Pleurocarpous Mosses: Systematics and Evolution

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The Systematics Association Special Volume Series 71

Pleurocarpous Mosses

Half Title Page

Systematics and Evolution

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The Systematics Association Special Volume Series Series Editor Alan Warren Department of Zoology,The Natural History Museum, Cromwell Road, London SW7 5BD, UK. The Systematics Association promotes all aspects of systematic biology by organizing conferences and workshops on key themes in systematics, publishing books and awarding modest grants in support of systematics research. Membership of the Association is open to internationally based professionals and amateurs with an interest in any branch of biology including palaeobiology. Members are entitled to attend conferences at discounted rates, to apply for grants and to receive the newsletters and mailed information; they also receive a generous discount on the purchase of all volumes produced by the Association. The first of the Systematics Association’s publications The New Systematics (1940) was a classic work edited by its then-president Sir Julian Huxley, that set out the problems facing general biologists in deciding which kinds of data would most effectively progress systematics. Since then, more than 70 volumes have been published, often in rapidly expanding areas of science where a modern synthesis is required. The modus operandi of the Association is to encourage leading researchers to organize symposia that result in a multi-authored volume. In 1997 the Association organized the first of its international Biennial Conferences.This and subsequent Biennial Conferences, which are designed to provide for systematists of all kinds, included themed symposia that resulted in further publications. The Association also publishes volumes that are not specifically linked to meetings and encourages new publications in a broad range of systematics topics. Anyone wishing to learn more about the Systematics Association and its publications should refer to our website at www.systass.org. Other Systematics Association publications are listed after the index for this volume.

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The Systematics Association Special Volume Series 71

Pleurocarpous Mosses

Title Page

Systematics and Evolution

Edited by

Angela E. Newton Natural History Museum London, U.K.

Raymond S. Tangney National Museum Wales Cardiff, U.K.

Boca Raton London New York

CRC Press is an imprint of the Taylor & Francis Group, an informa business

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The cover photo was taken by Neil Bell, and is of Rhizogonium distichum (Sw.) Brid. from Tasmania.

CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 © 2007 by Taylor & Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group, an Informa business No claim to original U.S. Government works Printed in the United States of America on acid-free paper 10 9 8 7 6 5 4 3 2 1 International Standard Book Number-10: 0-8493-3856-5 (Hardcover) International Standard Book Number-13: 978-0-8493-3856-4 (Hardcover) This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use. No part of this book may be reprinted, reproduced, transmitted, or utilized in any form by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying, microfilming, and recording, or in any information storage or retrieval system, without written permission from the publishers. For permission to photocopy or use material electronically from this work, please access www.copyright.com (http:// www.copyright.com/) or contact the Copyright Clearance Center, Inc. (CCC) 222 Rosewood Drive, Danvers, MA 01923, 978-750-8400. CCC is a not-for-profit organization that provides licenses and registration for a variety of users. For organizations that have been granted a photocopy license by the CCC, a separate system of payment has been arranged. Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe. Library of Congress Cataloging-in-Publication Data Pleurocarpous mosses : systematics and evolution / edited by Angela E. Newton and Raymond S. Tangney. p. cm. Includes bibliographical references (p. ). ISBN 0-8493-3856-5 (alk. paper) 1. Pleurocarpous mosses--Classification. 2. Pleurocarpous mosses--Evolution. I. Newton, Angela E. II. Tangney, Raymond S. QK538.P54 2006 588’.2--dc22 Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com and the CRC Press Web site at http://www.crcpress.com

2006048350

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Foreword This is the age of phylogenetics in biology. The working out of rigorous methods for phylogenetic inference in the 1970s and 1980s, combined with the massive influx of new data from the molecular level in the 1990s, resulted in increasingly better-supported and more believable phylogenetic trees for most groups of organisms. At the same time, a plethora of new comparative methods has been developed in order to use phylogenetic trees for understanding an incredibly broad spectrum of biological processes. Phylogenetic tree-thinking has led to fundamental advances in systematics, biogeography, coevolution, community assembly, macroevolution, medicine, behavior, evolution of development, physiology, population genetics, comparative genomics, and many other areas. This progress has been very evident in bryophyte biology as well. It wasn’t that long ago (less than one academic generation) that purely speculative stories about the evolution of major bryophyte groups were the norm, tending to give systematics and phylogeny-building a bad reputation among biologists as a whole. The wrong models were being used in bryology (as elsewhere at the time), with evolution viewed as some kind of ladder, a hold-over of the ancient “Great Chain of Being” concept. Articles and books were filled with arguments about which bryophyte groups are the most primitive or most advanced, and how best to linearly arrange the groups in between from lowest to highest (e.g., debates over whether the Polytrichaceae should go at the beginning or end of a moss flora!). Following another misleading mode of thinking that stems all the way back to Aristotle, people thought they needed to weight characters a priori by their importance (e.g., debates over whether sporophytic or gametophytic characters were more important in showing relationships) or to decide ahead of time what the evolutionary trends were. Every possible scenario about relationships and character change was put forward and supported by force of personality, with little to no objective means available for evaluating competing hypotheses. The Hennigian approach to phylogenetics cuts through these ancient and wrong-headed approaches, by applying the right model (a tree), and providing an objective method for evaluating evidence for branches on that tree one character at a time, without preconceptions, using a rigorous concept of homology. Instead of ordering taxa in a linear arrangement, the question became their relative recency of common ancestry — we realize now that extant taxa cannot be linked up in a linear series; they are all equally “advanced.” Character states on the other hand can (and should) be polarized into a transformation series through time along branches in a phylogenetic tree, with shared derived characters (synapomorphies) serving as evidence for the existence of nested monophyletic groups. By examining many independent characters that can each be inferred separately to have changed along a particular branch in the past, strong support can be built up for a monophyletic group descended from that branch. As in other groups of organisms, our phylogenetic trees are getting ever stronger in bryophytes, while the weak places remaining in the trees are becoming ever more clearly highlighted as targets for future research. What causes lack of resolution in parts of phylogenetic trees? Many biological processes can confuse the reconstruction of history, including hybridization or other forms of horizontal gene transfer, misleading extinctions of ancestral polymorphisms (called “lineage sorting”), and natural selection that may cause convergent evolution. One problematic situation that is of particular relevance to the subject of this book is highly unequal branch lengths, i.e., where short, deep branches may lack enough signal to reconstruct them correctly at some distant future time, and unrelated long branches may appear falsely to be related through accumulated non-homologous character-state matches (known as “long-branch attraction”). There were apparently times in the past, as in the early radiation of pleurocarpous mosses, when things happened fast. Many divergence

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events happened relatively quickly, one after another, allowing little time for character transformations along the temporally short lineages that existed until the next splitting event. In such cases there is precious little data that can potentially address the relative recency of branching order, and such data tends to slowly disappear over time as further mutations obscure the evidence. The pleurocarpous mosses, a morphologically and ecologically diverse group that contains a large proportion of the described species of mosses, have been one of these difficult regions of the tree of life to reconstruct, and are well worth a book-length treatment. The authors bring to bear considerable amounts of new data and careful analytical methods designed to help with such problems as long-branch attraction. It is clear from their efforts that, although such cases of deep and rapid radiation are extremely difficult to approach, they are not impossible. Careful choice of enough suitable markers for those short ancient branches, including slowly evolving genes and morphological characters (which can be really useful in such cases because of their episodic mode of change), has a hope of resolving them. This book provides a fascinating case study of what can happen when a large number of researchers tackle a thorny phylogenetic problem in a cooperative manner, and hopefully will serve as a model for other such efforts. This is the first book of its kind for the bryophytes — which are increasingly being recognized as important organisms for lab research, and as major players in the ecosystem. It is a rare type of book for any group of plants, an attempt to review all that is currently known about their phylogeny, and then to relate that to a full range of important topics regarding their biology. The topics range from overarching backbone relationships to detailed examination of specific taxonomic groups, followed by a variety of evolutionary studies. This is a fine effort by the editors and authors, which should serve to bring these interesting plants to the attention of botanists and evolutionary biologists in general, and stimulate continued efforts to refine the remaining uncertainties and to understand the causes and effects of this important radiation in land plants. Brent D. Mishler

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Preface The application of cladistic analysis and molecular data to the study of relationships of organisms has resulted in a revolution in the systematics of many groups of organisms, not least the mosses. We can now propose hypotheses about relationships in an objective manner, and use topologies resulting from analyses to ask questions about the evolutionary processes underlying the observed patterns. At the same time, there has been a paradigm shift, from the traditional, knowledge-based and synthetical methodology, where individuals “knew” the organisms and suggested classifications on that basis, to a data-based, analytical methodology where matrices of characters (molecular or morphological) are assembled and analysed using computers. Although morphological data and the older methods have been responsible for a very large proportion of our current knowledge at all taxonomic levels, some conclusions based on these have been erroneous, and other problems have proved intractable. The circumscription and relationships of the pleurocarpous mosses present a major example where traditional data have accomplished much but also leave much to be desired. The symposium on pleurocarpous mosses held at Cardiff in September 2004 provided an opportunity for many of the researchers active in the systematics of this group to meet and present the results of their studies. This event was held approximately ten years after the publication of the first major attempt (by Lars Hedenäs, in 1994) to study the relationships of pleurocarpous mosses using cladistic methodology, and gives a broad overview of the progress in our understanding of the relationships of the pleurocarpous mosses. In particular, this book draws on both molecular data and morphology (including morphology of molecules), and synthetical and analytical methodology, to highlight the areas of the pleurocarp phylogeny where there is some resolution, and to identify the regions where there are still intriguing questions to be addressed. In the introductory chapter, Bill Buck reviews the history of pleurocarp classification, identifying a cyclical pattern in the philosophical principles underlying efforts to resolve the classification of the pleurocarps, which revolved around the relative importance of the gametophyte and sporophyte generations as sources of characters. He notes that the classification of pleurocarpous mosses has traditionally lagged behind that of acrocarps (which is a reflection of the morphological diversity and distinctness of the acrocarp groups, in contrast to the morphological plasticity and close relationships of the pleurocarps). In one of the earliest classifications of mosses, based on sporophyte characters, Hedwig included 30 genera of acrocarps but only five genera of pleurocarps, despite the very similar number of species now recognized in these divisions. Subsequently classifications have alternated between emphasizing gametophyte and sporophyte characters, but the advent of molecular data has allowed bryologists to present classifications independent of morphology. Although initial work using one-gene trees resulted in faulty classifications, multiple-gene trees have refined the process. However, the Hypnales, the largest group among the mosses and a key pleurocarp group, still lacks phylogenetic resolution. A combination of multiple genes with carefully observed morphology should provide us with a stable classification. The two following chapters explore the relationships of the earliest-diverging lineages of mosses in which pleurocarpous morphology appeared, emphasizing molecular and morphological data, respectively. The majority of taxa in this region of the phylogeny, including the rhizogonian and hypnodendroid mosses, have a primarily Gondwanan distribution centered in Oceania, and represent only about 1% of the species in the pleurocarpous mosses. Terry O’Brien investigates the distribution of the phylogenetic diversity in pleurocarpous mosses through an analysis of a four-gene cpDNA dataset of 58 exemplar taxa. The results indicate that pleurocarpous and non-pleurocarpous members of the Rhizogoniaceae plus the acrocarpous genera Aulacomnium, Calomnion and Orthodontium

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Participants at the symposium on Pleurocarpous Mosses: Systematics and Evolution. Group photo taken on the steps of the National Museum of Wales, Cardiff, September 2004, by Misha Ignatov. From left to right: Niklas Pedersen; Lars Hedenäs; Philip Stanley; Ray Tangney; Gisela Oliván; Anastasia Gardiner; Terry O’Brien; Alan Orange; Bill Buck; Sean Russell; Neil Bell; Brian O’Shea; Dolores Gonzalez; Liz Kungu; Angie Newton; BoonChuan Ho; Efrain De Luna; Hans Kruijer; Rolf Blöcher; Yelitza León-Vargas; Roy Perry; Katherine Vint; Sanna Huttunen; Nancy Slack; Dietmar Quandt.

are the sister group or near sister group to the hypnodendroid pleurocarps and the Hypnidae (Hypnobryales, Hookeriales and Ptychomniales). These results highlight a marked asymmetry in the phylogenetic distribution of diversity of pleurocapous mosses similar to that found in angiosperms. Looking at the diversity of morphology in these taxa, Neil Bell and Angela Newton examine modular branching structure in exemplars from the rhizogoniaceous grade, in order to isolate discrete architectural types associated with the pleurocarpous condition. These are described and used as a basis for optimization of pleurocarpy sensu stricto onto a phylogeny derived from chloroplast and mitochondrial molecular sequence data. Characters closely associated with pleurocarpy in these taxa are also optimized, and the results used to examine scenarios for the evolution of modular form in the basal pleurocarpous clades. The results reveal that there is disproportionate diversity of pleurocarpous architectural types in the rhizogoniaceous grade compared with the hypnodendroid pleurocarps and the Hypnidae, and that these probably represent successive and varied novel adaptive strategies that utilize the potential of the key innovation of pleurocarpy. Another clade with a position among the early-diverging lineages of pleurocarpous mosses, with affinities to the Hookeriales, is the family Hypopterygiaceae, comprising 21 species distributed among seven or eight genera. These are characterized by a distinctive leaf arrangement and a diversity of branching architectures. In Chapter 4, Hans Kruijer and Rolf Blöcher give an overview of systematic studies in the family and present a phylogenetic study of relationships within the family using a combination of morphological and molecular data. Although their results, based on molecular data for 15 species of Hypopterygiaceae and nine species of related families, show support for monophyly of the family, the traditional circumscription of some of the genera needs to be reviewed. The authors consider that the homoplasy of the morphological characters suggested by the molecular data requires a new view of the morphology and that increased sampling will produce a fuller understanding of the evolutionary history of the family, resulting in a new generic classification of the Hypopterygiaceae. In Chapter 5, Boon-Chuan Ho and Hans Kruijer report on

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the plasticity of growth patterns in Calyptrochaeta, a small genus in the Hookeriaceae (Hookeriales) that grows mainly on decaying wood and tree bases in wet tropical mountain forests in Malesia and adjacent areas. These species display two different growth patterns in which there is no clear differentiation into axes of different hierarchical levels. These growth patterns are characterized by orthotropic axes and sympodial (basal) innovations, and by long plagiotropic axes showing indeterminate growth and monopodial branching. However, observations suggest that the plagiotropic growth pattern represents a character state derived from the orthotropic one, and that their striking difference should not be overestimated in taxonomic research on Calyptrochaeta. In the following section, Chapters 6 to 10 present the results of analyses, primarily of molecular data and using a variety of analytical techniques, to explore the relationships of families within the Hypnales. This group represents about 80% of the pleurocarpous moss species (and a third of all extant moss species) but relationships within and between the families are very poorly known. Sanna Huttunen, Anastasia Gardiner and Michael Ignatov review progress in understanding the Brachytheceaceae, one of the most diverse groups of mosses. Although a backbone phylogeny of the Brachytheciaceae has been suggested, problems remain with some groups. They present new data with additional species, utilizing POY alignment and analysis of the secondary structure of trnL intron. Their results highlight extensive parallelisms in the morphology of major lineages associated with ecological specialization. Most lineages within the family have subaquatic members with morphologies convergent across lineages in characters such as leaf shape, leaf orientation and costal structure. Similarly a tendency to epiphytism across lineages has led to homoplasy in peristome morphology. The authors address these repeated patterns of extreme ecological divergence and whether the divergent morphologies of these taxa should be reflected in paraphyletic genera. In the following chapter, Sanna Huttunen and Dietmar Quandt synthesize results from four phylogenetic analyses of the moss family Meteoriaceae and review the current generic relationships within the family. Phylogenies are used to evaluate morphological evolution within the family and to pinpoint the synapomorphies of the major clades. Previous classifications of the Meteoriaceae are seen to be characterized by extensive homoplasy of morphological, particularly cellular, characters. Although more extensive future sampling will be needed to test monophyly of the genera, at the subfamily level major divisions in the family are recognized, including a new subfamily. Important morphological features at this level are orientation of stem leaves and characters of the axillary hairs and peristome. The Trachypodaceae, long associated with the Meteoriaceae, is resolved as a grade basal to the Meteoriaceae. The Amblystegiaceae have been traditionally circumscribed by their mostly single and long leaf costa, cylindrical and curved spore capsule, and their preference for humid to wet environments. Lars Hedenäs and Alain Vanderpoorten examine the suggestions of late twentieth century studies, analysing comprehensive morphological datasets, that radical reclassification among the Amblystegiaceae was necessary. They found that phylogenetic studies based on both molecular and morphological data resolved many relationships at the generic level and provided strong evidence that the family should be split into the Amblystegiaceae s. str., with the taxa related to Amblystegium, Campylium, Drepanocladus, and Palustriella, and the Calliergonaceae, with the taxa around Calliergon, Scorpidium, and Warnstorfia. However, many relationships within the two families and their genera remain uncertain. For example, within Hygroamblystegium morphological and molecular evolution appear to be uncoupled, suggesting that several currently recognized morpho-species should be synonymized. A team headed by Michael Ignatov, again using a diversity of analytical methods and data, focuses in Chapter 9 on taxa traditionally classified in the Leskeaceae to reassess the relationships of mosses in the order Hypnales. They identify a basal grade and two main clades, and analyse the circumscription and changes in these and subclades under the different analytical methods. The split between Amblystegiaceae s. str. and the Calliergonaceae is again found by these authors although the taxon distribution is not identical. The Leskeaceae as traditionally circumscribed are not monophyletic but found in both main clades. Interestingly, the two main clades have some similarities to the traditional classification of pleurocarpous mosses into Leucodontales

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and Hypnales, a classification abandoned when earlier analyses of molecular data showed that the epiphytic leucodontalean taxa had been derived repeatedly from within the Hypnales. Relationships within the family Amblystegiaceae are examined in greater detail in Chapter 10, where Gisela Oliván, Lars Hedenäs and Angela Newton use molecular data to explore the phylogeny of Hygrohypnum and related taxa. Their results reveal the polyphyly of the genus and demonstrate that the morphological characters traditionally used to circumscribe the genus may reflect convergence. Within the genus there is strong support for two major clades, one with Hygrohypnum styriacum and H. luridum (the type of the genus) and the two species included as representatives of Amblystegiaceae s. str., while the other clade includes the remaining species of the genus plus Platydictya jungermannioides, Campylophyllum halleri and the two taxa chosen as representatives of Calliergonaceae, Calliergon cordifolium and Warnstorfia exannulata. These chapters have gone a long way towards suggesting some major relationships within the Hypnales, but large numbers of taxa are involved and many important families are barely represented. In order to adequately assess relationships of the remaining taxa, additional projects at a similar scale will be required. Morphology has been the primary source of information regarding pleurocarpous moss relationships in the past approximately 200 years, but has also undergone something of a revolution with the advent of cladistic methodology and the necessity to examine characters in sufficient detail to include them in data matrices. In Chapters 11 to 15 morphological character systems are explored in some depth. Lars Hedenäs, provides a review of morphological characters and their use in pleurocarpous moss systematics. The strategy of using a few “key characters,” while highly successful in many groups of organisms, has been distinctly misleading in the pleurocarpous mosses with their high levels of plasticity and parallel evolution of features. Only relatively recently have numerous and more obscure characters been studied systematically in numerous species. He outlines how in the last 20 years cladistics and the inclusion of molecular data for phylogenetic reconstruction have revolutionized our understanding of pleurocarpous moss relationships. As molecular information is largely independent of morphology, the reliability of the latter in reconstructing relationships can now be assessed. He notes that relationships that are well supported by molecular data are frequently suggested by morphology, but that morphology yields more ambiguous results than molecular data, most likely due to incorrect interpretations of homology. The latter is especially serious for taxa with orthotropous (earlier called “erect”), specialized spore capsules. However, morphology sometimes reveals relationships that have not yet been resolved by molecular data. Hedenäs concludes that molecular phylogenies can be fully interpreted only in the light of structural similarities or differences between taxa. Morphological characters used to delimit taxa within the African Entodontaceae are reevaluated by Elizabeth Kungu and Royce Longton. Characters available in both the sporophyte and gametophyte are described and assessed in the light of the restrictions incurred due to morphological reduction. Gametophyte structures are examined for characters to reinforce the taxonomic boundaries based on peristome ornamentation patterns which provide key characters for delimiting both genera and species within the Entodontaceae. However, the use of peristome ornamentation patterns is confounded by the high level of variation associated with peristome reduction. Examination of internal peristome structure demonstrates a relationship with function and proves that the major differences in surface ornamentation between papillose and striate reflect a difference in internal deposition. Morphology indicates that the family as currently recognized is probably not monophyletic and the status of Pylaisiobryum is unresolved. The homologies of stem structures in pleurocarpous mosses, especially pseudoparaphyllia and similar structures are revisited in Chapter 13 by Michael Ignatov and Lars Hedenäs, where they give an overview of current definitions of different stem structures in pleurocarps. Paraphyllia are usually considered as organs not concentrated around branch initials, but their observations reveal that positional and structural homologies in “paraphyllia” and “pseudoparaphyllia” suggest that the distinctions between paraphyllia, pseudoparaphyllia and proximal branch leaves remain unclear. A set of characters for the description of the diversity of foliose structures found at the base of branches

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or around branch initials is suggested, replacing the commonly generalized character of pseudoparaphyllia absence versus presence. The two following chapters (14 and 15) examine specific aspects of the branching structure of pleurocarpous mosses. Angela Newton discusses the history and application of the concepts of acrocarpy and pleurocarpy, and the implications of these features for the exploitation of morphological characters in the systematic study of pleurocarpous mosses. The necessity of “deconstructing” branching architecture into modules is emphasized. The components of branching architecture are analysed, described and figured, including case studies of individual species. Ray Tangney emphasizes structural concepts and examines the way in which architectural terms, as used in the analysis of Tracheophytes, have increased our understanding of branching in mosses. He differentiates between monopodial and sympodial growth and discusses repeated growth units. The concept of the architectural unit, not previously applied to mosses, is utilized to help recognize both the type of branching and the hierarchical level at which branching is occurring, aspects of branching analysis that have had insufficient emphasis. In doing so, differences are highlighted between sequential growth (branching that builds architectural units), and reiterative growth (growth that repeats the architectural units). The origins of pleurocarpous mosses are explored in Chapters 16 and 17, using fossil and molecular data. Reviewing Paleozoic and Mesozoic fossil mosses, Michael Ignatov and Dmitry Shcherbakov address the question of whether pleurocarpous mosses originated before the Cretaceous. They found that some Paleozoic, Triassic and Jurassic fossils are similar to extant pleurocarps in some respects, but that other peculiarities of these fossil mosses make their immediate placement in extant groups problematic. They describe a new genus and species from the Upper Jurassic of Transbaikalia, concluding that this species is probably the fossil most similar to extant pleurocarps among pre-Cenozoic fossils. This new fossil corroborates the conclusions of the team headed by Angela Newton and Niklas Wikström, who explore the patterns of diversification of the pleurocarps and estimate possible dates for their origins using molecular data, calibrated on the fossil date of 450 myr for the origin of land plants. Their results suggest that the earliest-diverging extant lineages in which pleurocarpy is found originated in the mid Jurassic (at 194–161 mya), significantly before the period in which the majority of the extant lineages diversified (about 165–131 mya), probably over a (geologically) short period of time. This radiation coincides with the diversification of the angiosperms in the early Cretaceous and is earlier than the period in which angiosperm forests came to dominate the terrestrial environment in the early Cenozoic, suggesting that pleurocarpous mosses were well established before the appearance of the highly structured forests that now exist. In the final two chapters evolutionary questions are explored. Niklas Pedersen and Angela Newton use Bayesian inference and maximum likelihood methods, with chloroplast and mitochondrial DNA sequence data, to evaluate phylogenetic relationships within the Ptychomniales. The genus Glyphothecium was found to be polyphyletic, and a new genus described. They then use the resulting topology to study evolution of 18 morphological characters, and to test whether the evolution of dwarf males is correlated with morphological variation and the epiphytic habit. Reconstructions of morphological characters using maximum parsimony and maximum likelihood are mostly congruent although maximum likelihood reconstructions indicate high uncertainties at most internal nodes. Correlation tests suggest that the evolution of dwarf males is significantly correlated with twelve of the morphological characters studied. In addition, the correlation tests indicate that the presence of dwarf males may promote morphological evolution. Continuing the theme of comparison between pleurocarps and angiosperms, in Chapter 19 Ray Tangney examines the distribution patterns of pleurocarpous mosses in the Australasian region. His analysis reveals patterns, also known for angiosperms, that form a network of general distribution tracks and highlight different areas within the region. The combination of this general pattern of distribution with vicariance, the spatial separation of closely related taxa, emphasizes a relationship between taxa and localities stronger than that expected if long-distance dispersal was a major determining factor in forming distributions. This suggests a major role for allopatric evolution, and a distinction is drawn between the timing of the origin of taxa and the time of the origin of the

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ancestral range. He concludes that differentiation of taxa may occur at different times within ancestral ranges and therefore that taxa of different ages and taxonomic levels may share the same present-day distribution through congruence of ancestral ranges and interaction with regional geological and ecological processes. Many important families of pleurocarpous mosses could not be included in this symposium, either because they have not been studied in sufficient depth, or through logistical constraints. The sheer size of the pleurocarpous moss clade, combined with the apparent rapid diversification of a large number of individual lineages, makes resolution of the relationships in this group a formidable task. The evidence presented here for the homoplastic nature of many of the morphological characters traditionally used to recognize and circumscribe many of the taxa, especially families, would seem to indicate that use of morphology as a source of systematic data is doomed. Yet at the same time it is evident that by careful examination and critical evaluation of characters, a great deal of useful information can be obtained, that is both interesting in its own right, and as a source of data for systematic and evolutionary studies. Further resolution of the relationships of the pleurocarpous mosses, although challenging, seems to be achievable. As in this symposium volume, building from both directions — dense sampling for genus and family level studies, combined with “backbone” analyses of broadly sampled regions of the topology — will allow us to resolve the relationships of the pleurocarpous mosses, and at the same time, explore some very interesting questions. The input of reviewers for the individual chapters is gratefully acknowledged. Amgueddfa Cymru — National Museum Wales provided facilities for the symposium, and the Natural History Museum contributed logistical support. Thanks also to the many others who supported and encouraged us in this project. Angela Newton Ray Tangney

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Editors Angela Newton is the Research Bryologist at the Natural History Museum, London, where her research focuses on the systematics of bryophytes, in particular the origins and relationships of lineages of pleurocarpous mosses, and the evolution of morphological features in mosses. Her current projects include research on dating the diversification of the pleurocarpous mosses using molecular sequence data, and relating these diversification events to the origins of angiosperm forests; studies of the role of dwarf males in promoting morphological and genetic diversity in mosses; floristic work in Central America and south-east Asia; and monographic studies of the pan-tropical Pterobryaceae. Dr. Newton received her M.Sc. in Plant Systematics at Reading University in 1983 and, after several years working as a curator in a local museum and in local and national biological records centres, moved to the United States, where she received her Ph.D. in Bryophyte Systematics from Duke University, North Carolina in 1993. She then worked as a post-doctoral researcher at the National Museum of Natural History in Washington, D.C. until 1997, then at the Instituto de Ecologia, in Xalapa, Mexico until 1998. She has carried out extensive field work in Central and South America, and in Australasia and is the author of over 30 research publications. She has served as a member of Council on the Systematics Association and the British Bryological Society, and is a member of the International Association of Bryologists, International Association of Plant Taxonomists, American Society of Plant Taxonomists, and the American Bryological and Lichenological Society. Ray Tangney is Head of Cryptogamic Botany and Curator of Bryophytes at Amgueddfa Cymru — National Museum Wales in Cardiff. His primary interests are the systematics, evolution and biogeography of the pleurocarpous mosses. His research is mainly specimen-based taxonomic study, augmented by DNA sequence data, addressing problems of classification and evolution. He also undertakes empirical and theoretical studies on the biogeography of mosses and has a strong interest in spatial patterns in the distributions of related taxa, and on branching in mosses, applying techniques of architectural analysis to problems of branching pattern. He has extensive field experience in New Zealand and its sub-antarctic regions, Australia and New Caledonia, and is the author of 20 research papers. He is undertaking continuing work on a monograph of the Lembophyllaceae and he is contributing treatments of the Polytrichaceae and Lembophyllaceae to the Moss Flora of New Zealand project. He is currently co-editing a book on biogeography in a changing world. Dr. Tangney received his Ph.D. at the University of Otago in 1994 and after teaching there for eight years moved to Wales in 2000. He has served on the Council of the Systematics Association and the British Bryological Society and he is a member of the International Association of Bryologists.

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Contributors Neil E. Bell Department of Botany Natural History Museum Helsinki, Finland

Sanna Huttunen Botanical Museum University of Helsinki Helsinki, Finland

Rolf Blöcher Nees-Institute for Biodiversity of Plants University of Bonn Bonn, Germany

Michael S. Ignatov Main Botanical Garden of Russian Academy of Science Moscow, Russia

Vera K. Bobrova Belozersky Institute of Physicochemical Biology Moscow State University Moscow, Russia

Hans (J.D.) Kruijer Nationaal Herbarium Nederland Universiteit Leiden Branch Leiden, The Netherlands

William R. Buck Institute of Systematic Botany New York Botanical Garden Bronx, New York Laura Lowe Forrest Department of Plant Biology Southern Illinois University Carbondale, Illinois

E. M. Kungu Royal Botanic Garden Edinburgh, Scotland Royce Longton School of Biological Sciences, Plant Sciences Laboratories University of Reading Reading, UK

Anastasia A. Gardiner Belozersky Institute of Physicochemical Biology Moscow State University Moscow, Russia

Irina A. Milyutina Belozersky Institute of Physicochemical Biology Moscow State University Moscow, Russia

Lars Hedenäs Swedish Museum of Natural History Department of Cryptogamic Botany Stockholm, Sweden

Angela E. Newton Department of Botany Natural History Museum London, UK

Boon-Chuan Ho Nationaal Herbarium Nederland Universiteit Leiden Branch Leiden, The Netherlands

Terry J. O’Brien Department of Biological Sciences Rowan University Glassboro, New Jersey

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Gisela Oliván Biology Department Duke University Durham, North Carolina Niklas Pedersen Department of Botany Natural History Museum London, UK Dietmar Quandt Botanisches Institut Technische Universität Dresden Dresden, Germany Dmitry E. Shcherbakov Paleontological Institute Russian Academy of Sciences Moscow, Russia

Ray Tangney Department of Biodiversity and Systematic Biology Amgueddfa Cymru — National Museum Wales Cardiff, UK Alexey V. Troitsky Belozersky Institute of Physicochemical Biology Moscow State University Moscow, Russia Alain Vanderpoorten Department of Life Sciences University of Liège Liège, Belgium Niklas Wikström Department of Systematic Botany, Evolutionary Biology Centre Uppsala University Norbyvägen, Sweden

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Contents Chapter 1

The History of Pleurocarp Classification: Two Steps Forward, One Step Back..............................................................................................................1

William R. Buck Chapter 2

The Phylogenetic Distribution of Pleurocarpous Mosses: Evidence from cpDNA Sequences.............................................................................19

Terry J. O’Brien Chapter 3

Pleurocarpy in the Rhizogoniaceous Grade...............................................................41

Neil E. Bell and Angela E. Newton Chapter 4

Reevaluation of the Phylogeny of the Hypopterygiaceae (Bryophyta) Based on Morphological and Molecular Data ...........................................................65

Hans (J.D.) Kruijer and Rolf Blöcher Chapter 5

Growth Patterns in Calyptrochaeta Desv. (Daltoniaceae).......................................111

Boon-Chuan Ho and Hans (J.D.) Kruijer Chapter 6

Advances in Knowledge of the Brachytheciaceae (Bryophyta)..............................117

Sanna Huttunen, Anastasia A. Gardiner and Michael S. Ignatov Chapter 7

Phylogenetic Relationships within the Moss Family Meteoriaceae in the Light of Different Datasets, Alignment and Analysis Methods....................145

Sanna Huttunen and Dietmar Quandt Chapter 8

The Amblystegiaceae and Calliergonaceae..............................................................163

Lars Hedenäs and Alain Vanderpoorten Chapter 9

On the Relationships of Mosses of the Order Hypnales, with Special Reference to Taxa Traditionally Classified in the Leskeaceae...................177

Michael S. Ignatov, Anastasia A. Gardiner, Vera K. Bobrova, Irina A. Milyutina, Sanna Huttunen, and Alexey V. Troitsky Chapter 10 Phylogeny of Hygrohypnum Lindb. Based on Molecular Data...............................215 Gisela Oliván, Lars Hedenäs, and Angela E. Newton

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Chapter 11 Morphological Characters and Their Use in Pleurocarpous Moss Systematics .....................................................................................................227 Lars Hedenäs Chapter 12 Character Reduction and Peristome Morphology in Entodontaceae: Constraints on an Information Source .....................................................................247 E. M. Kungu, Royce Longton, and L. Bonner (deceased) Chapter 13 Homologies of Stem Structures in Pleurocarpous Mosses, Especially of Pseudoparaphyllia and Similar Structures................................................................269 Michael S. Ignatov and Lars Hedenäs Chapter 14 Branching Architecture in Pleurocarpous Mosses...................................................287 Angela E. Newton Chapter 15 Sympodial and Monopodial Growth in Mosses: Examples from the Lembophyllaceae (Bryopsida) ...........................................................................309 Ray Tangney Chapter 16 Did Pleurocarpous Mosses Originate before the Cretaceous?.................................321 Michael S. Ignatov and Dmitry E. Shcherbakov Chapter 17 Dating the Diversification of the Pleurocarpous Mosses ........................................337 Angela E. Newton, Niklas Wikström, Neil Bell, Laura Lowe Forrest, and Michael S. Ignatov Chapter 18 Phylogenetic and Morphological Studies within the Ptychomniales, with Emphasis on the Evolution of Dwarf Males ...................................................367 Niklas Pedersen and Angela E. Newton Chapter 19 Biogeography of Austral Pleurocarpous Mosses: Distribution Patterns in the Australasian Region .......................................................................................393 Ray Tangney Index ..............................................................................................................................................409

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History of Pleurocarp 1 The Classification: Two Steps Forward, One Step Back William R. Buck CONTENTS Abstract ..............................................................................................................................................1 1.1 Introduction...............................................................................................................................1 1.2 History of Morphology-Based Classifications.........................................................................2 1.3 Molecular-Based Classifications ............................................................................................13 1.4 Conclusions.............................................................................................................................14 References ........................................................................................................................................15

ABSTRACT The classification of pleurocarpous mosses has traditionally lagged behind that of acrocarps. Hedwig had only five genera of pleurocarps, which he based on sporophyte characters. The first modern attempt to understand relationships was by Schimper, who sorted pleurocarps into families. Schimper relied primarily on gametophytic characters to sort out the group. Subsequently, based on Philibert’s peristome studies (focusing primarily on acrocarps), Fleischer proposed a new system that was primarily sporophyte-based. This system was picked up by Brotherus for Die natürlichen Pflanzenfamilien. It wasn’t until about the 1990s that once again a gametophyte-based classification gained favour. The advent of the use of molecular data has allowed bryologists to present classifications free of morphology. Initial work using one-gene trees resulted in faulty classifications. Multiple-gene trees have refined the process. A combination of multiple genes with carefully observed morphology should provide us with a stable classification. To date, though, the largest group among the mosses lacking phylogenetic resolution is the Hypnales.

1.1 INTRODUCTION Since my earliest days as a bryology graduate student, my overriding interest has been in how different mosses, and especially pleurocarps, are related to one another. I initially took the approach that insights into moss phylogeny were best gained through the examination of as many specimens as possible. Through the input of a large amount of data, and thinking about it, I developed my own ideas about pleurocarp relationships. Certainly, as I learned more, and examined more specimens and saw more species in the field, my ideas changed. I have relied heavily on my intuition but will admit that such methodology is difficult to transmit to others. Nevertheless, I have repeatedly been amused when younger people who have used more modern methodologies have wondered, often in irritation, how I “guessed” the same answer that their computers told them. I am not

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psychic. The fact that my study of plants has led me to answers that have been corroborated by other methodologies should be inspirational to others because the answers are there, just waiting to be found. Like many traditional systematists, I was at first leery of results from molecular data because of the odd results that were initially forthcoming. However, my goal of understanding how different pleurocarps are related to one another was more important than the means of how that knowledge was obtained. In 1997, at the annual meeting of the American Bryological and Lichenological Society in Montreal, Canada, both Terry Hedderson and Jon Shaw asked me if I would be interested in going to their labs to do molecular work on pleurocarps. It had never even occurred to me that I might do such a thing. In the end, though, I was most interested in the data. Also, since most people who knew me would have said that I was the last person they would have suspected of doing molecular work, this was also a motivation to give it a try. In the end, I chose to work with Jon Shaw because he was in the United States and I knew him better. That way, if I failed it would be less embarrassing and easier to slink back home. So, although I will definitely be discussing the impact of molecular data on pleurocarp classification, remember that we have over 200 years of history dealing solely with morphology, and so that aspect will dominate my essay. For this purpose I will be updating my earlier paper (Buck, 1991) on the subject. Since the earliest days of moss classification, pleurocarps have been the ugly stepchild of the mosses and have garnered an inappropriately small amount of attention. Based on Crosby et al.’s (2000) Checklist of the Mosses, pleurocarps constitute about 42% of all moss species. Although Hedwig (1801), in Species Muscorum Frondosorum, recognized 30 genera of acrocarps, he recognized but five genera of pleurocarps: Pterigynandrum, Fontinalis, Neckera, Leskea and Hypnum. All known tropical pleurocarps were forced into what are now considered primarily temperate genera. The classification of pleurocarpous mosses has undergone tremendous alterations since the time of Hedwig and his contemporaries. Not only have the classifications themselves changed, but the underlying philosophies upon which they were based have changed. This is particularly interesting because there seems to have been a cyclical pattern in the philosophic basis for pleurocarpous classification. Initially I will highlight the historic philosophic oscillations and the ramifications they have had on classification schemes. As mentioned earlier, the treatments accorded acrocarps and pleurocarps have always been somewhat disparate. This is particularly marked in the early literature. Nevertheless, acrocarp classification has undergone the same kinds of fluctuations that I discuss here for the pleurocarps. Finally, I will discuss the influence of molecular data on pleurocarp classification. In some ways it has been extraordinarily enlightening, but has completely failed us in other areas, at least so far.

1.2 HISTORY OF MORPHOLOGY-BASED CLASSIFICATIONS The very earliest work on mosses was hampered by a lack of both adequate optical equipment and an understanding of the life cycle. Early researchers tried to equate morphological structures in mosses with those in flowering plants. In particular, the capsule, or parts of it, was considered homologous to parts of the flower. For example, both Dillenius (1741) and Linnaeus (1753) considered the moss capsule to be homologous to the flower’s anther. It was not until Hedwig (1782, 1783, 1787–1789) (Figure 1.1) that the sexuality of mosses was understood. Despite the clarity of Hedwig’s prose and illustrations, there was still doubt and dissension. For example, Palisot de Beauvois (in de Jussieu, 1789) proposed that the moss capsule was hermaphroditic, with the spores as male pollen and the columella as the female. He later expanded this view (Palisot de Beauvois, 1805). According to Margadant (1968), his misinterpretation was based on observations of Brownian movement of a crushed columella under the microscope. Although Hedwig’s morphological interpretations were generally accepted and well received, the taxonomic implications he based on them were less popular. For example, Menzies (1798, p.

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FIGURE 1.1 Johann Hedwig (1730–1799).

64) complained that “his genera are too artificial, and that their characters are taken from parts so minute and difficult to examine, that they rather tend to perplex and discourage a young beginner in his investigations, than aid his pursuits in acquiring a scientific knowledge of this intricate tribe.” (You can almost hear those same words today!) Menzies therefore rejected characters such as the number of peristome teeth. Most of Hedwig’s earlier works were concerned primarily with the morphology and physiology of mosses. It was his posthumous Species Muscorum Frondosorum (1801) that took his understanding of mosses and translated it into a classification scheme for the mosses he knew. His classification was generally based on capsule and peristome characters and the position of the male in relation to the female inflorescence, i.e., the sexuality. He courageously described new genera rather than relying solely on the handful of ones used at that time. It is this latter point, the proliferation of genera, that drew the most criticism from cryptogamists of the day (e.g., Smith, 1804). However, he also had his defenders (e.g., Schwägrichen, 1810) who continued his precedence. Florschütz (1960) summarized Hedwig’s impact on bryology of the early nineteenth century. As mentioned earlier, Hedwig (1801) recognized only five pleurocarpous genera, but he made no attempt to speculate upon the relationships between them. The important point here, though, is that the genera were primarily differentiated on characters of the sporophyte. Also, Hedwig, following tradition, referred to perichaetia and perigonia as female and male flowers. This tradition has continued to the present in the use of the term inflorescence for the same structures. This association between capsule and flower is critical not only in understanding classifications of the late eighteenth and early nineteenth centuries, but in understanding assumptions that have persisted to the present. Despite criticism by some, the majority, if not all, of the major bryological workers of the first half of the nineteenth century followed the principles established by Hedwig. In other words, gametophytic characters were superseded in importance by sporophytic ones. For example, Hooker and Taylor (1827), disregarding Hedwig’s (1801) segregation, combined Dicranum and

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FIGURE 1.2 Wilhelm Philipp Schimper (1808–1880).

Fissidens into a single genus because of peristomial similarities. The obvious gametophytic divergences were accorded no taxonomic status. This practice flourished, although to a less extreme extent, until the mid-nineteenth century. The publication of the Bryologia Europaea (Bruch et al., 1836–1855) marked a turning point in the classification of pleurocarpous mosses. Prior to that time all moss families had been, at best, vague concepts and, except for morphologically odd groups (e.g., the Polytrichaceae), most mosses were in a single family. There can be little doubt that Schimper (Figure 1.2) was the driving force behind this advancement. The Bryologia Europaea itself did not provide familial descriptions, but rather, by way of a “Conspectus” at the front of each volume, generic inclusions were indicated for each family. Schimper’s Corollarium (1855), though, corrected that deficiency by offering descriptions of each family as well as revising familial concepts. Schimper’s contributions are particularly impressive in light of the fact that he was not just modifying a previous classification system as later workers were able to do. Rather, he took an unclassified agglomeration of genera and provided, for the first time, a unified classification. Vitt (1984) argued that Schimper primarily refined Bridel-Brideri’s classification (1826–1827), but I disagree, at least for the pleurocarps. Bridel-Brideri merely sorted the pleurocarps into groups based on presence or absence of peristome and whether the peristome was single or double. Schimper’s knowledge allowed him to reject boldly the notion of the overriding importance of the sporophyte in the pleurocarps and to construct a classificatory scheme based primarily on gametophytic characters. He realized that a system of classification based solely on the sporophyte led to the grouping together of many disparate elements. Most telling is his discussion under the description of the Hypno-Leskeaceae (Schimper, 1855, p. 111) (and I liberally translate his difficult Latin): Bryologists who place the priority of a system on the peristome alone, thereby separating closely related taxa, bring together almost the whole cohort of pleurocarpous mosses into one family, and whatever the external appearance may be, which is the only feature available to the inexpert beginner, they refer

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FIGURE 1.3 William Mitten (1819–1906). Hypna to the Leskeaceae and Orthothecia and Leskeae to the Hypnaceae, thereby creating an inextricable chaos in the so-called methodical disposition of mosses which obscures the approach to bryology.

Schimper, therefore, not only created the first modern familial classification of pleurocarpous mosses, but reversed the philosophy upon which the classification was based. His pioneering efforts laid the groundwork from which all subsequent classification attempts diverged. Following closely in the wake of Schimper, Mitten (1859) criticized many of his predecessors, especially Carl Müller and his Synopsis (1848–1851), for relying on sporophytic features. Mitten (Figure 1.3) perceived classifications based on capsular characters as artificial. Unlike Schimper, though, Mitten supplied arguments against sporophytic reliance. He documented the reduction processes of peristomes and was the first to relate them to capsular orientation: “it appears to be a general law, that the more the theca is inclined or pendulous, the greater is the development of the peristome” (Mitten, 1859, p. 3). Mitten placed primary emphasis on the mode of growth and especially on the morphology of the leaves. Although Mitten indeed did rely on some basic peristomial characters in his classification, for the pleurocarps they were used above the familial level. Since Mitten was the premier bryologist of the last half of the nineteenth century, his doctrine prevailed. The one real weakness with both Schimper’s and Mitten’s classifications is that they considered only regional floras. Since most pleurocarpous moss families occur over multi-continental ranges, it is often difficult for a parochial work to account for the total range of morphological variation in a family. Most regional floristicians are not familiar with the total possibilities of generic inclusions. This is particularly relevant for pleurocarps in which most of the families have a tropical center of diversity. However, Brotherus (Figure 1.4) remedied this particular criticism in his treatment (Brotherus, 1901–1909) of the mosses in the first edition of Die natürlichen Pflanzenfamilien. Although flawed by the complexities of such a large undertaking, Brotherus’ opus was the first to encompass all the mosses within a modern scheme based upon a well-considered philosophy. Although some earlier works attempted such a plan, e.g., Bridel-Brideri (1826–1827) and Müller (1848–1851),

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FIGURE 1.4 Viktor Ferdinand Brotherus (1849–1929).

many fewer taxa of pleurocarps were known, pleurocarpic generic concepts were broad and strongly heterogeneous, and relationships were ill conceived. Probably influenced by Schimper in particular, Brotherus’ classification of pleurocarpous mosses (1901–1909) is primarily weighted toward gametophytic characters. In other words, Brotherus took Schimper’s viewpoint and applied it globally to the pleurocarps. It is not unexpected that familial concepts in the pleurocarps would be artificial, since this was truly a first sorting. Many characters were misunderstood, and thus convergences (of both the gametophytic and sporophytic generations) were mistakenly aligned. Brotherus’ work, though, is best seen as the most magnificent expression of a philosophy about to be superseded. In 1884 Philibert (Figure 1.5) began a long series of articles, running until 1902, that changed the outlook of bryophyte classification. In this series, “Études sur le péristome,” Philibert, through the intricate study of peristome morphology with the compound microscope, proposed that classification of mosses be based primarily on peristomial similarities. The corollary was that gametophytic similarities without sporophytic congruencies were merely coincidences of nature not to be taken into account when speculating on relationships. Philibert considered peristomial characters to be evolutionarily conservative and thus the appropriate ones upon which to base a classification. His observations and the conclusions he drew from them marked the end of a gametophytedominated era of classification. Although Philibert’s observations were more detailed than those of Hedwig (indeed, the technological level of Hedwig’s microscopy did not allow such study), they nevertheless had the same general impact. That is, Philibert’s observations led toward a sporophytedominated classification. Philibert never proposed any sort of general classification. It should be noted, though, that Philibert primarily based his conclusions on the observations of acrocarpous mosses. He did discuss pleurocarps in the more general articles (especially those on the endostome), but his primary data were from acrocarps. However, he presented principles upon which a classification could be constructed. It was Max Fleischer (Figure 1.6) who took Philibert’s principles and applied them. Nominally treating a moss flora of Java, Fleischer’s “Die Musci der Flora von Buitenzorg” (1904–1923) greatly exceeded its bounds, and while it dealt with only regional species, it nevertheless discussed all

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FIGURE 1.5 Henri Philibert (1822–1901).

FIGURE 1.6 Max Fleischer (1861–1930).

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STAMMESGESCHICHTLICHE UEBERSICHT DER GATTUNGEN DER SEMATOPHYLLACEAE.

Clastobryopsis

Pterobryaceae

Struckia Clastobryella

Hageniella

Clastobryum Clastobyrophilum Aptychopsis Mastopoma Gammiella Heterophyllium

Acanthocladium Brotherella

Trismegistia Rhaphidorrhynchium

Pylaisiadelpha Schraderella

Schröterella

Sematophyllum

Schraderobryum

Warburgiella

Macrohymenium Rhaphidostichum Acroporium Trichosteleum Acanthorrhynchium

Pterogoniopsis Pterogonidium

Meiothecium

Meiotheciopsis

Potamium Chionostomum

Taxithelium Glossadelphus

Syringothecium

FIGURE 1.7 Diagram of evolutionary speculations in the Sematophyllaceae from Fleischer’s “Die Musci der Flora von Buitenzorg” (1904–1923).

moss genera known at that time. The pleurocarps in particular, perhaps because they came toward the end of the volumes when Fleischer had had more time for reflection, were treated in more detail, and it is the pleurocarps in which he suggested the most changes in classification. What made Fleischer’s monumental work so significant, though, was not just that it pursued Philibert’s principles, but that it was the first attempt to understand the evolutionary relationships among the pleurocarps. This is amply demonstrated by Fleischer’s use of diagrams showing postulated directions of evolution (Figure 1.7). Darwin’s (1859) Origin of Species had been published almost a half century earlier, but bryology has never been in the vanguard of plant sciences in adopting new ideas. The paucity of workers alone has primarily made it a field in which, even into the twentyfirst century, we are still scrambling to catalogue the world’s bryoflora. Therefore, it is significant that Fleischer tried to present a classification for the pleurocarpous mosses that reflected phylogeny. The fact that his understanding of evolution was seriously flawed is easily pardoned by the era in which he lived. Although the alternation of generations was well established by Fleischer’s time (Hofmeister, 1851; Strasburger, 1894) and the strict homology of capsules and flowers had long been abandoned, the consequent assumption of the conservative nature of the capsule remained. Fleischer (see vol. 1, pp. XIII–XVII) still referred to capsules as reproductive organs. Nevertheless, he was the first bryologist to recognize apparently natural relationships between genera and families of pleurocarps that are now taken for granted. His insights were surely gained in part by his intimate familiarity with both his native temperate zone flora, as well as his adopted tropical one in which pleurocarpous mosses are so diverse and abundant. Previous workers, from Hedwig and BridelBrideri to Schimper and Mitten, were familiar only with tropical taxa from dried herbarium specimens sent to them by collectors, who themselves, for the most part, were unfamiliar with the mosses. Fleischer, therefore, in a pioneering effort, was able to make truly significant strides in the

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FIGURE 1.8 Marshall Robert Crosby (1943– ).

classification of pleurocarps by an intimate field knowledge of a broad flora and the application of both Darwinian evolutionary and Philibertian peristomial hypotheses. In the same way that Brotherus (1901–1909) culminated the era in which classification of pleurocarpous mosses was dominated by the gametophyte, later on Brotherus (1924, 1925) took Fleischer’s lead in sporophytic emphasis and applied it across the board to the pleurocarps in the second edition of Die natürlichen Pflanzenfamilien. Dixon (1932) summarized this philosophy in Verdoorn’s Manual of Bryology. The Fleischer–Brotherus system dominated moss systematics to the end of the twentieth century. That is not to say that there have not been attempts to refine the classification, but they have been just that, modifications. For example, Crosby (Figure 1.8), probably the most modern ardent follower of Philibert’s principles, reexamined the Hookeriales and divided them into families along strictly peristomial lines (Crosby, 1974). I used primarily peristomial features in my refinement of the familial concept of the Entodontaceae (Buck, 1980). With a broader perspective, Vitt (1984) presented a family classification of all mosses. Each of these examples, and more could be cited, relied on the assumption, sometimes unstated, that characters of peristomial morphology are conservative and therefore are the best indicators of phylogenetic relationships among the pleurocarps. However, dissension was afoot. In the last two decades of the 1900s there was an ever increasing trend to study new morphological characters, especially gametophytic ones, for use in classification. Initially these studies focused just on the range of variation in characters and their potential for use. For example, Ireland (1971) studied the morphology and distribution of pseudoparaphyllia in North American mosses; Saito (1975) and Norris (1978) initiated the study of axillary hairs; and Crundwell (1979), Koponen (1982), and Hedenäs (1987a) supported the use of rhizoidal morphology and placement in taxonomy. Later workers then applied many of these gametophytic characters to suggest changes in the position of taxa (e.g., Hedenäs, 1987b, 1989). In spite of the fact that the generation emphasized in moss classification had oscillated repeatedly from one to the other, in the modern era there initially seems to have been a reluctance to suggest that the characters revealed by these gametophytic structures might be more useful or significant than those from sporophytic features in understanding familial relationships among the pleurocarps. However, it was these exploratory studies of new characters that were probably most influential in transferring reliance back to the gametophytic generation. The increase of additional

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FIGURE 1.9 Dale Hadley Vitt (1944– ).

characters, in most part unlinked with more traditional ones but that nevertheless correlate with them, has lent greater strength to the argument of gametophyte-based classifications. In 1986, along with Dale Vitt (Figure 1.9), I suggested changes in the classification of pleurocarpous mosses (Buck and Vitt, 1986). Although we explained that our methodology was cladistically influenced, we did not discuss the underlying philosophy upon which the scheme was based. However, many of the changes proposed were based not on peristomial congruencies but gametophytic similarities. Although not thought through at the time, there was obviously a reluctance on our part to go against the established ideas of Fleischer regarding the value of sporophytic versus gametophytic characters in the pleurocarps. However, through the study of additional plant material, it became more and more clear to me, as well as other researchers, that in some cases the reliance on sporophytic characters to build phylogenetic alliances among the pleurocarps not only is suspect but actually can lead to erroneous conclusions. Certainly some peristomial characters are valuable in phylogenetic speculation. Indeed, as pointed out initially by Edwards (1979, 1984) and subsequently by Shaw et al. (1987, 1989) and Shaw and Anderson (1988), basic developmental patterns in moss peristomes are reliable indicators of higher systematic relationships (but probably above the rank of family). Although virtually all the developmental data from these workers were derived from acrocarpous mosses, I have assumed that they are equally applicable to pleurocarps. However, these developmental processes do not necessarily manifest themselves through superficial peristomial structure. For example, a moss may be eperistomate but still have the same developmental pattern as a doubly peristomate one, as in the case of Nematocladia and Helicodontium, both in the Myriniaceae (see Buck, 1982). Reductionary depositional sequences of those cell walls destined to become peristome teeth are independent of basic developmental patterns in the moss capsule. Frequently, similar environmental pressures acting through reductionary sequences on different developmental patterns may result in identical morphological structures, i.e., convergent structures. For example, epiphytic members of both the Leskeaceae and Sematophyllaceae may have exostome teeth with papillose ornamentation. Therefore, peristomial structure and ornamentation may not necessarily be reflective of phylogenetic closeness.

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FIGURE 1.10 Howard Alvin Crum (1922–2002).

It was during my earlier work on the Hookeriales (Buck, 1987, 1988) that the potential deceptiveness of peristomial similarities became clear to me. The Hookeriales are a particularly instructive order from which such observations can be drawn because there are several generic pairs that are virtually inseparable on gametophytic criteria but whose peristomes are very different. Crosby’s (1974) earlier treatment had separated the members of such gametophytically defined pairs into different families. Such a scheme seemed counterintuitive because it required the convergent evolution of whole suites of seemingly unlinked gametophytic character states, not once but several times. Thus, I reversed the life cycle generation traditionally used as the basis for establishing familial classification in the Hookeriales. Not surprisingly, with the addition of molecular data, the classification has changed again (Buck et al., 2004). Howard Crum (Figure 1.10) and I (Buck and Crum, 1990) relied totally on gametophytic characters in defining familial boundaries of the Leskeaceae/Thuidiaceae complex even though traditionally the families were separated on sporophytic differences (sometimes even into different orders). We allowed, within a single family, sporophytic evolution in which fully developed hypnoid peristomes can become greatly reduced. We correlated these reduction sequences with differences in habitat. Although Mitten (1859) first pointed out how peristome complexity is often coupled with capsule orientation (i.e., the more curved the capsule the more perfect the peristome), and such observations have been independently confirmed (e.g., Buck, 1980, p. 77), the implications of this fact on the classification of pleurocarpous mosses have been neglected. In other words, although the basis for the assumption that peristome morphology and ornamentation are conservative has been shown to be faulty, the assumption itself has persisted. Some authors (e.g., Allen et al., 1985, p. 150) have argued that because the peristome develops inside of the protective operculum, its morphology is immune from the environment and thus is conservative. However, the time during which the peristome is functional is at spore dispersal, and it is therefore at that time when natural selection acts upon it, not prior to it. The strength behind the argument that sporophytic characters are modified by environmental parameters is the fact that the same modifications have occurred repeatedly in distantly related groups. For example, reduction series can be seen in genera such as Pylaisia and Platygyrium in the Hypnaceae and Brachymenium and Actinodontium in the Bryaceae. Many epiphytic genera, such as Cryphaea and Pterobryon, also exhibit a suite of modifications, but their terrestrial ancestors are not readily evident.

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FIGURE 1.11 William Russel Buck (1950– ).

Because of the persuasiveness of such arguments, I (Figure 1.11) proposed (Buck, 1991) that a strong reliance on peristomial ornamentation and superficial morphology in the construction of a family classification of pleurocarpous mosses is inappropriate. It has been amply demonstrated, for over 100 years, that sporophyte structure is correlated with habitat. Therefore peristomial characters may not necessarily be conservative. This is not to say that there is no use for the peristome in classification. Rather, its structure often proves to be of most use in separating genera within a family rather than families within an order. I have predicted (Buck, 1991) that all the primitive genera in an order that occur in broadly similar habitats, no matter what family they may be in, would have a similar peristomial structure. Certainly this is the case in the Hypnales where there is little differentiation between the peristomes of Hypnum (Hypnaceae), Brachythecium (Brachytheciaceae), and Thuidium (Thuidiaceae), although these genera have large gametophytic divergences. Although the argument is hundreds of years old, once again we are forced to decide if gametophytic characters are more immune from natural selection than sporophytic ones, and thus more conservative. Like all organisms, mosses, with their dominant gametophyte, certainly are responsive to natural selection; otherwise there would be no way to account for current levels of speciation. However, some characters, through observation, seem to be reliable when speculating on relationships at the family level. Although I (Buck, 1991) argued that costa structure is relatively stable and thus useful in phylogenetic speculation, recent molecular data (Buck et al., 2004) has shown that such is not the case, at least in the Hookeriales. One can only assume that once a robust phylogeny is available for the Hypnales, a similar situation will be found. Other kinds of characters in which the character states have presumed to be stable within pleurocarpous familial limits include cell shape, stem anatomy, axillary hair morphology, and calyptra structure. Future phylogenetic research will probably find these as faulty as assumptions about costal morphology. Nevertheless, the advantage of the gametophyte in postulating relationships is that it has so many more independent characters than does the peristome. Therefore, it can be more obvious when whole groups of characters are correlated. Certainly there can be and are gametophytic convergences, but because of the diverse assemblage of characters available, it is improbable that great numbers of different character states would converge together during evolution.

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It should be emphasized that throughout this essay I have been discussing evolutionary trends, not dogmatic principles with unwavering applicability. Because of the great diversity found within mosses, or even within pleurocarpous taxa, exceptions can be found to every generalization. Nevertheless, because the same general structural modifications have occurred over a broad taxonomic spectrum, I think ecumenical postulation is justified. In concluding this part of the chapter, we have now swung back to the position of Schimper and Mitten, in which gametophytic characters are given more weight in developing phylogenies than are sporophytic characters. Correlations of a diverse group of gametophytic characters currently appear more reliable and provide a more stable basis for familial classification. However, as pointed out by the research of Hedenäs (e.g., 2002) and others, sporophytic characters, when examined critically, can also be useful when they correlate with gametophytic features. Certainly peristome structure should not be ignored, and in some cases it can be extremely revealing. Unfortunately, we have been saddled (e.g., Brotherus, 1924, 1925) with the relatively crude use of sporophytic features (e.g., exostome teeth papillose versus striolate) that has led to misunderstandings of relationships. The use of all characters, without a priori weighting, leads to a more balanced approach to phylogenetic speculation and family classificatory construction.

1.3 MOLECULAR-BASED CLASSIFICATIONS In the last decade, the use of molecular data for understanding phylogeny, and thus forming the bases for classification, has gone from peripheral to primary. However, it has not always been a smooth road, and certainly there have been problems. In the early days of the use of DNA sequencing, the methodology was so time consuming that it limited its usefulness. Few taxa were sampled, and even fewer loci were sequenced. As a result, early application of genomic data to phylogeny resulted in obviously flawed trees because of the use of a single, and often inappropriate, locus. The quality of molecular research has greatly improved, but we can all remember published phylogenies based on a single gene. Almost any two genetic loci will result in different trees, and obviously both cannot accurately reflect the phylogeny of the whole organism. Of course, these different trees are different because they are not the phylogeny of the whole organism, but just that of the gene that was sequenced. Such gene phylogenies may or may not mirror the evolution of the whole organism. This is particularly problematic when sequenced loci are spacers or other genetic areas that do not directly impact the ability of the moss to survive. Such single-gene trees resulted in counterintuitive phylogenies and as a consequence turned some traditional systematists against the whole methodology. Probably no single locus can provide an accurate reflection of phylogeny across all the pleurocarps, let alone all mosses, even if reasonable resolution of all nodes was possible. Despite the flaws inherent in single-gene phylogenetic trees, they nevertheless were an important step in the use and understanding of sequence data (e.g., Goffinet and Vitt, 1998). Certainly they provided some insights into evolutionary relationships that previously had not been discerned on the basis of morphological evidence and study. Such examples are the seemingly close relationships between, for example, Leptobryum and the Meesiaceae (Goffinet et al., 2001) and Anacamptodon and the Amblystegiaceae (Buck et al., 2000). Initial knee-jerk reactions against such seemingly bizarre relationships were replaced by a closer look at the morphologies involved and, indeed, structural similarities could be found. This is similar to early work on the monocots where relationships suggested by molecular data were later verified by tedious but significant structural similarities, such as embryology. Because such relationships that initially seemed improbable have subsequently been verified (or perhaps corroborated is more accurate), the potential use of molecular sequence data has been validated. The fact that single-gene trees are inherently flawed has led to the use of multiple genes to reconstruct phylogenies. When one gene suggests a particular phylogeny, it may give us something to think about, but it would be foolish to follow it slavishly. However, when a whole suite of genes

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indicates the same evolutionary scenario, then it is time to look very closely at the suggested phylogeny. It is hard to imagine that non-linked loci, especially from different compartments that all provide the same story, could possibly be deceptive. This is particularly true when three, and preferably more, loci are sequenced. To my eye, some of the most impressive phylogenetic research on mosses being done today looks at as many genes as possible. The research of Shaw (e.g., Shaw et al., 2004) comes immediately to mind, where he has looked at numerous loci in his Sphagnum research. For the immediately foreseeable future, this seems to be a model to strive for. It is difficult to imagine that the sequencing of the entire genome of more than a handful of bryophytes will be possible anytime soon. It certainly will not be practical for understanding the vast majority of phylogenetic questions in pleurocarps. Some will ask why we should bother to look at a dozen genes when a very similar story can be garnered from just a handful. For those of us involved in pleurocarp research, this should be particularly obvious. By far the largest group of pleurocarpous mosses are the Hypnales, encompassing both the traditional Hypnobryales and the Isobryales (or Leucodontales). Indeed, it was genomic evidence from only a few loci that led us to merge the two traditional groups, and accept the fact that the largely epiphytic and tropical Isobryalean mosses must have evolved repeatedly from terrestrial Hypnobryalean mosses (De Luna et al., 2000; Buck et al., 2000). Through recent research on pleurocarps, phylogenetic systematists have been able to resolve the circumscription of some families, but there is still virtually no resolution to the relationships among the families of the Hypnales. As different as some families may appear to the traditional systematist, molecular data have still been unable to resolve even the most basic backbone. Sure, we can glance at the plants and immediately recognize, for example, the Thuidiaceae from the Brachytheciaceae. However, all evidence we have strongly suggests that the Hypnales have rapidly diversified in relatively recent geological times (cf. Kürschner and Parolly, 1999). Studies such as that by Shaw et al. (2003) have shown that despite the taxonomic diversity of the Hypnales, there is relatively little genetic diversity when compared to the much smaller Hookeriales and Ptychomniales. Understanding the backbone phylogeny of the Hypnales remains the frontier in pleurocarp phylogenetic research. The challenge will be to find appropriate loci to sequence that actually reflect the phylogeny of the order. However, not until such research is completed do we have any real hope for a stable classification for the pleurocarps. One advantage, and simultaneously a disadvantage, of molecular phylogenies is that because it is now so easy to sequence DNA, classifications are rapidly changing. For example, Buck and Goffinet (2000) published a classification for the mosses based primarily on molecular data, but supplemented by morphological data, especially when molecular data were unavailable or ambiguous. This classification was adopted by GenBank. However, in just four years, we (Goffinet and Buck, 2004) have published yet another classification, parts of which are significantly different from our previous classification. At least for the immediate future, such instability will remain a fact of life as we gain greater understanding of the relationships among mosses, and pleurocarps in particular. Fortunately, the nomenclatural novelties remain primarily at higher taxonomic levels and have little effect on species names. Even at the generic and species levels, though, we must expect some alterations as a greater percentage of mosses are sequenced and our understanding of relationships is refined (e.g., Ignatov and Huttunen, 2002). To date, almost all phylogenetic implications derived from molecular data have been reinforced by morphological data. A major exception, though, is in the Amblystegiaceae (Vanderpoorten et al., 2002). It is difficult to know if such incongruities between molecular and morphological data are based on inadequate sampling or reality.

1.4 CONCLUSIONS We now take for granted that our classification should reflect the phylogeny of the plants, and that in and of itself has been a significant step, albeit one that was quietly taken. Nevertheless, it is important that nomenclaturally recognized nodes on trees still be identified by morphological as well

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as molecular characters. If evolutionary distance exists between two groups of mosses, then there should be some visible sign of this divergence and careful observation will reveal it. Therefore, it is probably as important as ever that systematists not abandon studying the actual plants themselves. Any taxonomic category, whether it be from a lowly variety to a mighty order, will not gain favour in the systematic community if it cannot be identified morphologically. When DNA sequencing now takes so little time, that cannot be used as an excuse for not studying the plants themselves. I personally went into systematics because it was the plants themselves that attracted me and by studying them I have come to feel how they are related to one another. Trying to unravel that evolutionary puzzle is what has motivated me. Now, I find myself unsympathetic to the excuse I have heard from all too many students, that “morphology is too hard.” The future of pleurocarp phylogeny and classification is not one of the past based solely on morphology, or one of the present based on seemingly isolated molecular data, but a combination of both molecular and morphological data.

REFERENCES Allen, B. H., Crosby, M. R. and Magill, R. E. (1985 [1986]) A review of the genus Stenodictyon (Musci). Lindbergia, 11: 149–156. Bridel-Brideri, S. E. (1826–1827) Bryologia Universa seu Systematica ad Novam Methodum Dispositio, Historia et Descriptio Omnium Muscorum Frondosorum hucusque Cognitorum cum Synonymia ex Auctoribus Probatissimis. 2 volumes. Barth, Lipsiae. Brotherus, V. F. (1901–1909) Musci. In Die natürlichen Pflanzenfamilien, Vol. 1(3) (ed. A. Engler and K. Prantl). Verlag von W. Engelmann, Leipzig, pp. 277–1246. Brotherus, V. F. (1924) Musci. In Die natürlichen Pflanzenfamilien, Vol. 10, Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig, pp. 143–478. Brotherus, V. F. (1925) Musci. In Die natürlichen Pflanzenfamilien, Vol. 11, Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig, pp. 1–542. Bruch, P., Schimper, W. P. and Gümbel, W. (1936–1855) Bryologia Europaea seu Generum Muscorum Europaeorum Monographice Illustrata. 6 volumes. Schweizerbart, Stuttgartiae. Buck, W. R. (1980) A generic revision of the Entodontaceae. Journal of the Hattori Botanical Laboratory, 48: 71–159. Buck, W. R. (1982) Nematocladia tesserata genus et species novae (Myriniaceae). Brittonia, 34: 414–416. Buck, W. R. (1987) Taxonomic and nomenclatural rearrangement in the Hookeriales with notes on West Indian taxa. Brittonia, 39: 210–224. Buck, W. R. (1988) Another view of familial delimitation in the Hookeriales. Journal of the Hattori Botanical Laboratory, 64: 29–36. Buck, W. R. (1991) The basis for familial classification of pleurocarpous mosses. Advances in Bryology, 4: 169–185. Buck, W. R. and Crum, H. (1990) An evaluation of familial limits among the genera traditionally aligned with the Thuidiaceae and Leskeaceae. Contributions from the University of Michigan Herbarium, 17: 55–69. Buck, W. R. and Goffinet, B. (2000) Morphology and classification of mosses. In Bryophyte Biology (ed. A. J. Shaw and B. Goffinet). Cambridge University Press, Cambridge, pp. 71–123. Buck, W. R. and Vitt, D. H. (1986) Suggestions for a new familial classification of pleurocarpous mosses. Taxon, 35: 21–60. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL–trnF and rps4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. Buck, W. R., Cox, C. J., Shaw, A. J. and Goffinet, B. (2004 [2005]) Ordinal relationships of pleurocarpous mosses, with special emphasis on the Hookeriales. Systematics and Biodiversity, 2: 121–145. Crosby, M. R. (1974) Toward a revised classification of the Hookeriaceae (Musci). Journal of the Hattori Botanical Laboratory, 38: 129–141. Crosby, M. R., Magill, R. E., Allen, B. and He, S. (2000) A Checklist of the Mosses. Missouri Botanical Garden, St. Louis.

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Crundwell, A. C. (1979) Rhizoids and moss taxonomy. In Bryophyte Systematics Systematics Association Special Volume 14 (ed. G. C. S. Clarke and J. G. Duckett). pp. 347–363, Academic Press, London. Darwin, C. R. (1859) On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life, Murray, London. de Jussieu, A. L. (1789) Genera Plantarum Secundum Ordines Naturales Disposita, Juxta Methodum in Horto Regio Parisiensi Exaratum. Herissant and Barrois, Parisii. (See especially pp. 12–14 for A. M. F. J. Palisot de Beauvois’ explanation of moss sexuality.) De Luna, E., Buck, W. R., Akiyama, H., Arikawa, T., Tsubota, H., González, D., Newton, A. E. and Shaw, A. J. (2000) Ordinal phylogeny within the hypnobryalean pleurocarpous mosses inferred from cladistic analysis of three chloroplast DNA sequence data sets: trnL-F, rps4, and rbcL. Bryologist, 103: 242–256. Dillenius, J. J. (1741) Historia Muscorum in Qua Circiter Sexcentae Species Veteres et Novae ad Sua Genera Relatae Describuntur et Iconibus Genuinis Illustrantur cum Appendice et Indice Synonymorum. Sheldoniano, Oxford. Dixon, H. N. (1932) Classification of mosses. In Manual of Bryology (ed. F. Verdoorn). Martinus Nijhoff, The Hague, pp. 397–412. Edwards, S. R. (1979) Taxonomic implications of cell patterns in haplolepidous moss peristomes. In Bryophyte Systematics Systematics Association Special Volume 14 (ed. G. C. S. Clarke and J. G. Duckett). pp. 317–346, Academic Press, London. Edwards, S. R. (1984) Homologies and inter-relationships of moss peristomes. In New Manual of Bryology, Vol. 2 (ed. R. M. Schuster). The Hattori Botanical Laboratory, Nichinan, pp. 658–695. Fleischer, M. (1904–1923) Die Musci der Flora von Buitenzorg (zugleich Laubmoosflora von Java), 4 volumes. In Flore de Buitenzorg, Vème Partie. Brill, Leiden. Florschütz, P. A. (1960) Introduction to Hedwig’s “Species Muscorum”. In J. Hedwig, Species Muscorum Frondosorum, Reprint edition, Historiae Naturalis Classica 16: v–xxii. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239. Goffinet, B. and Vitt, D. H. (1998) Revised generic classification of the Orthotrichaceae based on a molecular phylogeny and comparative morphology. In Bryology for the Twenty-First Century (ed. J. W. Bates, N. W. Ashton and J. G. Duckett). Maney Publishing and the British Bryological Society, Leeds, pp. 143–159. Goffinet, B., Cox, C. J., Shaw, A. J. and Hedderson, T. A. J. (2001) The Bryophyta (mosses): Systematic and evolutionary inferences from a rps4 gene (cpDNA) phylogeny. Annals of Botany, 87: 191–208. Hedenäs, L. (1987a) North European mosses with axillary rhizoids, a taxonomic study. Journal of Bryology, 14: 429–439. Hedenäs, L. (1987b) On the taxonomic position of Tomentypnum Loeske. Journal of Bryology, 14: 729–736. Hedenäs, L. (1989) Some neglected character distribution patterns among the pleurocarpous mosses. Bryologist, 92: 157–163. Hedenäs, L. (2002) Important complexes of intercorrelated character states in pleurocarpous mosses. Lindbergia, 27: 104–121. Hedwig, J. (1782) Fundamentum Historiae Naturalis Muscorum Frondosorum Concernens Eorum Flores, Fructus, Seminalem Propagatonem Adjecta Generum Dispositione Methodica, Iconibus, Illustratis. 2 volumes. S. L. Crusium, Lipsiae. Hedwig, J. (1783) Theoria Generationis et Fructificationis Plantarum Cryptogamicarum Linnaei, mere Propriis Observationibus et Experimentis Superstructa. Academiae Impr. Scientiarum, Petropoli. Hedwig, J. (1787–1789) Descriptio et Adumbratio Microscopico-Analytica Muscorum Frondosorum nec non Aliorum Vegetantium e Classe Cryptogamica Linnaei Novorum Dubiisque Vexatorum. 4 volumes. I. G. Mülleriano, Lipsiae. Hedwig, J. (1801) Species Muscorum Frondosorum Descriptae et Tabulis Aeneis lxxvii Coloratis Illustratae. Joannis Ambrosii Barthii, Lipsiae. Hofmeister, W. (1851) Vergleichende Untersuchungen der Keimung, Entfaltung und Fruchtbildung höherer Kryptogamen (Moose, Farn, Equisetaceen, Rhizocarpeen und Lycopodiaceen) und der Samenbildung der Coniferen. F. Hofmeister, Leipzig.

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Hooker, W. J. and Taylor, T. (1827) Muscologia Britannica; Containing the Mosses of Great Britain and Ireland, Systematically Arranged and Described; with Plates Illustrative of the Characters of the Genera and Species. Second edition, corrected and enlarged. Longman et al., London. Ignatov, M. S. and Huttunen, S. (2002) Brachytheciaceae (Bryophyta) — A family of sibling genera. Arctoa, 11: 245–296. Ireland, R. R. (1971) Moss pseudoparaphyllia. Bryologist, 74: 312–330. Koponen, T. (1982) Rhizoid topography and branching patterns in moss taxonomy. In Bryophyte Taxonomy (ed. P. Geissler and S. W. Greene). Beihefte zur Nova Hedwigia, 71: 95–99. Kürschner, H. and Parolly, G. (1999) Pantropical epiphytic rain forest bryophyte communities — coenosyntaxonomy and floristic-historical implications. Phytocoenologia, 29: 1–52. Linnaeus, C. (1753) Species Plantarum, Exhibentes Plantas Rite Cognitas, ad Genera Relatas, cum Differentiis Specificis, Nominibus Trivialibus, Synonymis Selectis, Locis Natalibus, Secundum Systema Sexuale Digestas. Salvii, Holmiae. Margadant, W. D. (1968) Early Bryological Literature. A Descriptive Bibliography of Selected Publications Treating Musci during the First Decades of the Nineteenth Century and Especially of the Years 1825, 1826 and 1827. Hunt Botanical Library, Pittsburgh. Menzies, A. (1798) A new arrangement of the genus Polytrichum, with some emendations. Transactions of the Linnean Society of London, 4: 63–84, pls. 6, 7. Mitten, W. (1859) Musci Indiae Orientalis; an enumeration of the mosses of the East Indies. Journal of the Proceedings of the Linnean Society, Supplement to Botany, 1: 1–171. Müller, C. (1848–1851) Synopsis Muscorum Frondosorum Omnium Hucusque Cognitorum. 2 volumes. Foerstner, Berolini. Norris, D. H. (1978) New characters in moss taxonomy. American Bryological and Lichenological Society, abstracts of contributed papers presented at the annual meeting. Virginia Polytechnic Institute and State University, Blacksburg. Palisot de Beauvois, A. M. F. J. (1805) Prodrome des Cinquième et Sixième Familles de l’Aethéogamie. Les Mousses. Les Lycopodes. Fournier fils, Paris. Philibert, H. (1884–1902) De l’importance du péristome pour les affinities naturelles des mousses. Revue Bryologique 11: 49–52, 65–72 (1884); Études sur le péristome. Revue Bryologique 11: 80–87 (1884); 12: 67–77, 81–85 (1885); 13: 17–26, 81–86 (1886); 14: 9–11, 81–90 (1887); 15: 6–12, 24–28, 37–44, 50–60, 65–69, 90–93 (1888); 16: 1–9, 39–44, 67–77 (1889); 17: 8–12, 25–29, 39–42 (1890); 23: 36–38, 41–56 (1896); 28: 56–59, 127–130 (1901); 29: 10–13 (1902). Saito, K. (1975) A monograph of the Japanese Pottiaceae (Musci). Journal of the Hattori Botanical Laboratory, 39: 373–537. Schimper, W. P. (1855 [1856]) Corollarium Bryologiae Europaeae, Conspectum Diagnosticum Familiarum, Generum et Specierum, Adnotationes Novae Atque Emendations Complectens. Schweizerbart, Stuttgart. Schwägrichen, C. F. (1810) Über das Hedwig’sche System der Moose und Beschreibung einiger neuer Moose. Neues Journal für die Botanik, 4: 1–19, Tabs. I, II. Shaw, J. and Anderson, L. E. (1988) Peristome development in mosses in relation to systematics and evolution. II. Tetraphis pellucida (Tetraphidaceae). American Journal of Botany, 75: 1019–1032. Shaw, J., Anderson, L. E. and Mishler, B. D. (1987) Peristome development in mosses in relation to systematics and evolution. I. Diphyscium foliosum (Buxbaumiaceae). Memoirs of the New York Botanical Garden, 45: 55–70. Shaw, J., Anderson, L. E. and Mishler, B. D. (1989) Peristome development in mosses in relation to systematics and evolution. III. Funaria hygrometrica, Bryum pseudocapillare, and B. bicolor. Systematic Botany, 14: 24–36. Shaw, J., Cox, C. J., Goffinet, B., Buck, W. R. and Boles, S. B. (2003) Phylogenetic evidence of a rapid radiation of pleurocarpous mosses. Evolution, 57: 2226–2241. Shaw, J., Cox, C. J. and Boles, S. B. (2004) Phylogenetic relationships among Sphagnum sections: Hemitheca, Isocladus, and Subsecunda. Bryologist, 107: 189–196. Smith, J. E. (1804) Remarks on the generic characters of mosses, and particularly of the genus Mnium. Transactions of the Linnean Society of London, 7: 254–263. Strasburger, E. (1894) The periodic reduction of the number of chromosomes in the life-history of living organisms. Annals of Botany, 8: 281–316.

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Vanderpoorten, A., Hedenäs, L., Cox, C. J. and Shaw, A. J. (2002) Circumscription, classification, and taxonomy of Amblystegiaceae (Bryopsida) inferred from nuclear and chloroplast DNA sequence data and morphology. Taxon, 51: 115–122, 633. Vitt, D. H. (1984) Classification of the Bryopsida. In New Manual of Bryology, Vol. 2 (ed. R. M. Schuster). The Hattori Botanical Laboratory, Nichinan, pp. 696–759.

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Phylogenetic Distribution 2 The of Pleurocarpous Mosses: Evidence from cpDNA Sequences Terry J. O’Brien CONTENTS Abstract ............................................................................................................................................19 2.1 Introduction.............................................................................................................................20 2.2 Materials and Methods ...........................................................................................................23 2.2.1 Sampling and Extraction for DNA Data....................................................................23 2.2.2 DNA Amplification and Sequencing..........................................................................23 2.2.3 Sequence Alignment...................................................................................................28 2.2.4 Phylogenetic Analyses................................................................................................28 2.3 Results.....................................................................................................................................29 2.3.1 Properties of Dataset and Trees .................................................................................29 2.3.2 Tree Congruence and Gene Utility ............................................................................29 2.3.3 Phylogenetic Interpretations.......................................................................................31 2.3.3.1 Position of Hypnidae and Hypnodendroid Pleurocarps .............................31 2.3.3.2 Monophyly of Rhizogoniaceae, and Positions of Aulacomnium, Calomnion and Orthodontium ....................................................................32 2.3.3.3 Position of Rhizogonian Mosses within Bryidae .......................................32 2.3.3.4 Position of Mittenia ....................................................................................32 2.4 Discussion...............................................................................................................................32 2.4.1 Clade Resolution, Branch Support and Phylogenetic Inference ...............................32 2.4.2 Phylogenetic Relationships ........................................................................................33 2.4.2.1 Hypnidae and Hypnodendroid Pleurocarps................................................33 2.4.2.2 Circumscription and Phylogenetic Position of Rhizogoniaceae ................34 2.4.2.3 Position of Aulacomnium ............................................................................36 2.4.3 Phylogenetic Asymmetry in the Rhizogonian Mosses and Crown Pleurocarps .......36 2.5 Conclusions.............................................................................................................................37 Acknowledgments ............................................................................................................................37 References ........................................................................................................................................37

ABSTRACT A maximum parsimony analysis of a four-gene cpDNA dataset of 58 exemplar taxa indicates that pleurocarpous and non-pleurocarpous members of the Rhizogoniaceae plus the acrocarpous genera

19

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Pleurocarpous Mosses: Systematics and Evolution

Aulacomnium, Calomnion and Orthodontium are the sister group or near sister group to the hypnodendroid pleurocarps and the Hypnidae (Hypnobryales, Hookeriales and Ptychomniales). Monophyly of the rhizogonian mosses (including the Rhizogoniaceae, Aulacomnium, Calomnion and Orthodontium) is not supported, either due to paraphyly of the principal clades, or poor branch support in the consensus most parsimonious tree (MPT). The rhizogonian mosses have a primarily Gondwanan distribution centered in Oceania, and have about 1% of the species richness in the species-rich clade of hypnodendroid pleurocarps and Hypnidae. These results have implications for studies of diversification, adaptation, disparity, development and genome evolution of the crown pleurocarps, which, with about 5400 species, comprise more than half of extant mosses.

2.1 INTRODUCTION Mosses (Musci) include at least 10,000 species (e.g., Buck and Goffinet, 2000; Shaw et al., 2003) to as many as 12,000 extant species (Crosby et al., 2004; Goffinet and Buck, 2004). The bryalean pleurocarpous mosses (pleurocarps), including the Rhizogonianae and Hypnidae (Goffinet and Buck, 2004), are the focus of this chapter. The pleurocarps include as few as 5300 species (e.g., Shaw et al., 2003) to as many as 6600 species (Crosby et al., 2004). Altogether then, the pleurocarps comprise more than half of all moss species, underlining the importance of accurately knowing their phylogenetic origins and the phylogenetic distribution of the traits that contribute to pleurocarpy. In this chapter, I adopt the following nomenclature. The Hypnidae are as defined by Goffinet and Buck (2004; the Hypnanae sensu Buck and Goffinet, 2000), and include the Ptychomniales, Hookeriales and Hypnales. The hypnodendroid pleurocarps are as defined by Bell and Newton (2004), and include the families Hypnodendraceae, Racopilaceae, Cyrtopodaceae, Pterobryellaceae and Spiridentaceae, all as delimited by Buck and Goffinet (2000) and Goffinet and Buck (2004). The crown pleurocarps include the Hypnidae and hypnodendroid mosses. The rhizogonian mosses include the Rhizogoniaceae (Churchill and Buck, 1982; Buck and Goffinet, 2000; Goffinet and Buck, 2004) as well as Aulacomnium Schwägrichen, Calomnion J. D. Hooker & Wilson in J. D. Hooker and Orthodontium Schwägrichen. What is pleurocarpy, and what is known of its distribution within the Bryidae (bryalean mosses)? Pleurocarpy refers to the developmental origin and position of the archegonia-bearing perichaetia on moss stems. In pleurocarpous mosses, the perichaetia are produced on short, lateral innovations, and hence appear sessile on the stem (La Farge-England,1996; Newton and De Luna, 1999). Consequently, pleurocarpy also describes the origin and position of sporophytes. Recent studies of bryalean pleurocarpous mosses, based on evidence from DNA sequences (De Luna et al., 1999; Newton et al., 2000; Goffinet et al., 2001; Shaw et al., 2003; Bell and Newton 2004; Buck et al., 2005), indicate that they include a monophyletic group of nearly 5300 species, designated as the Hypnidae by Goffinet and Buck (2004). This group has been shown to consist of three major clades, the Hookeriales, Hypnales and Ptychomniales (Buck et al., 2000; Shaw et al., 2003; Buck et al., 2005). However, as noted by Newton and De Luna (1999), Bell and Newton (2004) and Goffinet and Buck (2004), pleurocarpy is not limited to the Hypnidae. Two additional groups with pleurocarpous taxa, the hypnodendroid mosses (Bell and Newton, 2004) and Rhizogoniaceae, include about 175 species. It is noteworthy, however, that the Rhizogoniaceae contain pleurocarpous and non-pleurocarpous taxa, the latter including Cryptopodium Bridel, Hymenodontopsis Herzog, Leptotheca Schwägrichen, Pyrrhobryum Mitten, and Rhizogonium Bridel (La Farge-England, 1996). This indicates that pleurocarpy in the bryalean mosses may have originated more than once, or that pleurocarpy has been lost in some lineages (or both). These observations reveal two important points: (1) the question of the monophyly of bryalean pleurocarps is more than the question of the monophyly of the Hypnidae; and (2) an understanding of the phylogenetic distribution of pleurocarpy is critical to unraveling the character state transformations involved in the evolutionary origin(s) or loss(es) of pleurocarpy.

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The Phylogenetic Distribution of Pleurocarpous Mosses: Evidence from cpDNA Sequences

21

The Rhizogoniaceae are a small family of mosses with an essentially Gondwanan distribution centered in Oceania. According to Churchill and Buck (1982), Crosby et al. (2004), Buck and Goffinet (2000) and Goffinet and Buck (2004), the Rhizogoniaceae include eight genera: Cryptopodium, Goniobryum Lindberg, Hymenodon J. D. Hooker & Wilson, Hymenodontopsis, Leptotheca, Mesochaete Lindberg, Pyrrhobryum and Rhizogonium. Early classifications considering the Rhizogoniaceae placed the family in a position phylogenetically distant from the Hypnidae (i.e., Fleischer [1904–1923]; Brotherus [1924–1925]; Vitt [1984] and Koponen [1988]). Within the past two decades, the classification of pleurocarps by Buck and Vitt (1986) and more recent phylogenetic analyses by Hedenäs (1994), Withey (1996), De Luna et al. (1999), Newton and De Luna (1999) and Cox et al. (2000) have all suggested that the nearest relatives of the crown pleurocarps may be within the Rhizogoniaceae. In more recent classifications, Buck and Goffinet (2000) and Goffinet and Buck (2004) included the Rhizogoniaceae in the superorder Rhizogonianae along with the hypnodendroid pleurocarps, apart from the Hypnidae. The phylogeny presented by Bell and Newton (2004) supports that the Rhizogoniaceae are instead a grade of lineages, sister to the monophyletic crown pleurocarps. The genus Aulacomnium is a small group of five or six acrocarpous species. Recent classifications treat Aulacomnium as the sole genus of Aulacomniaceae (Churchill and Buck, 1982; Vitt, 1984; Buck and Goffinet, 2000; Crosby et al., 2004; Goffinet and Buck, 2004), in contrast to earlier treatments by Fleischer (1904–1923) and Brotherus (1924–1925), who also included Leptotheca in the family. There are a variety of conclusions reached by previous authors about the nearest relatives of Aulacomnium within bryalean mosses. Brotherus (1924–1925) included his Aulacomniaceae (Aulacomnium and Leptotheca) in the suborder Bartramiineae, a group that also includes Bartramiaceae, Catoscopiaceae and Meesiaceae. Vitt (1984) proposed that Bartramiaceae, Catascopiaceae and Meesiaceae include the nearest relatives of Aulacomnium, and that the genus is rather distantly related within the non-pleurocarpous bryalean mosses to Rhizogoniaceae. Griffin and Buck (1989) suggested that Aulacomnium might “be nearer to the suborder Rhizogoniineae [= Rhizogoniaceae, in part] than previously thought,” a conjecture that has been supported by some subsequent studies. Buck and Goffinet (2000) and Goffinet and Buck (2004) include Aulacomnium within the basal bryalean mosses, and exclude it from their Rhizogoniales. In most more recent works that have relied on cladistic methods, Aulacomnium is positioned more closely to genera of Rhizogoniaceae. Hedenäs’ (1994) morphological dataset produced a consensus tree with Aulacomnium nested within a paraphyletic group of six genera of Rhizogoniaceae. The consensus MPT from a combined 18S rRNA–rbcL–rps4–trnL dataset assembled by Cox et al. (2000) positions Aulacomnium in a polytomy that includes the rhizogonian genus Pyrrhobryum and the pleurocarpous genera Racopilum, Hypnodendron and Bescherellia, but excludes the Hypnidae sampled. While these more recent studies suggest a close relationship of Aulacomnium and Rhizogoniaceae, their taxon sampling did not permit a clear assessment. More conclusive evidence about the position of Aulacomnium was presented by Bell and Newton (2004), who reported that it is within a grade of Rhizogoniaceae, Calomnion and Orthodontium. The genus Calomnion, which includes nine acrocarpous species (Vitt, 1995), has been regarded as having an unclear phylogenetic position (Vitt, 1984). The peristome is absent in all species, adding difficulty to the interpretation of its nearest relatives. Morphological characters suggest that the genus is a monophyletic group (Vitt, 1995). In Vitt’s (1984) classification, he included Calomnion within the Tetraphidales, a group distantly related to the Bryidae (Newton et al., 2000); however, more recently he suggested that the genus may be either within Tetraphidales or “in the general area of Rhizogoniaceae or the advanced Bryales” (Vitt, 1995). Waters et al. (1996) reported that 18S nrDNA sequences support the inclusion of Calomnion in an acrocarpous diplolepidous group of bryalean mosses, though no group is specified. Buck and Goffinet (2000) and Goffinet and Buck (2004) considered the Rhizogoniaceae to include the nearest relatives of Calomnion, and included the genus in their Rhizogoniales.

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22

Pleurocarpous Mosses: Systematics and Evolution

Buck and Goffinet (2000) and Goffinet and Buck (2004) positioned the acrocarpous genus Orthodontium in their superorder Bryanae, apart from their Rhizogonianae (= Rhizogoniaceae, hypnodendroid mosses and Calomnion). By comparison, Cox et al. (2000) reported a phylogeny from rbcL, rps4, trnL and 18S rRNA sequences which placed the acrocarpous genus Orthodontium as the sister group to the Hypnidae, although they used a small sample of Rhizogoniaceae, hypnodendroid pleurocarps and Hypnidae. More recently, Cox et al. (2004) and Bell and Newton (2004) confirmed the position of Orthodontium in a relationship close to or within pleurocarps. The most recent and intensive study of the phylogenetic distribution of basal bryalean pleurocarps is that of Bell and Newton (2004). They presented combined phylogenetic analyses of a dataset including 60 taxa and three genes, the mitochondrial nad5 region and chloroplast rbcL and rps4 regions. Working independently, I assembled a four-gene dataset of 58 taxa (O’Brien, 2001). The principal difference of the dataset compiled by Bell and Newton (2004) and the dataset used in this study is that I utilized sequences from the atpB–rbcL region, trnL–trnF region, rbcL gene and rps4 gene. Taxon sampling in these studies is similar, though the particular specimens used are different. With respect to the question of the distribution of pleurocarpy, their main findings were that: 1. The Hypnidae (Hypnanae in their paper) and hypnodendroid pleurocarps are sister groups and together form a monophyletic group; 2 The Rhizogoniaceae, Aulacomnium, Calomnion and Orthodontium are the nearest relatives of the Hypnidae and hypnodendroid mosses; 3. Monophyly of the Rhizogoniaceae is not supported; 4. The Rhizogoniaceae, Aulacomnium, Calomnion and Orthodontium can be tentatively assigned to three different clades. Additionally, they found clades within the rhizogonian grade (Aulacomnium, Calomnion and Orthodontium inclusive) that include both pleurocarpous and non-pleurocarpous taxa, raising the interesting possibility that pleurocarpy either originated more than once or that it was lost by reversion to acrocarpy. In summary, it appears from previous studies that Aulacomnium, Calomnion, Orthodontium, Rhizogoniaceae, the hypnodendroid mosses and Hypnidae should be the continued focus of attention for understanding the distribution of pleurocarpy within the bryalean mosses, and understanding a majority of the species richness of mosses. The use of gene sequences for the inference of phylogeny has been widely adopted in recent years. The costs of producing sequence data often impose a constraint on data collection, so that it remains common practice that a phylogeny is inferred from only one or two genes. An assumption of this practice is that the small sample of genes indicates the true phylogeny. It is known that processes such as gene duplication or deletion, introgression and lineage sorting can affect the inference of phylogeny from gene sequences, leading to the question of whether so few genes are adequate. One approach to assessing this question is to compare the number of shared clades of trees from genes (partitions) of the entire dataset (Johnson and Soltis, 1998). Phylogenetic studies that include several genes, such as this chapter, present the opportunity to evaluate the adequacy of using one or few genes. Understanding the phylogenetic patterns and morphological diversity in the pleurocarps is a central theme of the chapters in this book. In this chapter, I use evidence from four chloroplast gene sequences to address the questions of: (1) the position of Rhizogoniaceae within the basal bryalean mosses (Bryales); (2) monophyly of the Rhizogoniaceae; (3) the phylogenetic positions of Aulacomnium, Calomnion, Orthodontium and Mittenia and (4) relationship of these taxa to the hypnodendroid mosses and Hypnidae. My findings are consistent with the principal phylogenetic conclusions of Bell and Newton (2004). Importantly, my findings are based on two additional gene regions, and so offer a degree of independent support for their study. In addition to these questions

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The Phylogenetic Distribution of Pleurocarpous Mosses: Evidence from cpDNA Sequences

23

about phylogenetic pattern, I also evaluate the extent to which data partitions (gene sets) predict the best estimate of phylogeny inferred from combined evidence. Finally, given the phylogenetic results, I consider the asymmetry of species richness in the crown pleurocarps compared to the rhizogonian mosses.

2.2 MATERIALS AND METHODS 2.2.1 SAMPLING

AND

EXTRACTION

FOR

DNA DATA

Table 2.1 includes information on voucher specimens and GenBank accession numbers for all sequences used in this study. Within the bryalean mosses (Bryidae), 58 exemplars and 50 genera were sampled, concentrated in the rhizogonian mosses. The rhizogonian exemplars include three species of Aulacomnium, one each of Calomnion and Orthodontium, and all genera of the Rhizogoniaceae, representing 16 of 35 species of Rhizogoniaceae. Within the Hypnidae, 12 genera were selected from the Hookeriales, Hypnales and Ptychomniales. The hypnodendroid pleurocarps are represented by seven genera, including exemplars of the Hypnodendraceae, Racopilaceae, Cyrtopodaceae, Pterobryellaceae and Spiridentaceae. Non-pleurocarpous Bryidae included four exemplars of the Mniaceae and Bartramiaceae, three Orthotrichaceae, two Meesiaceae, and one each of Leptostomataceae and Rhacocarpaceae. Sampling from more distant relatives of pleurocarps included the haplolepidous mosses Dicranum Hedw., Grimmia Hedw., Mittenia Lindb. and Racomitrium Brid. Funaria Hedw. was included to serve as an outgroup. In summary, the taxon sampling is nonrandom, with the greatest concentration occurring within the rhizogonian mosses. Composite sequences from two or more vouchers within a genus were used if a complete gene set was not available for a species (Table 2.1). In using composite sequences, it was assumed that phylogenetic divergence is small between Operational Taxonomic Units (OTUs) used for composite sequences, relative to the divergence between them and all other OTUs. DNA was extracted from air-dried field collections or herbarium specimens with the DNeasy Plant Kit (Qiagen Inc., Valencia, California). One green shoot tip was used for extractions from large plants, or three to five green shoot tips from small plants. The extraction protocol provided by the manufacturer was used with the following modifications (provided by John Wheeler): (1) ground tissues were incubated in lysate buffer (kit Buffer AP1) 1 to 2 h; and (2) two 50-μl elutions (kit Buffer AE) were used in the final step, with each elution allowed to incubate 30 to 60 min.

2.2.2 DNA AMPLIFICATION

AND

SEQUENCING

Sequences were produced in the Molecular Phylogenetics Laboratory (University and Jepson Herbaria and the Museum of Paleontology, University of California at Berkeley), or obtained from GenBank. DNA sequences were obtained from four cpDNA genes: (1) approximately 400 bp of the atpB gene and the adjacent atpB–rbcL nontranscribed spacer (hereafter referred to as atpB); (2) rbcL; (3) rps4; and (4) the trnL–trnF gene region (hereafter trnL). Primers used for polymerase chain reaction (PCR) amplicons were as follows: atpB–rbcL region, matpB601F, M007R (John Wheeler, personal communication); rbcL, M07 (John Wheeler, personal communication), M636, M740R, M1390R (Lewis et al., 1997); rps4–rps5F, trnSR (Souza-Chies et al., 1997); trnL–trnF region, uniC, uniF (Taberlet et al., 1991). For rbcL, amplicons were produced using M07 and M1390R, and all four rbcL primers were used in cycle sequencing reactions. PCR contained the following components: 1 to 6 μl of DNA extract, 5.0 μl of 10× MgCl2 + PCR Buffer II (Perkin-Elmer Applied Biosystems), 1.0 μl of 10 mM dNTPs, 0.5 μl of each primer pair at 25 μM, 0.25 μl of Amplitaq Gold DNA Polymerase (Perkin-Elmer) and dH2O to a total volume of 50 μl. For most extractions, 1 to 4 μl of DNA yielded visible PCR product. The most frequently successful strategy when PCR reactions failed was to use 2 μl of 10- to 50-fold diluted extract. All PCR reactions were done with a GeneAmp 9600 thermocycler (Perkin-Elmer) or DNA Engine thermocycler (MJ Research). Each PCR reaction was preceded by 10 to 12 min at 95C (a

M. L. Sargent s.n. (UC-Culture) Buck 32568 (NY) J. R. Shevock 12973 (UC) D. H. Norris 87262 (UC) J. R. Shevock 16833 (UC) L. E. Anderson 27577 (UC) H. Streimann 50383 (UC) H. Streimann 61090 (UC) A. Withey 732 (DUKE) T. A. J. Hedderson 11763 (RNG) M. L. Sargent October 8, 1977 (UC-Culture) H. Streimann 61871 (UC) H. Streimann 38403 (RNG) D. Norris 79966 (UC) H. Streimann 57841 (UC) J. E. Beever 90-67 (UC) H. Streimann 54178 (NY) W. B. Schofield 61923 (UC) D. H. Vitt 29705 (UC) D. H. Vitt 29618 (DUKE) Mishler, Hopple & Thrall (DUKE). H. Streimann 56137 (NY) D. V. Basile October 6, 1978 (UC-Culture) B. Allen 20153 (MO) B. Allen Exsiccatae 109 (MO) M. L. Sargent June 6, 1980 (UC-Culture)

Collector, Number (Herbarium)

— — AF226818

AY853989 — AF231084 AF231067 — AF231074

AF413558 — — — — — — — —

AY853975 — AY853999 AY853982 AY853987

AF413551 — AF413556 AF413548 AF413549

Australia, Queensland — New Zealand Australia, Queensland New Zealand New Zealand Canada, British Columbia New Zealand New Zealand U.S., North Carolina Australia U.S., New Jersey — U.S., New York U.S., Illinois

AF231077 — AY853985 AY853976 AY853977 AY853978 AY853979 — AF231097 — AF158176

rbcL

— — AF413557 AF413566 AF413529 AF413534 AF413525 AF413552 — — AF413567

atpB

U.S., Indiana — U.S., California U.S., California U.S., California U.S., North Carolina Australia, New South Wales Australia, Queensland New Caledonia — U.S., Illinois

Locality Information

AF143064 — —

— AF023820 AY857774 AY857774 AY857781 AY306884 AY857772 AY857775 — — AY306907 —

— AF143031 AY857769 AY857790 AY857766 AY857767 AY857768 AY857793 — AF023818 —

rps4

— AF191534 —

— AF023745 AY857810 AY857812 AY857811 AY306718 AY857813 AY857802 — — AY306741 —

— AF161124 AY857808 AY857818 AY857795 AY857797 AY857796 AY857817 — AF023772 —

trnL

24

Fontinalis dalecarlica Bruch & Schimp. in B.S.G. Fontinalis dalecarlica Bruch & Schimp. in B.S.G. Funaria hygrometrica Hedw.

Anacamptodon splachnoides (Froel. ex Brid.) Brid. Anacamptodon splachnoides (Froel. ex Brid.) Brid. Anacolia laevisphaera (Taylor) Flowers in Grout Antitrichia californica Sull. in Lesq. Aulacomnium androgyum (Hedw.) Schwaegr. Aulacomnium heterostichum (Hedw.) Bruch & Schimp. Aulacomnium palustre (Hedw.) Schwaegr. Bescherellia elegantissima Duby Bescherellia elegantissima Duby Brachythecium rutabulum (Hedw.) Schimp. in B.S.G. Brachythecium salebrosum (Hoffm. ex Weber & D. Mohr) Schimp. in B.S.G. Braithwaitea sulcata (Hook.) A. Jaeger Braithwaitea sulcata (Hook.) A. Jaeger Breutelia pendula (Sm.) Mitt. Bryobrothera crenulata (Broth. & Paris) Ther. Calomnion complanatum (Hook. f. & Wilson) Lindb. Cladomnion ericoides (W. J. Hooker) Wils. in J. D. Hooker Conostomum tetragonum (Hedw.) Lindb. Cryptopodium bartramioides (Hook.) Brid. Cryptopodium bartramioides (Hook.) Brid. Dicranum scoparium Hedw. Euptychium robustum Hampe Fontinalis dalecarlica Bruch & Schimp. in B.S.G.

OTU/Taxon

TABLE 2.1 Voucher Specimens and GenBank Accessions for Sequences Used in this Study

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Pleurocarpous Mosses: Systematics and Evolution

Leucodon andrewsianus (H. A. Crum & L. E. Anderson) W. D. Reese & L. E. Anderson Leucolepis acanthoneura (Schwaegr.) Lindb. Macromitrium levatum Mitt. Meesia triquetra (H. Richt.) Angstr. Mesochaete undulata Lindb. Mesochaete undulata Lindb.

Leptotheca gaudichaudii Schwaegr. Leptotheca gaudichaudii Schwaegr. Leucodon julaceus (Hedw.) Sull.

Leptobryum pyriforme (Hedw.) Wilson Leptostomum macrocarpum (Hedw.) Bach. Pyl. Leptostomum macrocarpum (Hedw.) Bach. Pyl. Leptotheca boliviana Herzog Leptotheca boliviana Herzog

R. R. Halse 4883 (UC) T. Pocs, et al. 88102/N (RNG) T. J. O’Brien 2604 (UC) H. Streimann 35245 (CBG) H. Streimann 61888 (UC)

D. H. Norris 49382 (UC) J. E. Beever 90-72 (UC) D. H. Norris 67011 (UC) J. E. Beever 90-74 (UC) A. Withey 739 (DUKE) M. L. Sargent May 19, 1982 (UC-Culture) C. Cox 121 (RNG) Fletcher, s.n. (RNG) G. R. & J. E. Beever 90-71 (UC) S. P. Churchill 16400 (H) B. R. Ramirez & M.S. Gonzalez 9.058 (MO) H. Streimann 51199 (UC) H. Streimann (H) M. L. Sargent August 5 1989 (UC-Culture) W. R. Buck 32502 (NY)

Hymenodon angustifolium Sande Lac. Hymenodon pilifer Hook. f. & Wilson Hymenodontopsis stresemannii Herzog Hypnodendron comatum (Müll. Hal.) Touw Hypnodendron menziesii (Hook.) Paris Leptobryum pyriforme (Hedw.) Wilson

Hookeria acutifolia Hook. & Grev. Hookeria lucens (Hedw.) Sm.

C. J. Cox 148 (RNG) D. H. Norris 80013 (UC) H. Streimann 38105 (RNG) S. Schaffer Nov. 9, 1994 (UC) J. Christy 21771 (DUKE) M. L. Sargent August 30, 1981 (UC-Culture) B. Allen 20123 (MO) C. J. Cox 118 (RNG)

Funaria hygrometrica Hedw. Goniobryum subbasilare (Hook.) Lindb. Goniobryum subbasilare (Hook.) Lindb. Grimmia laevigata (Brid.) Brid. Grimmia pulvinata (Hedw.) Sm. Hookeria acutifolia Hook. & Grev.

U.S., Oregon — U.S., Oregon Australia, Queensland Australia, Queensland

—

New Zealand — Canada, Ontario

— — New Zealand — Colombia

Solomon Islands New Zealand Papua New Guinea New Zealand New Caledonia U.S., Indiana

— —

— New Zealand — U.S., California — U.S., Indiana

AF413564 — AF413560 — AF413535

—

AF413541 — —

— — AF413561 — AF413542

— AF413545 AF413544 AF413553 — —

— —

— AF413543 — — — AF413569

AY854005 — AY853986 AF231086 —

—

AY853980 — AF231075

— — AY853998 — AY854006

— AY853995 AY853997 — AF231093 AF231072

— —

— AY853991 — AF231081 — AF158170

AY857789 AF023813 AY857780 — AY857791

AF143005

AY857778 — —

AF023802 AF023790 — AF023816 —

AY857776 — AY857777 AY857779 — —

AF143071 —

AF023776 — AF023824 — AF222900 —

AY857821 AF023725 AY857820 — AY857798 Continued.

—

— AF023750 —

AF023736 AF023744 — AF023749 —

— AF215906 Continued. — AY857804 AY857803 AY857814 — —

AF023716 — AF023753 — — —

3856_book.fm Page 25 Saturday, March 3, 2007 12:29 PM

The Phylogenetic Distribution of Pleurocarpous Mosses: Evidence from cpDNA Sequences 25

Pyrrhobryum spiniforme (Hedw.) Mitt. Pyrrhobryum spiniforme (Hedw.) Mitt.

Plagiopus oederianus (Sw.) H. A. Crum & L. E. Anderson Pterobryella praenitens C. Mueller in Bescherelle Ptychomnion aciculare (Bridel) Mitten Pyrrhobryum bifarium (Hook.) Manuel Pyrrhobryum latifolium (Bosch & Sande Lac.) Mitt. Pyrrhobryum mnioides (Hook.) Manuel Pyrrhobryum mnioides (Hook.) Manuel Pyrrhobryum paramattense (Müll. Stuttg.) Manuel

T. Pocs, et al. 88110/BJ (RNG) D. H. Norris 77595 (UC)

H. Streimann s.n. June 16, 1999 (UC) C. J. Cox 115 (RNG) D. H. Vitt 35884 (ALTA) Hedderson s.n. (RNG) T. A. J. Hedderson 5745 (RNG) B. Goffinet 3162 (ALTA) M.L. Sargent May 11, 1980 (UC-Culture) J. Van Rooy 3459 (UC) H. Streimann 56079 (NY) H. Streimann 43623 (NY) D. H. Norris 79409 (UC) H. Streimann 61831 (UC) H. Streimann 58731 (UC) D. H. Norris 79901 (UC) H. Streimann s.n. June 16, 1999 (UC)

Collector, Number (Herbarium)

Mexico

—

Africa, Lesotho — Australia New Zealand Australia, Queensland Australia, Victoria New Zealand Australia

— — — — — U.S., Indiana

Australia

Locality Information

AF413540 —

AF413559 — — AF413536 AF413538 AF413539 — AF413537

— — — — — —

AF413563

atpB

— AY853984

AF023751 —

AY857773 AF307002 AY306983 AY857784 AY857786 — AY857785 AY857787

AF023796 — AF023800 AF023814 — —

— AF005518 AJ275174 — AF005536 MCU87082 AY853990 — — AY854001 AY854003 — AY854002 AY853983

AY857782

rps4 AY853988

rbcL

Continued. — AY857808

AY857809 AF509536 AY306817 AY857805 AY857806 AY857799 — AY857807

AF023767 — AF023768 AF023727 — —

AY857819

trnL

26

Mnium hornum Hedw. Mnium thomsonii Schimp. Orthodontium lineare Schwaegrichen Orthotrichum lyellii Hook. & Taylor Orthotrichum lyellii Hook. & Taylor Plagiomnium cuspidatum (Hedw.) T. J. Kop.

Mittenia plumula (Mitt. in Hook. f.) Lindb.

OTU/Taxon

TABLE 2.1 (Continued) Voucher Specimens and GenBank Accessions for Sequences Used in this Study

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Pleurocarpous Mosses: Systematics and Evolution

Taiwan Mexico Australia, Queensland

J. Shevock 15061 (UC) D. H. Norris 77393 (UC) H. Streimann 61878 July 28, 1998 (UC) H. Streimann 36688 (RNG) G. R. & J. E. Beever 90-73 (UC) D. H. Norris 79442 (UC) Ray Tangney RT 2-A (UC) A. Eddy 6232 (BM) J. McMurray s.n. (UC) A. Newton Nov 18, 1988 (DUKE) T. A. J. Hedderson 11763 (RNG) C. E. Darigo 2639 (UC) B. Goffinet 3161 (ALTA) T.A.J. Hedderson 11772 (RNG) — New Zealand New Zealand New Caledonia — — U.S., North Carolina — U.S., Alaska — —

— Australia, Victoria

Schaeffer Aug. 9, 1994 (UC) H. Streimann 61955 (UC)

— AF413547 — AF413550 — AF413568 — — AF413565 — —

AF413555 AF413562 AF413546

— AF413554

— AY853994 — AY853972 — — AF158177 — AY854004 AF005539 —

AY853973 AY854000 AY853993

AF231082 AY853974

AF023827 — AY857783 — AF023828 — — AF023819 AY857788 — AF023812

AY857794 AY857792 —

— —

AF023752 — AY857801 — AF023748 — — AF023770 AY857822 — AF023726

AY857816 AY857823 AY857800

— AY857815

Note: Taxon names are from Crosby et al. (2004). Sequences newly produced for this study are in boldface. Locality information is missing if it was not reported in the original publication or in GenBank.

Rhizogonium novae-hollandiae (Brid.) Brid. Rhizogonium novae-hollandiae (Brid.) Brid. Rhizogonium pennatum Hook. f. & Wilson Spiridens reinwardtii Nees Spiridens reinwardtii Nees Thuidium delicatulum (Hedw.) Schimp. in B.S.G. Thuidium delicatulum (Hedw.) Schimp. in B.S.G. Thuidium tamarascinum (Hedw.) Schimp. in B.S.G. Trachycystis flagellaris (Sull. & Lesq.) Lindb. Ulota obtusiuscula Müll. Hal. & Kindb. in Macoun Ulota phyllantha Brid.

Racomitrium fasciculare (Hedw.) Brid. Racopilum cuspidigerum (Schwegr. in Gaudich. in Freyc.) Angstr. Racopilum ferriei Ther. Rhacocarpus purpurascens (Brid.) Paris Rhizogonium graeffeanum (Müll. Stuttg.) A. Jaeger

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hot start) and followed by a 7 min final extension at 72C. The number of cycles, and denaturation, annealing and extension conditions used for each gene are as follows: atpB, 40 to 45 cycles of 95C/40 s, 54 to 57C/40 s, 72C/90 s; rbcL, 40 to 45 cycles of 95C/40 s, 56C/40 s, 72C/90 to 100 s; rps4, 40 cycles of 95C/40 s, 60C/40 s, 72C/75 s; trnL, 45 cycles of 95C/40 s, 58C/20 s, 72C/70 s. PCR products were purified using a microcentrifuge and the QIAQuick PCR Purification Kit (Qiagen, Inc.), with a final elution volume in Buffer EB of 20 to 40 μl. Quantification of PCR products for cycle sequencing was found to be unnecessary for this range of elution volumes. Sequencing reactions from cleaned PCR products were prepared with BigDye Terminator Cycle Sequencing Ready Reaction kits (Perkin-Elmer). Each reaction included 2 to 2.7 μl (1/4 or 1/3 reactions) of Terminator Ready Reaction Mix, 1 to 5 μl of purified PCR product (the highest volumes for weak PCR bands or amplicons >1000 bp), 1.0 μl of 10 mM primer, and dH2O. Sequencing reaction products were purified by precipitation for at least 30 min in 30 μl of 75% isopropanol, centrifugation for 15 min, and aspiration of the supernatants, followed by a second brief precipitation in 100 μl of 75% isopropanol, 5 min centrifugation, aspiration and vacuum centifugation for 30 min. The sequencing reaction products were electrophoresed through 4.8% acrylamide gels in an ABI 377 automated sequencer (Perkin-Elmer), and sequences were generated using ABI system software.

2.2.3 SEQUENCE ALIGNMENT Prior to the alignment of all OTU sequences for a gene, complementary sequences from forward and reverse primer pairs were used to assemble a consensus forward sequence (5 to 3) for each OTU. All consensus forward sequences for each gene were aligned with the computer program CLUSTAL V (Higgins, 1994), using equal matching and gap penalties of ten. Manual corrections to the computer alignment were made by comparing each position among all sequences and examining electropherograms. To minimize systematic error (Swofford et al., 1996), regions of ambiguity were excluded from the phylogenetic analyses. The data matrix is available from the author upon request.

2.2.4 PHYLOGENETIC ANALYSES All analyses were done with PAUP* software, version 4.0b10 (Swofford, 2002). A strict consensus of all MPTs was determined for the following gene sets: all genes (combined evidence; atpB, rbcL, rps4 and trnL), each of the four possible combinations of three genes, and each gene alone. Only the combined evidence tree is presented. In all analyses, included characters are equally weighted. For each gene set, several outgroups (Funariidae or Dicranidae) were substituted into separate analyses to confirm the stability of the ingroup branch topology in the consensus tree. Funaria was used as an outgroup in all final analyses except atpB alone (no atpB sequence was obtained for Funaria). For the atpB analysis, Mittenia was used as an outgroup (Bell and Newton [2004] presented evidence that Mittenia is haplolepidous). The procedure for identifying all MPTs for a gene set consisted of two heuristic searches: (1) identification of all tree islands (Maddison, 1991); and (2) identification of all MPTs from the islands represented by all trees saved from the first search. The support for each branch in the consensus trees was assessed with the decay index (DI: Bremer, 1994; Mishler, 1994) and bootstrap values (1000 replicates, using heuristic searches with random addition). The g1 value (Hillis, 1991; Huelsenbeck, 1991) was calculated with PAUP* from 500,000 randomly generated trees for all data partitions. The observations of Hillis (1991) on g1 values indicate that slightly negative values (approximately –0.2 or less) imply phylogenetic signal in a dataset with many characters. An additional measure of the signal in data is the number of resolved clades (Johnson and Soltis, 1998). To evaluate congruence in data partitions, the total number of resolved clades in trees from one-gene data partition trees was compared to that from the combined

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TABLE 2.2 Statistics for Strict Consensus Trees from Combined and Partial Evidence Dataset

N

Chars.

I

I/N

% Inf.

C.I.

R.I.

MPTs

Steps

Clades

g1

All genes, all taxa All genes, Bryidae only All genes, pleurocarps only atpB only rbcL only rps4 only trnL only All 1-gene sets

58 50 38 38 53 50 53 —

3210 3210 3210 832 1312 632 434 —

740 646 533 184 253 164 119 —

12.8 12.4 14.0 4.84 4.77 3.28 2.25 —

23.1 20.1 16.6 22.1 19.3 26.0 27.4 —

0.412 0.378 0.413 0.438 0.326 0.416 0.402 —

0.521 0.570 0.616 0.651 0.589 0.630 0.637 —

288 123 4 148 4 12 687 —

3704 2633 1832 632 1110 1397 515 —

48 42 31 18 28 16 12 42

–0.6823 –0.7424 –0.7162 –0.8691 –0.4205 –0.4093 –0.6561 —

Note: N = number of taxa; Chars. = alignable characters; I = informative alignable characters; % Inf. = percentage of informative alignable characters; C.I. = consistency index value, calculated without autapomorphies; R.I. = retention index value; MPTs = most parsimonious trees from all identified tree islands (see Materials and Methods); Steps = steps in parsimonious trees; Clades = clades resolved of those in the all-genes consensus tree; g1 = g1 value (Hillis, 1991).

evidence tree (Table 2.2). Although congruence of branch support is also important, it is not considered in this chapter.

2.3 RESULTS 2.3.1 PROPERTIES

OF

DATASET

AND

TREES

Table 2.2 summarizes statistics for the combined evidence (all genes) and partial gene sets. The dataset includes 58 OTUs and 195 gene sequences, of which 130 are original. Data are missing for 37 of a possible 232 sequences for the four genes (the effect of this on clade resolution or support is unknown). The combined evidence data includes 740 informative characters, or 23.1% of all characters, and 12.1 informative characters per OTU. The number of informative characters per taxon (I/N), an estimator of phylogenetic signal (Bremer et al., 1999), increases as more gene partitions are utilized. Values of the g1 statistic range from –0.4093 to –0.8691, indicating that the distribution of trees for all gene sets is skewed towards the shortest trees. This suggests phylogenetic signal in all data partitions considered. The strict consensus MPT from combined evidence (Figure 2.1) includes resolution of 48 clades, with CI = 0.424 and RI = 0.531. Combined evidence yields 288 MPTs from two tree islands. The deletion of all OTUs except the rhizogonian mosses and pleurocarps reduces the number of MPTs to four, and results in an increase of I/N. This suggests that the detectable phylogenetic signal is concentrated within 34 rhizogonian and pleurocarp exemplars. The DI values in the combined evidence consensus tree are approximately proportionate to branch lengths (Figure 2.1 and Figure 2.2; based on ACCTRAN optimization), indicating that over all characters included and all taxa sampled, longer branches consistently accumulate a more pronounced phylogenetic signal than shorter branches. This indicates that polytomies associated with short branches in the tree are generally a consequence of fewer synapomorphies rather than homoplasies.

2.3.2 TREE CONGRUENCE

AND

GENE UTILITY

Table 2.2 indicates tree congruence in one-gene data partitions compared to the combined evidence tree (Figure 2.1; trees from gene partitions not shown). Combined analysis of all genes results in six clades that are not produced in consensus MPTs from one-gene partitions. The consensus MPTs

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Pleurocarpous Mosses: Systematics and Evolution

100 100 73 22 31 4 51 2 2 76 62 6 75 2 100 1 > 40 3

66 2

54 2

2 1 51 2 2 59 3

1

2 60 3 53 2

1

62 2

1

70 4

2

1

58 2 2 94 4

1

1 1 82 5 91 57 5 100 5 > 40 93 100 5 > 40 100 35

1

98 2 18

72 1

61 2

52 2

82 3

93 4 94 16

100 100 34

95 5 52 2

1

99 19

Aulacomnium pal. Aulacomnium and. Aulacomnium het. Mesochaete Pyrrhobryum bifar. Hymenodontopsis Pyrrhobryummnioides Bryobrothers Hookeria Cladomniun Euptychium Ptychomniun Anacamptodon Fontinalis Brachythecium Thuidium Echinophyllum Leucodon Antitichia Spiridena Pterobryella Beacherella Hypnodendron Racopilum cuspid. Racopilum ferriel Braithwaitea Leptotheca gaud. Leptotheca boliv. Hymenodon Orthodontium Cryptopodium Calomniun Pyrrhobryum param. Pyrrhobryum latif. Pyrrhobryum spinif. Goniobryum Rhizogenium pen. gr. Rhizogenium nov. hol. Leptrostomum Leucolepis Trachychstis Mnium Plagiumnium Breutelia Conostomum Plagious Anacolia Rhacocarpus Meesia Leptobryum Orthotrichum Ulota Macromitrium Mittenia Grimmia Racomitrium Dicranum Funaria

A (13)

H y p n (5000) i d (6500) a e

H y p n (110) o d e n B (23)

C (28)

FIGURE 2.1 Strict consensus of 288 MPTs from combined analysis of atpB, rbcL, rps4 and trnL–trnF regions (Length = 3704; Informative characters = 740). Numbers above and below branches are bootstrap values and decay index values, respectively. Circles indicate non-pleurocarpous (acrocarpous or cladocarpous) taxa. Hypnoden = Hypnodendroid pleurocarps (Bell and Newton, 2004). Groups A, B and C are discussed in the text. Numbers in parentheses are species richness, with both lower and upper estimates provided for the Hypnidae.

from one-gene partitions include 25% to 58% of the 48 combined evidence clades. In the one-gene partitions, rbcL predicts the most combined evidence clades (28), whereas trnL and rps4 are relatively poor in resolution of combined evidence (12 and 16, respectively). Gene utility can also be assessed from the number of informative characters (I) and the percentage of informative characters (% Inf.). For this dataset, rbcL has the most informative characters (253), followed by atpB (184), rps4 (164) and trnL (119). The two genes (rps4, trnL) with the highest percentage of informative characters resolve the fewest combined evidence clades.

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Autacomnium pal. Autacomnium and. Autacomnium het. Mesochaete Pyrrhobryum bifar. Hynenodontopsis Pyrrhobryummnioides Bryobrothera Hookeria Cladomnion Euptychium Ptychomnium Anacamptodon Fontinalis Bracythecium Thurdium Echinophyllum Leucodon Antitrichia Spiridena Pterobryella Beacherellia Hypnodendron Braithwaitea Racopilum cuspid. Racopilum ferriei Leptotheca gaud. Leptotheca boliv. Hymenodon Orthodontium Cryptopodium Calomnion Pyrrhobryum param. Pyrrhobryum latif. Pyrrhobryum spinif. Goniobryum Rhizogenium pen. gr. Rhizogenium nov. hol. Leptostomum Leucolepis Mnium Plagiomnium Trachycystis Breutelia Conostomum Plagiopus Anacolia Rhacocarpus Meesia Leptobryum

31

A

H y p n i d a e

H y p n o d e n B

C

Orthotrichum Ulota Macromitrium Mittenia Dicranum Grimnia Racomitrium Funaria

50 changes

FIGURE 2.2 Branch lengths of one of 288 MPTs from parsimony analysis of atpB, rbcL, rps4, and trnL–trnF regions. Group labels correspond with those in Figure 2.1.

2.3.3 PHYLOGENETIC INTERPRETATIONS 2.3.3.1 Position of Hypnidae and Hypnodendroid Pleurocarps The strict consensus tree supports the following interpretations: 1. The Hypnidae and hypnodendroid pleurocarps together constitute a monophyletic group, though with at best a moderate branch support value (DI = 3, bootstrap = 59%);

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2. Within the crown pleurocarps, there is weak support for the monophyly of the Hypnidae (DI = 2; bootstrap = 51%) and moderate support for monophyly of its sister group, the hypnodendroid pleurocarps (DI = 3; bootstrap = 60%); 3. There is weak support (DI = 2; bootstrap = 54%) for the conclusion that the sister group to the Hypnidae and hypnodendroid pleurocarps includes Aulacomnium, Hymenodontopsis, Mesochaete and Pyrrhobryum Section Pyrrhobryum. The taxon sampling precludes further inferences about relationships within the Hypnidae and hypnodendroid pleurocarps. 2.3.3.2 Monophyly of Rhizogoniaceae, and Positions of Aulacomnium, Calomnion and Orthodontium The combined evidence tree does not support the monophyly of Rhizogoniaceae, and offers weak support for the conclusion that it is a paraphyletic group. The Rhizogoniaceae are dispersed in three clades, A to C, which are weakly resolved from each other (DI = 1; bootstrap <50%, and DI = 2; bootstrap = 54%). These branch support values offer either weak or inconclusive support for paraphyly of the Rhizogoniaceae. However, Aulacomnium, Calomnion and Orthodontium are dispersed in clades A to C, indicating that the Rhizogoniaceae alone are non-monophyletic. Clade A, comprised of Aulacomnium, Hymenodontopsis, Mesochaete and Pyrrhobryum Section Bifariella, is moderately supported (DI = 2; bootstrap = 66%). Within clade A, Mesochaete (DI = 4; bootstrap = 73%) is positioned as the sister group to Aulacomnium. The branch support for sister group relationship of Mesochaete with Aulacomnium is also supported by the consensus MPTs from individual analyses of atpB, rbcL and rps4 (not shown). Clade B (DI = 1; bootstrap <50%), comprised of Leptotheca, Hymenodon and Orthodontium, has inconclusive support. Clade C includes Calomnion, Cryptopodium, Goniobryum, Pyrrhobryum Section Pyrrhobryum and Rhizogonium. Internal clades within clade C have higher branch support than the clade as a whole. One well-supported internal clade includes Goniobryum and Rhizogonium (DI = 5; bootstrap = 93%), and a second includes Calomnion, Cryptopodium and Pyrrhobryum Section Pyrrhobryum (DI = 5; bootstrap = 91%). 2.3.3.3 Position of Rhizogonian Mosses within Bryidae For the taxa sampled here, a clade including Leptostomum and all exemplars from Mniaceae s. lat. are the sister group of the rhizogonian mosses, the hypnodendroid pleurocarps and the Hypnidae. However, the support for this interpretation is inconclusive (DI = 1; bootstrap <50%). The sister group of Leptostomum + Mniaceae is a clade that includes Bartramiaceae and Rhacocarpus. 2.3.3.4 Position of Mittenia The phylogenetic position of Mittenia complanata is consistent with inclusion in the haplolepidous mosses rather than diplolepidous-alternate mosses, from a combined evidence analysis using Funaria as an outgroup. Therefore, the use of Mittenia as an outgroup is justified in the atpB analysis. Taxon sampling prevents a more exact inference of its nearest relatives.

2.4 DISCUSSION 2.4.1 CLADE RESOLUTION, BRANCH SUPPORT

AND

PHYLOGENETIC INFERENCE

The issue of whether to rely on combined evidence trees or congruence of trees from separate datasets in phylogenetic inference has received considerable attention (e.g., Bull et al., 1993; de

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Queiroz et al., 1995; Huelsenbeck et al., 1996; Kluge, 1998). For the inference of phylogeny, it has been asserted that it is better to use combined evidence rather than congruence of trees from data partitions (de Queiroz et al., 1995; Kluge, 1998). However, there are two reasons that comparisons of trees from data partitions are useful. First, in some cases, trees from data partitions differ substantially and can reveal important processes such as gene duplication/deletion, introgression, and lineage sorting that effect the inference of phylogeny (de Queiroz et al., 1995; Baldwin et al., 1998; Doyle, 1997; Maddison, 1997; Wendell and Doyle, 1998; Shaw, 2000). A second reason for comparing trees from partitions of the entire dataset is that they provide insights into how well partial evidence predicts the phylogeny from all evidence. This is an important consideration when choosing the extent of gene sampling for any phylogenetic study. In this study, congruences in consensus MPTs from data partitions and the consensus MPT from combined evidence were compared using the number of resolved clades. None of the one-gene partitions predicted more than 58% of the number of combined evidence clades, and all but rbcL data predicted less than 40%. Furthermore, the combined evidence tree includes six emergent clades compared to any trees from the one-gene partitions. It is also noteworthy that rbcL data provided substantially better clade resolution than rps4 data, given that both genes have been commonly used in phylogenetic studies of bryophytes. An implication of these observations is that it should not be expected that a phylogenetic tree from one gene will include satisfactory clade resolution. Poor clade resolution or branch support can be a consequence of the study design. Choices in study design that can lead to poor resolution include restricted taxon sampling, selecting the “wrong” genes (Soltis et al., 1998) and inappropriate character weighting (Albert et al., 1993). The four genes selected in this study clearly differ in phylogenetic signal (as indicated by clade resolution); however, each offers some resolution of relationships. Within rhizogonian mosses, there are several rather weakly supported key nodes along the backbone of the tree that will directly impact inferences about the evolution of pleurocarpy. The choice of additional taxa or genes with the appropriate character variation are two strategies that may prove effective. Poor clade resolution or branch support can also be a result of underlying patterns of evolution. Processes that limit these properties of trees include radiations and extinctions (Baldwin et al., 1998), as well as reticulation and lineage sorting (Wendell and Doyle, 1998). Shaw et al. (2003) presented evidence for a rapid diversification (radiation) in the early history of the Hypnidae, but did not include hypnodendroid pleurocarps or rhizogonian mosses in their study. The results presented by Bell and Newton (2004) and in this study include relatively poor branch support values and short branch lengths supporting three main rhizogonian clades. Given the extent of taxon and character sampling in both of these studies, these observations appear to be caused by real evolutionary pattern. A rapid divergence of the main rhizogonian clades soon after their origin is a possible cause, worthy of further investigation.

2.4.2 PHYLOGENETIC RELATIONSHIPS 2.4.2.1 Hypnidae and Hypnodendroid Pleurocarps The segregation of the crown pleurocarps into two fundamental divisions is supported by the combined evidence presented here, which recognizes one clade comprised of hypnodendroid pleurocarps, and a second of the Hookeriales, Hypnales and Ptychomniales. This outcome coincides with relationships inferred by De Luna et al. (1999) and Newton and De Luna (1999) from a combined rbcL and morphology dataset, and which were confirmed by Bell and Newton (2004) with more extensive taxon sampling and a three-gene dataset. It is noteworthy that this study and the results of Bell and Newton (2004) support the findings of De Luna et al. (1999) from combined morphology and rbcL data. It appears that while morphology alone and single-gene molecular datasets alone may not yield the best inference of phylogeny, their combination can result in a best estimate that will match that from a larger molecular dataset. Thus, when given limited resources

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for obtaining molecular data, obtaining data from carefully studied morphology and one wellchosen gene can be an effective strategy for producing an accurate best estimate tree. The recognition of the hypnodendroid pleurocarps as the sister group to the Hypnidae is an important aspect of understanding the character transformations involved in generating pleurocarpy. Moreover, these results affirm that hypnodendroid pleurocarps are appropriate outgroups in phylogenetic reconstructions of the basal phylogenetic patterns or studies of character variation in the Hypnidae (e.g., Hedenäs, 1999). Buck and Goffinet (2000) and Goffinet and Buck (2004) inserted the hypnodendroid pleurocarps in the superorder Rhizogonianae, apart from the Hypnidae. The phylogeny presented here is in conflict with these classifications. The phylogeny presented here confirms in part the cladistic analyses by Hedenäs (1994) and Withey (1996), and exactly the combined-data cladistic analyses by De Luna et al. (1999), Newton and De Luna (1999) and Bell and Newton (2004) indicating that the hypnodendroid pleurocarps will be a critical study group in understanding pleurocarpy in the Hypnidae. 2.4.2.2 Circumscription and Phylogenetic Position of Rhizogoniaceae The phylogeny presented here places the genera traditionally assigned to Rhizogoniaceae (sensu Churchill and Buck, 1982) in a paraphyletic grade as the nearest relatives of the hypnodendroid pleurocarps and Hypnidae. The nearest relatives of the rhizogonian grade and crown pleurocarps mosses are a clade of Leptostomum R. Brown and Mniaceae s. lat. In the MPT, the sister group to all of these is a clade including either Rhacocarpaceae or Bartramiaceae; however, branch support for this interpretation is minimal, hence a better conclusion is that the sister group to the pleurocarps (rhizogonian mosses included) may include Leptostomataceae, Mniaceae, Rhacocarpaceae and/or Bartramiaceae. The general relationships in the transition from the non-pleurocarpous bryalean mosses to pleurocarpous mosses are consistent with those of Newton and Bell (2004). They are slightly different than those inferred by Cox et al. (2000) from a parsimony analysis of the relationships within the Bryidae; however, it should be noted that I did not sample from Bryaceae or Mielichhoferiaceae. Their reconstruction places Leptostomum in a position sister to the Bryaceae, and Pohlia Hedw. and Mielichhoferia Nees & Hornsch. as the sister group to Mniaceae. A more recent study by Cox et al. (2004) included similar taxon sampling within the Bryidae, with analyses from maximum likelihood and Bayesian inference as well as parsimony. Their best estimate trees indicate that the sister group to the pleurocarps includes Bryaceae, Mielichhoferiaceae and Mniaceae. The position of a clade including Mniaceae sister to Rhizogoniaceae is partially compatible with the interpretations of Koponen (1988 and his earlier works cited therein), who assembled a phylogeny treating Rhizogoniaceae and Mniaceae as an assumed monophyletic group. However, aside from the recognition of near relationships between the families, his interpretations of generic relationships are generally not supported by the present study. Cryptopodium, Hymenodontopsis, Leptotheca and Pyrrhobryum are not included in Mniaceae (which Koponen 1988 defined to include Leucolepis Lindb., Mnium Hedw. and Trachycystis Lindb., as well as these rhizogonian genera). These genera of rhizogonian mosses appear in different major clades within the rhizogonian grade. Koponen’s Rhizogoniaceae, consisting of Goniobryum, Hymenodon, Mesochaete and Rhizogonium, are also not a monophyletic group. The phylogeny presented here provides weak support that the nearest relatives of the pleurocarps is a clade that includes Aulacomnium, Mesochaete, Hymenodontopsis and Pyrrhobryum Section Bifariella (clade A). Trees from both parsimony and maximum likelihood analyses of Bell and Newton (2004) indicate that same sister clade of the hypnodendroid pleurocarps and Hypnidae (although their sampling did not include Hymenodontopsis). Unfortunately, branch support values do not permit a clear understanding of the overall relationships of the three primary clades (A to C) of rhizogonian mosses. Bell and Newton (2004) therefore summarized the basal relationships of the rhizogonian mosses as a polytomy. Regardless of the exact relationships within rhizogonian

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mosses, the fact that the same general phylogenetic position of rhizogonian was found in both studies is an indication of their critical nature in future studies of the crown pleurocarps. Pyrrhobryum was split into two sections by Manuel (1980), who recognized P. Section Bifariella and P. Section Pyrrhobryum. This view is partially supported by my results. I sampled two taxa, P. bifariella and P. mnioides, from Section Bifariella, and three taxa, P. latifolium, P. paramattense and P. spiniforme, from Section Pyrrhobryum. The taxa of Section Bifariella are in a clade (A) that includes Aulacomnium, Hymenodontopsis and Mesochaete, while the taxa of Section Pyrrhobryum sampled are in a clade (C) that includes Calomnion and Cryptopodium. The evidence from this study does not support the inclusion of these sections in a single genus, but supports the circumscription of the sections. Bell and Newton (2004) also found that the sections of Pyrrhobryum are non-monophyletic, and in their trees, the positions of the sections correspond to clades A and C. An additional seven species of Pyrrhobryum are known (Crosby et al., 2004) that were not sampled in this study, and these should be evaluated before taxonomic decisions are made. Both Hymenodontopsis and Hymenodon feature a reduced peristome compared to the fundamental bryalean type. However, Shaw and Anderson (1986) concluded that the modifications differ, indicating that the reductions are not a taxic homology. Species of both genera are epiphytic, usually found on tree ferns and, according to Koponen et al. (1986), resemble each other because of similar habitat rather than a near relationship within rhizogonian mosses. Koponen et al. (1986) note that “the leaf shape, the partially bistratose leaf border with geminate teeth, the dorsally toothed costa and the smooth leaf cells connect Hymenodontopsis more closely with Pyrrhobryum than Hymenodon.” The position of Hymenodontopsis within Pyrrhobryum Section Bifariella is not strongly supported in the combined evidence tree, but is consistent with their suggestions. The combined evidence tree provides weak support for the interpretation that Hymenodon, Leptotheca and Orthodontium are a monophyletic group, a finding also made by Bell and Newton (2004). In my study, this outcome should be viewed with particular caution, as the sequences of Hymenodon are a congeneric composite (Table 2.1), and the composite OTU exhibits inconsistent positions in one-gene trees (results not shown). Assuming these taxa do form a clade, there is an interesting occurrence within it of both acrocarpy (Leptotheca and Orthodontium) and pleurocarpy (Hymenodon). High branch support values are concentrated within clade C, supporting the position of Goniobryum as the sister lineage of Rhizogonium, and that Cryptopodium and Calomnion are a sister group of a clade including Pyrrhobryum Section Pyrrhobryum. There is less convincing support for the monophyly of clade C (DI = 2; bootstrap = 62%). Bell and Newton (2004) reported higher branch support (DI = 5; bootstrap = 81%) for clade C, as well as high branch support values for internal clades of Goniobryum/Rhizogonium and Calomnion/Cryptopodium/Pyrrhobryum Section Pyrrhobryum. On the strength of their findings, Bell and Newton proposed the informal name “core rhizogonioids” for these taxa. The occurrence of both acrocarpy and pleurocarpy in clade C (core rhizogonioids) is worthy of additional study. The combined evidence tree presented here places Calomnion in a well-supported clade that includes Cryptopodium and Pyrrhobryum Section Pyrrhobryum. Within this group, Cryptopodium represents a well-supported sister lineage to Calomnion. Bell and Newton (2004) included two species of Calomnion, C. complanatum and C. brownysei Vitt and H. A. Miller in Vitt in their taxon sampling. They also found that Cryptopodium is the sister group to Calomnion, and that Pyrrhobryum Section Pyrrhobryum is the sister group of the Cryptopodium–Calomnion clade. This clade is noteworthy from the standpoint of understanding the origins of pleurocarpy. Pyrrhobryum Section Pyrrhobryum is pleurocarpous, whereas both Calomnion and Cryptopodium are acrocarpous (see Bell and Newton, 2004, for additional discussion). Several authors (Brotherus, 1924–1925; Vitt, 1984; Buck and Goffinet, 2000; and others, summarized in Shaw, 1985 and Stone, 1986) have proposed classifications in which Mittenia is included within diplolepidous-alternate mosses. Vitt (1984) considered Rhizogoniaceae to be the sister group to Mittenia and Schistostega D. Mohr, whereas Buck and Goffinet (2000) include

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Mittenia within their concept of Rhizogoniales. These views are refuted by Bell and Newton (2004), based on an rps4 sequence of Mittenia, and by results reported here, based on four gene sequences. The tree reported here indicates that Mittenia is more closely related to Dicranum and the Grimmiaceae than Orthotrichaceae or basal bryalean mosses. In view of this, the anomalous peristome of Mittenia should not be interpreted as diplolepidous. The results of Bell and Newton (2004) and this study partly supports the interpretations of Stone (1961, 1986) and Shaw (1985), who studied peristomial structure in Mittenia and concluded that the peristome is not diplolepidous, and perhaps more closely related to haplolepidous mosses. The question remains whether Mittenia is closely related to Schistostega, a hypothesis advanced by Stone (1961, 1986). 2.4.2.3 Position of Aulacomnium The finding that Mesochaete represents the sister group to Aulacomnium is remarkable, and was also reported by Bell and Newton (2004). Mesochaete is endemic to eastern Australia, primarily in subtropical climates (Scott and Stone, 1976; Stone, 1983; Streimann and Curnow, 1989), whereas Aulacomnium is widely distributed in the Northern Hemisphere. With the exception of Bell and Newton (2004) and recent studies showing a near relationship of Aulacomnium and other rhizogonian genera (e.g., Cox et al., 2000, 2004), other literature considering the Rhizogoniaceae or Aulacomnium does not directly suggest that these genera are sister groups or even in the same family (e.g., Brotherus, 1924–1925; Scott and Stone, 1976; Churchill and Buck, 1982; Stone, 1983; Vitt, 1984; Koponen, 1988; Withey, 1996; Buck and Goffinet, 2000). However, Mesochaete has sulcate capsules like Aulacomnium, and has several traits similar to A. heterostichum, the sister group to the remaining species of Aulacomnium (O’Brien, 2001). Both Mesochaete and A. heterostichum occur on shaded mineral mesic soils, bear deciduous apical leaves (Crum and Anderson, 1981; Scott and Stone, 1976) and have undulate, oblong-ovate and asymmetrical leaves with smooth cells and coarsely toothed margins. All of these similarities may be taxic homologies. Mesochaete differs considerably in most of these traits from the remaining species of Aulacomnium, which, other than A. heterostichum, have accumulated apomorphies, resulting in most of its species bearing little morphological resemblance to Mesochaete.

2.4.3 PHYLOGENETIC ASYMMETRY CROWN PLEUROCARPS

IN THE

RHIZOGONIAN MOSSES

AND

It is noteworthy that the Hypnidae and hypnodendroid pleurocarps, consisting of approximately 5400 species, have a sister group (or grade) with few extant species — about 1% of the crown group. Clades A, B and C include 13, 23 and 28 species, respectively. This asymmetry is comparable to that of the angiosperm phylogeny (Qiu et al., 1999), in which the speciose crown group, including nearly 249,000 species, arose from a paraphyletic group of basal lineages including about 1000 species. Is such asymmetry unexpected? Guyer and Slowinski (1991), Farris and Kallersjo (1998) and Salisbury (1999) all demonstrated that structured datasets yield a high frequency of strongly asymmetrical trees, an observation that indicates that asymmetry in a phylogenetic tree does not require exceptional explanation from a biological cause. Alternatively, the asymmetry may be due to factors that have either limited the accumulation of species richness in rhizogonian mosses, or enhanced species richness in the crown pleurocarps (for a discussion of the latter, see Shaw et al., 2003). The latter question should be considered in light of morphological transitions compared with phylogeny. In the absence of this, I consider one factor that may have limited the diversity of the rhizogonian mosses. Specialization for substrate preference may be one cause of low diversity in rhizogonian mosses. Within the group, 19 of 34 species and 5 of 11 genera (excluding Orthodontium) have a substrate preference of tree fern trunks (compare ecological descriptions in Scott and Stone, 1976; Churchill and Buck, 1982; Beever, 1984; Koponen et al., 1986; Karttunen and Bäck, 1988; Beever et al.,

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1992; Vitt, 1995; Yano, 1996; and O’Brien, 2000). Tree fern preference is not confined to one of the three rhizogonian clades (A to C) indicated by this study; rather it is distributed over all of them, principally the genera Calomnion, Cryptopodium, Hymenodon, Hymenodontopsis and Leptotheca. Although branch support in the MPT is not sufficient to confidently interpret the phylogenetic pattern of substrate preference, there are two general explanations: (1) tree fern preference is a derived condition within the group and has arisen independently (by parallelism) at least three times; or (2) tree fern preference is the ancestral condition in all rhizogonian mosses, and has been lost one or more times. Regardless of which explanation is correct, substrate preference may offer a clue to the timing of origins of rhizogonian lineages, suggestive of origins of rhizogonian mosses that predate the diversification of the angiosperms.

2.5 CONCLUSIONS The best estimate of phylogeny presented in this chapter provides additional support for clades identified in the phylogenetic analysis of basal pleurocarps by Bell and Newton (2004). The pleurocarps include the hypnodendroid pleurocarps and their diverse sister group, the Hypnidae. The sister group of the hypnodendroid pleurocarps and Hypnidae is a grade of rhizogonian mosses, which include Rhizogoniaceae, Aulacomnium, Calomnion and Orthodontium. Monophyly of the rhizogonian mosses is not supported, although low branch support values within the basal clades indicate a need for additional taxon or character sampling to determine their precise relationships. The rhizogonian mosses include both pleurocarpous genera and the non-pleurocarpous genera Aulacomnium, Calomnion and Cryptopodium, Hymenodontopsis, Leptotheca, Orthodontium, Pyrrhobryum and Rhizogonium. These results have implications for studies of diversification, adaptation, disparity, development and genome evolution of the pleurocarpous mosses.

ACKNOWLEDGMENTS This chapter is derived from a Ph.D. thesis completed at the University of California at Berkeley under the supervision of Brent D. Mishler. Manuscripts were improved from comments by Brent, Tom Bruns, William R. Buck, and two anonymous reviewers. I am especially grateful to John Wheeler for his guidance on technical aspects of obtaining DNA sequences, and to Jessica Beever, Dan Norris and Heinar Streimann for providing specimens. Additional specimens or sequences were provided by Bruce Allen, Lewis Anderson, Paul Davison, Terry Hedderson, David Long, Norton Miller, Stuart McDaniel, Brent Mishler, Barbara Murray, Jim Shevock, Dale Vitt and MO. Financial support was provided by a Regents Fellowship from UC-Berkeley and a Graduate Research Fellowship from the Department of Integrative Biology, UC-Berkeley, and Rowan University.

REFERENCES Albert, V. A., Chase, M. W. and Mishler, B. D. (1993) Character-state weighting for cladistic analysis of protein-coding DNA sequences. Annals of the Missouri Botanical Garden, 80: 752–766. Baldwin, B. G., Crawford, D. J., Francisco-Ortega, J., Kim, S.-C., Sang, T. and Stuessy, T. F. (1998) Molecular phylogenetic insights on the origin and evolution of oceanic island plants. In Molecular Systematics of Plants, II: DNA Sequencing (ed. D. E. Soltis, P. S. Soltis and J. J. Doyle). Kluwer Academic Publishers, Dordrecht, pp. 410–441. Beever, J. B. (1984) Moss epiphytes of tree-ferns in a warm-temperate forest. Journal of the Hattori Botanical Laboratory, 56: 89–95. Beever, J., Allison, K. W. and Child, J. (1992) The Mosses of New Zealand. University of Otago Press, Dunedin. Bell, N. E. and Newton, A. E. (2004) Systematic studies of non-hypnanaean pleurocarps: Establishing a phylogenetic framework for investigating origins of pleurocarpy. Monographs in Systematic Botany from the Missouri Botanical Garden, 98: 290–319.

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Bremer, K. (1994) Branch support and tree stability. Cladistics, 10: 295–304. Bremer, B., Jansen, R. K., Oxelman, B., Backlund, M, Lantz, H. and Kim, K. (1999) More characters or more taxa for a robust phylogeny — case study from the coffee family (Rubiaceae). Systematic Biology, 48: 413–435. Brotherus, V. F. (1924–1925) Musci. In Die natürlichen Pflanzenfamilien, Vols. 10, 11, Ed. 2 (ed. A. Engler). Verlag von W. Engelmann, Leipzig, pp. 1–478. Buck, W. R. and Goffinet, B. (2000) Morphology and classification of mosses. In Biology of Bryophytes (ed. A. J. Shaw and B. Goffinet). Cambridge University Press, Cambridge, pp. 71–123. Buck, W. R. and Vitt, D. H. (1986) Suggestions for a new familial classification of pleurocarpous mosses. Taxon, 35: 21–60. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL–trnF and rps4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. Buck, W. R., Cox, C. J., Shaw, A. J. and Goffinet, B. (2005) Ordinal relationships of pleurocarpous mosses, with special emphasis on the Hookeriales. Systematic Biodiversity, 2: 121–145. Bull, J. J., Huelsenbeck, J. P., Cunningham, C. W., Swofford, D. L. and Waddell, P. J. (1993) Partitioning and combining data in phylogenetic analysis. Systematic Biology, 42: 384–397. Churchill, S. P. and Buck, W. R. (1982) A taxonomic investigation of Leptotheca (Rhizogoniaceae). Brittonia, 34: 1–11. Cox, C., Goffinet, B., Newton, A. E., Shaw, A. J. and Hedderson, T. A. J. (2000) Phylogenetic relationships among the diplolepidous-alternate mosses (Bryidae) inferred from nuclear and chloroplast DNA sequences. Bryologist, 103: 224–231. Cox, C. J., Goffinet, B., Shaw, A. J. and Boles, S. B. (2004) Phylogenetic relationships among the mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomic compartments. Systematic Botany, 29: 234–250. Crosby, M. R., Magill, R. E., Allen, B. and He, S. (2004) A Checklist of Mosses. Missouri Botanical Garden, St. Louis. Crum, H. and Anderson, L. E. (1981) Mosses of Eastern North America. Columbia University Press, New York. De Luna, E., Newton, A. E., Withey, A., González, D. and Mishler, B. D. (1999) The transition to pleurocarpy: A phylogenetic analysis of the main diplolepidous lineages based on rbcL sequences and morphology. Bryologist, 102: 634–650. De Luna, E., Buck, W. R., Akiyama, H., Arikawa, T., Tsubota, H., Gonzalez, D., Newton, A. E. and Shaw, A. J. (2000) Ordinal phylogeny within the hypnobryalean pleurocarpous mosses inferred from cladistic analyses of three chloroplast DNA sequence data sets: trnL-F, rps4 and rbcL. Bryologist, 103: 242–256. De Queiroz, A., Donoghue, M. J. and Kim, J. (1995) Separate versus combined analysis of phylogenetic evidence. Annual Review of Ecology and Systematics, 26: 657–681. Doyle, J. J. (1997) Trees within trees: Genes and species, molecules and morphology. Systematic Biology, 46: 537–553. Farris, J. S. and Kallersjo, M. (1998) Asymmetry and explanations. Cladistics, 14: 159–166. Fleischer, M. (1904–1923) Die Musci der Flora von Buitenzorg. 4 volumes. E. J. Brill, Leiden. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239. Goffinet, B., Shaw, J., Anderson, L. E. and Mishler, B. D. (1999) Peristome development in mosses in relation to systematics and evolution. V. Diplolepideae: Orthotrichaceae. Bryologist, 102: 581–594. Goffinet, B., Cox, C. J., Shaw, A. J. and Hedderson, T. A. J. (2001) The Bryophyta (mosses): systematics and evolutionary inferences from an rps4 gene (cpDNA) phylogeny. Annals of Botany, 87: 191–208. Griffin, D. I. and Buck, W. R. (1989) Taxonomic and phylogenetic studies on the Bartramiaceae. Bryologist, 92: 368–380. Guyer, C. and Slowinski, J. (1991) Comparisons of observed phylogenetic topologies with null expectations among three monophyletic lineages. Evolution, 39: 609–622. Hedenäs, L. (1994) The basal pleurocarpous diplolepidous mosses: A cladistic approach. Bryologist, 97: 225–243.

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Hedenäs, L. (1999) How important is phylogenetic history in explaining character states in pleurocarpous mosses? Canadian Journal of Botany, 77: 1723–1743. Higgins, D. G. (1994) CLUSTAL V: Multiple alignment of DNA and protein sequences. In Methods in Molecular Biology; Computer Analysis of Sequence Data, Part II (ed. A. M. Griffin and H. G. Griffin). Humana Press, Totowa, pp. 307–318. Hillis, D. M. (1991) Discriminating between phylogenetic signal and random noise in DNA sequences. In Phylogenetic Analysis of DNA Sequences (ed. M. M. Miyamoto and J. Cracraft). Oxford University Press, New York, pp. 278–294. Huelsenbeck, J. P. (1991) Tree-length distribution skewness: An indicator of phylogenetic information. Systematic Zoology, 40: 257–270. Huelsenbeck, J. P., Bull, J. J. and Cunningham, C. W. (1996) Combining data in phylogenetic analysis. Trends in Ecology and Evolution, 11: 152–158. Ignatov, M. S. (1990) Upper Permian mosses from the Russian Platform [USSR]. Palaeontographica Abteilung B Palaeophytologie, 217: 147–190. Johnson, L. A. and Soltis, D. E. (1998) Assessing congruence: Empirical examples from molecular data. In Molecular Systematics of Plants, II: DNA Sequencing (ed. D. E. Soltis, P. S. Soltis and J. J. Doyle). Kluwer Academic Publishers, Dordrecht, pp. 297–348. Karttunen, K. and Bäck, S. (1988) Taxonomy of Hymenodon (Musci, Rhizogoniaceae). Annales Botanici Fennici, 25: 89–96. Kluge, A. G. (1998) Combined evidence or taxonomic congruence: Cladistics or consensus classification. Cladistics, 14: 151–158. Koponen, T. (1988) The phylogeny and classification of Mniaceae and Rhizogoniaceae (Musci). Journal of the Hattori Botanical Laboratory, 64: 37–46. Koponen, T. and Norris, D. H. (1986) Bryophyte flora of the Huon Peninsula, Papua New Guinea. XVII. Grimmiaceae, Racopilaceae and Hedwigiaceae (Musci). Acta Botanica Fennica, 133: 81–106. Koponen, T., Touw, A. and Norris, D. H. (1986b) Bryophyte flora of the Huon Peninsula, Papua New Guinea. XIV. Rhizogoniaceae (Musci). Acta Botanica Fennica, 133: 1–24. La Farge-England, C. (1996) Growth form, branching pattern, and perichaetial position in mosses: Cladocarpy and pleurocarpy redefined. Bryologist, 99: 170–186. Lewis, L. A., Mishler, B. D. and Vilgalys, R. (1997) Phylogenetic relationships of the liverworts (Hepaticae), a basal embryophyte lineage, inferred from nucleotide sequence data of the chloroplast gene rbcL. Molecular Phylogenetics and Evolution, 7: 377–393. Maddison, D. R. (1991) The discovery and importance of multiple islands of most-parsimonious trees. Systematic Zoology, 40: 315–328. Maddison, W. P. (1997) Gene trees in species trees. Systematic Biology, 46: 523–536. Manuel, M. G. (1980) Miscellanea Bryologica. II. Classification of Rhizogonium Brid., Penzigiella hookeri Gangulee, and some nomina nuda. Cryptogamie Bryologique et Lichénologie, 1: 67–72. Miller, N. G. (1984) Tertiary and Quaternary fossils. In New Manual of Bryology (ed. R. M. Schuster). Hattori Botanical Laboratory, Nichinan, pp. 1194–1232. Mishler, B. D. (1994) Cladistic analysis of molecular and morphological data. American Journal of Physical Anthropology, 94: 143–156. Newton, A. E. and De Luna, E. (1999) A survey of morphological characters for phylogenetic study of the transition to pleurocarpy. Bryologist, 102: 651–682. Newton, A. E., Cox, C. J., Wheeler, J. A., Goffinet, B., Hedderson, T. A. J. and Mishler, B. D. (2000) Evolution of the major moss lineages: Phylogenetic analyses based on multiple gene sequences and morphology. Bryologist, 103: 187–211. O’Brien, T. J. (2000) A new synonym in Leptotheca Schwägr. (Musci; Rhizogoniaceae). Tropical Bryology, 18: 13–14. O’Brien, T. J. (2001) Systematic and reproductive studies of Aulacomnium Schwägrichen (Musci). Ph.D. thesis, University of California, Berkeley. Qiu, Y.-L., Lee, J., Bernasconi-Quadroni, F., Soltis, D. E., Soltis, P. S., Zanis, M., Zimmer, E. A., Chen, Z., Savolainen, V. and Chase, M. W. (1999) The earliest angiosperms: Evidence from mitochondrial, plastid and nuclear genomes. Nature (London), 402: 404–407. Salisbury, B. A. (1999) Misinformative characters and phylogeny shape. Systematic Biology, 48: 153–169. Scott, G. A. M. and Stone, I. G. (1976) The Mosses of Southern Australia. Academic Press, New York.

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Shaw, A. J. (1985) Peristome structure in the Mitteniales (ord. nov.: Musci), a neglected novelty. Systematic Botany, 10: 224–233. Shaw, A. J. (2000) Phylogeny of the Sphagnopsida based on chloroplast and nuclear DNA sequences. Bryologist, 103: 277–306. Shaw, A. J. and L. E. Anderson. (1986) Morphology and homology of the peristome teeth in Hymenodon and Hymenodontopsis (Rhizogoniaceae: Musci). Systematic Botany, 11: 446–454. Shaw, A. J., Cox, C. J., Goffinet, B., Buck, W. R. and Boles, S. B. (2003) Phylogenetic evidence of a rapid radiation of pleurocarpous mosses (Bryophyta). Evolution, 57: 2226–2241. Soltis, D. E., Soltis, P. S., Mort, M. E., Chase, M. W., Savolainin V., Hoot, S. B. and Morton, C. M. (1998) Inferring complex phylogenies using parsimony: An empirical approach using three large DNA data sets for angiosperms. Systematic Biology, 47: 32–42. Souza-Chies, T. T., Bittar, G., Nadot, S., Carter, L., Besin, E. and Lejeune, B. (1997) Phylogenetic analysis of Iridaceae with parsimony and distance methods using the plastid gene rps4. Plant Systematics and Evolution, 204: 109–123. Stone, I. G. (1961) The gametophore and sporophyte of Mittenia plumula (Mitt.) Lindb. Australian Journal of Botany, 9: 124–151. Stone, I. G. (1983) A re-evaluation of the species of Mesochaete Lindb. (Rhizogoniaceae). Journal of Bryology, 12: 351–357. Stone, I. G. (1986) The relationship between Mittenia plumula (Mitt.) Lindb. and Schistostega pennata (Hedw.) Web and Mohr. Journal of Bryology, 14: 301–314. Streimann, H. and Curnow, J. (1989) Catalogue of Mosses of Australia and its External Territories. Australian Government Publishing Service, Canberra. Swofford, D. L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Sinauer Associates, Sunderland. Swofford, D. L., Olsen, G. J., Waddell, P. J. and Hillis, D. M. (1996) Phylogenetic inference. In Molecular Systematics, Ed. 2 (ed. D. M. Hillis, C. Moritz and B. K. Mable). Sinauer Associates, Sunderland, pp. 407–514. Taberlet, P., Gielly, L., Pautou, G. and Bouvet, J. (1991) Universal primers for amplification of three noncoding regions of chloroplast DNA. Plant Molecular Biology, 17: 1105–1110. Vitt, D. H. (1984) Classification of the Bryopsida. In New Manual of Bryology (ed. R. M. Schuster). Hattori Botanical Laboratory, Nichinan, pp. 696–759. Vitt, D. H. (1995) The genus Calomnion (Bryopsida): Taxonomy, phylogeny, and biogeography. Bryologist, 98: 338–358. Waters, D., Goffinet, B., Vitt, D. and Chapman, R. (1996) The systematic affinities of the Calomniaceae (Bryopsida) based on 18S nrDNA nucleotide sequences. American Journal of Botany, 83 (Supplement): 27. Wendell, J. F. and Doyle, J. J. (1998) Phylogenetic incongruence: Window into genome history and molecular evolution. In Molecular Systematics of Plants, II: DNA Sequencing (ed. D. E. S. Soltis, P. S. Soltis and J. J. Doyle). Kluwer Academic Publishers, Dordrecht, pp. 265–296. Withey, A. (1996) Systematic studies of the Spiridentaceae (Musci). Ph.D. dissertation, Duke University, Durham. Yano, O. (1996) Criptógamos do Parque Estadual das Fontes do Ipiranga, São Paulo, SP. Briófitas, 1: Mniaceae, Rhizogoniaceae, Racopilaceae, Phyllogoniaceae e Leucobryaceae (Bryales). Hoehnea, 23: 81–98.

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in the 3 Pleurocarpy Rhizogoniaceous Grade Neil E. Bell and Angela E. Newton CONTENTS Abstract ............................................................................................................................................41 3.1 Introduction.............................................................................................................................42 3.1.1 Review: Modularity and Branching Hierarchy..........................................................42 3.1.2 Review: Pleurocarpy, Acrocarpy and Cladocarpy .....................................................44 3.2 Materials and Methods ...........................................................................................................45 3.2.1 Observations of Plant Architecture ............................................................................45 3.2.2 Character Optimizations.............................................................................................45 3.3 Results.....................................................................................................................................47 3.3.1 Observations of Plant Architecture ............................................................................47 3.3.1.1 Rhizogonium distichum, Pyrrhobryum paramattense, and Pyrrhobryum spiniforme .............................................................................47 3.3.1.2 Pyrrhobryum dozyanum, Pyrrhobryum mnioides, Mesochaete taxiforme, Spiridens camusii, and Bescherellia elegantissima ...................48 3.3.1.3 Pyrrhobryum bifarium, Pyrrhobryum vallis-gratiae, and Hypnodendron menziesii .............................................................................49 3.3.1.4 Hymenodon sericeus and Hymenodon pilifer .............................................49 3.3.1.5 Hymenodontopsis stresemannii ...................................................................50 3.3.1.6 Goniobryum subbasilare .............................................................................50 3.3.1.7 Typical Hypnalean Pleurocarp....................................................................50 3.3.1.8 Cryptopodium bartramioides, Leptotheca gaudichaudii, Orthodontium lineare, Calomnion complanatum, and Aulacomnium heterostichum .......................................................................50 3.3.2 Character Optimizations.............................................................................................51 3.4 Discussion...............................................................................................................................52 3.4.1 Coding Strategies and Primary Homology ................................................................61 3.4.2 Scenarios.....................................................................................................................61 Acknowledgments ............................................................................................................................63 References ........................................................................................................................................63

ABSTRACT Modular branching structure in exemplars from the rhizogoniaceous grade, identified in recent analyses as representing the earliest diverging pleurocarpous lineages, is examined in order to isolate discrete architectural types associated with the pleurocarpous condition. These are described and used as a basis for optimization of pleurocarpy sensu stricto onto an existing phylogeny derived from chloroplast and mitochondrial molecular sequence data. Characters closely associated

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with pleurocarpy in these taxa are also optimized, and the results used to examine scenarios for the evolution of modular form in the basal pleurocarpous clades. Brief reviews of modular hierarchical concepts and of pleurocarpy are provided in the introduction. The results reveal that there is disproportionate diversity of pleurocarpous architectural types in the rhizogoniaceous grade compared with the hypnodendroid pleurocarps and the Hypnidae, and that these probably represent successive and varied novel adaptive strategies that utilize the potential of the key innovation of pleurocarpy.

3.1 INTRODUCTION Recent molecular phylogenetic analyses place members of the Southern Hemisphere family Rhizogoniaceae, in addition to Aulacomnium, Calomnion, and Orthodontium, as the earliest diverging lineages (henceforth referred to as grade R; see Figure 3.1) in a clade that includes the higher pleurocarps (Bell and Newton, 2004, 2005; O’Brien, Chapter 2 in this volume). The latter occur as two well-supported clades, the subclass Hypnidae and the “hypnodendroid pleurocarps” sensu Bell and Newton (2005). Some members of grade R are acrocarpous. This grade thus spans the transition from acrocarpy to pleurocarpy, to the extent that intermediate states may be retained in extant taxa. Consistent with this, it is also uniquely variable with respect to combinations of states of characters that define or are closely associated with pleurocarpy. The status of individual members of the Rhizogoniaceae as acrocarps, pleurocarps or cladocarps has long been controversial, reflecting both different usage of these terms and different interpretations of morphology (e.g., Buck and Vitt, 1986; Koponen, 1988; Hedenäs, 1994; La Farge-England, 1996; Newton and De Luna, 1999; Buck et al., 2000; Shaw et al., 2003). The situation is further complicated by variation within the Rhizogoniaceae itself, especially as this does not always correspond to generic-level taxonomy. Although Bell and Newton (2004, 2005) saw most of the Rhizogoniaceae as pleurocarpous, other authors (e.g., Shaw et al., 2003) have equated the pleurocarps with the Hypnidae, implying that both the hypnodendroid pleurocarps and the Rhizogoniaceae are non-pleurocarpous. Although this usage to some extent reflects a systematic rather than a morphological view of pleurocarpy, even under La Farge-England’s (1996) restrictive definition, at least the hypnodendroid taxa are morphologically pleurocarpous. While ultimately it is the distribution of character states that is significant, in the case of pleurocarpy character definition is problematic. Due to the highly complex nature of the condition sensu lato, primary homologies (Patterson, 1982) are difficult to assess and many alternative coding strategies are possible. In this study we present detailed observations of branching architecture and perichaetial position for selected taxa within grade R in the context of modern, modular views of gametophyte structure (Mishler and De Luna, 1991; Newton, cited in Mishler and De Luna, 1991, p.150; La FargeEngland, 1996; Newton and De Luna, 1999). The pleurocarpous condition, and associated characters that are highly variable in the earliest diverging pleurocarp lineages, are optimized onto the phylogeny obtained by Bell and Newton (2004). This in turn allows evaluation of potential scenarios for the evolution of pleurocarpy. Due to lack of support for some critical nodes in the topology obtained under the parsimony criterion in Bell and Newton (2004) and conflict between optimal solutions under parsimony and likelihood, the effect of topology on character optimization is explored. Prior to describing these studies, we briefly review current notions of pleurocarpy as well as closely related concepts of modular branching in mosses.

3.1.1 REVIEW: MODULARITY

AND

BRANCHING HIERARCHY

White (1984) used the term “module” to describe the product of any single apical meristem. In moss gametophytes the apical meristem consists of a single apical cell with three or occasionally two “cutting faces.” Each cell produced directly by fission from the apical cell develops into a metamer, a unit eventually consisting of one leaf, tissue forming epidermis and cortex, and often

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FIGURE 3.1 Strict consensus of 24 MPTs based on three-gene molecular dataset as published in Bell and Newton (2004), with significant groups highlighted. Numbers above branches are bootstrap percentages, numbers below are decay indices. Pleurocarpans taxa (sensu Newton and De Luna, 1999) are in small capitals.

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a lateral bud, which has the potential to produce a new apical cell and hence a new module (Mishler and De Luna, 1991). A module is hence a series of metamers, each derived from a discrete cell lineage beginning with a single cell produced by division of the apical cell. Similarly, the leafy part of a gametophyte is a hierarchy of modules, each produced from a lateral bud on an older module (or, in the case of the first module, an apical cell differentiated from protonemal tissue). Any given module is further characterized by a heteroblastic series (Mishler and De Luna, 1991), as metamer morphology varies progressively from the base (produced when the module is immature) to the apex (produced when the module is mature). Historically, some authors (e.g., Argent, 1973) have referred to the branching of mosses in hierarchical terms. The synthesis of this perspective with a modular view of branching architecture led Newton (cited, for example, in Mishler and De Luna, 1991, p. 150) to define hierarchical levels of modularity in terms of differences in heteroblastic series. Hence, if a branch produced from one module has the same metamer morphology and heteroblastic series as its parent, it is of the same level of modularity, while if it has a distinctly different form it is of another level. Modules are thus referred to as “primary,” “secondary,” etc., depending on the position of the forms they exhibit in this hierarchy. Note the distinction between the hierarchy of individual modules that comprise a plant and the hierarchy of levels of modularity. A primary module may give rise to other primary modules, effectively identical in metamer morphology and heteroblastic series. It may also give rise to more than one type of secondary module, each having a discretely different form but each produced from a branch primordium on a primary module. However, there can be only one type of primary module, the form of which is that of the first module. The essence of these ideas appears to have its origin with Newton in the late 1980s in a series of seminars at Duke University and elsewhere and is cited in Mishler and De Luna (1991, p. 150) as personal communication. Although an explicit description has never been published, modular hierarchical concepts are assumed by La Farge-England (1996) and Newton and De Luna (1999).

3.1.2 REVIEW: PLEUROCARPY, ACROCARPY

AND

CLADOCARPY

The terms Acrocarpi and Pleurocarpi were first used by Nees von Esenbeck et al. (1823) to describe mosses that produce perichaetia “terminally” and “laterally,” respectively. All diplolepidous-alternate mosses produce perichaetia terminally on modules. The perception of a group with “lateral” perichaetia mirrors the existence of a large number of species in which perichaetia are produced terminally on specialized, highly reduced secondary modules. This condition is usually associated with a number of indirectly related features, such as a prostrate growth form, elongated thin-walled areolation and indeterminate primary module growth. The term cladocarpy, first used by Bridel (1826–1927), has been used subsequently to refer either to a third condition of perichaetial position or else has been treated as a form of either pleurocarpy (e.g., Mishler and De Luna, 1991) or of acrocarpy (e.g., the character coding of Hedenäs, 1994). Generally it refers to the production of perichaetia terminally on elongated secondary axes. A precise concept of pleurocarpy remained elusive until relatively recently. Buck and Vitt (1986) defined pleurocarpous mosses as those in which “perichaetial development (and hence the sporophyte) is lateral, with growth continuing apically.” Hedenäs (1994) used a more exacting definition: “archegonia on short specialised branches (always with more or less strongly modified perichaetial leaves).” The problem remained, however, that the distinction between pleurocarpy and “cladocarpy” was a matter of degree. La Farge-England (1996) attempted to define pleurocarpy, acrocarpy and cladocarpy in modular terms and to dispel misconceptions based on imprecise or inconsistent terminology. Pleurocarpy was defined as the production of perichaetia “along the primary module or secondary modules at the terminus of lateral innovations that lack subperichaetial branch primordia or developed branches.” In addition, La Farge-England claimed that juvenile leaf development on perichaetial branches was morphologically different from that of vegetative branches and that perichaetial leaf development was “+/- immediate.” In cladocarpy, perichaetia

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were “produced at the terminus of lateral branches (secondary or tertiary modules) that have subperichaetial branch primordia or developed branches,” and juvenile leaf development at the base of fertile branches was “morphologically similar to that of the vegetative branches.” Although La Farge-England’s terminology and diagrams express the modular hierarchical concepts outlined above, she does not explicitly refer to fertile axes in pleurocarps as a type of secondary module but rather calls them “innovations,” restricting the terms “branch” and “module” to the fertile axes of plants she considers to be acrocarpous or cladocarpous. Newton and De Luna (1999) stated explicitly that the fertile axis in pleurocarps is a secondary module, and that all plants in which the fertile axis is a primary module are acrocarps. As with La Farge-England’s model (1996), the complexities lie in distinguishing short branch cladocarpy from pleurocarpy, a distinction that is fairly discrete in nature but problematic in theory. Newton (personal communication) does not consider La Farge-England’s distinction between types of juvenile leaf development to be reliable, and Newton and De Luna (1999) did not accept that the presence of subperichaetial innovations precludes a plant from being pleurocarpous. Branch primordia may occur on the perichaetial modules of Anomodon longifolius and Warnstorfia exannulata (Hedenäs, 1998), and on those of Amblystegium serpens (Newton, personal communication), all unambiguously derived from within the large clade of “true pleurocarps” and having fertile modules that appear pleurocarpous in all other respects. Newton and De Luna (1999) thus distinguished pleurocarpy on the basis of the extent of development of the fertile module and its leaves at the time when the archegonia are produced. All plants in which distinct vegetative leaves are lacking on fertile modules and developing archegonia are “surrounded only by modified juvenile leaves, with the majority of perichaetial leaves developing after fertilisation” are viewed as pleurocarps. In this study, this definition is broadly accepted, and thus taxa in Pyrrhobryum section Pyrrhobryum and Rhizogonium that produce subperichaetial innovations on fertile modules are nonetheless regarded as pleurocarpous.

3.2 MATERIALS AND METHODS 3.2.1 OBSERVATIONS

OF

PLANT ARCHITECTURE

Specimens of selected taxa from grade R in addition to Hypnodendron menziesii were examined in order to determine underlying modular branching structure and to observe other characters directly related to pleurocarpy, such as presence or absence of subperichaetial innovations. For dioicous species observations were primarily of female plants, although male plants were also examined for some taxa. Thoroughly wetted herbarium specimens were carefully dissected under the dissecting microscope. Many species of Rhizogoniaceae produce multiple basal branches that are loosely attached in the mature plant and matted together with dense rhizoidal growth, making observation of branching structures difficult. Extreme care must be exercised in determining branching order in particular. Both reiterative primary modules and secondary fertile modules are often produced in very basal positions, and determining which shoot gives rise to which may be problematic. Several specimens were examined for each taxon, all of which are in the collections at BM. Voucher specimens are provided in Table 3.1.

3.2.2 CHARACTER OPTIMIZATIONS Pleurocarpy/non-pleurocarpy sensu Newton and De Luna (1999) was optimized onto one of the 24 most parsimonious trees (henceforth referred to as tree A) obtained from the molecular analysis in Bell and Newton (2004). In addition, the effects on optimization of using a slightly different topology (tree B), in which Leptotheca gaudichaudii is sister to Orthodontium lineare (as in the maximum likelihood tree in Bell and Newton, 2004), were explored. No other conflicts between topologies obtained under parsimony and likelihood criteria in Bell and Newton (2004) significantly

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TABLE 3.1 Voucher Specimens for Taxa Examined in the Morphological Studies, and for Scoring of Optimized Characters for Taxa in Grade R and the Hypnodendroid Pleurocarp Clade Taxon

Voucher

Aulacomnium androgynum Aulacomnium heterostichum Bescherellia elegantissima Braithwaitea sulcata Calomnion brownseyi Calomnion complanatum Cryptopodium bartramioides Cyrtopus setosus Goniobryum subbasilare Hymenodon pilifer Hymenodon sericeus Hymenodon sphaerothecius Hymenodontopsis stresemannii Hypnodendron comosum Hypnodendron dendroides Hypnodendron diversifolium Hypnodendron menziesii Hypnodendron spininervium Hypnodendron subspininervium Leptotheca gaudichaudii Mesochaete taxiforme Mesochaete undulata Orthodontium lineare Pterobryella praenitens Pyrrhobryum bifarium Pyrrhobryum dozyanum Pyrrhobryum medium Pyrrhobryum mnioides Pyrrhobryum novae-caledoniae Pyrrhobryum paramattense Pyrrhobryum spiniforme Pyrrhobryum vallis-gratiae Racopilum spectabile Rhizogonium distichum Rhizogonium graeffeanum Rhizogonium novae-hollandiae Rhizogonium pennatum Spiridens camusii

Bell, 1299 Schofield, 10196 Bell, 364 Rodway, s.n. Beveridge, s.n. Child, 2301 Child, 2344 Petrie, s.n. Hyvönen, 2786, (H) Weymouth, 2858 Eddy, 4096 Bell, 363 De Sloover, 46.860 Bell, 648 Gardner, 1 Eddy, 1709 Bell, 385 Bell, 601 Eddy, 6671 Child, 5444 Bell, 464 Bell, 500 Child, 1018 Streimann, 55850 (CBG) Child, 5476 Ikegami, s.n. 10/11/1957 Bell, 349 Bell, 698 Bell, 409 Streimann, 4781 Newton, 4341 Hedderson, 13377 Newton, 5351 Child, 3789 Bell, 429 Bell, 633 Bell, 720 Bell, 416

Note: All BM unless otherwise stated.

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alter optimization of the characters examined. Based partially on character concepts developed during the morphological investigations, presence/absence of subperichaetial innovations and position of perichaetial modules were optimized onto a pruned tree B (tree C). Tree C includes only grade R and the higher pleurocarps, thus minimizing optimization problems associated with inapplicable characters in non-pleurocarpous taxa. Tree A was selected on the basis that it is one of the most parsimonious trees (MPTs) in which Pyrrhobryum dozyanum is resolved as sister to P. section Pyrrhobryum, as in the preferred phylogenetic hypothesis of Bell and Newton (2004, Figure 7). Optimizations are unaltered if the alternative position of Pyrrhobryum dozyanum as sister to the larger clade that includes Cryptopodium and Calomnion is assumed. All other MPTs in Bell and Newton (2004) were otherwise identical to tree A within grade R, other than for resolution within Rhizogonium, all exemplars of which share the same states for all optimized characters. As two nodes in the “backbone” of grade R have no bootstrap support (Figure 3.1), the effects of collapsing these branches was tested for all optimizations. In all cases this either had no effect or else it eliminated the potential for existing equivocal optimization to be resolved by the use of ACCTRAN or DELTRAN alone (accelerated and delayed transformation, Swofford and Maddison, 1987). Character optimization was performed using MacClade 4.03 (Maddison and Maddison, 2001). Where it is not indicated that ACCTRAN or DELTRAN resolving options have been used, diagrams summarize any alternative optimizations and show conflict as equivocal. Vouchers for scoring of characters for taxa in grade R and in the hypnodendroid pleurocarp clade are provided in Table 3.1. Taxa in the Hypnidae were assumed to be pleurocarpous with distally produced perichaetial modules and to lack subperichaetial innovations, and taxa outside of the clade that includes grade R and the higher pleurocarps were assumed not to be pleurocarpous. Perichaetial module position and presence/absence of subperichaetial innovations were considered applicable to pleurocarpous taxa only (see discussion).

3.3 RESULTS 3.3.1 OBSERVATIONS

OF

PLANT ARCHITECTURE

Descriptions of modular branching structure and perichaetial position are provided below for taxa examined in detail. Species having an identical or nearly identical modular structure are treated together. Figure 3.2 provides diagrammatic representations of each distinct structural type identified for pleurocarpous taxa (sensu Newton and De Luna, 1999). 3.3.1.1 Rhizogonium distichum, Pyrrhobryum paramattense, and Pyrrhobryum spiniforme See Figure 3.2A. The production of reduced perichaetial modules basally characterizes the genus Rhizogonium and Pyrrhobryum sect. Pyrrhobryum (Manuel, 1980). On careful dissection it is apparent that the primary modules are erect, determinate, vegetative shoots that branch from the base (or extremely close to the base) to produce further primaries. The secondary perichaetial modules are also derived basally from primary modules and are very short with clearly differentiated perichaetial leaves and no normal vegetative leaves. In contrast with most pleurocarps, perichaetial modules may produce innovations giving rise to further perichaetial modules. Hence, these species are pleurocarps sensu Newton and De Luna (1999), but cladocarps under La Farge-England’s (1996) definitions. The possibility that reduced perichaetial modules could be at the primary level of the branching hierarchy was considered, but in none of the plants examined was there convincing evidence of this. Similarly, all innovations produced on perichaetial modules appeared to develop into other perichaetial modules rather than vegetative primary modules (i.e., the sequence of module types is hierarchical and unidirectional). Individual primary modules often produce both perichaetial mod-

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A

D

B

E

Vegetative primary module (determinate)

C

F

G

Pleurocarpous perichaetial module

Pleurocarpous perichaetial module with subperichaetial innovations Vegetative primary module (continuously growing) Vegetative secondary module (determinate)

FIGURE 3.2 Diagrammatic representations of modular architecture types found in pleurocarpous members of the Rhizogoniaceae, Hypnodendron and typical Hypnalean pleurocarps. (A) Rhizogonium type; (B) Pyrrhobryum sect. Bifariella type; (C) Hypnodendron type; (D) Hymenodon type; (E) Hymenodontopsis type; (F) Goniobryum type; (G) typical Hypnalean pleurocarp (e.g., Eurhynchium).

ules and further primary modules from immediately adjacent positions at the extreme base of the stem, and the continued production of upright determinate shoots basally seems to be the principal method of vegetative propagation. All Rhizogoniaceae are dioicous with the exception of Pyrrhobryum spiniforme, which is synoicous. On studying male plants of R. distichum it became apparent that at least some perigonial modules are produced directly from rhizoids, which themselves emerge from the adaxial edge of leaf axils, a condition that is termed “rhizautoicy” in autoicous moss species. Perigonial modules produced in this manner often produced innovations giving rise to other perigonial modules. 3.3.1.2 Pyrrhobryum dozyanum, Pyrrhobryum mnioides, Mesochaete taxiforme, Spiridens camusii, and Bescherellia elegantissima Although some of these plants are very different in habit, size, orientation and general morphology, they are similar or identical in modular terms (Figure 3.2B). According to Manuel (1980), Pyrrhobryum sect. Bifariella is characterized by perichaetia produced “laterally on gametophores” and rhizoids that often form a tomentum extending some distance up the stem. On examination of Pyrrhobryum dozyanum it is apparent that the upright primary modules are determinate and may innovate from positions within a broad central zone on the shoot, giving rise either to further primaries or to perichaetial modules. Primary modules alone may also reiterate basally. Perichaetial

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modules are very short and were not observed to produce subperichaetial innovations. Pyrrhobryum mnioides differs slightly (at least in the Australasian specimens examined) in that branching of primaries from a distinctly basal position was not observed, although as the lower parts of stems are often decomposed this is difficult to confirm. Mesochaete taxiforme, although having a very different morphology and a semiprostrate growth form, is structurally identical to Pyrrhobryum dozyanum, with determinate vegetative primary modules reiterating from both basal and distal positions and highly reduced perichaetial modules produced distally. Spiridens camusii and Bescherellia elegantissima, robust epiphytes with a horizontal to pendulous growth form, also have the same underlying structure. As in Rhizogonium distichum, male plants of P. mnioides were observed to produce innovations on perigonial modules giving rise to further perigonial modules, although modules arising from rhizoids were not observed. 3.3.1.3 Pyrrhobryum bifarium, Pyrrhobryum vallis-gratiae, and Hypnodendron menziesii See Figure 3.2C. Pyrrhobryum bifarium has a similar branching structure to other members of P. section Bifariella with the addition of a distinct second level of vegetative modularity that confers a dendroid or subdendroid morphology. Fully developed primary modules (effectively stipes) are four-angled at the base, with longly decurrent, spirally arranged leaves that become larger further up the stem. Further primary modules may be produced from the base and, occasionally, from a central position. The secondary vegetative modules are very distinct from the primaries in having distichously arranged, asymmetric leaves that are considerably shorter and more ovate than those of the primary module. As in Hypnodendron, the leaf form and orientation of the primary module switches to resemble that of the secondary modules after these are produced. Again, perichaetial modules are short and sessile, originate from an approximately central position and do not appear to produce innovations. P. bifarium is in fact structurally identical to Hypnodendron menziesii (and other Hypnodendron species), although fewer secondary vegetative modules are produced, plants are much smaller and the overall form is more loosely dendroid. In H. menziesii, as in Pyrrhobryum bifarium, primaries may sometimes reiterate distally as well as basally, although this is not the case for all Hypnodendron taxa (Touw, 1971; Bell and Newton, 2005). Pyrrhobryum vallis-gratiae has a similar structure, although the presence of vegetative secondary modules is less clear-cut. Gametophores usually have a fairly dendroid appearance, with a pronounced heteroblastic series on the older shoots (basal leaves on the “stipe” are highly differentiated from those further up the module). The higher vegetative branches are considerably shorter with a much more compact heteroblastic series, although (unlike in P. bifarium) the mature leaf morphology is very close or identical to that of the primary modules. 3.3.1.4 Hymenodon sericeus and Hymenodon pilifer Species of Hymenodon (Figure 3.2D) are often described as innovating basally (e.g., Koponen et al., 1986), implying that their structure is similar or identical to that of Rhizogonium and Pyrrhobryum sect. Pyrrhobryum. If the dense tangle of rhizoids at the base of the stem is dissected, however, it is apparent that primary modules are usually produced from other primaries some distance up the shoot, although they are generally restricted to the lower quarter. By contrast, perichaetial modules appear always to innovate from primaries in a distinctly basal position. Interpretation can be difficult, as often a primary will arise from another primary some distance from the base and immediately give rise to a basal perichaetial module, giving the false impression that a distally produced perichaetial module is innovating to produce a primary module. In none of the specimens examined was there conclusive evidence of any innovations on perichaetial modules, the latter being very short and typically pleurocarpous.

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3.3.1.5 Hymenodontopsis stresemannii The structure of this plant (Figure 3.2E) initially seems similar to that of Hymenodon, although primary modules tend to innovate from other primaries still further from the base. Unlike in Hymenodon, however, perichaetial modules, although generally restricted to the basal portion of the primary, are not distinctly basal. Typically, a primary module will produce a succession of two or three perichaetial modules from the basal region of the shoot before switching over to the production of further primaries higher up. Structurally the plant is like a “stretched out” Hymenodon, with successive branching of primary modules from central positions creating a complicated network of shoots. Most of this structure is usually obscured by the dense felt of rhizoids that clothes the lower parts of the mature plant. This tomentum appears to be produced from the lower parts of primaries, so as new primaries are produced by innovations higher up the gametophore, new rhizoid growth initiated at the bases of the young shoots extends the tomentum further up the plant. 3.3.1.6 Goniobryum subbasilare This species produces upright, determinate primaries that innovate vegetatively from the base, although perichaetial modules are produced slightly further up the shoot (Figure 3.2F). As such, the structure of the plant is in some respects the opposite of that of Hymenodon, in which perichaetial modules are basal and vegetative branching is more distal. Uniquely in the taxa examined that produce fertile modules distally, subperichaetial innovations giving rise to further perichaetial modules were observed in some specimens. 3.3.1.7 Typical Hypnalean Pleurocarp Although the derived forms of pleurocarpy found in the Hypnidae were not formally examined for this study, Figure 3.2G is provided as an illustration of a typical architectural type found in the group (common in the Hypnaceae or Brachytheciaceae, for example). The higher pleurocarps include a great diversity of forms (see Newton, Chapter 14 and Tangney, Chapter 15 in this volume), but many have a structure similar or identical to that shown in Figure 3.2G, in which the primary module is continuously growing and determinate secondary vegetative modules are produced. Often the primary module will also reiterate from an approximately central position, as illustrated here. The continuous growth of the primary is usually associated with a more or less prostrate habit, and if determinate secondaries are regularly initiated, a pinnate morphology results. Many Hypnales (especially those previously classified in the Leucondontales) do not produce determinate secondaries, and branching may be exclusively by the reiteration of primaries. Such plants have traditionally been described as “sympodial,” although this terminology is misleading and lends itself to misapplication. Many so called “monopodial” plants with abundant and obvious determinate secondary branching are actually sympodial, as branching by primary module reiteration also occurs. Some of the earlier diverging Hypnidae (e.g., in the Ptychomniales and Hypopterygiaceae) have determinate primaries and forms similar to some of those found in grade R and the hypnodendroid pleurocarps, although true basal production of perichaetial modules does not occur and subperichaetial innovations are a rare atavism in isolated lineages. 3.3.1.8 Cryptopodium bartramioides, Leptotheca gaudichaudii, Orthodontium lineare, Calomnion complanatum, and Aulacomnium heterostichum All of these plants are acrocarpous and will be considered together, although they represent at least three slightly different modular architectures. All are members of grade R, although only Cryptopodium and Leptotheca are currently classified in the Rhizogoniaceae.

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Cryptopodium is acrocarpous, despite sharing a large number of gametophytic characters with Pyrrhobryum. Some previous authors (e.g., Sainsbury, 1955) have described it as producing perichaetia both “laterally” and terminally. In fact, there is only a single type of module, which in female plants is terminated by a perichaetium. Modules are often moderately short and produce innovations immediately below the perichaetium, such that a succession of modules superficially gives the impression of a single long stem with lateral perichaetia. The “interrupted” look of such “false” stems, caused by large leaves at the top of one module being succeeded by small ones at the base of the next, reveals their true nature. When two innovations are produced from a single module the false stem appears to “branch.” Not all female specimens of Cryptopodium have this “interrupted false stem” habit, some having individual modules that are more elongated. Male plants have a more conventional acrocarpous habit and consist of modules that are considerably elongated. In Leptotheca, fertile female primary modules branch to give rise to further primaries from immediately underneath the perichaetium. There are usually several new branches initiated from the apex of each mature primary module, these being fairly elongated. Branching is also common from a central position on the primary module, with a clear distinction between the two alternative points of origin. The initiation of apically derived branches is clearly associated with the termination of parent module growth. Calomnion complanatum appears to have the simplest modular structure possible, consisting only of unbranched primary modules producing terminal perichaetia when mature. Often, many individual stems grow closely together and may be matted with rhizoids and/or protonemata at their extreme bases. This, in combination with the very small size of the plants, makes it difficult to exclude the possibility that modules may reiterate from the extreme base, although in none of the stems examined did this appear to be the case. The separate male plants have a similar structure, producing perigonia terminally on unbranched stems. The heteroblastic series is clearly different, however, with leaves very distantly inserted and not obviously distichous and heteromorphous as in female plants. Aulacomnium heterostichum appears to consist of a single type of module, often moderately short, that branches fairly extensively. While modules are often fertile, many others within an individual plant may be sterile. As fertile and nonfertile modules seem otherwise identical and appear fairly random in their relationships to each other, it is assumed that they represent the same type of module. Orthodontium is an unusual plant with unique features. Apparently an acrocarp, many modules are moderately to very short and appear to reiterate. In addition, vegetative, reduced perichaetial and perigonial modules may be derived from stem epidermal cells. These give rise to highly shortened rhizoids that produce a small cluster of cells, one of which will differentiate into an apical cell and produce a short branch. This branch remains loosely attached to the parent module via the short rhizoid and may produce innovations. This form of module production cannot be fitted easily into concepts of module hierarchy, as it involves the production of axes by a method other than branch primordia. The mechanism may be homologous with that of “rhizautoicy,” although it may give rise to perichaetial and vegetative modules in addition to perigonial ones. More study is required to establish homologies between modules produced in this manner by Orthodontium and those derived from normal branching mechanisms in mosses.

3.3.2 CHARACTER OPTIMIZATIONS Figure 3.3A shows the result of optimizing presence or absence of pleurocarpy sensu Newton and De Luna (1999) onto tree A. Pleurocarpy is shown to be independently derived in Hymenodon and in the ancestral lineage of the clade that includes the remainder of grade R and the higher pleurocarps. Aulacomnium (as represented by A. androgynum) and the Calomnion–Cryptopodium clade represent reversals to acrocarpy. Optimizing the same character onto tree B, however, in which Leptotheca gaudichaudii and Orthodontium lineare are assumed to be sisters, produces an ambiguous result for the origin of pleurocarpy with different solutions under ACCTRAN and

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DELTRAN. Under DELTRAN, favouring parallelisms at the expense of reversals, the result is identical to that shown in Figure 3.3A. Under ACCTRAN, there is a single origin of pleurocarpy at the base of grade R and the Leptotheca–Orthodontium clade represents an additional reversal to acrocarpy (Figure 3.3B). The result of optimizing the presence or absence of pleurocarpous subperichaetial innovations onto tree C is shown in Figure 3.4. The character is shown as derived from within grade R, either once, at the base of the clade that includes Rhizogonium, Pyrrhobryum sect. Pyrrhobryum, Goniobryum subbasilare, Pyrrhobryum dozyanum, Cryptopodium and Calomnion (ACCTRAN, Figure 3.4A), or else independently in Pyrrhobryum sect. Pyrrhobryum and the Rhizogonium–Goniobryum clade (DELTRAN, Figure 3.4B). The result is the same if Leptotheca is assumed to be sister to Hymenodon, as in tree A. Thus, if pleurocarpy is assumed to have a single origin (Figure 3.3B), then subperichaetial innovations are derived, either once or twice, from ancestors that were pleurocarpous but lacked them. If pleurocarpy has two origins (Figure 3.3A), then it may be hypothesized, although only under ACCTRAN (Figure 3.4A), that the form of pleurocarpy independently derived in the major pleurocarpous clade was primitively associated with the presence of subperichaetial innovations. Figure 3.5 shows optimization of pleurocarpous perichaetial module position onto tree C. Under ACCTRAN (Figure 3.5A), the production of perichaetial modules distally on primaries (the state found in all higher pleurocarps) is synapomorphic for the clade that includes all pleurocarps except Hymenodon. Both Rhizogonium and Pyrrhobryum sect. Pyrrhobryum represent independent reversals to basal production of perichaetial modules. As the character is only applicable to pleurocarpous taxa and states dichotomize basally, the condition at the ancestral node of grade R remains ambiguous. Under delayed transformation (Figure 3.5B), this ambiguity perpetuates to more distal branches, and the condition of all deeper nodes outside of the clade that includes Mesochaete, most of Pyrrhobryum sect. Bifariella and the higher pleurocarps cannot be unambiguously reconstructed. Under DELTRAN, therefore, the character must be polarized in order for optimization to be meaningful. Figure 3.6 shows the results of optimizing perichaetial module position onto tree C under DELTRAN, with the character alternatively polarized by the addition of an artificial root to assume that either distal (Figure 3.6A) or basal (Figure 3.6B) module position is primitive. In the former case, basal perichaetial module production is independently derived three times in Rhizogonium, Pyrrhobryum sect. Pyrrhobryum and Hymenodon. If basal module production is plesiomorphic (Figure 3.6B), then the equally parsimonious scenario of an independent origin of distal module production in Pyrrhobryum dozyanum, Goniobryum subbasilare and the clade that includes Mesochaete, most of Pyrrhobryum sect. Bifariella and the higher pleurocarps must be assumed. Polarization does not affect ACCTRAN optimization other than to determine the state of the basal node, and thus which branch of the initial dichotomy is apomorphic. None of these optimizations are altered if Leptotheca is assumed to be sister to Hymenodon, as in Figure 3.3A.

3.4 DISCUSSION The results demonstrate that the pleurocarpous taxa currently classified in the Rhizogoniaceae represent a number of distinctly different architectures that exploit the key innovation of pleurocarpy sensu stricto, i.e., the production of perichaetia on specialized, highly reduced secondary modules. These take the form of alternative combinations of secondary pleurocarpous traits, such as position of fertile modules, form and position of vegetative branching, and presence or absence of subperichaetial innovations. By contrast, the Hypnidae and the hypnodendroid pleurocarps are relatively conservative in terms of pleurocarpous architecture, being based on a much more restricted range of fundamental modular structures. Optimization of pleurocarpy and associated traits onto current

FIGURE 3.3 (A) Optimization of pleurocarpy/non-pleurocarpy onto tree A.

A Non-Pleurocarpous Pleurocarpous

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare Hedwigia ciliata Rhacocarpus purpurascens Bartramia halleriana Philonotis fontana Pohlia nutans Mnium hornum Plagiomnium Bryumalpinum Ulota crispa Dicranum scoparium Schistostega pennata Funaria hygrometrica

Continued. Pleurocarpy in the Rhizogoniaceous Grade

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Non-Pleurocarpous Pleurocarpous

ACCTRAN

FIGURE 3.3 (B) Optimization of pleurocarpy/non-pleurocarpy onto tree B under accelerated transformation (ACCTRAN).

B

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare Hedwigia ciliata Rhacocarpus purpurascens Bartramia halleriana Philonotis fontana Pohlia nutans Mnium hornum Plagiomnium Bryumalpinum Ulota crispa Dicranum scoparium Schistostega pennata Funaria hygrometrica

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Subpericaetial innovations on pleurocarpous perichaetial modules

FIGURE 3.4 Optimization of presence/absence of subperichaetial innovations on pleurocarpous perichaetial modules onto tree C. (A) Under accelerated transformation (ACCTRAN). Continued.

A Subpericaetial innovations on pleurocarpous perichaetial modules not observed

ACCTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare

Pleurocarpy in the Rhizogoniaceous Grade

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Subpericaetial innovations on pleurocarpous perichaetial modules

FIGURE 3.4 Optimization of presence/absence of subperichaetial innovations on pleurocarpous perichaetial modules onto tree C. (B) under delayed transformation (DELTRAN).

B Subpericaetial innovations on pleurocarpous perichaetial modules not observed

ACCTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare

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Equivocal

Pleurocarpous perichaetial modules produced distally

FIGURE 3.5 Optimization of perichaetial module position onto tree C. (A) Under accelerated transformation (ACCTRAN).

A Pleurocarpous perichaetial modules produced basally

ACCTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare

Continued. Pleurocarpy in the Rhizogoniaceous Grade

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Equivocal

FIGURE 3.5 Optimization of perichaetial module position onto tree C. (B) under delayed transformation (DELTRAN).

B Pleurocarpous perichaetial modules produced distally

Pleurocarpous perichaetial modules produced basally

DELTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare

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Pleurocarpous perichaetial modules produced distally

FIGURE 3.6 Optimization of perichaetial module position onto tree C under delayed transformation (DELTRAN). (A) Distally produced perichaetial modules assumed to be plesiomorphic. Continued.

A Pleurocarpous perichaetial modules produced basally

DELTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare ROOT

Pleurocarpy in the Rhizogoniaceous Grade

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Pleurocarpous perichaetial modules produced distally

FIGURE 3.6 Optimization of perichaetial module position onto tree C under delayed transformation (DELTRAN). (B) basally produced perichaetial modules assumed to be plesiomorphic.

B Pleurocarpous perichaetial modules produced basally

DELTRAN

Thamnobrum alopecurum Pterogonium gracile Rhytidiadelphus triquetrus Fontinalis antipyretica Rutenbergia madagassa Hookeria lucens Bryobrothera crenulata Lopidium concinnum Cyathophorum bulbosum Glyptothecium sciuroides Garovaglia elegans Hampeella alaris Hypnodendron comosum Hypnodendron dendroides Hypnodendron subspininervum Hypnodendron spininervum Spiridens camusii Cyrtopus setosus Bescherellia elegantissima Hypnodendron diversifolium Hypnodendon menziesii Pterobryella praenitens Braithwaitea sulcata Powellia involutifolia Racopilum spectabile Aulacomnium androgynum Mesochaete taxiforme Mesochaete undulata Pyrrhobryum vallis-gratiae Pyrrhobryum bifarium Pyrrhobrum mnioides Pyrrhobrum medium Pyrrhobrum novae-caledoniae Pyrrhobryum spiniforme Pyrrhobryum paramattense Pyrrhobryum dozyanum Cryptopodium bartramioides Calomnion complanatum Calomnion brownseyi Rhizogonium novai-hollandiae Rhizogonium pennatum Rhizogonium distichum Rhizogonium graeffeanum Goniobryum subbasilare Hymenodon sphaerothecius Hymenodon pilifer Leptotheca guadichaudii Orthodontium lineare ROOT

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hypotheses of phylogeny reveals a limited set of alternative evolutionary scenarios for the initial development of pleurocarpy within grade R.

3.4.1 CODING STRATEGIES

AND

PRIMARY HOMOLOGY

Due to the close association between characters such as, for example, extreme reduction of perichaetial modules and lack of subperichaetial innovations, there are several different ways in which characters relating to pleurocarpy may be coded, and character definitions may carry assumptions of primary homology that require justification. When optimizing characters onto a preexisting phylogeny, however, the effects of different coding strategies are more transparent than in phylogeny reconstruction. Also, as coded here, position of perichaetial modules and the presence or absence of subperichaetial innovations are properties of pleurocarpous fertile modules that are not applicable to acrocarps, and hence are subject to theoretical problems associated with missing data in phylogeny reconstruction (Maddison, 1993; Hawkins et al., 1997; Lee and Bryant, 1999; Strong and Lipscomb, 1999). The presence or absence of subperichaetial innovations on pleurocarpous fertile modules might be considered equally applicable to non-pleurocarpous fertile modules. As perichaetial branches in pleurocarps are secondary modules, however, it is not clear whether innovations could be considered homologous to those on acrocarpous primary modules. More significantly, due to the highly reduced nature of pleurocarpous perichaetial modules, it is not possible to state whether innovations are apical (i.e., truly subperichaetial, initiated in association with module growth termination), basal or nonspecific, and thus they cannot be homologized with, for example, subperichaetial innovations in cladocarps. Similarly, in the case of position of perichaetial module production on the primary module, given the highly specialized form and function of the pleurocarpous perichaetial module it is questionable if this character could be identified with the position of the elongated fertile module in cladocarps. An alternative coding strategy would be to treat one or more of the various forms of pleurocarpy found in grade R as separate states of a single character in which acrocarpy and “conventional pleurocarpy” were also states. This would inappropriately link characters that appear to vary independently, however, such as pleurocarpy sensu stricto and production of subperichaetial innovations. The result would be a highly artificial character with a large number of states, in which transformational independence would be compromised (Lee and Bryant, 1999).

3.4.2 SCENARIOS Conflict between optimizations, especially under accelerated versus delayed transformation, as well as sensitivity to topological uncertainty, result in more than one equally plausible scenario for the early evolution of pleurocarpy. Rather than adopt a universal preference for, say ACCTRAN over DELTRAN a priori, it is useful to examine conflicting scenarios individually in the light of the nature of the morphological transformations they require. The results are consistent with pleurocarpy sensu stricto either being independently derived in Hymenodon or having a single origin at the base of grade R (Figures 3.3A and 3.3B). The single origin hypothesis requires that the acrocarpous Leptotheca gaudichaudii not be sister to Hymenodon. This is at odds with the most parsimonious tree in Bell and Newton (2004) but not with their maximum likelihood tree, and there is no support for the clade with Hymenodon and Leptotheca under parsimony. Furthermore, although the optimization algorithms favour loss and gain of characters equally, it is clearly more plausible to assume a single loss of pleurocarpy in a hypothetical Leptotheca–Orthodontium clade than the independent origin of such a distinctive key innovation in two closely related taxa, especially as other reversals to acrocarpy are known to occur elsewhere within grade R. Arguably, this may be true even if the most parsimonious topology is preferred

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and a single extra step assumed. Thus, it is hypothesized that pleurocarpy sensu Newton and De Luna (1999) is a synapomorphy for the clade that includes grade R and all higher pleurocarps. Assuming the above, the plesiomorphic form of pleurocarpy is characterized by a lack of subperichaetial innovations on fertile modules (Figure 3.4), which is the state found in nearly all of the higher pleurocarps. The production of subperichaetial innovations giving rise to further perichaetial modules is an adaptation found in a small number of early diverging pleurocarpous lineages, and is either a synapomorphy for the clade that includes Rhizogonium and Pyrrhobryum sect. Pyrrhobryum, or a parallelism in Pyrrhobryum sect. Pyrrhobryum and the Goniobryum–Rhizogonium clade (Figure 3.4). Pleurocarpy potentially confers a competitive advantage by decoupling vegetative growth and sporophyte production. Whereas acrocarps and cladocarps must invest time and physical resources in producing an elongated leafy shoot for each perichaetium, pleurocarps may produce many perichaetia for an equivalent investment in vegetative growth. Where perichaetial modules are exclusively basal, however, physical space on the primary module and/or availability of branch primordia may be limiting factors in the number of perichaetia that may be produced. Reiteration by means of subperichaetial innovations circumvents this problem, just as reiteration of vegetative modules basally circumvents limitations on horizontal propagation imposed by an upright, tufted habit. It therefore seems plausible that subperichaetial innovations could be an adaptive response to the limitations inherent in the production of pleurocarpous perichaetial modules in an exclusively basal position. Conflict between ACCTRAN and DELTRAN optimizations of this character derives from the anomalous position of Pyrrhobryum dozyanum, a member of Pyrrhobryum sect. Bifariella having distinctly distal perichaetial modules that lack innovations. The position of this taxon as well as that of Goniobryum, in which perichaetial modules are distal but subperichaetial innovations are sometimes present, also confounds optimization of the character representing perichaetial module position. Although the earliest diverging pleurocarpous lineage, Hymenodon, produces perichaetial modules basally, only under DELTRAN optimization is it most parsimonious to assume that this state is plesiomorphic in the clade that includes the rest of the pleurocarps (Figures 3.5 and 3.6). Furthermore, this is ambiguous unless the character is artificially polarized (Figure 3.6). Of the available scenarios for the evolution of this character, the least credible is that deriving from DELTRAN optimization where distal modules are assumed to be primitive (Figure 3.6A). This would require three independent origins of basal perichaetial modules from ancestors with distal modules, unlikely given that basally produced fertile modules are unique to the Rhizogoniaceae and appear never to have arisen among the higher pleurocarps. More plausible is that the first pleurocarpous mosses produced perichaetial modules basally, and that either (1) distal modules arose in the ancestor of the clade that includes Rhizogonium and the higher pleurocarps with reversals to basal module production in Rhizogonium and Pyrrhobryum sect. Pyrrhobryum (Figure 3.5A), or (2) there were three independent origins of distal modules, in the clade that includes Mesochaete and the higher pleurocarps, in Pyrrhobryum dozyanum and in Goniobryum (Figure 3.6B). As distal perichaetial module production appears to be a highly successful strategy, as witnessed by the large number of species in the Hypnidae, the latter scenario is marginally preferable. Bringing all of these strands together, a general hypothesis can be proposed, in which there is a single origin of pleurocarpy associated with highly reduced basal perichaetial modules that lack subperichaetial innovations in the ancestral lineage of grade R and the higher pleurocarps. Having developed from acrocarps or cladocarps, these plants would have been adapted in a number of different ways to an upright or tufted existence with determinate primary module growth, even if pleurocarpy theoretically permitted continuous growth of vegetative modules. Basal production of pleurocarpous fertile modules would confer an advantage in terms of maximizing sporophyte production, although this would be limited by availability of primordia at the base of the primary module. In the Rhizogonium–Pyrrhobryum sect. Pyrrhobryum clade, subperichaetial innovations developed as an adaptive strategy for further maximizing sporophyte production, one particularly

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suited to the tufted pleurocarpous growth form. This was usually associated with exclusively basal vegetative module reiteration and often with a preference for terrestrial substrates or dead wood. An alternative strategy, involving acquisition of the ability to produce pleurocarpous perichaetial modules in nonbasal positions, probably developed independently in the ancestor of the clade that includes Mesochaete and the higher pleurocarps, in Pyrrhobryum dozyanum and in Goniobryum. Usually associated with this was the development of distal reiteration of primary modules and in some cases production of vegetative secondary modules, although with the retention of distinctly basal vegetative reiteration. Pyrrhobryum dozyanum may, like the common ancestor of the Mesochaete–higher pleurocarp clade, have evolved from a lineage that had not developed subperichaetial innovations, or it may have lost them in response to the acquisition of distal module production. In Goniobryum this structural type is not fully developed, with perichaetial modules usually produced on the lower sections of primaries, subperichaetial innovations retained and distal vegetative branching not present. This form of pleurocarpous architecture (Figure 3.2B, C and E), i.e., an upright or horizontal to pendulous, determinate growth form coupled with distal perichaetial module production and vegetative reiteration from distal and usually also basal positions, is remarkably successful and characterizes most of the earlier pleurocarpous lineages, including many of the earliest diverging Hypnidae, such as the Ptychomniaceae and the Hypopterygiaceae (although the primary module in Hypopterygium is initially stoloniferous; Kruijer, 2002). It perhaps finds its ultimate expression in the large dendroid mosses of the Hypopterygiaceae and the hypnodendroid pleurocarps. A subsequent novel architectural exploitation of the potential offered by pleurocarpy was the abandonment of forms based on determinate vegetative growth in favour of a prostrate, creeping habit with continuous primary module growth and often extensive secondary vegetative branching. This occurred independently in the Racopilaceae (Bell and Newton, 2005) and in the higher Hypnidae and is outside the scope of this study. Although this architecture is often regarded as characteristic of pleurocarpy (e.g., Buck et al., 2000), it is better seen as the latest and most successful in a line of adaptive strategies based on pleurocarpy sensu stricto, and the one that is most removed from the constraints of plesiomorphic acrocarpous forms.

ACKNOWLEDGMENTS The majority of the work for this study was conducted as part of the lead author’s Ph.D. research at the Natural History Museum (NHM), London and the Department of Plant Sciences at the University of Reading, funded by the Botany Department at the NHM. Production of the published version of the manuscript took place at the Botanical Museum of the University of Helsinki and was funded by the Academy of Finland, initially under Jaakko Hyvönen’s “Bryosphere” project (No. 50620) and latterly the project (No. 108629) “Polytrichales: towards a modern phylogenetic monograph and the development of a model of sporophyte evolution”.

REFERENCES Argent, G. C. G. (1973) A taxonomic study of African Pterobryaceae and Meteoriaceae. Journal of Bryology, 7: 353–378. Bell, N. E. and Newton, A. E. (2004) Systematic studies of non-hypnanean pleurocarps: Establishing a phylogenetic framework for investigating the origins of pleurocarpy. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 290–319. Bell, N. E. and Newton, A. E. (2005) The paraphyly of Hypnodendron and the phylogeny of related nonhypnanaean pleurocarpous mosses inferred from chloroplast and mitochondrial sequence data. Systematic Botany, 30: 34–51.

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Bridel, S. E. (1826–1927) Bryologia universa seu Systematica ad Novam Methodum Dispositio, Historia et Descriptio omnium Muscorum Frondosorum Hucusque cognitorum cum Synonymia ex Auctoribus Probatissimis. Vols. 1, 2. J. A. Bartholomew, Leipzig. Buck, W. R. and Vitt, D. H. (1986) Suggestions for a new familial classification of pleurocarpous mosses. Taxon, 35: 21–60. Buck, W. R., Goffinet, B. and Shaw, A. J. (2000) Testing morphological concepts of orders of pleurocarpous mosses (Bryophyta) using phylogenetic reconstructions based on trnL-trnF and rps4 sequences. Molecular Phylogenetics and Evolution, 16: 180–198. Goffinet, B. and Buck, W. R. (2004) Systematics of the Bryophyta (mosses): From molecules to a revised classification. In Molecular Systematics of Bryophytes (ed. B. Goffinet, V. Hollowell and R. Magill). Missouri Botanical Garden Press, St. Louis, pp. 205–239. Hawkins, J. A., Hughes, C. E and Scotland, R. W. (1997) Primary homology assessment, characters and character states. Cladistics, 13: 275–283. Hedenäs, L. (1994) The basal pleurocarpous diplolepidous mosses — A cladistic approach. Bryologist, 97: 225–243. Hedenäs, L. (1998) Cladistic studies on pleurocarpous mosses: Research needs, and use of results. In Bryology for the Twenty-First Century (ed. J. Bates, N. Ashton and J. Duckett). Maney Publishing and the British Bryological Society, Leeds, pp. 125–141. Koponen, T. (1988) The phylogeny and classification of Mniaceae and Rhizogoniaceae. Journal of the Hattori Botanical Laboratory, 64: 37–46. Koponen, T., Touw, A. and Norris, D. H. (1986) Bryophyte flora of the Huon Peninsula, Papua New Guinea. XIV. Rhizogoniaceae (Musci). Acta Botanica Fennica, 133: 1–24. Kruijer, H. (2002) Hypopterygiaceae of the world. Blumea, Supplement 13: 1–388. La Farge-England, C. (1996) Growth form, branching pattern, and perichaetial position in mosses: Cladocarpy and pleurocarpy redefined. Bryologist, 99: 170–186. Lee, D. and Bryant, H. N. (1999) A reconsideration of the coding of inapplicable characters: Assumptions and problems. Cladistics, 15: 373–378. Maddison, D. R. and Maddison, W. P. (2001) MacClade 4: Analysis of Phylogeny and Character Evolution, Version 4.03. Sinauer Associates, Sunderland, Massachusetts. Maddison, W. P. (1993) Missing data versus missing characters in phylogenetic analysis. Systematic Biology, 42: 576–581. Manuel, M. G. (1980) Miscellanea bryologica. II. Classification of Rhizogonium Brid., Penzigiella hookeri Gangulee, and some nomina nuda. Cryptogamie: Bryologie, Lichenologie, 1: 67–72. Mishler, B. D. and De Luna, E. (1991) The use of ontogenetic data in phylogenetic analyses of mosses. Advances in Bryology, 4: 121–167. Nees von Esenbeck, C. G., Hornschuch, F. and Sturm, J. (1823) Bryologia germanica, oder Beschreibung der in Deutschland und in der Schweiz wachsenden Laubmoose. J. Sturm, Nürnberg. Newton, A. E. and De Luna, E. (1999) A survey of morphological characters for phylogenetic study of the transition to pleurocarpy. Bryologist, 102: 651–682. Patterson, C. (1982) Morphological characters and homology. In Problems of Phylogenetic Reconstruction (ed. K. Joysey and A. Friday). Academic Press, London, pp. 21–74. Sainsbury, G. O. K. (1955) A handbook of the New Zealand mosses. Royal Society of New Zealand Bulletin, 5: 1–490. Shaw, A. J., Cox, C. J., Goffinet, B., Buck, W. R. and Boles, S. B. (2003) Phylogenetic evidence of a rapid radiation of pleurocarpous mosses (Bryophyta). Evolution, 57: 2226–2241. Strong, E. E. and Lipscomb, D. (1999) Character coding and inapplicable data. Cladistics, 15: 363–371. Swofford, D. L. and Maddison, W. P. (1987) Reconstructing ancestral character states under Wagner parsimony. Mathematical Biosciences, 87: 199–229. Touw, A. (1971) A taxonomic revision of the Hypnodendraceae (Musci). Blumea, 19: 211–354. White, J. (1984) Plant metamerism. In Perspectives on Plant Population Ecology (ed. R. Dirzo and J. Sarukhán). Sinauer Associates, Sunderland, Massachusetts, pp. 15–47.

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of the 4 Reevaluation Phylogeny of the Hypopterygiaceae (Bryophyta) Based on Morphological and Molecular Data Hans (J.D.) Kruijer and Rolf Blöcher CONTENTS Abstract ............................................................................................................................................65 4.1 Introduction.............................................................................................................................66 4.2 Historical Background............................................................................................................70 4.3 Reevaluation of the Phylogeny ..............................................................................................81 4.3.1 Taxon and DNA Sampling .........................................................................................81 4.3.2 Phylogenetic Analyses................................................................................................86 4.4 Results.....................................................................................................................................94 4.5 Discussion...............................................................................................................................99 4.5.1 Clade Composition and Character State Evolution ...................................................99 4.5.2 Evolution of Morphological Characters...................................................................103 4.5.3 Systematic Implications............................................................................................104 Acknowledgments ..........................................................................................................................106 References ......................................................................................................................................106

ABSTRACT The pleurocarpous moss family Hypopterygiaceae comprises 21 species distributed among 7 or 8 genera. This chapter gives an overview of systematic studies in the family and presents a phylogenetic study on the relationships within the family using a combination of morphological and molecular data (rps4 gene and trnL–trnF region of cpDNA, ITS2 of nr ribosomal DNA; 15 species of Hypopterygiaceae and 9 species of related families). The results lend support to the monophyly of the Hypopterygiaceae and indicate that Catharomnion and Canalohypopterygium, the Lopidium species, and Dendrocyathophorum and Cyathophorum africanum form well-supported monophyletic clades, that Cyathophorum and Dendrohypopterygium s. lat. are polyphyletic, and that Cyathophorum hookerianum is nested in a Hypopterygium grade. The high amount of homoplasy indicates that a new view on morphology is necessary for understanding evolutionary history. A different generic classification of the Hypopterygiaceae is nearing, but a final decision awaits more data.

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FIGURE 4.1 Colony of Dendrohypopterygium arbuscula (Brid.) Kruijer growing in a moist and shaded habitat on the forest floor of a native forest between Petrohué and Cayutué at Lago Todos los Santos, Llanquihue Province, Chile. (Photograph by permission of Hans Kruijer.)

4.1 INTRODUCTION The Hypopterygiaceae Mitt. are a family of usually attractive pleurocarpous mosses of humid, temperate to tropical forests of, in particular, the Southern Hemisphere (Figure 4.1). The family has a mainly Gondwanic distribution. The highest diversity is found in Indo-Malaysia and Australasia; occurrences in subtropical and temperate areas of the Northern Hemisphere are restricted to the Indian subcontinent, the Pacific Rim, Central America, and the Caribbean. The family is morphologically well defined and characterized by the following combination of character states: (1) a distally or entirely complanate foliate shoot axis, (2) a dorsi-ventrally oriented, three-ranked leaf arrangement in the parts of shoot axes with complanate foliation, where (3) the leaves are arranged in two rows of asymmetrical lateral leaves and one ventral row of smaller symmetrical amphigastria (“heterophylly”, Figure 4.2). The family Hypopterygiaceae was revised recently by Kruijer (2002) and comprises 21 species distributed among 7 or 8 genera: Canalohypopterygium W. Frey and Schaepe, Catharomnion Hook. f. and Wilson, Cyathophorum P. Beauv., Dendrocyathophorum Dixon, Hypopterygium Brid., Lopidium Hook. f. and Wilson, and Dendrohypopterygium Kruijer, of which Arbusculohypopterygium Stech, T. Pfeiffer, and W. Frey has been split off (Stech et al., 2002). The splitting of Dendrohypopterygium s. lat. is one of the subjects of this study and, for reasons of clarity, we follow Kruijer’s (2002) circumscription of Dendrohypopterygium unless otherwise indicated. Since the 1970s, and especially the last decade of the twentieth century, the Hypopterygiaceae have received special attention from bryologists (below), including the authors of this chapter. This interest may partly be explained by the beauty of the plants, but from a scientific point of view it is in particular the family’s predominantly Gondwanic distribution and its probably late Mesozoic Gondwanic origin (e.g., Kruijer, 2002) combined with the high amount of morphological diversity (Figures 4.3 to 4.6) that attracts the attention. Since Blöcher (the second author) started a molecular study on Hypopterygiaceae in 1999 as part of his master’s degree study in biology under the supervision of Ingrid Capesius (Ruprecht-Karls Universität Heidelberg), he has developed a great interest in the phylogeny of the family and he continued to do molecular work on this family during his PhD study in the Bryology Department of the Nees Institute for Biodiversity of Plants at the University of Bonn. Kruijer (the first author) has been hooked on Hypopterygiaceae since 1989,

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FIGURE 4.2 Leaf arrangement in Cyathophorum bulbosum (Hedw.) Müll. Hal. (ventral view). Epiphytic plant from densely shaded, living roots of a tree near a streamlet in remnant of native forest, White Pine Bush, Hawke’s Bay, North Island, New Zealand (Van Zanten 73.12.68, GRO). (Photograph courtesy and by permission of Ben van Zanten.)

FIGURE 4.3 Colony of Hypopterygium tamarisci (Sw.) Brid. ex Müll. Hal. growing on a piece of lava boulder on a balcony in Leiden, the Netherlands. (Photograph courtesy and by permission of Cris Hesse and Hans Kruijer.)

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FIGURE 4.4 Colony of Lopidium concinnum (W. Hook) Wilson growing in a shaded and moist habitat on a small tree in native forest at Punta Huano, Lago Todos los Santos, Llanquihue Province, Chile (Van Zanten & Kruijer 86.01.987, GRO). (Photograph courtesy and by permission of Ben van Zanten.)

FIGURE 4.5 Colony of Cyathophorum bulbosum (Hedw.) Müll. Hal. growing on densely shaded roots in a native forest near Lake Mahinapoua, Westland, South Island, New Zealand (Van Zanten 74.02.886, GRO). (Photograph courtesy and by permission of Ben van Zanten.)

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A B 1 mm 1 cm

E

C D 1 mm 1 mm 1 mm

FIGURE 4.6 Habit variation in Hypopterygiaceae, examples from dendroid to simple. (A) Dendrohypopterygium filiculiforme (Hedw.) Kruijer (Hamlin 2266, WELT); (B) Hypopterygium didictyon Mull. Hal. (Streimann 51282, L); (C) Lopidium concinnum (W. Hook) Wilson (dorsal view, Telford 4207, L); (D) Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer (dorsal view, Meijer B7598, L); and (E) Cyathophorum africanum Dixon (ventral view, Pócs & Harris 6158/B, L). (From Kruijer, J.D. (H.), Blumea Supplement, 13: 106, 147, 257, 286 and 332, 2002. With permission. Drawings by Joop Wessendorp.)

when, in what is now the Leiden University branch of the Nationaal Herbarium Nederland (NHN), he started his PhD study preparing a systematic revision of the Hypopterygiaceae based on morphological data and cladistic analyses — a few years before molecular techniques became widely used in systematic studies (cf. Hedenäs, Chapter 12 in this volume). In this chapter, we joined our skills in order to present a “total evidence” phylogeny of the Hypopterygiaceae, based on our DNA sequences and morphological data. We intend to demonstrate why the Hypopterygiaceae, despite the low number of species, are a moss family of special systematic interest and include an overview of the systematic studies on Hypopterygiaceae, performed by us and other bryologists, such as the researchers in Wolfgang Frey’s research group at the Freie Universität Berlin (e.g., Frey et al., 1999; Pfeiffer, 2000; Pfeiffer et al., 2000; Stech et al., 1999), and the significant progress that has been made in unravelling the systematics of the family.

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Other Genera

Cyathophorum

Cyathophorella

Dendrocyathophorum

Hypopterygium

Lopidium

Canalohypopterygium

Catharomnion

TABLE 4.1 Schematic Overview of Nineteenth and Early Twentieth Century Classifications of Hypopterygiaceae Mitt. sensu Kruijer (2002) by Various Authors

Bridel (1827)

Hypopterygiaceae

Hypopterygiaceae + R.

Müller (1851)

Hypopterygiaceae

Hypopterygiaceae + R. & H.

Wilson (1855)

Hypopterygiaceae

Mitten (1859)

Hypopterygiaceae

Hypopt. Hypopterygiaceae

Jaeger (1876)

Hypopterygiaceae

Kindberg (1898, 1899, 1900)

Hypopterygiaceae

Cyathophoraceae

Brotherus (1907)

Hypopterygiaceae

Hypopterygiaceae

Fleischer (1908)

Hypopterygiaceae

Hypopterygiaceae

Brotherus (1925)

Hypopterygiaceae

Hypopterygiaceae + R. & S.

Hypopterygiaceae

Note: R. = Racopilum P. Beauv.; H. = Helicophyllum Brid.; S. = Schimperobryum Margad. Cells with grey background refer to classification in, respectively, the Cyathophoraceae Kindb. or the subfamilial inclusion of this taxon within the Hypopterygiaceae.

4.2 HISTORICAL BACKGROUND The Hypopterygiaceae are nested in the core of the pleurocarpous mosses, i.e., the superorder Hypnanae W.R. Buck et al. (Buck and Goffinet, 2000; Buck et al., 2005), which accommodates the Hookeriales (M. Fleisch.) M. Fleisch. and the Hypnales (M. Fleisch.) W.R. Buck and Vitt (sensu Buck et al., 2000a). The Hypopterygiaceae are closely related to the Hookeriales, either as a sister to the Hookeriales s. str. or as a basal family within the Hookeriales (Buck et al., 2000a, 2000b, 2005; Cox et al., 2000; Hedenäs, 1994, 1995; De Luna et al., 1999, 2000; Goffinet and Buck, 2004; cf. Blöcher and Capesius, 2002). However, the relationships within the family are less clear. The morphological diversity in Hypopterygiaceae has led to various theories on the classification of the family and its representatives. Before the 1970s the Hypopterygiaceae were usually treated as a single family placed systematically in the Hookeriales (Table 4.1 and references therein). By the late nineteenth and early twentieth centuries, mainly as a result of Kindberg’s work (Kindberg, 1898, 1899, 1901), the idea evolved that cyathophoroid and hypopterygioid genera should be classified into separate groups that are distinct on the subfamilial level (Brotherus, 1907, 1925; Fleischer, 1908). This idea was based mainly on differences in the direction of the sporophyte and the seta length (Figure 4.7).

Hookeriaceae

Hypopterygiaceae

Cyathophorum

Cyathophorella H.

Daltoniaceae

Hookeriaceae

D.

Cyathophoraceae

Lopidium

Canalohypopterygium ← Hypopterygiaceae

Hypopterygiaceae

Hypopterygiaceae

Hypopterygiaceae

Cyathophorella

Dendrocyathophorum

Catharomnion

a

Robinson (1971) presents only the family names in his classification scheme.

Note: D. = Daltoniaceae; H. = Hookeriaceae. Cells with grey background refer to classification in other families. The arrow indicates Whittemore and Allen’s (1989) presumption of relationship (see text).

Whittemore & Allen (1989)

Buck (1987, 1988)

Buck & Vitt (1986)

Crosby (1974) (followed by Walther [1983])

Robinson (1971)a

Miller (1971)

D.

Catharomnion

Hypopterygiaceae

Canalohypopterygium

Noguchi (1951, 1952)

Lopidium Hypopterygiaceae

Dendrocyathophorum

Dixon (1929, 1936, 1937)

Hypopterygium

Bryales

Hypopterygium

Hookeriales

Cyathophorum

TABLE 4.2 Schematic Overview of Mid- and Late Twentieth Century Classifications Until the 1990s of Hypopterygiaceae Mitt. by Various Authors

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1 cm

A

1 cm

B

0

FIGURE 4.7 Examples of differences in sporophyte orientation and seta length. (A) Dendrohypopterygium arbuscula (Brid.) Kruijer (Van Zanten & Kruijer 86.02.1137, GRO) and (B) Cyathophorum bulbosum (Hedw.) Müll. Hal. (ventral view, Streimann 51671, L). (From Kruijer, J.D. (H.), Blumea Supplement, 13: 112 and 298, 2002. With permission. Drawings by Joop Wessendorp.)

Since the 1970s, the monophyly of the family and its systematic position within the pleurocarpous mosses have been the subject of debate (Table 4.2 and references therein). Crosby (1974) classified the genera with poorly developed peristomes (Catharomnion and Cyathophorella (Broth.) M. Fleisch.; Figure 4.8) in the Daltoniaceae Schimp., and the genera with a well-developed peristome (Cyathophorum, Dendrocyathophorum, Lopidium and Hypopterygium, including Canalohypopterygium and Dendrohypopterygium s. lat.; Figure 4.9) in the Hookeriaceae Schimp. Both families belong to the Hookeriales. Buck and Vitt’s (1986) and Buck’s (1987, 1988) familial classifications of the pleurocarpous mosses, on the other hand, were based on both sporophytic and gametophytic characters, which included organization of the leaf costa, stem anatomy, axillary hair morphology, presence or absence of scale leaves, and calyptral ornamentation and anatomy. Examples of the variability within the Hypopterygiaceae in some of these characters are presented in Figures 4.10 to 4.13. Buck transferred the Hypopterygiaceae s. str. to the Bryales and placed the remaining genera Cyathophorum, Cyathophorella and Dendrocyathophorum in the Hookeriaceae (Hookeriales), but it should be remarked that Buck’s classification of the hypopterygiaceous genera is mainly based on the study of Hypopterygium and Cyathophorum. Whittemore and Allen’s (1989) study on relationships within the Hookeriales was based on Buck’s (1987) classification, but they considered Dendrocyathophorum to be a representative of the Hypopterygiaceae s. str. Whittemore and Allen also classified Cyathophorum and Cyathophorella in the Hookeriales, but transferred them to the Daltoniaceae. They remarked, however,

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D

B

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C

E

FIGURE 4.8 Examples of Hypopterygiaceae with a poorly developed peristome. (A) Detail of the processes of the endostome of Catharomnion ciliatum (Hedw.) Wilson (Beever 70-26, CBG); (B) exostome of Cyathophorum parvifolium Bosch and Sande Lac. (Meijer B9095, L); (C) basal part of exostome tooth of Cyathophorum adiantum (Griff.) Mitt. (Decoly & Schaul, BL 2571, S); (D) exo- and endostome of Cyathophorum africanum Dixon (Pócs & Harris, 6158/B, EGR); (E) exo- and endostome of Cyathophorum adiantum (Griff.) Mitt. (Decoly & Schaul, BL 2571, S). (A) and (C): scale bar equals 10 μm; (B), (D) and (E): scale bar equals 50 μm. (Compiled from Kruijer, J.D. (H.), Blumea Supplement, 13: 48, 50 and 51, 2002. With permission. SEM photographs by Hans Kruijer and Ben Kieft.)

that the resemblance of several representatives of the Hypopterygiaceae s. str. (Dendrocyathophorum in particular) to Cyathophorum and Cyathophorella is striking and suggested that the traditional classification of the Hypopterygiaceae in the Hookeriales might be correct. Whittemore and Allen pointed, furthermore, to the striking resemblance between Dendrocyathophorum and Canalohypopterygium (as Hypopterygium commutatum Müll. Hal.) in stem anatomy. Both monotypic taxa have stem cavities, which are always central in Dendrocyathophorum (Noguchi, 1936; Kruijer, 2002; Figure 4.13), but cortical in stem and branches and only central in the rudimentary branches in Canalohypopterygium (Reimers, 1953; Frey et al., 1983; Frey and Schaepe, 1989; Kruijer, 2002; Figure 4.13). Central and cortical cavities occur in several other representatives of the Hypopterygiaceae (Kruijer, 1995b, 2002; Magill and Van Rooy, 1998; Noguchi, 1936; Whittemore and Allen, 1989; Figure 4.13) and often contain solid or liquid inclusions (Noguchi, 1936; Kruijer, 1995b; Figure 4.13). Central cavities are present in stems and branches of Lopidium struthiopteris (Brid.) M. Fleisch., the distal part of stem and branches of Dendrohypopterygium arbuscula (Brid.) Kruijer, D. filiculiforme (Hedw.) Kruijer and Hypopterygium sandwicense Broth., and occasionally in stems of Cyathophorum africanum Dixon. Cortical cavities are present in stems and branches of L. concinnum (W. Hook.) Wilson and Catharomnion ciliatum (Hedw.) Wilson. The cavity system is most complex in the New Zealand endemics and monotypic genera Canalohypopterygium and Catharomnion (Reimers, 1953; Frey et al., 1983; Frey and Schaepe, 1989; Kruijer, 1995b, 2002), which differ considerably in gametophytic and sporophytic characters, in particular in habit (Figure 4.14), leaf dentation and morphology of the peristome (Frey and Schaepe, 1989; Kruijer, 2002; compare Figures 4.8A and 4.9E). They share, however, a character unique for mosses, i.e., short, usually leafless rudimentary branches, which are mainly located in the frond (Figure 4.15) and were misinterpreted in the past by Kindberg (1901), Brotherus (1907, 1925), and Sainsbury (1955) as being bristle-like amphigastria or metamorphosed leaves. The rudimentary branches of

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FIGURE 4.9 Examples of Hypopterygiaceae with a well-developed peristome. (A) Peristome of Cyathophorum bulbosum (Hedw.) Müll. Hal. (Van Zanten 1285, L); (B) peristome of Lopidium concinnum (W. Hook.) Wilson (Beckett 854, L); (C) detail of exostome tooth of Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer (Meijer B7598, L); (D) peristome of Hypopterygium tamarisci (Sw.) Brid. ex Müll. Hal. (Herzog 2730, L); and (E) peristome of Canalohypopterygium tamariscinum (Hedw.) Kruijer (Visch s.n., ‘19.11.1972’, L). (A), (D) and (E): scale bar equals 100 μm; (B): scale bar equals 50 μm; (C): scale bar equals 10 μm. (Compiled from Kruijer, J.D. (H.), Blumea Supplement, 13: 48 and 50, 2002. With permission. SEM photographs by Hans Kruijer and Ben Kieft.)

Catharomnion and Canalohypopterygium are similar in morphology and anatomy, but are arranged in three rows in Catharomnion and in eight and three rows in Canalohypopterygium. Each rudimentary branch is associated with a single, superposed leaf and contains a central cavity, which continues in the cortex of the axis bearing the rudimentary branch (Reimers, 1953; Frey et al., 1983; Kruijer, 1995b, 2002; Figures 4.13 and 4.15). The cavities are usually filled with oil droplets, which are colourless to pale yellow in Catharomnion and pale yellow to brownish in Canalohypopterygium (Frey and Schaepe, 1989; Reimers, 1953; Kruijer, 1995b; Figure 4.15). Pelser et al. (2002) attempted to reveal the biological function of the rudimentary branches of Canalohypopterygium and the oil within. They calculated that Canalohypopterygium contains approximately 25 to 35 nl of oil per gametophore. The oil is more or less evenly distributed among the cavities of the rudimentary branches and those of the stipe and branches. It consists mainly of apolar hydrocarbons, some of them alkanes and fatty acids; evidence for the presence of compounds with an aromatic ring moiety was also found. However, Pelser et al. (2002) did not find evidence for a biological function of the rudimentary branches and the oil in the cavity system and pointed to the possibility that the rudimentary branches of Canalohypopterygium and Catharomnion are historical relics. Although field studies in New Zealand on possible biological functions of the cavity system and the oil within are very much needed before Pelser et al.’s (2002) hypothesis can be accepted or rejected, support for their hypothesis is found in the phylogeny reconstruction of the Hypopterygiaceae by Kruijer (2002), which shows reduction of ramification as a general pattern in the evolutionary history of the family. Many, if not all, of the morphological characters used in the systematic studies and classification proposals presented here show variability within the family, much of which has only been recognized since the mid-1990s. This variability is the underlying problem that hampered — and

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A B

1 mm

C D

E

F

FIGURE 4.10 Examples of morphological and anatomical variation in leaves of Hypopterygiaceae. (A) Stipe and rachis leaves of Dendrohypopterygium arbuscula (Brid.) Kruijer (Van Zanten & Kruijer 86.02.1137, GRO); (B) rachis and branch leaves of the “normal” variant and the dwarfish “Northern New Zealand” variant of Hypopterygium didictyon Mull. Hal. (Streimann 51282, L; the ventral and two lateral leaves in the central row and the second dorsal leaf and the second amphigastrium at the top in the right row at the corner are drawn from Fleischer B76, a representative of the “Northern New Zealand” variant); (C) rachis and branch leaves of Lopidium concinnum (W. Hook.) Wilson (Telford 4207, L); (D) stipe, rachis and branch leaves of Catharomnion ciliatum (Hedw.) Wilson (Beever 70-26, CBG); (E) leaves of Cyathophorum hookerianum (Griff.) Mitt. (left lateral leaf and central amphigastrium at top: Norkett 7398, BM; the lateral leaf left at bottom: s. coll., s.n., “Fruct. Neckera hookeriana Griff.”!, NY); the two amphigastria to the right: Burkill 37737, BM); (F) leaves of Cyathophorum bulbosum (Hedw.) Müll. Hal. (Streimann 51671, L). (Compiled from Kruijer, J. D. (H.), Blumea Supplement, 13: 114, 134, 148, 270, 306 and 351, 2002. With permission. Drawings by Hans Kruijer and Jan van Os.)

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F

A

B

C

G

D

E

J M

I

L

H

K

O

N

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FIGURE 4.11 Examples of axillary hairs of Hypopterygiaceae. (A) Dendrohypopterygium filiculiforme (Hedw.) Kruijer (Hamlin 2266, WELT); (B) D. arbuscula (Brid.) Kruijer (Van Zanten & Kruijer 86.02.1137, GRO); (C) Canalohypopterygium tamariscinum (Hedw.) Kruijer (Martin 274.9, CHR); (D) Catharomnion ciliatum (Hedw.) Wilson — axillary hairs are rare in this species (Van Zanten 7401243, L); (E) Hypopterygium didictyon Müll. Hal. — the terminal cell of the axillary hairs in this species are frequently covered with white, waxy substances (the three axillary hairs to the left, Streimann 51282, L, a representative of the “normal” variant of the species; the two to the right, Fleischer B76, L, a representative of the dwarfish “Northern New Zealand” variant); (F) H. flavolimbatum Mull. Hal. (Igbal 646, L); (G) H. sandwicense Broth. (Hoe 704.0, NICH); (H) Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer (the two axillary hairs to the left, Bor 95, BM; the ones to the right, Boeken 81.03.2587, GRO); (I) Lopidium concinnum (W. Hook.) Wilson (Telford 4207, L); (J) L. struthiopteris (Brid.) M. Fleisch. (Van der Wijk 453, L); (K) Cyathophorum africanum Dixon (Crosby & Pócs 8711, L); (L) Cyathophorum hookerianum (Griff.) Mitt. (left: Williams 1671, NY; central: Norkett 7398, BM; right: Elmer 8544, S); (M) Cyathophorum parvifolium Bosch and Sande Lac. (left, Touw 18479, L; the two axillary hairs to the right, Meijer B9095, L); (N) Cyathophorum tahitense Besch. (left, Vesco s.n., PC; the two axillary hairs to the right, Whittier 2501, BM); (O) Cyathophorum adiantum (Griff.) Mitt. (left and top right, Chen, MSE 92, S; central, Griffith 185/509?, BM; right, Touw 9198, L); (P) Cyathophorum bulbosum (Hedw.) Müll. Hal. (left, Streimann (field no 1), L; right, Van Balgooy 217, L); and (Q) Cyathophorum spinosum (Müll. Hal.) H. Akiyama (the two axillary hairs to the left, Brass 12934, FH; the one to the right, Brass 25066, FH). (Compiled from Kruijer, J. D. (H.), Blumea Supplement, 13: 116, 126, 134, 148, 176, 248, 272, 288, 308, 324, 334, and 352. With permission. Drawings by Hans Kruijer and Jan van Os.)

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FIGURE 4.12 Examples of morphological variation of calyptrae in Hypopterygiaceae. (A) Dendrohypopterygium filiculiforme (Hedw.) Kruijer (Ruinard 98.10.31.02, L); (B) Canalohypopterygium tamariscinum (Hedw.) Kruijer (Martin 274.9, CHR); (C) Catharomnion ciliatum (Hedw.) Wilson (Beever 70–26, CBG); (D) Hypopterygium didictyon Mull. Hal. – (Weymouth s.n., hb. Bartram sub no 6457, FH); (E) Lopidium struthiopteris (Brid.) M. Fleisch. (Streimann 2396, L); (F) Lopidium concinnum (W. Hook.) Wilson (Streimann 30553, L); (G) Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer (Boeken 81.03.2587, GRO); (H) Cyathophorum bulbosum (Hedw.) Mull. Hal. (left: Streimann 51671, L); (I) Cyathophorum africanum Dixon (Pócs & Harris 6158/B, L); (J) Cyathophorum hookerianum (Griff.) Mitt. (left: mitrate calyptra of Burkill 37737, BM; right: cucullate calyptra of Kanai et al. s.n., ‘Nov. 15, 1963’, NICH); and (K) Cyathophorum parvifolium Bosch and Sande Lac. (Meijer B9095, L). (Compiled from Kruijer, J. D. (H.), Blumea Supplement, 13: 108, 126, 134, 148, 270, 288, 306, 334 and 351, 2002. With permission. Drawings by Hans Kruijer and Jan van Os.)

still hampers — the delimitation of separate groups of species within the family and the determination of their mutual evolutionary relationships. That is actually what can be seen; there was no consensus among bryologists on the classification of the Hypopterygiaceae up to about 1990 (e.g., Table 4.2). Since 1989 Kruijer has tried to unravel the phylogeny of the Hypopterygiaceae using morphological characters of both generations in the life cycle, starting with a critical evaluation of the characters that could be used to clarify the question whether the Hypopterygiaceae are monophyletic or polyphyletic. After the evaluation of approximately 150 characters, more than 50 characters were selected that could be used in phylogenetic analyses, some of which were shown above (Figures 4.6 to 4.13 and 4.15). However, selecting the useful and informative characters, finding the best coding for the character states in the data matrices, and finding a well-balanced selection of outgroup species turned out to be problematic. In addition, the phylogenetic analyses were hampered by the high amount of homoplasy in the dataset. In 1995, Kruijer (1995a, 1995b) tentatively suggested that the Hypopterygiaceae are polyphyletic, because Cyathophorum seemed to be closely related to the Hookeriaceae (Figure 4.16). The analyses in 1995 resulted in 234 most parsimonious trees, which differed mainly in the topology of the paraphyletic genus Hypopterygium. Dendrocyathophorum, Lopidium and Cyathophorella were placed in a single monophyletic clade. The results of the analyses in 1995 were the best that could be obtained with the (morphological) data at that date, but the phylogeny of the Hypopterygiaceae was neither reliably nor completely satisfactorily resolved. The selection of Hypnodendron diversifolium Broth. and Geh. in the outgroup proved to be a disturbing source of homoplasy. In addition, the relationship between Hypopterygium filiculiforme (Hedw.) Brid. and the other Hypopterygiaceae (the base of the Hypopterygiaceae clade) needed further study. The outcome that Cyathophorella and Cyathophorum were shown as distantly related was also strange, considering their strong resemblance in morphology in both generations, with the exception of calyptra and peristome characters. These problems led to a critical evaluation of outgroup sampling, character selection and coding of the character states, whereby adjustments in the original dataset were tested each time against the objective criterion that each adjustment should result in more reliable phylogenetic signal; i.e., the phylogenetic analyses should result in more stable, shorter trees with higher support values. In 1996, Kruijer’s phylogenetic analyses based on 59 characters and 32 species of Hypopterygiaceae and representatives

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FIGURE 4.13 Examples of stem anatomical variation in Hypopterygiaceae. (A) Central strand in rachis and central cavity with and without droplet of oil in ultimate branches of Dendrohypopterygium filiculiforme (Hedw.) Kruijer (Hamlin 2266, WELT); (B) central strand in rachis and central cavity in process of formation with degenerating strand cells in branch of Hypopterygium sandwicense Broth. with droplets of oil (still) mainly kept in strand cells; (C) central strand and cortical cavities in rachis and branch and central cavity in rudimentary branches of Canalohypopterygium tamariscinum (Hedw.) Kruijer with droplets of oil trapped in cavities or still kept in the “epithelium cells” of the cavities (Visch s.n., ‘19.11.1072’, L); (D) central strand and cortical cavities in rachis and branch and central cavity in rudimentary branches of Catharomnion ciliatum (Hedw.) Wilson with droplets of oil trapped in cavity or still kept in the “epithelium cells” of the cavities (Beever 70–26, CBG); (E) cortical cavities in rachis of Lopidium concinnum (W. Hook.) Wilson (Telford 4207, L); (F) central cavity in rachis of Lopidium struthiopteris (Brid.) M. Fleisch. (Van der Wijk 453, L); (G) central cavity with trapped droplet of oil in rachis of Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer (Meijer B7598, L); (H) central cavity in process of formation and with droplets of oil probably just released from degenerating strand cells in stem of Cyathophorum africanum Dixon (Pócs & Harris 6158/B, L). (Compiled from Kruijer, J. D. (H.), Blumea Supplement, 13: 108, 126, 134, 248, 270, 288 and 334, 2002. With permission. Drawings by Hans Kruijer and Jan van Os.)

of potentially related families eventually resulted in better resolved trees with slightly better support values, in which the Hypopterygiaceae were monophyletic and Cyathophorella closely related to Cyathophorum (Kruijer, 1996). Although the results of the analyses were more reliable than the ones obtained in 1995, two problems remained. The analyses were still hampered by a high amount of homoplasy and the circumscription of a few species of the Hypopterygiaceae, in particular Hypopterygium flavolimbatum Müll. Hal. and H. tamarisci (Sw.) Brid. ex Müll. Hal., was not completely clear. After completion of his revision, Kruijer (2002) conducted a series of phylogenetic analyses based on 57 morphological characters and 34 species including representatives of the Hypopterygiaceae and potentially related families (Figure 4.17). However, the topology of the base of the Hypopterygiaceae clade to some extent remained unclear. The high number of equivocal character

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FIGURE 4.14 Habit of two New Zealand related endemics. (A) Canalohypopterygium tamariscinum (Hedw.) Kruijer (Visch s.n., ‘19.11.1972’, L); (B) and (C) Catharomnion ciliatum (Hedw.) Wilson. (B) Female plant (dorsal view); (C) male plant (ventral view) (both from Beever 70–26, CBG). (From Kruijer, J. D. (H.), Blumea Supplement, 13: 124, 132 and 133, 2002. With permission. Drawings by Joop Wessendorp.)

FIGURE 4.15 Oil trapped in the cavity system of (A) branch of Canalohypopterygium tamariscinum (Hedw.) Kruijer (Allison KW 2935, CHR; ventral view); and (B) branch of Catharomnion ciliatum (Hedw.) Wilson (Van Zanten 7401562, GRO; dorsal view). (Photographs courtesy of Cris Hesse.)

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Daltoniaceae Hookeriaceae Cyathophorum Racopilum Hypnodendron Hypopterygium filiculiforme Hypopterygium arbuscula Canalohypopterygium Catharomnion Hypopterygium didictyon Hypopterygium elatum Hypopterygium flavolimbatum tristichous Hypopterygium species Hypopterygium sandwicense Dendrocyathophorum Lopidium Cyathophorella

FIGURE 4.16 Phylogeny of the Hypopterygiaceae based on Kruijer’s (1995a, 1995b) analyses of morphological data. (From Kruijer, J.D. (H.), Buxbaumiella, 38: 32, 1995b. With permission.)

states at the base of the clade led to the conclusion that the underlying problem might be that the Hypopterygiaceae are more distantly related to the non-hypopterygiaceous species used in the analyses than expected. Blöcher and Capesius (2002) tried to unravel the phylogeny of the Hypopterygiaceae using rps4 cpDNA sequence data (26 species of Hypopterygiaceae and potentially related families; Figures 4.18 and 4.19). The topology of their trees is intriguingly different from Kruijer’s (2002) trees based on morphological data. Blöcher and Capesius’ (2002) trees show that the core of the Hypopterygiaceae is monophyletic, as in Kruijer’s trees, but provide evidence that Dendrohypopterygium s. lat. is actually polyphyletic (Figure 4.19) and show that the position of Cyathophorum bulbosum (Hedw.) Müll. Hal. and C. adiantum (Griff.) Mitt. is ambiguous (Figure 4.18). The latter two species are both grouped in a single clade, which is either placed in a basal position in the Hypopterygiaceae s. str. or in a basal position in the “pleurocarpous mosses.” Stech et al. (2002) performed phylogenetic analyses using trnLUAA intron cpDNA, and ITS2 nrDNA sequence data (Figures 4.20 and 4.21). Their trees differ in topology from the ones presented by Blöcher and Capesius (2002), but also provide evidence for the polyphyly of Dendrohypopterygium s. lat. (mainly based on trnL data) and also show an ambiguous position for the Cyathophorum bulbosum–C. adiantum clade. An intriguing difference is the position of the monotypic genus Dendrocyathophorum, which in Blöcher and Capesius’s (2002) trees is nested in a clade consisting of the Catharomnion–Canalohypopterygium clade in a terminal position, and Dendrohypopterygium arbuscula or D. filiculiforme in a basal position. In the Stech et al. (2002) trees, Dendrocyathophorum is either grouped in a clade with the Lopidium clade in a terminal position, or in a clade with the Lopidium clade in a terminal position and Dendrohypopterygium arbuscula (as Arbusculohypopterygium arbuscula [Brid.] Stech, T. Pfeiffer & W. Frey) in a basal position, or in a terminal or inconclusive position in a clade with D. arbuscula and Cyathophorum adiantum.

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The trees obtained by Buck et al. (2005; not shown), based on phylogenetic analyses using trnL–trnF, rps4 cpDNA, nad5 mtDNA and 26S nrDNA sequence data, presents the Hypopterygiaceae, including Cyathophorum, as a monophyletic taxon and sister to the remainder of the Hookeriales. Within the Hypopterygiaceae, the Cyathophorum bulbosum–C. adiantum clade is placed in a basal position as sister to the core of the Hypopterygiaceae. In this core, the Lopidium clade is placed in a basal position to the remaining species, where this clade has a terminal position in the trees obtained by Blöcher and Capesius (2002) and most of those obtained by Stech et al. (2002). In the Buck et al. (2005) trees, as in those of Blöcher and Capesius (2002), Dendrocyathophorum is nested in a clade with Dendrohypopterygium arbuscula in a basal position and the Catharomnion–Canalohypopterygium clade in a terminal position. Most interesting in the Buck et al. (2005) trees is the clade sister to these four taxa, which comprises Hypopterygium tamarisci and Cyathophorum hookerianum (Griff.) Mitt. The remarkable position of Cyathophorum hookerianum in the core of the Hypopterygiaceae, well separated from the Cyathophorum bulbosum–C. adiantum clade, is most intriguing. We obtained a similar position for Cyathophorum hookerianum in the results of the phylogenetic analyses preliminary to our present study that are based on molecular sequence data and those of the preliminary phylogenetic analyses that are based on a combination of morphological and molecular data, albeit with low support in the latter. Despite the obvious differences in tree topology, the recent morphological and molecular studies provide supporting evidence for the monophyly of the Hypopterygiaceae. Within the family two clades are well supported, one formed by the monotypic genera Catharomnion and Canalohypopterygium, the other by the two Lopidium species. The phylogenies in the morphological study present Hypopterygium and Dendrohypopterygium s. lat. as paraphyletic grades with low levels of support. The molecular studies, however, indicate that Hypopterygium is presumably monophyletic and Dendrohypopterygium s. lat. in all probability polyphyletic. Stech et al. (2002) proposed the genus Arbusculohypopterygium to accommodate the South American species of Dendrohypopterygium s. lat. The studies based on molecular data indicate that Cyathophorum in Kruijer’s (2002) circumscription is polyphyletic. The incongruences between these recent morphological and molecular studies led to our initiative to reevaluate the phylogeny of the Hypopterygiaceae by conducting a series of phylogenetic analyses with a combination of morphological and molecular data.

4.3 REEVALUATION OF THE PHYLOGENY In our present study, we try to get new insights into the evolutionary history of the Hypopterygiaceae through a “total evidence” approach using a combination of morphological and molecular sequence data (rps4, trnL–trnF region of cpDNA, and ITS2 of nr ribosomal DNA). Our study focuses on the ancestral origin of the family, the relationship between Dendrocyathophorum and the other genera, in particular Cyathophorum, Catharomnion and Canalohypopterygium, and the relationships within Cyathophorum. Of particular interest are the position of Cyathophorum hookerianum and the relationship of Dendrocyathophorum decolyi (Broth. ex M. Fleisch.) Kruijer with the African species Cyathophorum africanum — the only Cyathophorum species that occasionally has a central stem cavity, which contains conspicuous inclusions and shows a remarkable resemblance to that of Dendrocyathophorum (Figure 4.13). In contrast to the earlier phylogenetic analyses of morphological data, we included a representative of the Ptychomniaceae M. Fleisch., Ptychomnion cygnisetum (Müll. Hal.) Kindb., since it has recently become clear that the Ptychomniales W.R. Buck, C. Cox, A. J. Shaw and B. Goffinet represents the sister of the Hypnales and the Hookeriales (e.g., Buck et al., 2005; Shaw et al., 2003).

4.3.1 TAXON

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FIGURE 4.17 Four phylogenies of the Hypopterygiaceae based on Kruijer’s (2002) analyses of morphological data. Figures 4.17A–C represent (combined majority rule with superimposed strict) consensus trees; Figure 4.17D represents the single MPT of an analysis solely with Hypopterygiaceae. Numbers under branches refer to bootstrap values and, between parentheses, decay values. Kruijer’s (2002) generic classification of the Hypopterygiaceae is based on these trees. Symbols * and ° refer to the classification previously of the marked species in, respectively, Hypopterygium Brid. and Cyathophorella (Broth.) M. Fleisch. Cyathophorella spinosa (Müll. Hal.) M. Fleisch. was the first Cyathophorella species that was transferred to Cyathophorum P. Beauv. (Akiyama, 1988, 1992). (From Kruijer, J. D. (H.), Blumea Supplement, 13: 68, 2002. With permission.) Continued.

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FIGURE 4.18 Strict consensus tree of 15 MPTs obtained by Blöcher and Capesius (2002) based on rps4 gene sequences of 26 representatives of the Hypopterygiaceae, Hookeriales, Hypnales, Bryales, Splachnales, Funariales and Timmiales. Numbers above branches refer to bootstrap values; numbers under branches refer to decay values. Capitals refer to clades discussed in the original paper. (From Blöcher, R. and Capesius, I., Cryptogamie, Bryologie, 23(3): 199, 2002. With permission.)

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FIGURE 4.19 Single MPT obtained by Blöcher and Capesius (2002) based on rps4 gene sequences of nine representatives of the Hypopterygiaceae and the outgroup species Hookeria lucens (Hedw.) Sm., Schimperobryum splendidissimum (Mont.) Margad., Hypnum cupressiforme Hedw., and Neckera crispa Hedw. Numbers above branches refer to bootstrap values; numbers under branches refer to the numbers of characters supporting each branch (left) or decay values (right). Capitals refer to clades discussed in the original paper. (From Blöcher, R. and Capesius, I. Cryptogamie, Bryologie, 23(3): 202, 2002. With permission.)

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Cyathophorum bulbosum Cyathophorum adiantum Hookeria lucens Distichophyllum crispulum

FIGURE 4.20 Single MPT obtained by Stech et al. (2002) based on trnL intron sequences of 22 specimens from 13 species of the Hypopterygiaceae and two specimens of the outgroup species Distichophyllum crispulum (Hook. f. and Wilson) Mitt. and Hookeria lucens (Hedw.) Sm. Numbers above branches refer to bootstrap values. Stech et al. (2002) placed Dendrohypopterygium arbuscula (Brid.) Kruijer in the monotypic genus Arbusculohypopterygium Stech, T. Pfeiffer, and W. Frey. (From Stech et al., New Zealand Journal of Botany, 40: 216, 2002. With permission.)

selection was based on earlier sampling for a morphological data set by the first author (Kruijer, 2002) and limited by the availability of sequences from the cpDNA and nrDNA regions for these taxa. Sequence data available from GenBank of the trnL–trnF region, the rps4 gene and ITS2 were used. The rps4 and trnL–trnF region were newly sequenced for Ptychomnion cygnisetum and Cyathophorum africanum. Sequences of the trnL–trnF and ITS2 region of Schimperobryum splendidissimum (Mont.) Margad. were kindly provided by Dietmar Quandt (Technical University of Dresden). DNA isolation, polymerase chain reactions (PCR) and sequencing reactions were carried out as described in Blöcher and Capesius (2002) for the rps4 gene and Quandt et al. (2000) for the trnL–trnF region. Table 4.3 presents a list of the sampled species and the GenBank accession numbers of the sequences used in the analyses. Vouchers of the newly sequenced species are preserved in L. Table 4.4 presents the definition of morphological characters and coding of character states used by Kruijer (2002). Table 4.5 presents the morphological dataset for the species sampled for the present study. The data was extracted from Kruijer’s (2002) original dataset; for Ptychomnion cygnisetum, new morphological data was obtained by the examination of herbarium specimens following Kruijer’s (2002) character state coding.

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80

Hypopterygium tamarisci South Africa Hypopterygium tamarisci Bolivia

98

Hypopterygium tamarisci Malaysia

76

Hypopterygium discolor

94

Hypopterygium flavolimbatum Hypopterygium didictyon New Zealand 66

81

74

Dendrocyathophorum decolyi Arbusculohypopterygium arbuscula Cyathophorum adiantum

100

Lopidium concinnum New Zealand Lopidium concinnum Chile Hookeria lucens Distichophyllum crispulum

FIGURE 4.21 One out of three MPTs obtained by Stech et al. based on combined trnL intron/ITS2 sequences of 11 specimens from 8 species of the Hypopterygiaceae and 2 specimens of the outgroup species Distichophyllum crispulum (Hook. f. and Wilson) Mitt. and Hookeria lucens (Hedw.) Sm. Numbers above branches refer to bootstrap values. (From Stech et al., New Zealand Journal of Botany, 40: 218, 2002. With permission.)

4.3.2 PHYLOGENETIC ANALYSES Ptychomnion cygnisetum was selected as the outgroup. All analyses were carried out using the complete dataset, which consists of morphological data and sequence data of the trnL intron and trnL 3-exon, trnL–trnF spacer, ITS2 region, rps4–trnS spacer and rps4 gene. This combined dataset amounts to a total of 1847 characters (Table 4.6). Sequences were aligned manually with the manual sequence alignment editor Align (Hepperle, 2002). Heuristic searches under the parsimony criterion were carried out under the following options: all characters unweighted and unordered, gaps coded as missing data, performing a tree bisection reconnection (TBR) branch swapping, collapse zero branch length branches, MulTrees option in effect, random addition sequence with 1000 replicates. Furthermore, the datasets were analysed using winPAUP 4.0b10 (Swofford, 2002) executing the command files generated by PRAP (Parsimony Ratchet Analyses using PAUP; Müller, 2004), employing the implemented parsimony ratchet algorithm (Nixon, 1999). For the parsimony ratchet the following settings were employed: 10 random addition cycles of 200 iterations each with a 40% upweighting of the characters in the PRAP iterations. Decay values (Bremer, 1988; Donoghue et al., 1992) were also calculated with PRAP with the same settings as for the parsimony ratchet analyses without additional random addition cycles. Heuristic bootstrap searches (Felsenstein, 1985) under parsimony criterion were performed with 1000 replicates, 10 random addition cycles per bootstrap replicate and the same options in effect as the heuristic search for the most parsimonious tree (MPT). The consistency index (CI, Kluge and Farris, 1969), retention index (RI), and rescaled consistency index (RC, Farris, 1989) were calculated to assess homoplasy. In addition to our MP analyses we performed Bayesian inferences with MrBayes 3.0 (Huelsenbeck and Ronquist, 2001). Modeltest 3.5 (Posada, 2004) was used to select DNA substitution models for the molecular dataset (gamma shape distribution, six substitution types). Six data

AY306853 AY306856 AJ 269694 AJ269695 AJ315872 AJ862340 AJ269693 AY306890 AJ271645 AJ252293 AJ252290 AY306902 AJ269689

Achrophyllum dentatum Adelothecium bogotense Canalohypopterygium tamariscinum

Catharomnion ciliatum

Cyathophorum adiantum

Cyathophorum africanum Cyathophorum bulbosum

Cyathophorum hookerianum Dendrocyathophorum decolyi

Dendrohypopterygium arbuscula

Dendrohypopterygium filiculiforme

Distichophyllum pulchellum Hookeria lucens

rps4

AF152380

AF134638 AY306736

AF134637

AF363280

AF134634 AY306724

AF363281 AJ876600

AF134633

AF134632

AY306687 AY306690

trnL

AJ252137

AY091478

AY091480

AY091481

ITS2

Germany

Chile NZ

Kenia NZ NZ Thailand Japan

Japan

New Zealand

New Zealand

Australia

Origin

Blöcher 980328/1 Stech B880404.8

Frey & Frey 95-17 Frahm 31-17 Frey 94-76

Solga s.n., (‘22.09.2003’) Frahm 1-1a Frey 1-4901 Akiyama Th-39 Matsui s.n.

Frahm 9-1 Frey 94-79 Frey & Pfeiffer 98-Z 132 B van Zanten 7401243 Yamaguchi s.n.

Voucher

Shaw et al. 2003 Shaw et al. 2003 Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS2) Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS2) Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS2) This chapter Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL) Shaw et al. 2003 Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS2) Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS2) Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL) Shaw et al. 2003 Blöcher & Capesius 2002 (rps4) Stech et al. 1999 (trnL) Continued.

Reference

TABLE 4.3 GenBank Accession Numbers for the Regions Sequenced and, Respectively, Voucher Information and Literature References for Samples Included in the Molecular Analyses

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AJ252292

AJ252291 AJ269688 AJ252289

AJ252288 AJ269692 AJ862331 AJ315873

Hypopterygium didictyon

Hypopterygium discolor Hypopterygium flavolimbatum Hypopterygium tamarisci

Leucodon sciuroides

Lopidium concinnum

Lopidium struthiopteris

Neckera crispa

Ptychomnion cygnisetum Schimperobryum splendidissimum AJ507770

AY050280 AJ862681

AF363283

AF033233

AF397786

AF265217

AF363282 AY098638

AF170592

AF472483

trnL

AJ862692

AY050296

AY029369

AF403634

AY091475

AY091473 AY091476 AY091477

ITS2

Chile Chile

Ireland

Germany Russia NZ

Australia China South Africa

New Zealand

Germany

Origin

Blöcher 130 & 131 Blöcher 01-09-1

Blöcher 990705/2

O’Shea 99C14b

Blöcher 961115/7 Huttunen & Wahlberg 819 Frahm 1-1b Frey 92-72

Streimann 52819 Tan 99-143 O’Shea 99E28a

Frahm 9-7 (‘NZ-9’)

Capesius 95-12

Voucher

Blöcher & Capesius 2002 (rps4) Pedersen & Hedenäs 2002 Blöcher & Capesius 2002 (rps4) Pfeiffer 2000 (trnL) Stech et al. 2002 (ITS2) Stech et al. 2002 (trnL + ITS) Stech et al. 2002 (trnL + ITS) Blöcher & Capesius 2002 (rps4) Stech et al. 2002 (trnL + ITS) Blöcher & Capesius 2002 (rps4) Huttunen & Ignatov 2004 Blöcher & Capesius 2002 (rps4) Frey et al. 1999 Stech & Frahm 2001 (ITS) Blöcher& Capesius 2002 (rps4) Stech et al. 2002 (trnL) Blöcher & Capesius 2002 (rps4) Stech et al. 2003 (trnL + ITS2) This chapter Blöcher & Capesius 2002 (rps4) D. Quandt (unpublished)

Reference

88

Note: Cyathophorum africanum Dixon and Ptychomnion cygnisetum (Müll. Hal.) Kindb. were newly sequenced for the analyses presented here; the remaining sequences were obtained from Dietmar Quandt, earlier studies by the second author, and GenBank.

AJ269690

Hypnum cupressiforme

rps4

TABLE 4.3 (Continued) GenBank Accession Numbers for the Regions Sequenced and, Respectively, Voucher Information and Literature References for Samples Included in the Molecular Analyses

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TABLE 4.4 Definition of Morphological Characters and Coding of Character States, after Kruijer (2002) Characters of the Gametophore 1. Ramification: sympodial: state 1; monopodial: state 2. 2. Habit: strictly palmate or umbellate: state 1; pinnate, bipinnate, or flabellate to palmate or umbellate: state 2; pinnate to bipinnate or flabellate (occasionally somewhat dendroid): state 3; usually simple, less often set with a few innovations or weakly branched (branches may function as new shoots): state 4. 3. Phyllotaxis of the basal part of the stem (stipe): 3/8: state 1; 5/13: state 2; 2/5: state 3; 1/3 or nearly so (i.e., 4/11, or 8/21): state 4. 4. Phyllotaxis of the distal parts of the stem (distal parts of the rachis and branches): 3/8: state 1; 5/13: state 2; 2/5: state 3; 1/3 or nearly so (i.e., 4/11, or 8/21): state 4. 5. Foliation of the basal part of the stem (stipe): not or weakly complanate: state 1; distinctly complanate: state 2. 6. Foliation of the distal parts of the stem (distal parts of the rachis and branches): not or weakly complanate: state 1; distinctly complanate: state 2. 7. Foliation of the basal part of the stem (stipe): homophyllous: state 1; heterophyllous: state 2. 8. Foliation of the distal parts of the stem (distal parts of the rachis and branches): homophyllous: state 1; heterophyllous: state 2. 9. Orientation of the foliation: not orientated in any direction or dorsi-ventral: state 1; dorsal: state 2; ventral: state 3. 10. Compression of the non-gemmiferous parts of the stem (stipe and rachis): entirely dorsi-ventral or partly uncompressed: state 1; mainly dorsi-ventral, but partly lateral (near the stipe base) in a few specimens of the species at least: state 2; lateral: state 3. 11. Central strand cells (in cross sections without central cavities): present: state 1; occasionally present: state 2; absent: state 3. 12. Axial cavities in the basal and middle parts of the stem (the stipe and the basal and middle parts of the rachis): absent: state 1; central: state 2; cortical: state 3. Species for which the character state of this character is coded as state 2 or 3 do not necessarily possess cavities in every cross section. 13. Axial cavities in ultimate branches: absent: state 1; present: state 2. This character state is coded as unknown for species lacking ultimate branches, viz. for species lacking any ramification, for species usually lacking ramification in which the rare branches are similar to the main axis or show indeterminate growth, and for species with indeterminate growth of branches. 14. Rudimentary branches: absent: state 1; present, not gemmiferous but naked or only set with a few scaly leaves: state 2; present, gemmiferous: state 3. 15. Scaly leaves at primordia: occasionally present at least: state 1; absent: state 2. 16. Intermediate cells of axillary hairs (at stipe, rachis, or branches): present: state 1; occasionally present: state 2; absent: state 3. 17. Outline of terminal cell of axillary hairs (at stipe, rachis, or branches): short-linear to linear and rectangular: state 1; short-elliptic to elongate-rectangular: state 2; short and elliptic, subcircular, or circular: state 3. 18. Margin of lateral leaves in the distal part of the frond: entire or truly ser