diphenyl ethers in Great Lakes herring gull eggs. Environ. Sci. Technol., 36, 4783e4789. Novotny, E. A., Raveche, E. S., Sharrow, S., Ottinger, M. A., & Steinberg, A. D. (1983). Analysis of thymocyte sub-populations following treatment with sex hormones. Clinical Immunology and Immunopathology, 28, 205e217. National Research Council (NRC). (1999). Hormonally Active Agents in the Environment. Washington, D.C, WA. National Academy Press. Orlando, E. F., Kolok, A. S., Binzcik, G. A., Gates, J. L., Horton, M. K., Lambright, C. S., et al. (2004). Endocrine-disrupting effects of cattle feedlot effluent on an aquatic sentinel species, the fathead minnow. Environ. Health Perspect., 112(3), 353e358. Ottinger, M. A. (1998). Male reproduction: testosterone, gonadotropins, and aging. In C. V. Mobbs, & P. R. Hof (Eds.), Functional Endocrinology of Aging, Vol. 29 (pp. 105e126). Basel, Germany: Interdiscipl Top Gerolotol, Karger. Ottinger, M. A., & Abdelnabi, M. A. (1997). Neuroendocrine systems and avian sexual differentiation. Amer. Zool., 37, 514e523. Ottinger, M. A., Abdelnabi, M. A., Henry, P. F. P., McGary, S., Thompson, N., & Wu, J. (2001b). Neuroendocrine and behavioral implications of endocrine disrupting chemicals in quail. Horm. Behav., 40, 325e383. Ottinger, M. A., Abdelnabi, M., Quinn, M. J., Jr., Goldern, N., Wu, J., & Thompson, N. (2002). Reproductive consequences of EDCs in birds: what do laboratory effects mean in field species. Neurotoxicol. Teratol., 24(1), 17e28. Ottinger, M. A., & Brinkley, H. J. (1978). The relationship of testosterone and sexual behavior during maturation of the male Japanese quail. Horm. Behav., 11, 174e182. Ottinger, M. A., & Bakst, M. R. (1981). Peripheral androgen concentrations and testicular morphology in embryonic and young male Japanese quail. Gen. Comp. Endocrinol., 43, 170e177. Ottinger, M. A., & Brinkley, H. J. (1979a). The ontogeny of crowing and copulatory behavior in Japanese quail. Behav. Proc., 4, 43e47. Ottinger, M. A., & Brinkley, H. J. (1979b). Testosterone and sex-related morphology during maturation of the male Japanese quail. Biol. Reprod., 20, 905e909. Ottinger, M. A., Pitts, S., & Abdelnabi, M. A. (2001a). Steroid hormones during embryonic development in Japanese quail: plasma, gonadal, and adrenal levels. Poultry Sci., 80, 795e799. Ottinger, M. A., Thompson, N., Viglietti-Panzica, C., & Panzica, G. C. (1997). Neuroendocrine regulation of GnRH and behavior during aging in birds. Brain Res. Bullet., 44(4), 471e477. Ottinger, M. A., & Vom Saal, F. S. (2002). In D. Pfaff, A. Arnold, A. Etgen, & R. Rubin (Eds.), Impact of environmental endocrine disruptors on sexual differentiation in birds and mammals, Vol 4 (pp. 325e383). Academic Press. Ottinger, M. A., Abdelnabi M Li, Q., Chen, K., Thompson, N., Harada, N., & Viglietti-Panzica Panzica, G. C. (2004). The Japanese quail: a model for studying reproductive aging of hypothalamic systems. Experimental Gerontology, 39, 1679e1693. Ottinger, M. A., Wu, J. M., Hazelton, J. L., Abdelnabi, M. A., Thompson, N., Quinn, M. J., Jr., et al. (2005). Assessing the consequences of the pesticide methoxychlor: neuroendocrine and behavioral

259

measures as indicators of biological impact of an estrogenic environmental chemical. Brain Rese. Bull., 65(3), 199e209. Ottinger, M. A. (2007). Neuroendocrine aging in birds: comparing lifespan differences and conserved mechanisms. Special issue of Aging Research Reviews entitled: Genetics of Aging in Vertebrates, 6(1), 46e53. Ottinger, M. A., Lavoie, E. T., Abdelnabi, M., Quinn, M. J., Jr., Marcell, A., & Dean, K. (2009a). An overview of dioxin-like compounds, PCB, and pesticide exposures associated with sexual differentiation of neuroendocrine systems, fluctuating asymmetry, and behavioral effects in birds. J. Envir. Sci. Health C Environ. Carcinog. Ecotoxicol. Rev., 27(4), 286e300. Ottinger, M. A., Lavoie, E. T., Thompson, N., Bohannon, M., Dean, K., & Quinn, M. J., Jr. (2009b). Is the gonadotropin releasing hormone system vulnerable to endocrine disruption in birds? Gen. Comp. Endocrinol., 163, 104e108. Owens, I. P. F., & Short, R. V. (1995). Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. TREE, 10, 44e47. Panzica, G. C., Garcia-Ojeda, E., Viglietti-Panzica, C., Aste, N., & Ottinger, M. A. (1997). Role of testosterone in the activation of sexual behavior and neuronal circuitries in the senescent brain. In G. Filogamo et al. (Eds.), Brain Plasticity (pp. 237e287). New York, NY: Plenum Press. Panzica, G. C., Garcia-Ojeda, E., Viglietti-Panzica, C., Thompson, N. E., & Ottinger, M. A. (1996). Testosterone effects on vasotocinergic innervation of sexually dimorphic medial preoptic nucleus and lateral septum during aging in male quail. Brain Res., 712, 190e198. Panzica, G. C., Viglietti-Panzica, C., Mura, E., Quinn, M. J., Jr., Palanza, P., & Ottinger, M. A. (2007). Effects of xenoestrogens and xenoandrogens on the differentiation of behaviorally relevant neural circuits. Frontiers in Neuroendocrinology, 28(4), 179e200. Payne, R. B. (1972). Mechanisms and control of molt. In D. S. Farner, & J. R. King (Eds.), Avian Biology (pp. 103e155). New York, NY: Academic Press. Perrin, F. M. R., Stacey, S., Burgess, A. M. C., & Mittwoch, U. (1995). A quantitative investigation of gonadal feminization by diethylstilboestrol of genetically male embryos of the quail. Coturnix coturnix japonica. J. Reprod. Fert., 103, 223e226. Quinn, M. J., Jr., French, J. B., McNabb, F. M. A., & Ottinger, M. A. (2002). The effects of polychlorinated biphenyls (aroclor 1242) on thyroxine, estradiol, molt, and plumage characteristics in the American kestrel (Falco sparverius). Environ. Toxicol. Chem., 21, 1417e1422. Quinn, M. J., Jr., French, J. B., McNabb, F. M. A., & Ottinger, M. A. (2005). The role of thyroxine on the production of plumage in the American kestrel (Falco sparverius). J. Raptor Res., 39, 84e88. Quinn, M. J., Jr., McKernan, M., Lavoie, E., & Ottinger, M. A. (2007). Immunotoxicity of trenbolone acetate in Japanese quail. J. Toxicol. Environ. Health, Part A., 70(1), 88e93. Quinn, M. J., Jr., Summitt, C. L., & Ottinger, M. A. (2008). Consequences of in ovo exposure to p,p’-DDE on reproductive development and function in Japanese quail. Hormones and Behavior, 53(1), 153e249. Ralph, C. L. (1969). The control of color in birds. Am. Zool., 9, 521e530. Rattner, B. A., & Ottinger, M. A. (1984). Reduced plasma LH concentration in quail exposed to the organophosphorus insecticide parathion. J. Steroid Biochem., 20(62), 1568.

260

Rattner, B. A., Melancon, M. J., Custer, T. W., Hothem, R. L., King, K. A., LeCaptain, L. J., et al. (1993). Biomonitoring environmental contamination with pipping black-crowned night heron embryos: induction of cytochrome P450. Environ. Toxicol. Chem., 12(9), 1719. Rattner, B. A., Pearson, J. L., Golden, N. H., Cohen, J. B., Erwin, R. M., & Ottinger, M. A. (2000). Contaminant exposure and effects: terrestrial vertebrates database: trends and data gaps for Atlantic coast estuaries. Environmental Monitoring and Assessment, 63, 131e142. Richardson, V. M., Staskal, D. F., Ross, D. G., Dilberto, J. J., DeVito, M. J., & Birnbaum, L. S. (2008). Possible mechanisms of thyroid hormone disruption in mice by BDE-47, a major polybrominated diphenyl ether congener. Toxicol. Appl. Pharmocol., 226, 244e250. Rissman, E. F., Ascenzi, M., Johnson, P., & Adkins-Regan, E. (1984). Effect of embryonic treatment with oestradiol benzoate on reproductive morphology, ovulation, and oviposition and plasma LH concentrations in female quail (Coturnix coturnix japonica). J. Reprod. Fert., 71, 411e417. Ronis, M. J. J., Ingelman-Sundberg, M., & Badger, T. M. (1994). Induction, suppression and inhibition of multiple hepatic cytochrome p450 isozymes in the male rat and bobwhite quail (Colinus virginianus) by ergosterol biosynthesis inhibiting fungicides (EBIFs). Biochem. Pharmacol., 48(10), 1953e1965. Schantz, S. L. (1996). Developmental neurotoxicity of PCBs in humans: what do we know and where do we go from here? Neurotoxicol. Teratol., 18(3), 217e227. Scheib, D., Mignot, T. M., & Guichard, A. (1984). Effects of early tamoxifen treatment on hormonal content of 15-day quail embryo gonads. Gen. Comp. Endocrinol., 56, 425e432. Shelby, M. D., Newbold, R. R., Tully, D. B., Chae, K., & Davis, V. L. (1996). Assessing environmental chemicals for estrogenicity using a combination of in vitro and in vivo assays. Environ. Health Perspect., 104(12), 1296e1300. Shimada, A. K., Yoshida, K., & Saito, N. (1996). Effects of aromatase inhibitor on sex differentiation and levels of P45017 and P450arom messenger ribonucleic acid of gonads in chicken embryos. Gen. Comp. Endocrinol., 102, 241e246. Shore, L. S. (1993). In Estrogen as an environmental pollutant (Gurevitz and Shemesh Ed); Bull. Environ. Contam. Toxicol., 1993, vol. 53(3), 361e366. Short, P., & Colborn, T. (1999). Pesticide use in the U.S. and policy implications: a focus on herbicides. Toxicol. Ind. Health, 15(1-2), 240e275. Stromborg, K. L. (1986). Reproduction of bobwhites fed different dietary concentrations of an organophosphate insecticide, methamidophos. Arch. Environ. Contam. Toxicol., 15(2), 143e147. Stoll, R., Ichas, F., Faucounau, N., & Maraud, R. (1993). Action of estradiol and tamoxifen on the Mullero-regressive activity of the chick embryonic testis assayed in vivo by organotypic grafting. Anat. Embryol. (Berl)., 187(4), 379e384. Tilson, H. A., & Kodavanti, P. R. S. (1998). The neurotoxicity of polychlorinated biphenyls. Neurotoxicology, 19(4-5), 517e526. Tori, G. M., & Peterle, T. J. (1983). Effects of PCBs on mourning dove courtship behavior. Bull. Environ. Contamin. Toxicol., 30, 44. Vajda, A. M., & Norris, D. O. (2005). Effects of steroids and dioxin (2,3,7,8TCDD) on the developing Wolffian ducts of the tiger salamander (Ambystoma tigrinum). Gen. Comp. Endocrinol., 141(1), 1e11.

Hormones and Reproduction of Vertebrates

Valle, S., Panero, M. A., & Shor, L. (2007). Pollution prevention and management strategies for polycyclic aromatic hydrocarbons in the New York/New Jersey harbor. New York, NY: New York Academy of Sciences. Van den Berg, M., Craanem, B. L. H. J., Sinnigem, T., Van Mourik, S., Dirksen, S., Boudewijn, T., et al. (1994). Biochemical and toxic effects of polychlorinated biphenyls(PCBs), dibenzo-p-dioxins(PCDDs) and dibenzofurans (PCDFs) in the cormorant (Phalacrocorax carbo) after in-ovo exposure. Environ. Toxicol. Chem., 13(5), 803e816. Vann, S. L., Sparling, D. W., & Ottinger, M. A. (2000). Effects of white phosphorus on mallard reproduction. Environ. Toxicol. Chem., 19 (10), 2525e2531. Vanson, A., Arnold, A. P., & Schlinger, B. A. (1996). 3ß-hydroxysteroid dehydrogenase/isomerase and aromatase activity in primary cultures of developing zebra finch Telencephalon: dehydroepiandrosterone as substrate for synthesis of androstenedione and estrogens. Gen. Comp. Endocrinol., 102, 342e350. Varghese, R. G., Bursian, S. J., Tobias, C., & Tanaka, D., Jr. (1995). Organophosphorus-induced delayed neurotoxicity: a comparative study of the effects of tri-ortho-tolyl phosphate and triphenyl phosphite on the central nervous system of the Japanese quail. Neurotoxicology, 16(1), 45e54. Vom Saal, F. S. (1995). Environmental estrogenic chemicals: Their impact on embryonic development. Human Ecol. Risk Assess., 1(2), 3e15. Vom Saal, F. S., & Timms, B. G. (1999). The role of natural and manmade estrogens in prostate development. In R. K. Naz (Ed.), Endocrine Disruptors: Effects on Male and Female Reproductive Systems (pp. 307e327). Boca Raton, FL: CRC Press. Wade, J., & Arnold, A. P. (2004). Sexual differentiation of the zebra finch song system. Ann. NY Acad. Sci., 1016, 540e559. Watson, J. T., & Adkins-Regan, E. (1989b). Activiation of sexual behavior by implantation of testosterone propionate and estradiol enzoate into the preoptic area of the male Japanese quail (Coturnix japonica). Horm. Behav., 23, 251e268. Watson, J. T., & Adkins-Regan, E. (1989a). Testosterone implanted in the preoptic area of male Japanese quail must be aromatized to activate copulation. Horm. Behav., 23, 432e447. Wehler, E. K., Brunstrom, B., Rannug, U., & Bergman, A. (1990). 3’,4,4’-tetrachlorobiphenyl: metabolism by the chick embryo in ovo and toxicity of hydroxylated metabolites. Chem.-Biol. Interact., 73, 121. Zacharewski, T. (1998). Identification and assessment of endocrine disruptors: limitations of in-vivo and in-vitro assays. Environ. Health Perspect., 106(Suppl 2), 577e582. Zhang, C., Fang, C., Liu, L., Xia, G., & Qiao, H. (2002). Disrupting effects of polychlorinated biphenyls on gonadal development and reproductive functions in chickens. J. Environ. Sci. Health, Part A, 37, 509e519. Zhou, T., Ross, D. G., De Vito, M. J., & Crofton, K. M. (2001). Effects of short-term in-vivo exposure to polybrominated diphenyl ethers on thyroid hormones and hepatic enzyme activities in weanling rats. Tox. Sci., 61, 76e82. Zoeller, R. T. (2008). Environmental neuroendocrine and thyroid disruption: relevance for reproductive medicine? Fertil. Steril., 89 (2 Suppl), e99ee100.

Species Index Index Aegolius acadius, 221 Agelaius phoeniceus, 29, 133 Aimophila, 43 Aimophila carpalis, 31 Alectoris, 74 Alectura lathami, 183 Anas acuta, 45, 133 Anas discors, 80 Anas platyrhnchos, 28, 103, 133, 219, 242 Anser anser, 133 Anser caerulescens, 79 Anser indicus, 190 Aphelocoma californica, 195 Aphelocoma coerulescens, 52, 132, 195 Aphelocoma ultramarina, 187 Aptenodytes forsteri, 31, 78, 185 Aptenodytes patagonicus, 31, 184 Apteryx mantelli, 79 Apus apus, 162 Axis axis, 41

Coturnix japonica, 74, 154, 156, 195 Cuculus canorus, 194 Cyanistes caeruleus, 109, 132, 222

Bonasa umbellus, 185 Branta leucopsis, 218 Bubulcus ibis, 109

Falco sparverius, 96, 187 Ficedula albicollis, 104, 192 Ficedula hypoleuca, 133, 162, 189, 222 Fringilla montifringilla, 212 Fulica americana, 109 Fulica atra, 80

Calcarius lapponicus, 133, 142, 220 Calcarius ornatus, 192 Calcirius pictus, 133 Calidris, 218 Calidris alpina, 216 Calidris canutus, 211 Calidris mauri, 133, 221 Calidris melanotos, 135 Calidris pusilla, 133, 135, 187, 221 Calidris tenuirostris, 211 Campylorhynchus brunneicapillus, 132 Canis lupus familiaris, 30 Cardeulis flammea, 43, 132 Cardeulis pinus, 43 Carduelis chloris, 46 Carina moschata, 50 Carpodacus cassinii, 43 Carpodacus mexicanus, 46, 95, 133, 141 Centropus grillii, 161, 185 Cervus elaphus, 41 Ceryle rudis, 194 Cettia diphone, 137 Chen rossi, 191 Chrotophaga ani, 109 Ciconia ciconia, 133 Colinus virginianus, 242 Columba livia, 30, 95, 227 Corvus brachyrhynchos, 30, 41 Cossypha heuglini, 170 Coturnix coturnix japonica, 41, 211

Daceo novaeguineae, 194 Dendroica caerulescens, 46 Dendroica coronata, 221 Dendroica occidentalis, 50 Dendroica petechia, 133, 189 Dendroica townsendi, 50 Diomedea, 190 Diomedea exulans, 133, 191 Dolichonyx oryzivorus, 211 Dromaius novaehollandiae, 40, 41 Dumetella carolinensis, 218 Emberiza bruniceps, 37, 41, 212 Empidonax oberholseri, 132, 193 Erythrura gouldiae, 50 Eudocimus albus, 185

Gallus domesticus, 72, 140, 217 Gallus gallus, 84, 183 Gallus gallus domesticus, 41, 141 Hirundo rustica, 47, 78, 80, 100, 102, 132, 141 Hylophylax naevioides, 40, 41 Junco hyemalis, 28, 95, 132, 185, 212 Lagopus, 45 Lagopus lagopus, 191 Larus argentatus, 133, 252 Larus glaucenscens, 191 Larus michahellus, 96 Larus ridibundus, 96 Leipoa ocellata, 183 Limosa lapponica, 220 Limulus polyphemus, 221 Lonchura punctulata, 219 Loxia, 42, 78 Loxia curvirostra, 43, 208 Loxia leucoptera, 31 Luscinia svecica, 46 Macerocephalon maleo, 79 Maluris lamberti assimilis, 40

Malurus cyaneus, 46, 194 Manorina melanophrys, 194 Megadyptes antipodes, 133, 185, 192 Meleagris gallopavo, 41, 157, 185 Melopsittacus undulatus, 28, 158, 183 Melospiza melodia, 41, 133, 155, 189, 210, 225 Melospiza melodia morphna, 42 Mesocricetus auratus, 41 Microtus agrestis, 41 Microtus ochrogaster, 30 Microtus pennsylvanicus, 227 Molothrus ater, 44, 154, 186 Morus capensis, 188 Otus flammeolus, 221 Ovis musimin, 41 Pagadroma nivea, 133, 194 Pan troglodytes, 30 Parabuteo unicinctus, 133, 185 Parus caeruleus, 210 Parus major, 31, 51, 92, 192, 216 Passer domesticus, 29, 41, 95, 102, 133, 141, 162, 185 Passer montanus, 51, 132, 158 Passerculus sandwichensis, 46 Pelecanus erythrothynchos, 80, 191 Perdicula asiatica, 37 Perdix perdix, 100, 155 Petrochelidon pyrrhonota, 132 Phaeton rubricauda, 190 Phalaropus fulicaria, 135 Phalaropus lobatus, 186 Phalaropus tricolor, 29, 164, 186 Phasianus colchicus, 103 Phasianus colchicus karpowi, 31, 41 Phodopus sungorus, 41 Phylloscopus trochilus, 133, 218 Pica pica, 42 Picoides borealis, 195 Plectrophenax nivalis, 133 Plocepasser mahali, 194, 225 Ploceus cucullatus, 183 Podiceps cristatus, 218 Podiceps nigricollis, 218 Poecile gambeli, 133, 217 Psittacula krameri, 37, 41 Pterodroma leucopter, 191 Puffinus tenuirostris, 226 Pygoscelis adeliae, 31, 132, 142, 187 Quelea quelea, 183

261

262

Rissa tridactyla, 109, 132, 193 Saxicola torquata axillaries, 211 Saxicola torquata rubicola, 211 Scolopax rusticola, 136 Serinus canaria, 41, 43, 93, 94, 157, 182 Sialia sialis, 100 Somateria mollissima, 132, 141, 184 Spheniscus magellanicus, 31 Spizella arborea, 132, 142 Sterna hirundo, 132 Sternus vulgaris, 30, 41, 74, 96, 132, 139, 154, 163, 192, 210, 216 Streptopelia risoria, 92, 154, 156, 182 Strix occidentalis caurina, 133 Struthio camelus, 31 Sturnus unicolor, 101 Sula dactylatra, 190 Sula leucogaster, 109

Species Index

Sula nebouxii, 109, 132 Sula sula, 133, 188 Sylvia atricapilla, 220 Sylvia borin, 31, 227 Tachycineta bicolor, 109, 183 Taeniopygia guttata, 41, 93, 94, 133, 139, 141, 155, 156, 183, 226, 243 Thallasarche melanophris, 132, 194 Thryothorus nigricapillus, 225 Toxostoma curvirostre, 52, 132 Troglodytes aedon, 109 Tryoglodytes troglodytes, 182 Turdoides bicolor, 191 Turdus merula, 52, 54, 132 Tyto alba, 132, 139, 162 Uria aalge, 132, 142, 191 Uta stansburiana, 143

Vireo olivaceus, 46, 185, 220 Vireo solitarius, 185 Zonotrichia albicollis, 169, 170, 212 Zonotrichia atricapilla, 212 Zonotrichia capensis, 41, 205 Zonotrichia leucophrys, 28, 74, 136, 139, 142, 154, 205, 210 Zonotrichia leucophrys gambelii, 101, 136, 137, 161, 205, 207, 211, 212, 217, 219, 224, 226, 227, 228 Zonotrichia leucophrys nutalli, 205, 206, 207, 210, 224, 225, 227 Zonotrichia leucophrys oriantha, 136, 137, 205, 206, 217, 219, 226 Zonotrichia leucophrys pugetensis, 41, 133, 136, 205, 206, 210, 217, 219, 224, 227

Subject Index Index ABP, see Androgen-binding protein Activin, testicular function, 37 AMH, see Anti-Mu¨llerian hormone Androgen receptor (AR) androgen-active compounds trenbolane acetate, 251 vinclozolin, 251 brain distribution dynamics in breeding behavior, 161 females, 160e161 males, 159e160 embryo expression timing, 107 Androgen-binding protein (ABP), testicular function, 39 Androstenedione, egg levels and effects, 92, 96, 100e101, 103, 106, 115e117 Anti-Mu¨llerian hormone (AMH) ovarian function, 75, 81 testicular development role, 28 AR, see Androgen receptor Arginine vasotocin (AVT) oviposition regulation, 8 testosterone mediation in male courtship and mating behavior, 168 Aromatase courtship and mating behavior control brain distribution females, 163e164 males, 162 nontraditional steroid effects, 162e163 testosterone regulation of levels, 162 testosterone aromatization to estrogen, 155e156 D-Aspartate, testicular function, 39 AVT, see Arginine vasotocin B cell, ovary, 77e78 BMPs, see Bone morphogenetic proteins Bone morphogenetic proteins (BMPs), follicular selection role, 83 Brood parasite obligate brood parasite hormonal control, 194 testicular development, 44 CBG, see Corticosterone-binding globulin Climate change, potential effects on testicular function, 51e52 Clock ovarian function, 86 seasonal reproduction role, 12 Clutch size factors affecting, 79e80 pace of life and brood value, 131e134

Corticosterone, see also Stress egg levels and effects, 92, 94e96, 102e104 foraging/feeding young effects, 142 incubation response, 184 migratory birds metabolic regulation, 216e218 receptors, 217e218 vernal migratory stage, 220e222 parental behavior response to stress, 193e194 secretion regulation annual regulation, 136 body condition and reactivity, 138 geographic regulation, 136e138 overview, 134 parental care and within-breedingseason regulation, 134e135 singing and territorial behavior effects, 141e142 testicular function, 38e39 yolk concentration, 77 Corticosterone-binding globulin (CBG), 39, 107, 134, 222 Courtship and mating behavior aromatase control brain distribution females, 163e164 males, 162 nontraditional steroid effects, 162e163 testosterone regulation of levels, 162 brain receptor distribution dynamics in breeding behavior, 161 females androgen receptor, 160e161 estrogen receptor, 160e161 progesterone receptor, 161 males androgen receptor, 159e160 estrogen receptor, 160 brain regions, 158e159 female steroid hormone control estrogen environmental and social stimuli effects on levels, 158 implant studies, 157 mechanisms of action, 170e171 ventromedial hypothalamus actions, 168e169 progesterone, 157e158 songbird responses auditory response endocrine influences, 169 estrogen-sensitive circuits, 169 sexually-motivated response endocrine influences, 169e170

nest building interactions, 182 overview, 153 prospects for study, 171 testosterone control in males castration effects, 155 courtship song medial preoptic nucleus regulation, 166e167 sensorimotor aspect control, 166 stimulation, 165e166 environmental and social stimuli effects on levels, 154e155 mechanisms of action, 167e168 medial preoptic nucleus actions, 164e165 metabolite mediation, 155e157 DDT, metabolite anti-androgenic activity, 251 DHT, see Dihydrotestosterone Dihydrotestosterone (DHT) courtship and mating behavior role in males, 156e157 egg levels and effects, 92, 106e107, 117 DMRT1, sex determination, 72e73 Domestication, effects on hormonal and behavioral patterns, 195 Dopamine, testosterone mediation in male courtship and mating behavior, 168 EDCs, see Endocrine-disrupting chemicals EGF, see Epidermal growth factor Egg hormones accumulation, 94e95 activational and organizational effects, 105 binding proteins, 107 clutch variation between clutch female quality, 115e116 food, 114e115 male quality, 114 parasites, 116 season, 115 social interactions, 113e114 within clutch bet hedging, 113 egg quality, 111e112 laying order and sibling competition, 109, 111 parentage, 112 sex, 112e113 differential regulation of yolk and circulating levels, 95e96 embryonic uptake, 106 embryonic versus maternal hormone effects, 106

263

264

Egg hormones (Continued ) levels, 93 metabolism, 106e106 offspring effects early development begging/competitiveness, 100 endocrine system, 101 immune system, 101 metabolic rate, 100e101 sex allocation, 101e102 survival, 101 time to hatching and growth, 96e100 indirect effects on other family members, 104 long-term effects behavioral syndromes or personalities, 103 coloration, morphology and song, 102e103 competitiveness, 102 dispersal, 102 endocrine system, 104 reproduction, 103 survival, 104 parenteoffspring conflict and coadaptation, 118 production, 94 prospects for study, 119 receptors, 107 species comparisons of effects parasite exposure, 116e117 predation risk, 117 social stimulation, 116 types, 92e93 Egg incubation, see Incubation Endocrine-disrupting chemicals (EDCs), see also specific chemicals androgen-active compounds trenbolane acetate, 251 vinclozolin, 251 challenges in study, 243 DDT metabolite anti-androgenic activity, 251 estrogen-active compounds methoxychlor, 249 phytoestrogens, 250 polychlorinated biphenyls, 250 exposure modes and models, 241e243 immune function and stress response effects, 253e254 Japanese quail studies, 246e247 laboratory studies, 248e249 overview, 239e241 prospects for study, 254 risk assessment, 243 testicular effects, 52 thyroid-disrupting compounds, 251e253 vulnerability timing altricial birds, 244e245 overview, 243e244 precocial birds, 244e246 sexual differentiation, 244 wild population studies, 247e248

Subject Index

Epidermal growth factor (EGF), ovarian function, 75 Epididymal lithiasis, testicular dysfunction, 50 Erythropoiesis, migratory birds, 219 Estradiol benzoate, testicular dysfunction, 52e53 Estrogen brood-patch formation role, 185 courtship and mating behavior control in females environmental and social stimuli effects on levels, 158 implant studies, 157 mechanisms of action, 170e171 songbird responses auditory response endocrine influences, 169 estrogen-sensitive circuits, 169 sexually-motivated response endocrine influences, 169e170 ventromedial hypothalamus actions, 168e169 courtship and mating behavior role in males, 155e157 E2 aromatization from testosterone, see Aromatase egg levels and effects, 92, 95, 106 endocrine-disrupting chemicals methoxychlor, 249 phytoestrogens, 250 polychlorinated biphenyls, 250 incubation effects, 188 nest building role, 183 Estrogen receptor brain distribution dynamics in breeding behavior, 161 females, 160e161 males, 160 embryo expression timing, 107 phytoestrogen affinity, 250 ER, see Estrogen receptor Finite state machine, application to migration and breeding, 207e208 Flexible breeder, 43 Flight muscle, hypertrophy in migratory birds, 218e219 Follicle-stimulating hormone (FSH) ovarian function, 74, 76, 82e83 ovulation regulation, 7 seasonal changes, 10e12 testicular development role, 27 testicular function, 31, 36 Folliculogenesis, see Ovary Food egg hormone response, 114e115 hyperphagia, see Migration testicular function effects, 42e43 FSH, see Follicle-stimulating hormone Ghrelin, migratory bird hyperphagia and fattening, 216 Glucagon, migratory bird hyperphagia and fattening, 214

Glucocorticoids, see Corticosterone; Stress GnIH, see Gonadotropin-inhibiting hormone GnRH, see Gonadotropin-releasing hormone Gonadotropin-inhibiting hormone (GnIH) neuron release, 5e6 ovarian function, 75 receptor, 6e7 reproduction effects, 6e7 testicular development role, 27e28 testicular function, 36e37 Gonadotropin-releasing hormone (GnRH) detection, 4e5 luteinizing hormone release, 5 receptors, 5 seasonal changes, 11e12 structure, 3e4 testicular development role, 27 HPS, see Hypothalamus-pituitary system Hypothalamus-pituitary system (HPS), overview, 2e3, 206 Id proteins, follicular selection role, 83 IGFs, see Insulin-like growth factors Incubation brood-patch formation, 185e186 costs, 183e184 initiation and maintenance, 186e188 laying, incubation, and asynchronous hatching, 186 overview, 183 prolactin response, 184 role, 185e189 secretion regulation, 188e189 renesting and responses to nest failure, 189 sex roles, 184e185 steroid hormone effects, 188 Inhibin ovarian function, 75 testicular function, 37 Insulin, migratory bird hyperphagia and fattening, 214 Insulin-like growth factors (IGFs), ovarian function, 75 Laying order, egg hormone effects, 109 Leptin, migratory bird hyperphagia and fattening, 216 Leydig cell, 28e29 LH, see Luteinizing hormone Luteinizing hormone (LH) courtship and mating behavior role in males, 154 ovarian function, 74e76, 82e85 ovulation regulation, 7e8 release regulation, 5 seasonal changes, 10e12 testicular development role, 27 testicular function, 31 Mating, see Courtship and mating behavior Medial preoptic nucleus, see Courtship and mating behavior

265

Subject Index

Melatonin migratory birds, 220 seasonal reproduction role, 13e14 testicular function, 37 Mesotocin (MST), oviposition regulation, 8 Methoxychlor, estrogenic activity, 249 Migration autumn migratory stage developmental phase hyperphagia and fattening, 226e227 photoperiod and refractoriness, 226 mature capability phase, 227e228 termination phase, 228 breeding life-history stage developmental phase latitude and photoperiod, 223e224 white-crowned sparrow, 224e225 termination phase photorefractoriness, 225e226 thyroid hormone, 226 finite state machine theory application to migration and breeding, 207e208 testicular effects, 43e44 timing with breeding cycles developmental phase regulation, 212 environmental factors, 209 models of Lofts and Murton, 210e211 morphological evidence for separate control systems, 215e216 overview, 208e209 photoinduction cue responses, 211e212 photoperiod responsiveness, 209e210 vernal migratory stage corticosterone metabolic regulation, 216e218 receptors, 217e218 erythropoiesis, 219 flight muscle hypertrophy, 218e219 hyperphagia and fattening carbohydrate and lipid metabolism, 214 ghrelin, 216 glucagon, 214 gonadectomy studies, 215 insulin, 214 leptin, 216 overview, 213e214 prolactin, 215e216 mature capability phase corticosterone, 220e221 corticosterone-binding globulin, 222 fueling and flight cycles, 220 melatonin, 220 metabolic adjustments during fueling and flight cycles, 222e223 migration modulation hypothesis, 221e222 termination phase, 223 white-crowned sparrow annual cycles, 206e207 life history and ecology of subspecies, 205e206 MST, see Mesotocin

Nest building courtship behavior interactions, 182 hormonal control, 182e183 sex roles, 182 Nitric oxide (NO), testicular function, 39 NO, see Nitric oxide Norepinephrine, testosterone mediation in male courtship and mating behavior, 168 Opportunistic breeder, 43 Ovary development embryonic organization, 72e73 postembryonic development, 73e74 follicular development clock genes, 86 follicular atresia, 85e86 follicular selection, 82e83 overview, 80e81 ovulation, 84e85 preovulatory growth and final differentiation, 83e84 primordial follicular reserve and initial recruitment, 81 immune response, 77e78 regulation prostaglandins, 77 protein hormones, 74e76 steroids and steroidogenesis, 76e77 thyroid hormone, 77 seasonal reproduction ovarian growth mediation by environmental cues, 78e79 overview, 78 ovulationeoviposition cycles, 79e80 regression during photorefractory period and molt, 80 Oviposition cycles, 79e80 regulation, 8 Ovulation, see also Ovary cycles, 79e80 regulation, 7, 84e85 Pace of life, see Stress Parental behavior care of young altricialeprecocial spectrum, 189 parentechick interactions, 191e192 prolactin and posthatching parental behavior, 190e191 domestication effects on hormonal and behavioral patterns, 195 helping at nest, 194e195 incubation brood-patch formation, 185e186 costs, 183e184 initiation and maintenance, 186e188 laying, incubation, and asynchronous hatching, 186 overview, 183

prolactin response, 184 role, 185e189 secretion regulation, 188e189 renesting and responses to nest failure, 189 sex roles, 184e185 steroid hormone effects, 188 nest building courtship behavior interactions, 182 hormonal control, 182e183 sex roles, 182 obligate brood parasites, 194 overview, 181e182 prospects for study, 195e196 stress response, 193e194 testosterone and male behavior, 192e193 PBDEs, see Polybrominated diphenyl ethers PCBs, see Polychlorinated biphenyls Period ovarian function, 86 seasonal reproduction role, 12 PGC, see Primordial germ cell Photophase ovarian growth effects, 78e79 testicular function effects, 40e41 Photoreceptor, seasonal reproduction regulation, 12 Phytoestrogens estrogen receptor affinity, 250 testicular dysfunction, 49 Pineal gland, clock genes, 12 POF, see Postovulatory follicle Polybrominated diphenyl ethers (PBDEs), thyroid disruption, 252e253 Polychlorinated biphenyls (PCBs) estrogenic activity, 250 nest building impact, 183 thyroid-disrupting compounds, 252 Postovulatory follicle (POF), regression, 85 Precipitation, testicular function effects, 40e42 Primordial germ cell (PGC), ovarian development, 72, 81 PRL, see Prolactin Progesterone brood-patch formation role, 185 courtship and mating behavior control in females, 157e158 egg levels and effects, 92, 102, 104 incubation effects, 188 ovarian function, 85 ovarian synthesis, 76 receptor distribution in female brain, 161 Prolactin (PRL) incubation response, 184 role, 185e189 secretion regulation, 188e189 migratory bird hyperphagia and fattening, 215e216 ovarian function, 74e75, 80 parental behavior response to stress, 193e194

266

Prolactin (PRL) (Continued ) posthatching parental behavior regulation, 190e191 secretion regulation, 8e9 testicular function, 38 Prostaglandins, ovarian function, 77 Renesting, hormonal control, 189 Seasonal reproduction, see also Migration biological clock, 12e13 clutch variation, 115 gonadotropin-releasing hormone seasonal changes, 11e12 melatonin role, 13e14 ovary ovarian growth mediation by environmental cues, 78e79 overview, 78 ovulationeoviposition cycles, 79e80 regression during photorefractory period and molt, 80 overview, 9e11 photoreceptors, 12 testes regression, 30 thyroid hormone role, 14e15 Seminiferous tubules, 29 Sex determination endocrine-disrupting chemical effects, 244 genes, 72e73 Simulated territorial intrusion (STI), glucocorticoid studies, 141e142 Song brain regions in control, 159 courtship song female songbird responses auditory response endocrine influences, 169 estrogen-sensitive circuits, 169 sexually-motivated response endocrine influences, 169e170 testosterone mediation in males medial preoptic nucleus regulation, 166e167 sensorimotor aspect control, 166 stimulation, 165e166 egg hormone late effects, 102e103 glucocorticoid effects, 141e142 Species hybridization, infertility, 49e50 Sperm motility induction, 30 spermatogenesis, 29e30 testosterone and quality, 45 Sperm competition, theories, 47e48 SRY sex determination, 72 testicular development role, 28 StAR, see Steroidogenic acute regulatory protein Steroidogenic acute regulatory protein (StAR), ovarian function, 76e77

Subject Index

STI, see Simulated territorial intrusion Stress, see also Corticosterone allostasis, 129e130 direct fitness metrics of response overview, 142e143 reproduction, 143 survival, 143e144 tradeoffs, 144e145 endocrine-disrupting chemical effects on response, 253e254 glucocorticoids reproduction study classification, 131 secretion regulation annual regulation, 136 body condition and reactivity, 138 geographic regulation, 136e138 overview, 134 parental care and within-breedingseason regulation, 134e135 intermediate performance measures of reproduction effects behavior foraging/feeding young, 142 singing and territorial behavior, 141e142 morphology, 138e139 physiology body composition, 139 immune function, 139e141 pace of life brood value, 131e134 overview, 130e131 parental behavior response, 193e194 testicular effects, 38e39 T cell endocrine-disrupting chemical effects, 253 glucocorticoid response, 140 ovary, 77e78 Testes abiotic factors in function food, 42e43 photophase, 40e41 precipitation, 40e42 anatomy gross anatomy, 28 Leydig cell, 28e29 seminiferous tubules, 29 androgen synthesis, 29 anthropogenic effects climate change, 51e52 endocrine disruption and urbanization, 52 introduced species, 50e51 development central mechanisms, 27e28 endocrine influence, 28 dysfunction pathology, 50 phytoestrogens, 49 species hybridization and infertility, 49e50 hormone expression and receptors, 31e35

life history in function breeding strategy, 43 brood parasitism, 44 migratory versus sedentary species, 43e44 social cues, 44e45 prospects for study, 52e54 regulation activin, 37 androgen-binding protein, 39 D-aspartate, 39 corticosterone and stress effects, 38e39 follicle-stimulating hormone, 31, 36 gonadotropin-inhibiting hormone, 36e37 inhibin, 37 luteinizing hormone, 31 melatonin, 37 nitric oxide, 39 prolactin, 38 seasonal regression, 30 size correlates age and body size, 45e46 evolutionary explanations for size asymmetry, 47 geography, 46e47 negative consequences of large testes, 48e49 sperm competition, 47e48 testosterone levels, 46 spermatogenesis, 29e30 Testosterone aromatization to estrogen, see Aromatase courtship and mating behavior control in males castration effects, 155 courtship song medial preoptic nucleus regulation, 166e167 sensorimotor aspect control, 166 stimulation, 165e166 environmental and social stimuli effects on levels, 154e155 mechanisms of action, 167e168 medial preoptic nucleus actions, 164e165 metabolite mediation, 155e157 egg levels and effects, 92e96, 100e107, 109, 114e117 female steroid hormone control inactivation, 156 nest building role, 182e183 parental behavior effects in males, 192e193 receptor, see Androgen receptor sperm quality studies, 45 testicular size correlation, 46 testicular synthesis, 29 Transthyretin (TTR), thyroid hormone binding, 107 Thyroid hormone egg levels and effects, 93e94, 104 embryo expression timing of receptor, 107 endocrine-disrupting chemicals, 251e253

267

Subject Index

migratory birds, 226 ovarian function, 77 seasonal reproduction role, 14e15 testicular development role, 27 TLR, see Toll-like receptors TNF-a, see Tumor necrosis factor-a Toll-like receptors (TLRs), ovary, 77 Trenbolane acetate, androgenic activity, 251 TTR, see Thansthyrethrin

Tumor necrosis factor-a (TNF-a), ovarian function, 76 Vasoactive intestinal peptide (VIP) ovarian function, 75 prolactin secretion regulation, 9 testicular development role, 27 Very-low-density lipoprotein (VLDL), yolk incorporation, 84 Vinclozolin, androgenic activity, 251

VIP, see Vasoactive intestinal peptide Vitellogenin, yolk incorporation, 84 VLDL, see Very-low-density lipoprotein White-crowned sparrow, see Migration Yellow semen syndrome (YSS), testicular dysfunction, 50 Yolk hormones, see Egg hormones YSS, see Yellow semen syndrome

Color Plates

FIGURE 3.1 Working model for cell-signaling mechanisms proposed to prevent premature differentiation of granulosa cells from prehierarchical follicles. Epidermal growth factor family ligands (EGFRLs) and bone morphogenetic proteins (BMPs) (including BMP2 and growth and differentiation factor-9 (GDF9)) bind to their cognate receptors to activate mitogen-activated protein kinase (MAPK) and phosphorylate extracellular regulated kinase (Erk-P) or phosphorylate Smad (Smad-P; specifically, Smad-1, -5, or -8), respectively. These inhibitory signals mediate the active suppression of folliclestimulating hormone receptor (FSHR) transcription. cAMP, cyclic adenosine monophosphate. Adapted from Johnson and Woods (2008).

FIGURE 3.2 Epidermal growth factor family ligand (EGFL)-, bone morphogenetic protein-2 (BMP2)-, and growth and differentiation factor-9 (GDF9)induced expression of Id1, Id3, and/or Id4 proteins (Id) prevents the binding of basic helix-loop-helix (bHLH) transcription factors (TFs) to an E-box site (canonical sequence, CANNTG) within the follicle-stimulating hormone receptor (FSHR) promoter region. In the absence of transcriptional activator binding to the E-box site, transforming growth factor-b (TGFb)- and activin-induced Smad2 binding to Smad binding elements (SBEs) fails to fully potentiate FSHR mRNA transcription. As a consequence, FSHR-mediated cyclic adenosine monophosphate (cAMP) formation and signaling is maintained at relatively low levels. See text for additional details.

FIGURE 3.3 Following an alleviation of inhibitory signaling via epidermal growth factor family ligands (EGFLs) and bone morphogenetic proteins (BMPs), levels of Id1, Id3, and Id4 rapidly decrease due to the loss of supportive signaling (not depicted). The decrease in Id1, Id3, and Id4 levels enables one or more basic helix-loop-helix (bHLH) transcription factors (TFs) to bind the follicle-stimulating hormone receptor (FSHR) promoter to enable enhanced FSHR expression (Johnson, Haugen, & Woods, 2008). As a result, increasing cyclic adenosine monophosphate (cAMP) formation stimulates upregulation of Id2 protein. It is proposed that Id2 indirectly promotes FSHR mRNA transcription by preventing a corepressor (CoR) from attenuating promoter activity. Collectively, these actions enable transforming growth factor-b (TGFb) and activin (acting via Smad2 binding to a Smad binding element (SBE)) to fully potentiate FSHR transcription. Enhanced levels of FSHR generate the increasing amounts of cAMP required to initiate luteinizing hormone receptor (LHR) expression (not depicted). GDF9, growth and differentiation factor-9.

FIGURE 5.4 Three species of shorebird, each with different roles for males and females in raising the young. In the polygynous pectoral sandpiper (Calidris melanotos), the female raises the brood; in the monogamous semipalmated sandpiper (Calidris pusilla), parental care is shared; in the polyandrous red phalarope (Phalaropus fulicaria), the male raises the brood (parental care denoted by egg above bar). Stress-induced corticosterone secretion is inversely related to the load of parental care in each species. Redrawn from O’Reilly and Wingfield (2001), with permission.

FIGURE 5.5 Population location and total corticosterone (CORT), corticosterone-binding globulin (CBG), and free CORT levels in three populations of white-crowned sparrows with varied amounts of time to breed. Blue, Zonotrichia leucophrys gambelii; green, Zonotrichia leucophrys pugetensis; black, Zonotrichia leucophrys oriantha. Redrawn from Breuner et al. (2003), with permission.

FIGURE 5.8 Matching clutch need to maternal ability: if a poor-condition mother (wing-clipped) produces a poor condition brood (corticosterone (CORT)-treated), she will raise fewer young that year (upper graph) but increase her survival probability 10-fold over poor-condition mothers raising a full brood (lower graph). Redrawn from Love and Williams (2008), with permission.

FIGURE 8.10 Lifecycles of five divisions of whitecrowned sparrow with distinct breeding localities that range from high- and mid-latitude migratory forms to lower latitude sedentary populations. The length of vernal migratory period increases with latitude, whereas territoriality decreases. The profile of testosterone secretion is most brief in the arctic and expands in more southerly populations. Postnuptial molt is apparent in all races but only migratory species have an autumnal migratory stage and prenuptial molt. Species: tundra white-crowned (Zonotrichia leucophrys gambelii), taiga (Z. l. gambelii), mountain (Z. l. oriantha), Puget Sound (Z. l. pugetensis), and Nuttall’s (Z. l. nuttalli) sparrows.

MXC gel capsules (50 mg/day) 2750

a MXC bolus

2500

a

2250

Methoxychlor (ppb)

2000

a

1750 1500

b

1250

Day -2 -1 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

n 4 2 4 5 4 3 2 3 3 4 1 3 2 2 2 2 2 2

b 1000

bcf

750

bce

500

cd

250 0

d -2

de -1

df 0

de

d 1

2

3

4

5

6

7

8

9

10

de

d

de

de

de

11

12

13

14

15

Day of Experiment

parental exposure

embryonic exposure

FIGURE 9.2 Exposure in birds occurs via maternal transfer. Reproduced from Ottinger et al. (2004).

FIGURE 9.3 The impact of exposure pattern on field birds.

FIGURE 9.4 Overview of development with birth and movement of gonadotropin-releasing hormone-I (GnRH-I) cells; role of steroid hormones and maturation-related increase in hormones with initiation of gonadal function and reproductive behavior. E2, 17b-estradiol; GnRH, gonadotropin-releasing hormone; HPG, hypothalamicepituitaryegonadal. Reproduced from Ottinger and Brinkley (1979).