Evolution of Society (Philosophical Transactions of the Royal Society series B)

RSTB_364_1533_Cover.qxd 09/26/09 12:15 PM Page 1 volume 364 . number 1533 . pages 3125–3309 The evolution of socie...

Author: T. Clutton-Brock | S. West | F. Ratnieks | R. Foley

14 downloads 1046 Views 5MB Size Report

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

Report copyright / DMCA form

DOWNLOAD PDF

RSTB_364_1533_Cover.qxd

09/26/09

12:15 PM

Page 1

volume 364

. number 1533 . pages 3125–3309

The evolution of society Papers of a Discussion Meeting issue organized and edited by T. Clutton-Brock, S. West, F. Ratnieks and R. Foley Introduction The evolution of society T. Clutton-Brock, S. West, F. Ratnieks & R. Foley

3127

Articles 3135

Beyond society: the evolution of organismality D. C. Queller & J. E. Strassmann

3143

Social evolution in micro-organisms and a Trojan horse approach to medical intervention strategies S. P. Brown, S. A. West, S. P. Diggle & A. S. Griffin

3157

The evolution of extreme altruism and inequality in insect societies F. L. W. Ratnieks & H. Helanterä

3169

Social stability and helping in small animal societies J. Field & M. A. Cant

3181

Lifetime monogamy and the evolution of eusociality J. J. Boomsma

3191

Adaptation and the genetics of social behaviour L. Keller

3209

The evolution of cooperative breeding in birds: kinship, dispersal and life history B. J. Hatchwell

3217

Structure and function in mammalian societies T. Clutton-Brock

3229

Nepotistic cooperation in non-human primate groups J. B. Silk

3243

Evolving the ingredients for reciprocity and spite M. Hauser, K. McAuliffe & P. R. Blake

3255

The ecology of social transitions in human evolution R. Foley & C. Gamble

3267

Culture and the evolution of human cooperation R. Boyd & P. J. Richerson

3281

The evolutionary and ecological roots of human social organization H. S. Kaplan, P. L. Hooper & M. Gurven

3289

Trust and cooperation among economic agents P. Dasgupta

3301

Founded in 1660, the Royal Society is the independent scientific academy of the UK, dedicated to promoting excellence in science Registered Charity No 207043

volume 364

number 1533

pages 3125–3309

In this issue

The evolution of society Papers of a Discussion Meeting issue organized and edited by T. Clutton-Brock, S. West, F. Ratnieks and R. Foley

The evolution of society

Formalizing Darwinism and inclusive fitness theory A. Grafen

Phil. Trans. R. Soc. B | vol. 364 no. 1533 pp. 3125–3309 | 12 Nov 2009

12 November 2009

ISSN 0962-8436

The world’s longest running science journal

rstb.royalsocietypublishing.org Published in Great Britain by the Royal Society, 6–9 Carlton House Terrace, London SW1Y 5AG

12 November 2009

RSTB_364_1533_Cover.qxd

09/26/09

12:15 PM

Page 2

GUIDANCE FOR AUTHORS

Editor Professor Georgina Mace Publishing Editor Claire Rawlinson Editorial Board Neuroscience and Cognition Dr Brian Billups Dr Andrew Glennerster Professor Bill Harris Professor Trevor Lamb Professor Obaid Siddiqi Professor Andrew Whiten Cell and developmental biology Professor Julie Ahringer Dr Buzz Baum Dr Louise Cramer Dr Anne Donaldson Professor Richard Gardner Professor John Gray Professor Keith Gull Professor Laurence Hurst Professor Fotis Kafatos Professor Elliot Meyerowitz Dr Tanja van Mourik Publishing Editor: Claire Rawlinson (tel: +44 (0)20 7451 2602; fax: +44 (0)20 7976 1837; [email protected])

Production Editor: Jessica Mnatzaganian

6–9 Carlton House Terrace, London SW1Y 5AG, UK rstb.royalsocietypublishing.org

Professor Anthony Pawson Dr Stephen Tucker Organismal, environmental and evolutionary biology Dr Will Cresswell Professor Georgina Mace Professor Yadvinder Malhi Professor Manfred Milinski Professor Peter Mumby Professor Peter Raven Professor Karl Sigmund Professor Monkombu Swaminathan Health and Disease Professor Zhu Chen Professor Mark Enright Professor Peter Goodfellow Professor Michael Malim Professor Lap-Chee Tsui Professor Nicholas Wald Professor Joanne Webster

Selection criteria The criteria for selection are scientific excellence, originality and interest across disciplines within biology. The Editors are responsible for all editorial decisions and they make these decisions based on the reports received from the referees and/or Editorial Board members. Many more good proposals and articles are submitted to us than we have space to print, we give preference to those that are of broad interest and of high scientific quality. Publishing format Phil. Trans. R. Soc. B articles are published regularly online and in print issues twice a month. Along with all Royal Society journals, we are committed to archiving and providing perpetual access. The journal also offers the facility for including Electronic Supplementary Material (ESM) to papers. Contents of the ESM might include details of methods, derivations of equations, large tables of data, DNA sequences and computer programs. However, the printed version must include enough detail

Conditions of publication Articles must not have been published previously, nor be under consideration for publication elsewhere. The main findings of the article should not have been reported in the mass media. Like many journals, Phil. Trans. R. Soc. B employs a strict embargo policy where the reporting of a scientific article by the media is embargoed until a specific time. The Executive Editor has final authority in all matters relating to publication.

Electronic Submission details For full submission guidelines and access to all journal content please visit the Phil. Trans. R. Soc. B website at rstb.royalsocietypublishing.org.

AIMS AND SCOPE Each issue of Phil. Trans. R. Soc. B is devoted to a specific area of the biological sciences. This area will define a research frontier that is advancing rapidly, often bridging traditional disciplines. Phil. Trans. R. Soc. B is essential reading for scientists working across the biological sciences. In particular, the journal is focused on the following four cluster areas: neuroscience and cognition; organismal and evolutionary biology; cell and developmental biology; and health and disease. As well as theme issues, the journal publishes papers from the Royal Society’s biological discussion meetings. For information on submitting a proposal for a theme issue, consult the journal‘s website at rstb.royalsocietypublishing.org. Reviews. The journal also publishes reviews in the broad areas of research listed above. Review articles will often be commissioned, but the Editor is happy to consider suggestions / proposals for unsolicited review articles. Please submit an abstract and a covering letter to the Editorial Office for approval for consideration. 6000 words is usually a maximum length for reviews.

The Royal Society is an independent scientific academy founded in 1660 and self-governing under Royal Charter. The Society has three roles, as the scientific academy of the United Kingdom, as a learned society, as a funding body. The objectives of the Royal Society are to

• recognise excellence in science • support leading-edge scientific research and its applications

ISBN: 978-0-85403-780-3

Copyright © 2009 The Royal Society

• stimulate international interaction

Except as otherwise permitted under the Copyright, Designs and Patents Act, 1988, this publication may only be reproduced, stored or transmitted, in any form or by any other means, with the prior permission in writing of the publisher, or in the case of reprographic reproduction, in accordance with the terms of a licence issued by the Copyright Licensing Agency. In particular, the Society permits the making of a single photocopy of an article from this issue (under Sections 29 and 38 of this Act) for an individual for the purposes of research or private study.

• further the role of science, engineering

SUBSCRIPTIONS In 2010 Phil. Trans. R. Soc. B (ISSN 0962-8436) will be published twice a month. Full details of subscriptions and single issue sales may be obtained either by contacting our journal fulfilment agent, Portland Customer Services, Commerce Way, Colchester CO2 8HP; tel: +44 (0)1206 796351; fax: +44 (0)1206 799331; email: [email protected] or by visiting our website at http://royalsocietypublishing.org/info/subscriptions. The Royal Society is a Registered Charity No. 207043.

to satisfy most non-specialist readers. Supplementary data up to 10Mb is placed on the Society's website free of charge. Larger datasets must be deposited in recognised public domain databases by the author.

• promote the public’s understanding of science • provide independent authoritative advice on • encourage research into the history of science

printed version plus electronic access

Europe

USA & Canada

All other countries

£2145/€2788

$4058

£2317/US$4153

Typeset in India by Techset Composition Limited, Salisbury, UK. Printed by Latimer Trend, Plymouth. This paper meets the requirements of ISO 9706:1994(E) and ANSI/NISO Z39.48-1992 (Permanence of Paper) effective with volume 335, issue 1273, 1992. Philosophical Transactions of the Royal Society B (ISSN: 0962-8436) is published twice a month for $4058 per year by the Royal Society, and is distributed in the USA by Pitney Bowes International Mailing Services Inc. as mailing agent. Periodicals postage paid at Kearny, NJ. and additional mailing offices. POSTMASTER: Send address changes to PB International Mailing Services Inc. 500 US Hwy 46, Clifton, NJ, 07011.

Research Support (UK grants and fellowships) Research appointments: 2547 Research grants: 2539 Conference grants: 2540 Science Advice General enquiries: 2585 Science Communication General enquiries: 2572

and technology in society

matters relating to science, engineering and technology

Subscription prices 2010 calendar year

For further information on the Society’s activities, please contact the following departments on the extensions listed by dialling +44 (0)20 7839 5561, or visit the Society’s Web site (www.royalsociety.org).

International Exchanges (for grants enabling research visits between the UK and most other countries (except the USA)) General enquiries: 2550 Library and Information Services Library/archive enquiries: 2606

Cover image: Cooperation in micro-organisms. Clockwise from top left: A cooperating swarm of Pseudomonas aeruginosa cells (left) envelops a group of non-cooperating cheats. (Image courtesy of Edgar Lissel and Stephen Diggle.) Guards at the nest entrance of the neotropical bee Tetragonisca angustula, known in Brazil as Jatai. Jatai is unique in having both standing (shown) and hovering guards. Hovering guards detect intruders of different species, by their different colour or volatile odour. Standing guards detect intruders from other Jatai colonies. (Photo courtesy of F. Ratnieks.) Pied babblers (Turdoides bicolor) live in stable groups of 5–10 consisting of a single breeding pair and natal helpers of both sexes that assist in rearing their young. (Image courtesy of T. H. Clutton-Brock.) Cooperative breeding also occurs in a number of mammals. Meerkats (Suricata suricatta) live in groups of 5–50, consisting of a single dominant individual of each sex and a variable number of helpers of both sexes that contribute to rearing their offspring. Dominants are the parents of most juveniles born in the group and subordinate females rarely breed successfully. Field studies show that breeding success rises with helper number. (Image courtesy of T. H. Clutton-Brock.) Allo-grooming in Barbary macaques (Macaca sylvanus) plays an important role in maintaining relationships between non-kin as well as between kin. (Image courtesy of Robert Foley.) Human societies differ from those of most other animals in regularly involving cooperative behaviour between unrelated individuals maintained by cultural norms. (Image courtesy of Mehdi Moussaïd and Simon Gariner from Proceedings of the Royal Society B 2009;276: 2755–2762, doi:10.1098/rspb.2009.0405.)

The evolution of society Papers of a Discussion Meeting issue organized and edited by T. Clutton-Brock, S. West, F. Ratnieks and R. Foley

Contents

Introduction The evolution of society T. Clutton-Brock, S. West, F. Ratnieks and R. Foley

3127

Articles Formalizing Darwinism and inclusive fitness theory A. Grafen

3135

Beyond society: the evolution of organismality D. C. Queller and J. E. Strassmann

3143

Social evolution in micro-organisms and a Trojan horse approach to medical intervention strategies S. P. Brown, S. A. West, S. P. Diggle and A. S. Griffin

3157

The evolution of extreme altruism and inequality in insect societies F. L. W. Ratnieks and H. Helantera¨

3169

Social stability and helping in small animal societies J. Field and M. A. Cant

3181

Lifetime monogamy and the evolution of eusociality J. J. Boomsma

3191

Adaptation and the genetics of social behaviour L. Keller

3209

The evolution of cooperative breeding in birds: kinship, dispersal and life history B. J. Hatchwell

3217

Structure and function in mammalian societies T. Clutton-Brock

3229

Nepotistic cooperation in non-human primate groups J. B. Silk

3243

Evolving the ingredients for reciprocity and spite M. Hauser, K. McAuliffe and P. R. Blake

3255

The ecology of social transitions in human evolution R. Foley and C. Gamble

3267

Culture and the evolution of human cooperation R. Boyd and P. J. Richerson

3281

3125

3126

Contents

The evolutionary and ecological roots of human social organization H. S. Kaplan, P. L. Hooper and M. Gurven

3289

Trust and cooperation among economic agents P. Dasgupta

3301

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3127–3133 doi:10.1098/rstb.2009.0207

Introduction

The evolution of society

Although the social mechanisms responsible for the development and maintenance of societies in animals and man have fascinated and intrigued philosophers and scientists since classical times, the first systematic consideration of their evolution appears in the Origin of species (Darwin 1859/1958). Much of Darwin’s thinking about the evolution of societies in animals and humans has a distinctly modern feel about it and he commonly anticipates theoretical developments that only occurred 100 years later. Although he did not confront the problem of altruistic behaviour directly, he was aware of the challenge to his theory posed by the evolution of sterile castes in some social insects (Darwin 1859/1958). In Chapter VIII of the ‘Origin of species’, he describes how he thought, at first, that this was fatal to his whole theory of natural selection. Then, in a paragraph that presages Hamilton’s subsequent extension of evolutionary theory, he describes how he realised that ‘the problem is lessened, or, as I believe, disappears, when it is remembered that selection may be applied to the family, as well as to the individual, and may thus gain the desired end.’ (Darwin 1859, p. 230). In The descent of man (1871), Darwin turned to the evolution of human societies. In Chapter VI, he stresses the contrast between humans and other animals ‘I fully subscribe to the judgement of those writers who maintain that of all the differences between man and the lesser animals, the moral sense or conscience is by far the most important’ (The descent of man, p. 97). He then goes on to argue that the evolution of mutual assistance and the moral senses in humans and other animals are maintained by benefits shared by members of cooperative groups, a suggestion that clearly parallels modern theories of social evolution (Boyd & Richerson 1996; Clutton-Brock 2002). He goes on to point out that many animals live in groups and cooperate with each other and describes how ‘wolves and some other beasts of prey hunt in packs, and aid one another in attacking their victims’, how ‘pelicans fish in concert’ and ‘social animals mutually defend each other’. He describes how vervet monkeys stretch out and groom each others coats and ends by telling a story illustrating the benefits of cooperation: ‘an eagle seizes a young Cercopithecus, which by clinging to a branch, was not at once carried off; it cried

One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

loudly for assistance, upon which the other members of the troop, with much uproar, rushed to the rescue, surrounded the eagle, and pulled out so many feathers, that he no longer thought of his prey, but only how to escape. This eagle as Brehm [the source of the story] remarks, assuredly would never again attack a single monkey of a troop’ (p. 101, 102).

For nearly a 100 years from Darwin’s death, scientific attention was focussed on mechanistic and developmental questions rather than functional ones and Darwin’s interest in social evolution and his holistic view of biological adaptation were eclipsed by the growth of other biological subdisciplines. A continuing interest in social behaviour was maintained though the research and writings of naturalists like Henri Fabre, Eugene Marais, the Keatons, Edmund Selous and Eliot Howard. However, although they were experienced naturalists and observers, they lacked Darwin’s theoretical structure, his compelling interest in principles and his readiness to confront exceptions and difficulties. Not until the late 1930s did a substantial number of professional biologists start to work on the social behaviour of animals. They fell into three main groups. First, there were the founding fathers of animal behaviour, including Julian Huxley (1934, 1938), Konrad Lorenz (1927, 1931, 1935), Niko Tinbergen (1931, 1935, 1936, 1937), Karl von Frisch (1938), Frank Fraser Darling (1937, 1938), Solly Zuckerman (1929, 1932) and Clarence Ray Carpenter (1934, 1935, 1940). Their primary focus was usually on questions concerning the control and development of behaviour, though their research sometimes encompassed functional or comparative aspects of reproductive behaviour. Second, there were a number of animal ecologists, including David Lack (1932, 1933, 1935, 1939, 1943) and A. F. Skutch (1935, 1945, 1960) whose primary interests were the regulation of population density and the evolution of reproductive parameters, including egg size and clutch size. And third, there were the population geneticists, including Ronald Fisher (1930) and J. B. S. Haldane (1932) and later, G. C. Williams (1957) whose principal focus was on the operation of natural selection and the evolution of genetic systems, but whose interests also encompassed the evolution of life histories and social behaviour. Unlike the first two groups, they were well aware of the problems raised by social and altruistic behaviour, though these were tangential to their main interest and usually attracted only passing comments.

3127

This journal is q 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3128

T. Clutton-Brock et al.

Introduction. The evolution of society

These three distinct lines of thinking persisted into the 1950s and they were still largely separate by the end of that decade. For example, neither of Niko Tinbergen’s two synthetic books, Social behaviour in animals (1953) and The study of instinct (1955) cite either Darwin or Fisher. However, by 1960, both theoretical and empirical research was beginning to turn to topics that overlapped all three areas of interest. Comparative studies of social behaviour (especially studies of birds by Gordon Orians (1961, 1962) and John Crook (1962, 1964, 1965) revealed that the size and structure of social groups and the form of mating systems were closely related to variation in habitat and diet, stimulating interest in functional interpretations of social behaviour and providing detailed examples both of selfish and altruistic behaviour. In addition, research on population dynamics in birds showed that territoriality played an important part in regulating population density, focusing the interests of ecologists and ethologists on its evolution and function (Lack 1954, 1966). Finally, the development of a theoretical framework accounting for the evolution of life histories (Medawar 1952; Cole 1954; Williams 1957) led to a growing interest in the adaptive significance of apparently altruistic behaviour. Two specific developments acted as catalysts for the rapid changes that followed. The first was the publication of Wynne Edwards’ monumental book Animal dispersion in relation to social behaviour (1962). Wynne Edwards claimed that many animals adaptively limited their numbers in advance of resource shortage to improve the probability that the group or population would survive. Group displays had evolved, he suggested, to allow their members to assess population density and to adjust their reproductive output accordingly. Other aspects of social behaviour, including territoriality and dominance hierarchies, were closely involved in the regulation of animal numbers and had evolved for this purpose. Wynne Edwards’ theory was directly contrary both to Darwin’s persistent emphasis on individual variation in reproduction as the keystone of evolution as well as to the perception of many ecologists that animal populations were limited directly by the availability of resources (Lack 1954, 1966) so neither population geneticists nor ecologists could ignore the challenge. The general application of Wynne Edwards’ theory was attacked and refuted (Hamilton 1963; Maynard Smith 1964; Lack 1966; Williams 1966a,b) and the ensuing controversy drew attention to the fact that many functional explanations of social and reproductive behaviour relied on putative benefits to groups or populations. This eventually led to a critical revaluation of many of these ideas, culminating in G. C. Williams’ influential review of adaptation (1966). The second development was the explanation of altruism and sterility in Hymenoptera by W. D. Hamilton. In 1963, Hamilton published a brief paper arguing that altruism could evolve if it increased the fitness of relatives and, the following year, introduced the concept of inclusive fitness to account for the evolution of worker sterility in Hymenoptera and of alarm calls in vertebrates (Hamilton 1964). Subsequently, Phil. Trans. R. Soc. B (2009)

Maynard Smith (1964) named Hamilton’s process ‘kin selection’ to distinguish it from group selection and used it to produce a formal model of the evolution of alarm calls (Maynard Smith 1965). In contrast to many of his contemporaries working on the evolution of vertebrate-breeding systems (see above), Hamilton’s thinking owed much to Fisher. He describes how his interest in the evolution of animal societies and altruism. ‘began for me while I was an undergraduate reading natural sciences at the University of Cambridge in 1958. I discovered R. A. Fisher’s The genetical theory of natural selection in the St John’s College Library and immediately realised that this was the key to the understanding of evolution that I had long wanted. I became a Fisher freak and neglected whole courses in my efforts to grasp the book’s extremely compressed style and reasoning. I quickly noticed, however, that Fisher’s arguments implied a basically different interpretation of adaptation from what I was hearing from most of my lecturers and reading in other books. Was adaptation mainly for the benefit of species (the lecturers’ view) or for the benefit of individuals (Fisher’s view)? Clearly it was Fisher who had thought out his Darwinism properly; where interpretations differed, therefore, he must be right—but were the others always wrong? I started on what seemed the key theme in this puzzle—altruism. Did it exist? Could one evolve it in a model? (Hamilton 1988, p. 15)

Hamilton’s theory of kin selection (Hamilton 1964) provided the basis for adaptive interpretations of many forms of altruistic and cooperative behaviour. However, there were some types of cooperation that could not be explained in this way. In particular, why should members of different species (who could not possibly be closely related) cooperate with each other? And why should unrelated conspecifics sometimes assist each other? One possible explanation was that, as Darwin had suggested, cooperating individuals gained shared mutualistic benefits but explanations of this kind smacked of group selection and had difficulty in explaining why cooperation was not replaced by cheating strategies. An alternative explanation of apparently altruistic actions involving unrelated individuals was produced by R. L. Trivers in 1971. Trivers argued that if individuals assisted each other in turn and the costs of assistance were relatively low to donors while the benefits were high to recipients, reciprocal assistance (reciprocity) could evolve among individuals that were unrelated to each other. Cheats (individuals who accepted favours but did not return them) might initially be at an advantage but selection would subsequently favour individuals that discriminated against them and cooperated selectively with individuals that had assisted them in the past. This form of cooperation was originally referred to as ‘reciprocal’ altruism but this can lead to confusion since cooperation of this kind is mutually beneficial in the long term rather than altruistic (Dugatkin 1997; West et al. 2007; Clutton-Brock in press). The theoretical basis of much of our current understanding of the evolution of breeding systems was laid during the decade following the publication of

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Introduction. The evolution of society Hamilton’s theory of kin selection (Hamilton 1964). Hamilton’s (1971) ‘selfish herd’ theory showed that sociality itself could confer benefits to individuals without benefiting the entire group if the chance that an individual would be selected by a predator was diluted as the number of individuals close to it increased. He subsequently examined the conditions favouring selfish and spiteful behaviour within social groups (Hamilton 1964, 1971, 1972). Maynard Smith (1974) and Parker (1974) introduced game theory models to explain why competitors did not always seek to maximize damage to their opponents and to account for ‘ritualization’ of aggressive behaviour. Trivers (1974) explored conflicts of interest between parents and their offspring arguing that, in sexually reproducing organisms, the genetic interests of parents will commonly differ from those of their progeny, who should often favour higher levels of parental expenditure higher than their parents’ optima. Darwin’s writing on sexual selection was re-examined and extended. Trivers (1972) argued that the reasons why males typically compete more intensely for mates than do females was linked to their lower expenditure on progeny, coining the term ‘parental investment’ to cover all forms of parental expenditure associated with rearing offspring. Fisher’s (1930) explanation of the equality of most vertebrate sex ratios was re-assessed and Hamilton (1967) showed that the strongly female-biased sex ratios could be favoured where competing males were close relatives. Trivers & Willard (1973) argued that, in sexually dimorphic vertebrates where sons were more costly to rear than daughters, females who conceived sons but could not afford to rear them should prematurely terminate investment in their progeny—and suggested that this might account for the common trend for mortality to be higher in juvenile males than females. Adaptive explanations of life histories developed in a less dramatic fashion. A number of important reviews laid the basis of what is now known as life-history theory (Gadgil & Bossert 1970; Wilson & Bossert 1971; Pianka 1974; Stearns 1976; Charlesworth 1980). Over the same period, empirical studies of animal breeding systems began to proliferate, focusing more and more on issues of theoretical interest (Lack 1968; Wilson 1971; Clutton-Brock 1974; Jarman 1974). This period of rapid development of theory culminated in a second monumental book. E. O. Wilson’s Sociobiology, the new synthesis (Wilson 1974) contained relatively few new developments but provided comprehensive reviews of relevant areas of population genetics, demography, life-history theory and animal behaviour. Wilson stressed their inter-relatedness and defined a new sub-discipline, sociobiology, whose principal goal should be ‘an ability to predict features of social organization from a knowledge of population parameters combined with information on the behavioural constraints imposed by the genetic constitution of the species’. He argued that an understanding of the evolution of population parameters (including life history variables) should be one of the principal aims of evolutionary ecology and population biology and predicted that, by the year 2000, sociobiology and behavioural ecology would Phil. Trans. R. Soc. B (2009)

T. Clutton-Brock et al.

3129

have become closely allied with population biology and genetics, while traditional ethology and comparative psychology would have been progressively integrated with neurophysiology. The first component of his prediction came about more rapidly than he had anticipated for the theoretical issues raised by the papers of Hamilton, Trivers and Maynard Smith rapidly became the focus of attention in behavioural biology and soon led to the development of an integrated conceptual framework for explaining the ecology and evolution of social behaviour (Krebs & Davies 1978). After the publication of Wilson’s (1975) review, research on social evolution expanded rapidly. The ideas of Hamilton, Trivers, Maynard Smith and Parker were explored, extended and tested (Krebs & Davies 1984; Krebs & Davies 1991, 1997). A combination of theoretical and empirical studies investigated the contrasts and parallels between cooperative and competitive interactions at different levels—between genes on the same chromosome, between cells and groups of cells, between individuals, families, groups and populations (Wilson 1980; Maynard Smith & Szathmary 1995; Michod & Roze 2001; Hoekstra 2003; Okasha 2006). Building on research on the development of social relationships (Hinde 1974, 1983), research on social vertebrates (and primates in particular) explored the development and maintenance of relationships and the ways by which individuals attempt to manipulate the behaviour of others to their own advantage (Clutton-Brock & Parker 1995a,b; Whiten & Byrne 1997), and the tactics they use to resolve conflicts (de Waal 1993; Aureli & de Waal 2000). New fields of research developed round the evolution of signalling systems (Zahavi 1975; Grafen 1990), cooperation between nonrelatives (Axelrod 1984; Sachs et al. 2004; Bergmuller et al. 2007a), the evolution of cooperative breeding (Brown 1987), the extent and causes of reproductive suppression (Vehrencamp 1983a,b) and the resolution of conflicts within social groups (Trivers & Hare 1976; Ratnieks 1988; Boomsma & Grafen 1990; Ratnieks et al. 2006). The adaptive significance of life-history parameters was explored and examined and new theories were developed to account for variation in fecundity (Stearns 1976; Alexander 1991; Bourke 1999), mate choice (Lande 1980; Lande & Arnold 1983), sex allocation (Charnov 1982; Bull 1983; Frank 1990; West 2009), parental care (CluttonBrock 1991; Godfray 1995a,b) and longevity (Bourke 2007). Following the development of genetic techniques capable of identifying paternity ( Jeffreys et al. 1985) it soon came to be appreciated that competition between males extended beyond mating (Birkhead & Møller 1992). These empirical advances were associated with theoretical developments that clarified the links between inclusive fitness and other branches of evolutionary theory, including population and quantitative genetics (Grafen 1985; Frank 1986; Taylor 1990; Queller 1992; Taylor 1996; Wolf et al. 1999; Rousset & Ronce 2004; Gardner et al. 2007), making it easier to develop more general models (Taylor & Frank 1996; Frank 1998) and allowing the biology to lead the maths, rather than vice versa.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3130

T. Clutton-Brock et al.

Introduction. The evolution of society

Over the same period, long-term studies of recognizable individuals provided novel insights into animal societies as well as the information necessary to explore new questions (Clutton-Brock et al. 1982; Woolfenden & Fitzpatrick 1984; Koenig & Mumme 1987; Betzig et al. 1988; Hoogland 1995). In addition, the increasing range of societies that had been examined in detail generated reviews of social behaviour and breeding systems in insects (Wilson 1971; Bourke & Franks 1995; Choe & Crespi 1997), fishes (Thresher 1984), birds (Brown 1987; Koenig & Dickinson 2004) and non-human mammals (Jarman 1974; Smuts 1986a,b; Gittleman 1989; Mann et al. 2000; Wolff & Sherman 2007). Quantitative comparisons of interspecific data were used to test evolutionary hypotheses and to explore relationships between social behaviour, life histories and ecological parameters (Clutton-Brock 1974; Clutton-Brock & Harvey 1978, 1979; Harvey & Pagel 1991). The framework of evolutionary thinking was also extended to the analysis of human behaviour, relationships and societies (Daly & Wilson 1983; Betzig et al. 1988; Barrett et al. 2002; Hrdy 2009). Theoretical studies investigated the evolution of the unusual characteristics of humans, including the development of culturally acquired adaptations (Boyd & Richerson 1996). In parallel, empirical studies of tribal societies generated quantative data on behaviour, energetics, life-history parameters and demography that could be used to test ecological and evolutionary theories and predictions (Betzig et al. 1988; Borgerhoff Mulder 1988; Hill & Hurtado 1996). Today, we understand more about the evolution of society than Darwin did. Nevertheless, the field of social evolution continues to develop rapidly and there are still many unresolved problems and many contentious areas. There is an ongoing debate as to whether social systems should be regarded as superorganisms with adaptive characteristics of their own or whether they are best interpreted as byproducts of the adaptive strategies of individuals (Okasha 2006; Wilson & Wilson 2007). There is still disagreement about the distinction between kin selection and group selection as well as about the relative importance of selection operating at different levels (West et al. 2007, 2008; Wilson & Wilson 2007) and the relative importance of mutualism, reciprocity and coercion in maintaining cooperative behaviour is contentious (Clutton-Brock 2002, in press; West et al. in press). Evolutionary explanations of sex differences have recently been the target of criticism (Gowaty 2004; Tang-Martinez & Ryder 2005) and some would even like to see the theory of sexual selection abandoned altogether (Roughgarden et al. 2006; Roughgarden 2009). Contrasting models of variation in reproductive skew and the proximate mechanisms responsible for reproductive suppression in cooperative societies are still widely debated (Vehrencamp 1983a,b; Reeve & Keller 1995; CluttonBrock 1998; Clutton-Brock et al. 2001b; Creel & Creel 2001; Magrath et al. 2004). Finally, there is little agreement over the origins of human society; the sequence in which human characteristics developed or the relevance of studies of animal societies to understanding those of humans (Rodseth et al. 1991; Wrangham et al. 1999; Zhou et al. 2004; Hrdy 2009). Phil. Trans. R. Soc. B (2009)

This issue of Philosophical Transactions brings together papers presented at a Discussion Meeting in January 2009 where 15 scientists were invited to review important issues relevant to our understanding of the evolution of society in animals and man. Our aim was to explore similarities and contrasts in evolutionary mechanisms in different groups of organisms and the relevance of studies of animal societies to humans. In the opening chapter, Grafen examines the current status of inclusive fitness theory, while Queller compares the cooperative interactions between different types of units to identify the level at which selection and adaptation occur. West explores the evolution of cooperative and cheating strategies in bacteria and suggests that an understanding of these processes may provide novel ways of controlling populations. Social insects provide many examples of the most highly developed and best studied animal societies and four subsequent chapters explore the origins of eusociality (Boomsma), the distribution of reproductive success and cooperative behaviour within groups (Field & Cant), the evolutionary mechanisms maintaining extreme altruism and reproductive inequality (Ratnieks & Helantera¨) and the genetic mechanisms controlling behaviour on which selection operates (Keller). The four subsequent chapters examine the less specialized societies of non-human vertebrates. Hatchwell reviews the distribution of cooperative breeding in birds, while Clutton-Brock reviews our understanding of mammalian societies and their consequences for the evolution of life histories. Silk subsequently investigates the extent of nepotism in primates, while Hauser assesses the importance of reciprocity and spite in relationships between nonrelatives. The last four chapters examine the evolution of human societies. Foley & Gamble review our current understanding of the societies of hominids and early humans; Boyd & Richerson explore the role of cultural adaptation and geneculture coevolution in the development of pro-sociality in humans; Kaplan assesses the importance of ecological benefits and energetic constraints on the evolution of human societies; and Dasgupta explores the role of trust in the development and maintenance of cooperation between economic units. By the end of the meeting, there was a general consensus that the integration of different approaches to investigating the evolution of society and of studies of contrasting organisms was overdue and should be an important component of future research. Our hope is that this issue will contribute to this process.

T. Clutton-Brock1,*, S. West2, F. Ratnieks3 and R. Foley4 1 Department of Zoology, and 4Human Evolutionary Studies, University of Cambridge, Cambridge, UK 2 Department of Zoology, University of Oxford, Oxford, UK 3 Department of Biological and Environmental Science, University of Sussex, Brighton, UK *Author for correspondence ([email protected]).

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Introduction. The evolution of society REFERENCES Alexander, R. D. 1991 The evolution of eusociality. In The biology of the naked mole-rat (eds P. W. Sherman, J. U. M. Jarvis & R. D. Alexander), pp. 3–44. Princeton, NJ: Princeton University Press. Aureli, F. & de Waal, F. B. M. 2000 Natural conflict resolution. San Francisco, CA: University of California Press. Axelrod, R. 1984 The evolution of cooperation. New York, NY: Basic Books. Barrett, L., Dunbar, R. & Lycett, J. E. 2002 Human evolutionary psychology. Princeton, NJ: Princeton University Press. Bergmuller, R., Bshary, R., Johnstone, R. A. & Russell, A. F. 2007a Integrating cooperative breeding and cooperation theory. Behav. Process. 76, 61–72. (doi:10.1016/j. beproc.2007.07.001) Betzig, L., Borgerhoff Mulder, M. & Turkes, P. (eds) 1988 Human reproductive behaviour. Cambridge, UK: University Press. Birkhead, T. R. & Møller, A. P. 1992 Sperm competitions in birds. London, UK: Academic Press. Boomsma, J. J. & Grafen, A. 1990 Intraspecific variation in ant sex ratios and the Trivers –Hare hypothesis. Evolution 44, 1026–1034. (doi:10.2307/2409564) Borgerhoff Mulder, M. 1988 Reproductive success in three Kipsigi cohorts. In Reproductive success (ed. T. H. CluttonBrock), pp. 419–435. Chicago, IL: University Press. Bourke, A. F. G. 1999 Colony size, social complexity and reproductive conflict in social insects. J. Evol. Biol. 12, 245 –257. (doi:10.1046/j.1420-9101.1999.00028.x) Bourke, A. F. G. 2007 Kin selection and the evolutionary theory of aging. Ann. Rev. Ecol. Syst. 38, 103–128. Bourke, A. F. G. & Franks, N. R. 1995 Social evolution in ants. Princeton, NJ: Princeton University Press. Boyd, R. & Richerson, P. J. 1996 Why culture is common, but cultural evolution is rare. Proc. Br. Acad. 88, 77–93. Brown, J. L. 1987 Helping and communal breeding in birds. Princeton, NJ: Princeton University Press. Bull, J. J. 1983 Evolution of sex determining mechanisms. Menlo Park, CA: Benjamin/Cummings. Charlesworth, B. 1980 Evolution in age-structured populations. Cambridge, UK: Cambridge University Press. Charnov, E. L. 1982 The theory of sex allocation. Princeton, NJ: Princeton University Press. Choe, J. L. & Crespi, B. J. (eds) 1997 Mating systems in insects and arachnids. Cambridge, UK: University Press. Clutton-Brock, T. H. 1974 Primate social organisation and ecology. Nature 250, 539 –542. (doi:10.1038/250539a0) Clutton-Brock, T. H. 1991 The evolution of parental care. Princeton, NJ: Princeton University Press. Clutton-Brock, T. H. 1998 Reproductive skew: disentangling concessions from control. A reply to Emlen and Reeve. Trends Ecol. Evol. 13, 459. (doi:10.1016/S01695347(98)01470-0) Clutton-Brock, T. H. 2002 Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69– 72. (doi:10.1126/science.296.5565.69) Clutton-Brock, T. In press. Cooperation between non-kin: reciprocity, mutualism or manipulation? Nature. Clutton-Brock, T. H. & Harvey, P. H. 1978 Mammals, resources and reproductive strategies. Nature 273, 191– 195. (doi:10.1038/273191a0) Clutton-Brock, T. H. & Harvey, P. H. 1979 Comparison and adaptation. Proc. R. Soc. Lond. B 205, 547 –565. (doi:10. 1098/rspb.1979.0084) Clutton-Brock, T. H. & Parker, G. A. 1995a Punishment in animal societies. Nature 373, 209–216. (doi:10.1038/ 373209a0) Clutton-Brock, T. H. & Parker, G. A. 1995b Sexual coercion in animal societies. Anim. Behav. 49, 1345–1365. (doi:10.1006/anbe.1995.0166) Phil. Trans. R. Soc. B (2009)

T. Clutton-Brock et al.

3131

Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. 1982 Red deer: the behaviour and ecology of two sexes. Edinburgh, UK: University Press. Clutton-Brock, T. H. et al. 2001b Cooperation, conflict and concession in meerkat groups. Science 291, 478– 481. (doi:10.1126/science.291.5503.478) Cole, L. C. 1954 The population consequences of life history phenomena. Quart. Rev. Biol. 29, 103–137. Creel, S. & Creel, N. M. 2001 The African wild dog: behavior, ecology and conservation. Princeton, NJ: University Press. Daly, M. & Wilson, M. 1983 Sex, evolution and behavior. Boston, MA: Willard Grant Press. Darwin, C. 1859/1958 The origin of species. New York, NY: The Modern Library. de Waal, F. B. M. 1993 Primate social conflict (eds W. A. Mason & S. P. Mendoza). Albany, NY: State University of New York Press. Dugatkin, L. A. 1997 Cooperation among animals: an evolutionary perspective. Oxford, UK: University Press. Frank, S. A. 1986 Hierarchical selection theory and sex ratios. I. General solutions for structured populations. Theoret. Popul. Biol. 29, 312 –342. (doi:10.1016/00405809(86)90013-4) Frank, S. A. 1990 Sex allocation theory for birds and mammals. Ann. Rev. Ecol. Syst. 21, 13–56. (doi:10.1146/ annurev.es.21.110190.000305) Frank, S. A. 1998 Foundations of social evolution. Princeton, NJ: University Press. Gadgil, M. & Bossert, W. H. 1970 Life historical consequences of natural selection. Am. Nat. 104, 1 –24. (doi:10.1086/282637) Gardner, A., West, S. A. & Barton, N. H. 2007 The relation between multilocus population genetics and social evolution theory. Am. Nat. 169, 207– 226. (doi:10.1086/ 510602) Gittleman, J. L. 1989 Carnivore group living: comparative trends. In Carnivore behaviour, ecology and evolution (ed. J. L. Gittleman), pp. 183 –207. Ithaca, NY: Cornell University Press. Godfray, H. C. J. 1995a Evolutionary theory of parent– offspring conflict. Nature 376, 133–138. (doi:10.1038/ 376133a0) Godfray, H. C. J. 1995b Signaling of need between parents and young: parent –offspring conflict and sibling rivalry. Am. Nat. 146, 1–24. (doi:10.1086/285784) Gowaty, P. A. 2004 Sex roles, contests for the control of reproduction and sexual selection. In Sexual selection in primates (ed. P. Kappeler), pp. 163 –221. Cambridge, UK: University Press. Grafen, A. 1985 A geometric view of relatedness. Oxford Surv. Evol. Biol. 2, 28 –29. Grafen, A. 1990 Biological signals as handicaps. J. Theoret. Biol. 144, 517 –546. (doi:10.1016/S0022-5193(05) 80088-8) Hamilton, W. D. 1963 The evolution of altruistic behavior. Am. Nat. 97, 354 –356. (doi:10.1086/497114) Hamilton, W. D. 1964 The genetical evolution of social behaviour. I. II. J. Theoret. Biol. 7, 1 –52. (doi:10.1016/ 0022-5193(64)90038-4) Hamilton, W. D. 1971 Geometry for the selfish herd. J. Theoret. Biol. 31, 295–311. (doi:10.1016/0022-5193(71) 90189-5) Hamilton, W. D. 1972 Altruism and related phenomena, mainly in social insects. Ann. Rev. Ecol. Syst. 3, 193– 232. (doi:10.1146/annurev.es.03.110172.001205) Hamilton, W. D. 1988 The genetical theory of social behaviour 1. Citation classic in Current Contents No. 40, p. 16. [J. Theor. Biol. 7, 1–16]. Harvey, P. H. & Pagel, M. D. 1991 The comparative method in evolutionary biology. Oxford, UK: University Press.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3132

T. Clutton-Brock et al.

Introduction. The evolution of society

Hill, K. & Hurtado, M. A. 1996 Ache life history. New York, NY: Aldine de Gruyter. Hinde, R. A. 1974 Biological bases of human social behaviour. New York, NY: McGraw Hill. Hinde, R. A. 1983 Primate social relationships. Oxford, UK: Blackwells. Hoekstra, R. 2003 Power to the genome: who suppresses the outlaw? In Genetic and cultural evolution of cooperation (ed. P. Hammersteiin), pp. 257– 270. Dahlem Workshop Reports series. Cambridge, MA: MIT Press. Hoogland, J. L. 1995 The black-tailed prairie dog: social life of a burrowing mammal. Chicago, IL: University of Chicago Press. Hrdy, S. B. 2009 Mothers and others. Harvard, USA: Belknap Press. Jarman, P. J. 1974 The social organisation of antelope in relation to their ecology. Behaviour 48, 215 –267. (doi:10.1163/156853974X00345) Jeffreys, A. J., Wilson, V. & Thein, S. L. 1985 Hypervariable ‘minisatellite’ regions in human DNA. Nature 314, 67–73. (doi:10.1038/314067a0) Koenig, W. & Dickinson, J. (eds) 2004 Ecology and evolution of cooperative breeding in birds. Cambridge, UK: University Press. Koenig, W. D. & Mumme, R. L. 1987 Population ecology of the cooperatively breeding acorn woodpecker. Princeton, NJ: Princeton University Press. Krebs, J. R. & Davies, N. B. 1978 Behavioural ecology: an evolutionary approach. Oxford, UK: Blackwell Scientific Publications. Krebs, J. R. & Davies, N. B. 1984 Behavioural ecology: an evolutionary approach. Oxford, UK: Blackwell Scientific Publications. Krebs, J. R. & Davies, N. B. 1991 Behavioural ecology: an evolutionary approach. Oxford, UK: Blackwell. Krebs, J. R. & Davies, N. B. 1997 An introduction to behavioural ecology, 4th edn. Oxford, UK: Blackwell Scientific. Lack, D. 1954 The natural regulation of animal numbers. Oxford, UK: University Press. Lack, D. 1966 Population studies of birds. Oxford, UK: University Press. Lack, D. 1968 Ecological adaptation for breeding in birds. London, UK: Methuen. Lande, R. 1980 Sexual dimorphism, sexual selection and adaptation in polygenic characters. Evolution 34, 292 –305. (doi:10.2307/2407393) Lande, R. & Arnold, S. J. 1983 The measurement of selection on correlated characters. Evolution 37, 1210–1226. (doi:10.2307/2408842) Magrath, R. A., Johnstone, R. A. & Heinsohn, R. G. 2004 Reproductive skew. In Ecology and evolution of cooperative breeding in birds (eds W. Koenig & J. Dickinson), pp. 157 –176. Cambridge, UK: University Press. Mann, J., Connor, R. C., Tyack, P. L. & Whitehead, H. (eds) 2000 Celacean societies. Chicago, IL: University Press. Maynard Smith, J. 1964 Group selection and kin selection. Nature 201, 1145– 1147. (doi:10.1038/2011145a0) Maynard Smith, J. 1965 The evolution of alarm calls. Am. Nat. 99, 59–63. Maynard Smith, J. 1974 The theory of games and the evolution of animal conflicts. J. Theor. Biol. 47, 209 –221. Maynard Smith, J. & Szathmary, E. 1995 The major transitions in evolution. New York, NY: Freeman. Medawar, P. B. 1952 An unsolved problem of biology. London, UK: H.K. Lewis & Co. Michod, R. E. & Roze, D. 2001 Cooperation and conflict in the evolution of multicellularity. Heredity 86, 1–7. (doi:10.1046/j.1365-2540.2001.00808.x) Okasha, S. 2006 Evolution and the levels of selection. Oxford, UK: University Press. Phil. Trans. R. Soc. B (2009)

Parker, G. A. 1974 Assessment strategy and the evolution of fighting behaviour. J. Theor. Biol. 47, 223 –243. Pianka, E. R. 1974 Evolutionary ecology. New York, NY: Harper and Row. Queller, D. C. 1992 Quantitative genetics; inclusive fitness and group selection. Am. Nat. 139, 540 –558. (doi:10. 1086/285343) Ratnieks, F. L. W. 1988 Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132, 217 –236. (doi:10.1086/284846) Ratnieks, F. L. W., Foster, K. R. & Wenseleers, T. 2006 Conflict resolution in insect societies. Ann. Rev. Entomol. 51, 581 –608. (doi:10.1146/annurev.ento.51.110104. 151003) Reeve, H. K. & Keller, L. 1995 Partitioning of reproduction in mother – daughter versus sibling associations: a test of optimal skew theory. Am. Nat. 145, 119–132. (doi:10. 1086/285731) Rodseth, L., Wrangham, R. W., Harrigan, A. & Smuts, B. B. 1991 The human community as a primate society. Curr. Anthropol. 32, 221–254. (doi:10.1086/203952) Roughgarden, J. 2009 In The genial gene: deconstructing Darwinian selfishness. San Francisco, CA: University of California Press. Roughgarden, J., Oishi, M. & Akcay, E. 2006 Reproductive social behavior: cooperative games to replace sexual selection. Science 311, 965– 969. (doi:10.1126/science. 1110105) Rousset, F. & Ronce, O. 2004 Indirect fitness for traits affecting metapopulation demography. Theoret. Popul. Biol. 65, 127– 141. (doi:10.1016/j.tpb.2003.09.003) Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull, J. J. 2004 The evolution of cooperation. Quart. Rev. Biol. 79, 135 –160. Smuts, B. B. 1986a Sexual competition and mate choice. In Primate societies (eds B. B. Smuts, D. L. Cheney, R. M. Seyfarth, W. R. Wrangham & T. T. Struhsaker). Chicago, IL: University of Chicago Press. Smuts, B. B. 1986b Gender, aggression and influence. In Primate societies (eds B. B. Smuts, D. L. Cheney, R. M. Seyfarth, W. R. Wrangham & T. T. Struhsaker). Chicago, IL: University of Chicago Press. Stearns, S. C. 1976 Life-history tactics: a review of the ideas. Quart. Rev. Biol. 51, 3–48. Tang-Martinez, Z. & Ryder, T. B. 2005 The problem with paradigms: Bateman’s world view as a case study. Integr. Comp. Biol. 45, 821 –830. (doi:10.1093/icb/45.5.821) Taylor, P. D. 1990 Allele-frequency change in a class structured population. Am. Nat. 135, 95–106. (doi:10.1086/ 285034) Taylor, P. D. 1996 Inclusive fitness arguments in genetic models of behaviour. J. Math. Biol. 34, 654–674. (doi:10.1007/BF02409753) Taylor, P. D. & Frank, S. A. 1996 How to make a kin selection model. J. Theoret. Biol. 180, 27–37. (doi:10.1006/ jtbi.1996.0075) Thresher, R. E. 1984 Reproduction in reef fishes. Neptune City, NJ: T. F. H. Publications. Trivers, R. L. & Hare, H. 1976 Haplo-diploidy and the evolution of the social insects. Science 191, 249 –263. (doi:10. 1126/science.1108197) Vehrencamp, S. L. 1983a A model for the evolution of despotic versus egalitarian societies. Anim. Behav. 31, 667 –682. (doi:10.1016/S0003-3472(83)80222-X) Vehrencamp, S. L. 1983b Optimal degree of skew in cooperative societies. Am. Zool. 23, 327– 335. West, S. A. 2009 Sex allocation. Princeton, NJ: University Press. West, S. A., Griffin, A. S. & Gardner, A. 2007 Social semantics: altruism, cooperation, mutualism, strong reciprocity

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Introduction. The evolution of society and group selection. J. Evol. Biol. 20, 415 –432. (doi:10. 1111/j.1420-9101.2006.01258.x) West, S. A., Griffin, A. S. & Gardner, A. 2008 Social semantics: how useful has group selection been? J. Evol. Biol. 21, 374– 385. West, S. A., Mouden, C. E. & Gardner, A. In press. Social evolution theory and its application to the evolution of cooperation in humans. Whiten, A. & Byrne, R. W. 1997 Machiavellian Intelligence II. Cambridge, UK: University Press. Williams, G. C. 1957 Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411. (doi:10.2307/2406060) Williams, G. C. 1966a Adaptation and natural selection: a critique of some current evolutionary thought. Princeton, NJ: University Press. Williams, G. C. 1966b Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am. Nat. 100, 687– 690. (doi:10.1086/282461) Wilson, E. O. 1971 The insect societies. Cambridge, MA: Belknap Press. Wilson, E. O. 1974 Sociobiology, the new synthesis. Boston, MA: Harvard University Press. Wilson, D. S. 1980 The natural selection of populations and communities. Menlo Park, CA: Benjamin Cummings.

Phil. Trans. R. Soc. B (2009)

T. Clutton-Brock et al.

3133

Wilson, E. O. & Bossert, W. H. 1971 A primer of population biology. Sunderland, MA: Sinauer Associates. Wilson, D. S. & Wilson, E. O. 2007 Rethinking the theoretical foundation of sociobiology. Quart. Rev. Biol. 82, 327–348. Wolf, J. B., Brodie, E. D. & Moore, A. J. 1999 Interacting phenotypes and the evolutionary process. II. Selection resulting from social interactions. Am. Nat. 153, 254– 266. (doi:10.1086/303168) Wolff, J. O. & Sherman, P. W. 2007 Rodent societies as model systems. In Rodent societies (eds J. O. Wolff & P. W. Sherman). Chicago, IL: University Press. Woolfenden, G. E. & Fitzpatrick, J. W. 1984 The Florida scrub jay: demography of a cooperative-breeding bird. Princeton, NJ: University Press. Wrangham, R. W., Jones, J. H., Laden, G., Pilbeam, D. & Conklin-Brittain, N. 1999 The raw and the stolen—cooking and the ecology of human origins. Curr. Anthropol. 40, 567–594. (doi:10.1086/300083) Zahavi, A. 1975 Mate selection: a selection for a handicap. J. Theoret. Biol. 53, 205 –214. (doi:10.1016/00225193(75)90111-3) Zhou, W.-X., Sornette, D., Hill, R. A. & Dunbar, R. 2004 Discrete hierarchical organisation of social group sizes. Proc. R. Soc. Lond. B 272, 439 –444. (doi:10.1098/rspb. 2004.2970)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3135–3141 doi:10.1098/rstb.2009.0056

Review

Formalizing Darwinism and inclusive fitness theory Alan Grafen* St John’s College, Oxford OX1 3JP, UK Inclusive fitness maximization is a basic building block for biological contributions to any theory of the evolution of society. There is a view in mathematical population genetics that nothing is caused to be maximized in the process of natural selection, but this is explained as arising from a misunderstanding about the meaning of fitness maximization. Current theoretical work on inclusive fitness is discussed, with emphasis on the author’s ‘formal Darwinism project’. Generally, favourable conclusions are drawn about the validity of assuming fitness maximization, but the need for continuing work is emphasized, along with the possibility that substantive exceptions may be uncovered. The formal Darwinism project aims more ambitiously to represent in a formal mathematical framework the central point of Darwin’s Origin of Species, that the mechanical processes of inheritance and reproduction can give rise to the appearance of design, and it is a fitting ambition in Darwin’s bicentenary year to capture his most profound discovery in the lingua franca of science. Keywords: formal Darwinism; fitness optimization; Price equation; uncertainty; dynamic insufficiency

1. INTRODUCTION Darwin’s Origins of species was published 150 years and 10 months ago and brought fully within the ambit of science subjects such as anatomy and physiology. A conference on optimal wing design, or comparative renal morphology, would certainly have fitted that 150-year anniversary. However, the Evolution of Society relies on selection of mental attributes, emotions and cooperation. It was not until 1871, in the Descent of man, that Darwin claimed the moral universe for biology, and in some ways 2021 would be a more appropriate date for this meeting. However, this is also the 200th anniversary of Darwin’s birth, and so all of his work can justly be celebrated on that score. My paper is appropriately traced to the Origin, as I have been asked to speak on inclusive fitness and on formalizing Darwinism. Inclusive fitness is a basic element of the modern understanding of natural selection and goes back directly to the ideas in the Origin, without the need of the further developments of the Descent. Inclusive fitness is now a building block of our current understanding of natural selection, and in a meeting on the Evolution of Society, it is likely to be taken for granted, simply assumed, and then used to erect more advanced and complex ideas. It is the building block that tells us, when we focus on just the behaviour of one individual, how selection will bear on her actions. The higher reaches of the subject

*[email protected] One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

will ask how individuals get into their situations, how the collective behaviours will interact and whether emergent properties do in fact emerge. My first purpose is to issue a mainly reassuring message—yes, it is sensible to use inclusive fitness as a building block—but with some reservations. We are not quite sure what inclusive fitness is in any but very simple circumstances, and relatedness might be more complicated than we think. Theoretical work on inclusive fitness can help us in extending the circumstances in which inclusive fitness is known to work, in telling us how to calculate relatedness and in warning us in what kinds of cases inclusive fitness may be liable to break down. A second purpose is to say not all qualified biologists agree that inclusive fitness maximization is a sound biological principle, contrary to my first reassuring point. The orthodox position among mathematical population geneticists is that natural selection does not lead to any maximization principle at all. There has been a history of misunderstanding over what fitness maximization means, and theoretical work on inclusive fitness theory can help to sort out that misunderstanding. Third, I will discuss current research on the theory of inclusive fitness, emphasizing my own formal Darwinism project. This theoretical programme aims to help us understand inclusive fitness and seeks to explain what biologists mean by inclusive fitness maximization. In addition, it also has a grander goal, which may be thought relevant at an anniversary meeting of this kind, of formalizing Darwin’s core argument in the Origin in a fully mathematical, fully rigorous framework. After all, if Newton, Maxwell and Einstein

3135

This journal is # 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3136

A. Grafen Review. Fitness optimisation

have their ideas encapsulated in mathematical terms, why should not Darwin too? The obvious answer to this question is that the physicists first enunciated their theories mathematically. A second answer is that Darwin’s ideas are so rich and varied, a dry mathematical account cannot capture everything. Let me accept this point and say that the mathematical framework is designed to represent one central argument of the Origin, namely, that the mechanical processes of inheritance and reproduction can give rise to the appearance of design.

2. WHAT IS INCLUSIVE FITNESS? To read elementary accounts of inclusive fitness in undergraduate textbooks, one would not think there was any problem in the definition of inclusive fitness or in the security of its place in biological theory. Nor would one doubt that natural selection leads to the maximization of inclusive fitness by organisms, or at least, the ‘as-if maximization’. I want at the beginning of this part of the discussion to point out how much of the advance in behavioural ecology since 1960 depends on applying the idea of fitness maximization and, where social behaviour is involved, inclusive fitness maximization. The concept of adaptation as analysed by Williams (1966), clutch-size optimization as studied by Lack (1968) and all subsequent organismal optimization theory, all the innovative theories of Trivers and co-workers (including Trivers 1971, 1972, 1974; Trivers & Willard 1973; Trivers & Hare 1976) and the use of optimization ideas such as evolutionarily stable strategies (Maynard Smith & Price 1973) and inclusive fitness itself (Hamilton 1964, 1970) only make sense if there is a maximand of natural selection. Having established that a lot is at stake, I need to persuade you that there is reason to think inclusive fitness as a concept is not fully and logically established. The obvious place to start is with mathematical population genetics, and the clear message of Ewens (2004) that there is no quantity maximized by the operation of natural selection. In fact, one of the recurrent sports of mathematical population geneticists since 1960 has been showing that natural selection does not lead to maximization of anything (pioneered by Moran (1964) and reviewed by Ewens (2004)). Fortunately, for behavioural ecologists and most students of the behaviour of whole organisms, this very negative conclusion is based on a misunderstanding of what fitness optimization means. It is natural for those with mathematical training, when starting with a dynamical system such as gene frequency change equations, and faced with claims of maximization, to think of established mathematical tools widely used by physicists such as Lyapunov functions and gradient functions. However, these are very far from what biologists mean by fitness maximization, and it is worth spending a moment to see why. Consider a Lyapunov function, which in this context is a function that attaches a real number to each point in genotype frequency space. Its crucial property is that as the system evolves through time, the associated real number never increases. A gradient function also Phil. Trans. R. Soc. B (2009)

attaches a real number to each point of genotype frequency space and has the stronger property that the dynamic path through genotype frequency space always takes the direction of fastest increase of the associated real number. Now the reason that these do not reflect a biologist’s concept of fitness maximization is not hard to see. Both these functions are about a choice of direction in genotype frequency space and a direction that is taken by the whole population. The biological concept of fitness maximization is quite different. It is about a choice of some phenotypic trait, perhaps size or sex ratio, clarity of cornea or strength of bone, and where the trait is a property of an individual. Further, the choice is subject to constraints from physiology, physics and information. Thus, these are quite different kinds of optimization ideas. It is not surprising that this confusion should have arisen, and it could be argued that Fisher (1930) did not help with his choice of verbal expression of his fundamental theorem of natural selection. But there is no longer any excuse for perpetuating this misunderstanding. What, then, is the correct understanding of the biologist’s concept of fitness maximization? I argue (Grafen 2002) that we need to set out an optimization programme, which is a mathematical tool familiar in operations research, game theory and economics. This specifies an instrument—the variable whose value is to be chosen; a constraint set—the set of values from which the instrument is to be chosen and a maximand—a function of the instrument that says how successful that value of the instrument is. The choice of instrument and the constraint set are determined by the biological system being studied, but where is the maximand to come from? In other words, how are we to define fitness? The known processes of natural selection are gene frequency change. We therefore need to begin with the dynamic equations of gene frequency change and try to prove links to the optimization programme. If we can prove strong enough links, including defining the maximand, then that will show how natural selection relates to fitness maximization. That, in essence, is the logic of my formal Darwinism project, which currently consists of five core papers (Grafen 1999, 2000, 2002, 2006a,b), a bunch of applications (Grafen 2007a,c; Grafen & Archetti 2008; Gardner & Grafen 2009) and two introductory and expository papers, one non-mathematical (Grafen 2007b) and one mathematical (Grafen 2008).

3. CURRENT WORK ON INCLUSIVE FITNESS I now want to say a few words about current theoretical work on inclusive fitness. As well as my own project, there are three main branches of which I am aware. Two are on the pure side of population genetics. Peter Taylor and co-workers (recent papers include Taylor 1996; Day & Taylor 1998, 2000; Irwin & Taylor 2000, 2001; Taylor & Irwin 2000; Taylor et al. 2000, 2007a,b; Wild & Taylor 2004) have consistently extended the range of mathematical models in which inclusive fitness is defined and predicts gene frequency change. A second school

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Fitness optimisation of Franc¸ois Rousset, Laurent Lehmann and their co-workers (recent works include Rousset & Billiard 2000; Rousset 2004; Lehmann et al. 2006, 2007a,b; Lehmann & Balloux 2007) has developed very powerful methodologies for analysing gene frequency change using inclusive fitness and applied them to tough theoretical problems. See Gardner et al. (2007) for a similar approach. For theoreticians, the details of this work are very important, but for more practical biologists, there are two messages. The positive message is the range of circumstances in which inclusive fitness is known to apply is always being extended. The negative message is that range is still quite small, and there is a long way to go to cover the situations that most empirical biologists would consider usual. A further useful aspect of this theoretical work is that both groups redefine exactly what inclusive fitness is as they extend it, providing a deeper and more refined conceptual understanding. The third branch is associated with the name of Steve Frank (including Taylor & Frank 1996; Frank 1997a,b, 1998). Frank and co-workers provide very powerful tools for biologists who wish to apply the idea of inclusive fitness. If you have a sex ratio problem, or a dispersal problem, and you want to know how to understand it in inclusive fitness terms, this is the body of work to consult. My own formal Darwinism project, as discussed earlier, is based on linking gene frequency change to optimization programmes. A basic model presents these links for non-social behaviour, in discrete nonoverlapping generations, but with arbitrary uncertainty and arbitrary ploidies (Grafen 2002). Further papers deal with extensions such as the existence of classes such as sexes or sizes (Grafen 2006b). and social behaviour (Grafen 2006a). The tasks for the future include allowing continuous time and overlapping generations and uniting all the extensions into a single over-arching model. These bodies of work vary along a number of dimensions. A key difference is that the two more theoretical branches (Taylor and Rousset) retain the ‘gold standard’ property of population genetics models known as dynamic sufficiency. This restricts their range to models with very precise assumptions. The two more applied branches (Frank and Grafen) have abandoned the gold standard, for what might be called a ‘plastic standard’, to indicate that it aims for applied usefulness rather than decoration. They operate with fewer assumptions about gene frequencies, with the consequence that their conclusions apply more widely when they can find them, but there are many kinds of conclusions they cannot attain, because of missing information. The tradeoff is that the unattainable conclusions are mainly about highly technical dynamic things such as interior equilibria and linkage disequilibrium, which are not the focus of empirical work at the organismal level, and not even demonstrably useful to it. The attainable conclusions are about quantities more likely to be significant at a meeting like this, such as the maximization of inclusive fitness and optimized trait values. The theory is certainly ripe for an overview, in which one key question would be: what lessons should be Phil. Trans. R. Soc. B (2009)

A. Grafen

3137

drawn from current theory about the widespread assumption among behavioural ecologists and others, that organisms act so as to maximize their inclusive fitness?

4. INCLUSIVE FITNESS CONTRASTED WITH KIN SELECTION The terms inclusive fitness (introduced by Hamilton 1964) and kin selection (introduced by Maynard Smith 1964) now have long histories and are often discussed as though their meanings are clear and fixed. However, authors differ as to those meanings, and at the level of work discussed in this article, their meanings have to be considered as a subject of discussion. Let us begin with what can be regarded as uncontroversial about the terms. Inclusive fitness is certainly the name of a mathematical quantity that attaches to individuals (or possibly to genotypes), whose function is to capture how natural selection acts on social behaviour by taking the place of Darwinian fitness in the simpler case of non-social behaviour. Kin selection is the name of a process, parallel to Darwinian selection or natural selection, that causes individuals to behave differently (and generally more favourably) towards more closely than to less closely related conspecifics. These points are easy to agree upon, but many aspects are left in the air. I would add to inclusive fitness the requirement that it is a quantity that natural selection tends to cause individuals to act as if maximizing, just as Darwinian fitness tends to be maximized in the non-social case. This is a controversial point for reasons elaborated earlier, namely, that the sense of maximization has not always been understood. Furthermore, the tendency towards maximization, its strength and power and its exact nature will depend on further assumptions whose delineation is an important part of theoretical work. A crucial point for contrast with kin selection is that inclusive fitness maximization can be shown for cases in which the interactants have no special kin links, and this is discussed further below. The definition of inclusive fitness is a precise issue, and one can expect theoretical work to apply with mathematical exactness. Kin selection, on the other hand, is a loose term. Its strongest useful attachment may now be towards facts—there is overwhelming evidence, too much to cite here, that individuals of many species do behave more favourably towards relatives than towards nonrelatives. These differences between the terms reflect their origins. The contrast that will be suggested here is that a mathematical quantity called inclusive fitness can be defined, such that gene frequency dynamics tend to cause individuals to act as if maximizing inclusive fitness. Sometimes this results in a tendency to act favourably towards individuals in a way that is fully explained by their links of common ancestry—in this case, we would say that inclusive fitness underlies kin selection, and the two are in harmony. Sometimes, however, the as-if maximization of inclusive fitness will lead individuals to act more favourably to other individuals based on some other feature. The simplest

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3138

A. Grafen Review. Fitness optimisation

case would be green beard genes, when individuals with green beards act favourably towards other individuals bearing the same trait. Here inclusive fitness is still, in a relevant sense, being maximized, but we would not want to call this process kin selection— and so in this case inclusive fitness and kin selection are not in harmony. These prefatory remarks will be expanded in the rest of this section, which can be read as an elaboration of arguments made by and positions adopted by Hamilton (1975), who characteristically anticipated many sophisticated points not understood by others for decades, updated in the light of more recent theoretical work. I pursue the theme through the development of the formal Darwinism project to incorporate social interactions (Grafen 2006a). The aim of this section is to give a flavour of the complications that might arise in justifying inclusive fitness maximization, and to point to where more research would be useful. The extension of the project to incorporate social behaviour follows Hamilton’s two main derivations (Hamilton 1964, 1970). It shows that, under the assumptions of finite population, finite uncertainty and additivity of fitness interactions, selection of social behaviour can be interpreted as maximizing the arithmetic average of relative inclusive fitness. Here, relative means relative to the population mean number of offspring. This very general conclusion supports the idea that inclusive fitness is the natural way to understand selection on social behaviour and is a sufficient tool. The theory shows how to calculate relatednesses, but it does not straight away give the kind of relatednesses with which most biologists are familiar, that is, the kind in which sibs are related by a half, parents and offspring are related by a half and cousins are related by an eighth. The relatednesses provided by the theory I will call ‘inclusive fitness relatednesses’ because it is those relatednesses that guarantee the link between inclusive fitness and selection. The familiar relatednesses I will call ‘ancestral relatedness’ because they are calculated from patterns of common ancestry. What kinds of objects are the inclusive fitness relatednesses? How are they calculated if not from common ancestry? We need to know the genotypes of all individuals in the population, and relatedness itself is a weighted regression coefficient of the recipient’s genotypic value on the actor’s genotypic value. The weights depend on the fitness increments that represent the effects on offspring production of the social action whose selection is being studied. A relatedness is calculated for a given allele, for a given information state of the actor, and for a given social action. A selection of early work on these ideas is Crozier (1970), Orlove (1975), Orlove & Wood (1978), Michod & Hamilton (1981) and Seger (1981). But ancestral relatednesses do not depend on a particular allele, on the information state of the actor or on the given social action. To justify the familiar relatednesses from the abstract theory therefore requires further assumptions, and it is an open area of theory just what assumptions are required. Some cases are simple. With a panmictic population and random Phil. Trans. R. Soc. B (2009)

mating, and individuals selected as interactants solely with reference to their kin links, the inclusive fitness relatednesses and the ancestral relatednesses are equal. But it would be useful to know more. What kinds of properties of dispersal group formation, or of choice of interactants, guarantee that the two kinds of relatedness are equal? Those are assumptions that are needed to justify the current emphasis on ancestral relatednesses. Let us now turn to ask what follows when the ancestral and inclusive fitness relatednesses are not equal. In most cases, we would find that the inclusive fitness relatednesses were different for different loci and even for different alleles at the same locus. Selection at different loci would therefore be pulling in different directions. The simplest example of this phenomenon is green beard genes, but we press on to more general considerations. The power of selection to create adaptations and design requires that selection operates at many loci. If loci vary a lot in relatedness, then social behaviour is likely not to be very well designed. Selection wastes itself by opposing itself at different loci. A building with different sets of builders working to different blueprints, with one group taking down what another is in the process of erecting, is unlikely to develop a complex and functioning design. In fact, there is one major feature of genomes that does produce these ‘different groups of workers’. The analytical arguments so far have all assumed that the loci in question share their pattern of inheritance, but different patterns of inheritance do produce conflicts in the phenomenon of intra-genomic conflict (Haig & Westoby 1989; Burt & Trivers 2005). In these cases, it is common for one group of workers (in vertebrates the autosomal genes) to tie up the other groups (genes on sex chromosomes and mitochondrial chromosomes) as part of their work to complete the building. So long as one group of loci is numerically much larger than the others, this is the probable outcome, and in that case, complex design again becomes possible. The significance of relatednesses being equal across a large solid majority of the genome is therefore very great. If it holds, then we can expect selection to be pushing in the same direction across the whole genome and to find an organism whose parts all function together, to maximize inclusive fitness. Of course, the methods of estimating relatedness from sequenced genes initiated by Queller & Goodknight (1989) could be adapted to allow an empirical investigation of whether relatedness is indeed the same across loci. I conclude by stating briefly the contrast I am proposing between inclusive fitness and kin selection. Theory increasingly shows that inclusive fitness applies very broadly under wide assumptions, but the relatednesses required could, in principle, be affected by many factors. It makes sense to say that kin selection is operating simply, when the only or dominant force determining the relatednesses is common ancestry. In that case, relatednesses will be equal across alleles and loci, and selection will act in concert across the genome and across the organs of the body. Inclusive fitness will be a property of the individual. Where other factors influence relatedness to a significant

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Fitness optimisation extent, inclusive fitness is still being maximized, but with different selective effects at different alleles and different loci, and so an individual will not have a single inclusive fitness. An important task of theory is to establish under what conditions the simpler, coherent, situation obtains, in which inclusive fitness theory implies simple kin selection.

5. NEW WAYS TO EVOLVE ALTRUISM Hamilton (1964) was excited to discover a theory of altruism and has generated a large literature as a consequence. Many later authors have claimed to discover a new and separate theory of altruism, and all of them have been wrong. They have mistaken the strength of Hamilton’s achievement: he did not produce just one way of evolving altruism, rather he produced an analysis of how selection acts on social behaviour. All social behaviour must therefore conform to his conclusions. Let us review two recent examples of ‘new ways to evolve altruism’. Killingback et al. (2006) produced a model of a grouped population with variably sized groups and claimed that some kinds of social games showed altruism at work because of that variability. But the example fell within the assumptions of Grafen (2006a), and so the results must conform to inclusive fitness theory. Grafen (2007a) produced the relevant analysis and showed that common ancestry produced relatednesses that fully explained the results of the model. The second example is interesting new work using graph theory, where Ohtsuki et al. (2006) claim that their conclusions bear some resemblance to, but are distinct from, inclusive fitness. A number of papers (Grafen 2007c; Lehmann et al. 2007a; Grafen & Archetti 2008) show that the graph theory work can be illuminatingly understood as fully in line with inclusive fitness theory. The powerful analysis of Hamilton (1964, 1970), supported by the mathematically more explicit derivation of Grafen (2006a), allows an analysis of the natural selection of social behaviour within reasonable assumptions. This is a single theory of social behaviour for biology and is widely known and understood. Authors who produce new biological models of social behaviour would greatly assist readers by setting each new model in that canonical context.

6. FURTHER QUESTIONS The titles of the papers in this meeting suggest further questions to pursue in a theory of formal Darwinism. The theory of inclusive fitness in Grafen (2006a) applies regardless of whether the population has sexual or asexual reproduction and regardless of ploidy. It does assume that the population is of uniform ploidy, but even this assumption is made only to allow a simpler notation. Thus, it should apply to asexual populations including bacteria, and the formulae for relatedness are applicable in that case. However, this abstract connection leaves many questions unanswered. In diploids, relatedness is usually calculated using kinship links, whereas in asexual haploids, these calculations give either zero Phil. Trans. R. Soc. B (2009)

A. Grafen

3139

(for unrelated) or one (for clone-members). One mollifying factor, which allows graded outcomes, incorporates the chance that a specified individual is a clone-mate or not. But, an unfamiliar factor is that mutation may need to be tracked to calculate relatednesses. The concept of clone-mate is probably not well defined. Practical and applicable ways of calculating relatedness in bacteria will be very useful in analysing their social behaviour and will be discovered only through understanding the nature of their social behaviour more closely. A second further question is whether relatedness can be defined across species. Certainly, current models of which I am aware do not allow this. But then those models contain only one species and therefore have no inter-species interactions. It is tempting to hope that a green-beard-like mechanism could operate across species boundaries. Third, the foregoing discussion of the importance of uniformity of relatedness across loci raises a question about memes. In the genetic theory, the number of offspring is the same for all loci (assuming that they all have the same pattern of inheritance), and it is in relatedness, once social behaviour is considered, that we saw the possibility of discordance. But with cultural inheritance, the number of offspring will be different for each culturgen, and we should therefore not expect to find well-designed cultural phenotypes.

7. DISCUSSION I begin the concluding discussion with the statement that the existing theory suggests that it is reasonable to proceed with caution in assuming fitness maximization, while recognizing there may be theoretical discoveries that limit the range of circumstances in which we can expect fitness to be approximately maximized. This applies to fitness in general and to inclusive fitness when social behaviour is considered. The current methods of calculating relatednesses are probably usually fine, but this too is subject to revision. To be a little more concrete, inbreeding tends to make relatednesses different for different alleles at the same locus, a population that is not mating at random can be viewed as inbreeding, and so all real populations suffer from one of the potential causes of difficulties with fitness maximization. Next, it is worth considering what the purposes of formalizing Darwinism are. Most immediately, from the point of view of this meeting, it would be useful to know more about when the assumption of fitness maximization is reasonable, and how fitness should be defined. In the presence of social interactions, that includes the calculation of relatednesses so that inclusive fitness can be calculated. It is also important that the theoretical results should apply to circumstances such as conditional behaviour, appropriate use of information and realistic population structures and include environmental uncertainty and possibly overlapping generations. Some of these factors have been dealt with, while some have not, as discussed earlier, but my present point is that this theoretical justification for ongoing empirical work is one reason for formalizing Darwin.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3140

A. Grafen Review. Fitness optimisation

A second reason is to set down exactly what Darwin’s point was, in formal terms, to avoid doubt and make it easier for other scientists to learn about. It was noted in Darwin’s obituary published in the Society’s Proceedings that the Origin is a difficult book to read and that many more people think they understand evolution by natural selection than they in fact do. Darwin could not have formalized his point mathematically. As well as not being a good mathematician, the necessary mathematics had not yet been invented, and anyway, it is necessary to know about Mendelian genetics, which had not been discovered in 1859. My approach uses measure theory, which also had not been invented. But mathematics is the lingua franca of science, and if we want physicists and mathematicians to understand what biologists are doing, and why they are doing it, it is in my view essential to express the key points mathematically. Then they have no excuse for not understanding. This is almost a defensive reason, and it applies to many biologists as well. There are two tendencies I have encountered among biologists about Darwin that lead to a less than full-throated acceptance of his work. First, there is what we might call ‘radical empirical provisionalism’, which says, in effect, ‘Darwin may or may not have been right—we need to do more experiments to find out’. Second, there is a ‘theoretical reserve’, which says ‘Models of natural selection don’t bear out what Darwin said, so he may been approximately right, but only further theoretical work can tell how approximately’. A fully rigorous treatment of Darwin’s central point would set out Darwin’s achievement in a clear and unambiguous way. Finally, my favourite reason for formalizing Darwin is not any of those things. The grand theories of physics are all equations, with a few words to interpret the meanings of the symbols into the reader’s language of choice. Darwin’s idea, afforced by Mendelian genetics, is an extremely important scientific discovery. We will understand it better, more precisely, more generally, if we have a formal mathematical framework in which the idea can be expressed. Not a model that is an example, but a model that captures the idea at its full level of generality. One advance of Darwinism is represented by this meeting, by the ambition to explain more of the natural world in Darwinian terms. Another advance is to understand his central ideas more fully and more generally. These two directions of work support and inform each other and allow us to benefit, with ever increasing effectiveness, from the intellectual legacy of that remarkable thinker, Charles Darwin. I am grateful to Stu West, Andy Gardner, Joao Alpedrinha and Claire El Mouden for very helpful comments on the manuscript.

REFERENCES Burt, A. & Trivers, R. L. 2005 Genes in conflict: the biology of selfish genetic elements. Cambridge, MA: Harvard University Press. Crozier, R. H. 1970 Coefficients of relationship and the identity of genes by descent in the Hymenoptera. Am. Nat. 104, 216–217. (doi:10.1086/282654) Phil. Trans. R. Soc. B (2009)

Day, T. & Taylor, P. D. 1998 Unifying genetic and game theoretic models of kin selection for continuous traits. J. Theor. Biol. 194, 391–407. (doi:10.1006/jtbi.1998. 0762) Day, T. & Taylor, P. D. 2000 A generalization of Pontryagin’s maximum principle for dynamic evolutionary games among relatives. Theor. Popul. Biol. 57, 339–356. (doi:10.1006/tpbi.2000.1459) Ewens, W. J. 2004 Mathematical population genetics I. Theoretical introduction. Berlin, Germany: Springer. Fisher, R. A. 1930 The genetical theory of natural selection. Oxford, UK: Oxford University Press. OUP published in 1999 a variorum edition of the 1930 and 1958 editions. Frank, S. A. 1997a Multivariate analysis of correlated selection and kin selection, with an ESS maximization method. J. Theor. Biol. 189, 307–316. (doi:10.1006/jtbi.1997.0516) Frank, S. A. 1997b The Price equation, Fisher’s fundamental theorem, kin selection, and causal analysis. Evolution 51, 1712–1729. (doi:10.2307/2410995) Frank, S. A. 1998 The foundations of social evolution. Princeton, NJ: Princeton University Press. Gardner, A. & Grafen, A. 2009 Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659–671. (doi:10.1111/j.1420-9101.2008.01681.x) Gardner, A., West, S. A. & Barton, N. H. 2007 The relation between multilocus population genetics and social evolution theory. Am. Nat. 169, 207–226. (doi:10.1086/ 510602) Grafen, A. 1999 Formal Darwinism, the individual-asmaximising-agent analogy, and bet-hedging. Proc. R. Soc. Lond. B 266, 799–803. (doi:10.1098/rspb.1999.0708) Grafen, A. 2000 Developments of Price’s equation and natural selection under uncertainty. Proc. R. Soc. Lond. B 267, 1223– 1227. (doi:10.1098/rspb.2000.1131) Grafen, A. 2002 A first formal link between the Price equation and an optimisation program. J. Theor. Biol. 217, 75–91. (doi:10.1006/jtbi.2002.3015) Grafen, A. 2006a Optimisation of inclusive fitness. J. Theor. Biol. 238, 541 –563. (doi:10.1016/j.jtbi.2005.06.009) Grafen, A. 2006b A theory of Fisher’s reproductive value. J. Math. Biol. 53, 15–60. (doi:10.1007/s00285-0060376-4) Grafen, A. 2007a Detecting kin selection at work using inclusive fitness. Proc. R. Soc. B 274, 713–719. (doi:10. 1098/rspb.2006.0140) Grafen, A. 2007b The formal Darwinism project: a mid-term report. J. Evol. Biol. 20, 1243–1254. (doi:10.1111/j. 1420-9101.2007.01321.x) Grafen, A. 2007c Inclusive fitness on a cyclical network. J. Evol. Biol. 20, 2278–2283. (doi:10.1111/j.1420-9101. 2007.01413.x) Grafen, A. 2008 The simplest formal argument for fitness optimization. J. Gene. 87, 421 –433. (doi:10.1007/ S12041-008-0064-9) Grafen, A. & Archetti, M. 2008 Natural selection of altruism in inelastic homogeneous populations. J. Theor. Biol. 252, 694 –710. (doi:10.1016/j.jtbi.2008.01.021) Haig, D. & Westoby, M. 1989 Parent-specific gene expression and the triploid endosperm. Am. Nat. 134, 147 –155. (doi:10.1086/284971) Hamilton, W. D. 1964 The genetical evolution of social behaviour. J. Theor. Biol. 7, 1–52. (doi:10.1016/00225193(64)90038-4) Hamilton, W. D. 1970 Selfish and spiteful behaviour in an evolutionary model. Nature 228, 1218– 1220. (doi:10. 1038/2281218a0) Hamilton, W. D. 1975 Innate social aptitudes of man: an approach from evolutionary genetics. In Biosocial anthropology (ed. R. Fox), pp. 133–153. London, UK: Malaby Press.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Fitness optimisation Irwin, A. & Taylor, P. D. 2000 Evolution of dispersal in steppingstone populations with overlapping generations. Theor. Popul. Biol. 58, 321–328. (doi:10.1006/tpbi.2001.1490) Irwin, A. & Taylor, P. D. 2001 Evolution of altruism in steppingstone populations with overlapping generations. Theor. Popul. Biol. 60, 315–325. (doi:10.1006/tpbi.2001.1533) Killingback, T., Bieri, J. & Flatt, T. 2006 Evolution in groupstructured populations can resolve the tragedy of the commons. Proc. R. Soc. B 273, 1477–1481. (doi:10. 1098/rspb.2006.3476) Lack, D. 1968 Ecological adaptations for breeding in birds. London, UK: Methuen. Lehmann, L. & Balloux, F. 2007 Natural selection on fecundity variance in subdivided populations: kin selection meets bet hedging. Genetics 176, 1 –17. (doi:10. 1534/genetics.106.066910) Lehmann, L., Perrin, N. & Rousset, F. 2006 Population demography and the evolution of helping behaviors. Evolution 60, 1137–1151. Lehmann, L., Keller, L. & Sumpter, D. 2007a The evolution of helping and harming on graphs: the return of the inclusive fitness efiect. J. Evol. Biol. 20, 2284 –2295. (doi:10.1111/j.1420-9101.2007.01414x) Lehmann, L., Roze, D., Rousset, F. & Keller, L. 2007b Strong reciprocity or strong ferocity? A population genetic view of the evolution of altruistic punishment. Am. Nat. 170, 21– 36. (doi:10.1086/518568) Maynard Smith, J. 1964 Group selection and kin selection. Nature 201, 1145–1147. (doi:10.1038/2011145a0) Maynard Smith, J. & Price, G. R. 1973 The logic of animal conflict. Nature 246, 15–18. (doi:10.1038/2460145a0) Michod, R. E. & Hamilton, W. D. 1981 Coefficients of relatedness in sociobiology. Nature 288, 694–697. (doi:10. 1038/288694a0) Moran, P. A. P. 1964 On the nonexistence of adaptive topographies. Ann. Hum. Genet. 27, 383–393. Ohtsuki, H., Hauert, C., Lieberman, E. & Nowak, M. 2006 A simple rule for the evolution of cooperation on graphs and social networks. Nature 441, 502–505. (doi:10. 1038/nature04605) Orlove, M. J. 1975 A model of kin selection not involving coefficients of relationship. J. Theor. Biol. 49, 289 –310. Orlove, M. J. & Wood, C. 1978 Coefficients of relationship and coefficients of relatedness in kin selection: a covariance form for the RHO formula. J. Theor. Biol. 73, 679 –686. (doi:10.1016/0022-5193(78)90129-7) Queller, D. C. & Goodknight, K. 1989 Estimation of relatedness from allozyme data. Evolution 43, 258 –275. (doi:10. 2307/2409206)

Phil. Trans. R. Soc. B (2009)

A. Grafen

3141

Rousset, F. 2004 Genetic structure and selection in subdivided populations. Princeton, NJ: Princeton University Press. Rousset, F. & Billiard, S. 2000 A theoretical basis for measures of kin selection in subdivided populations: finite populations and localized dispersal. J. Evol. Biol. 13, 814 –825. (doi:10.1046/j.1420-9120-9101.2000. 00219.x) Seger, J. 1981 Kinship and covariance. J. Theor. Biol. 91, 191–213. (doi:10.1016/0022-5193(81)90380-5) Taylor, P. D. 1996 Inclusive fitness arguments in genetic models of behaviour. J. Math. Biol. 34, 654– 674. (doi:10.1007/BF02409753) Taylor, P. D. & Frank, S. A. 1996 How to make a kin selection model. J. Theor. Biol. 180, 27–37. (doi:10. 1006/jtbi.1996.0075) Taylor, P. D. & Irwin, A. 2000 Overlapping generations can promote altruistic behavior. Evolution 54, 1135– 1141. Taylor, P. D., Irwin, A. & Day, T. 2000 Inclusive fitness in finite deme-structured and stepping-stone populations. Selection 1, 83–93. Taylor, P. D., Day, T. & Wild, G. 2007a Evolution of cooperation in a finite homogeneous graph. Nature 447, 469–472. (doi:10.1038/nature05784) Taylor, P. D., Day, T. & Wild, G. 2007b From inclusive fitness to fixation probability in homogeneous structured populations. J. Theor. Biol. 249, 101– 110. (doi:10.1016/ j.jtbi.2007.07.006) Trivers, R. L. 1971 The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57. (doi:10.1086/406755) Trivers, R. L. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man, 1871–1971 (ed. B. Campbell), chap. 7, pp. 136–179. Chicago, IL: Aldine. Trivers, R. L. 1974 Parent –offspring conflict. Am. Zool. 14, 249–264. (doi:10.1093/icb/14.1.249) Trivers, R. L. & Hare, H. 1976 Haplodiploidy and the evolution of the social insects. Science 191, 250–263. (doi:10. 1126/science.1108197) Trivers, R. L. & Willard, D. E. 1973 Natural selection of parental ability to vary the sex of offspring. Science 179, 90–92. (doi:10.1126/science.179.4068.90) Wild, G. & Taylor, P. D. 2004 Fitness and evolutionary stability in game theoretic models of finite populations. Proc. R. Soc. Lond. B 271, 2345–2349. (doi:10.1098/ rspb.2004.2862) Williams, G. C. 1966 Adaptation and natural selection. Princeton, NJ: Princeton University Press.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3143–3155 doi:10.1098/rstb.2009.0095

Beyond society: the evolution of organismality David C. Queller* and Joan E. Strassmann Department of Ecology and Evolutionary Biology, Rice University, 6100 Main Street, Houston, TX 777005, USA The evolution of organismality is a social process. All organisms originated from groups of simpler units that now show high cooperation among the parts and are nearly free of conflicts. We suggest that this near-unanimous cooperation be taken as the defining trait of organisms. Consistency then requires that we accept some unconventional organisms, including some social insect colonies, some microbial groups and viruses, a few sexual partnerships and a number of mutualistic associations. Whether we call these organisms or not, a major task is to explain such cooperative entities, and our survey suggests that many of the traits commonly used to define organisms are not essential. These non-essential traits include physical contiguity, indivisibility, clonality or high relatedness, development from a single cell, short-term and long-term genetic cotransmission, germ – soma separation and membership in the same species. Keywords: organism; organismality; individuality; social evolution; cooperation; conflict

1. COMPETITORS, SIMPLE GROUPS, SOCIETIES AND ORGANISMS How important is cooperation in the grand scheme of life? We tend to think first of the spectacular social insects like honeybees or leaf-cutter ants, and by extension the simpler social insects and vertebrate societies that most approach them in reproductive cooperation. We might also think of human and other primate societies, whose cooperation does not ordinarily include reproductive specialization, but is remarkable in other ways. Impressive as some of these are, when we consider all three life domains on Earth—Archea, Bacteria and Eukarya with its animals, plants, protists and fungi (Woese & Olsen 1986)—one could argue that this is a pretty meagre showing for cooperation, and be tempted to chalk it up to the Darwinian imperative to compete. One might conclude that cooperation is very difficult and therefore rare. But that is much too narrow a view, for several reasons. First, we tend to restrict our attention to the organisms that are most obvious or most familiar. If we look beyond them, we find cooperation much more widely. For example, it is now becoming appreciated how often microbes are cooperative (Crespi 2001; Velicer 2003; Foster in press). Second, there are some forms of cooperation that we know are common, but that we overlook. Pollination, for example, is a very common form of cooperation between species. And we sometimes forget the sexual bond, which, for all the conflicts it engenders, is an important and pervasive form of cooperation. Finally, there is another kind of cooperation that we tend to forget because the cooperators have become so

* Author for correspondence ([email protected]). One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

intimate as to blur their boundaries. We are referring here to organisms—not to the societies made up of organisms but to the individual organism itself. We now recognize that there are several levels of organism and that each level was attained by merging formerly separate individuals from a lower level (Buss 1987; Maynard Smith & Szathma´ry 1995; Michod 2000). Multi-cellular individuals are cooperative groups of cells, eukaryotic cells are cooperative assemblages of multiple prokaryotic lineages and prokaryotic cells must have emerged by assembly of formerly independent replicators. These major transitions in evolution construct new levels of organism out of separate individuals. Thus, the theory and experience we have accumulated on animal societies over the last few decades turn out to be relevant to truly central questions about the organization of life. In this paper, we focus on organismality as a social phenomenon. The use of this slightly awkward 6-syallable noun deserves some justification. Buss used ‘individuality’ to mean something similar, a usage that has venerable roots (Huxley 1912). But the indivisibility implied by this word is among the features we want to de-emphasize, and individuality gets us unnecessarily tied up in issues that only philosophers love. ‘Unit of selection’ is relevant, but has been used for both units of heritability and units of interaction. The latter, called interactors (Hull 1980) or vehicles (Dawkins 1982), comes closer to our conception, but may sometimes be used for any phenotypic effect. Having settled on a term, we should defend the concept, for it has been suggested that little may hang on the concept of the organism (Wilson 2000). That may be true in an instrumental sense—we do not necessarily need to define the organism to do most of our work as biologists (but see Pepper & Herron 2008). But we have in mind something more basic, not something that explains, but something

3143

This journal is q 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3144

D. C. Queller & J. E. Strassmann Organismality

that needs to be explained. Probably the first thing that anyone would notice about how life is organized, even more fundamental than species groupings, is that life is divided into organisms. The organism is at least as fundamental to biology as cities or firms should be to economics, or molecules to chemistry. Explaining organismality should therefore be a central task of biology. What is it that needs explaining? A common approach to defining the organism involves listing characteristics of ‘paradigm organisms’, especially animals, and then trying to decide which combinations of these characteristics are sufficient for organismality when some are missing (see reviews by Santelices 1999; Wilson 1999; Pepper & Herron 2008). The list can include indivisibility, functional integration, contiguity, development from a single cell, membership in a single lineage, genetic uniformity, cotransmission, no partner change and germ–soma separation. Our approach is the opposite. We begin broadly with what we consider to be the essential characteristics of all organisms, and view the other traits as secondary, though potentially important in explaining how organismality was achieved in different taxa. The most salient feature of organisms is adaptation, the seeming goal-directedness that makes organisms different from merely physical entities. Not all adaptations are organismal. Meiotic drive is adaptive for the drive genes, but not for the individual in which they reside (Burt & Trivers 2006). But, such examples notwithstanding, adaptations do tend to be strongly bundled into what we call organisms. Every organism has numerous adaptations, all directed to the growth, development and reproduction of that organism (and sometimes its kin). We suggest that the essence of organismality lies in this shared purpose; the parts work together for the integrated whole, with high cooperation and very low conflict. Specifically, the organism is the largest unit of near-unanimous design; the qualifying ‘near’ is required because some conflicts, like meiotic drive, probably remain in all organisms. All organism concepts emphasize function and integration; ours differs in stressing unanimity, and in ignoring other traits. Our definition is a social one; the organism is simply a unit with high cooperation and very low conflict among its parts. That is, the organism has adaptations and it is not much disrupted by adaptations at lower levels. A related argument for the organism (or superorganism) as the unit of adaptation has recently been advanced based on a formal analysis of the relationship between the potential for selection and adaptation (Gardner & Grafen 2009). Our approach is complementary in the sense that we start at the empirical end and ask what kinds of entities might be considered organismal. It differs however in focusing on actual, rather than potential, cooperation and conflict. This distinction between potential and actual conflict has been proved fruitful in the study of insect societies (Ratnieks et al. 2006). We believe that organisms should be defined by what they actually do, and only subsequently explained by the potentials engendered by factors like high relatedness and suppression of conflict. Phil. Trans. R. Soc. B (2009)

One consequence of the decision to focus on actual behaviour is that we consider cooperation and conflict separately. In theory, the same factors that lead to high potential cooperation also lead to low potential conflict, but in reality, the two are far from perfectly correlated. For example, a clone of non-social aphids has zero potential conflict and great potential cooperation because their genetic interests are identical. In reality, they do show little conflict, but do not show much cooperation, presumably because there is rather little they can usefully do. At the other end, we have human societies and mutualistic groupings where there is extensive cooperation among non-relatives in spite of great conflict. As a framework, we use a graphical representation of societies or social groups (figures 1– 3). It provides a fourfold classification, although it is really a continuous classification in two dimensions: the extent of cooperation and the extent of conflict. We have plotted conflict on a decreasing scale in order to put the most organismal of groups in the upper-right quadrant. These traits are not quantified in a manner that justifies numerical scales. But they suffice for our qualitative and far-from-perfect judgments of where different kinds of groups fall (figures 1– 3). We hope this scheme provides a useful way to think about the issues surrounding organismality. We show this continuous space of sociality divided by two lines. Our intent is to divide the space in a way that separates organismal groups from others; we view groups placed close to the lines as hard to classify. Conventional organisms fall somewhere in the upperright quadrant, with sufficiently high cooperation and sufficiently low conflict. In the opposite quadrant reside the many groups that are unlike organisms in terms of both cooperation and conflict—too little cooperation and too much conflict. We call these competitors. At the lower right are ‘simple groups’ that have little enough conflict to be considered organisms, but lack the degree of cooperation required. Finally, we limit the term ‘societies’ (upper left) to groups, like the human groups for which the term was originally coined, that have high cooperation, but mixed in with considerable conflict. Our goal in this paper is to survey the landscape of actual conflict and cooperation, a first step in the process of explaining it in terms of theory, which would include, but not be restricted to, the amount of potential conflict. In practice, however, our knowledge of potential conflicts will sometimes colour our judgments when too little is known of actual conflicts.

2. GROUPS OF CELLS The cooperation/conflict space can be explored at several different levels (figures 1– 3). We begin with groups of cells where the issue of organismality is most obvious. Figure 1 shows how we could place some of these groups in the cooperation/conflict space. Here we are considering conflicts among cells only, leaving conflicts among genes within cells for later discussion. The classical organisms are the bilaterian animals; discrete, with highly specialized and integrated

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Organismality more cooperation

societies

organisms whale

Tasmanian devil

marmoset

Plasmodium in mosquito

biofilm

more conflict

E.coli bacteriocin producer

mouse nematode redwood liverwort Trichoplax

Volvox Dictyostelium

Myxococcus Gonium

less conflict

yeast flocs Chlamydomonas

competitors

less cooperation

simple groups

Figure 1. Cooperation and conflict in groups of cells. Only cellular conflicts are considered here, but within-cell conflicts are discussed in the text.

organs, tissues and cell types (Davidson et al. 1995). Each develops from a single fertilized cell, leading to an essentially genetically uniform group. This is why we have plotted them at the extreme low-conflict end. The only obvious cell conflicts must therefore involve new mutations. Traits like germline sequestration might have evolved to control selfish mutations (Buss 1987; Michod & Roze 1999), though the single-cell bottleneck may have been sufficient by itself (Queller 1997). Current conflicts are largely limited to cancer, though in some ways cancer seems like any other somatic mutation, in that it will be eliminated in the single-cell bottleneck leading to the next generation. But the replication of cancer cells does lend them a selfish social dimension, however short-lived (Frank & Nowak 2004). We have therefore placed large, many-celled organisms, like whales and redwoods, as having slightly more conflict than smaller ones. More serious conflict occurs only when there are violations of the single-cell bottleneck rule. In marmosets, cells regularly mix between fraternal twins in utero, and the adults can be complex chimeras that may have some conflict (Ross et al. 2007). Conflict that is a threat to organization at the organismal level arises if a cancer is transmissible, as in the fatal facial cancer of Tasmanian devils (Sarcophilus harrisii; McCallum & Jones 2006). This case points out that the single-cell bottleneck is not a sufficient explanation for organismal cooperation in animals; one also needs the ability to exclude foreign conspecific cells. We rank plants (redwoods and liverwort in figure 1) somewhat higher for conflict than most animals because growth from a multi-cellular meristem offers greater potential for competition among cells (Pineda-Krch & Lehtila 2004), though here we are speculating that this leads to some actual conflict. We also rank plants a bit lower for cooperation because their semimodular nature sometimes means many interactions are more local than global. Nevertheless, plants are still clearly organismal. Phil. Trans. R. Soc. B (2009)

D. C. Queller & J. E. Strassmann 3145

With little cellular conflict in clonal organisms, their position depends more on the extent of cooperation. In the well-known series of volvicine algae, Volvox is organismal, with cells and strong differentiation between reproductive and vegetative cells (Herron & Michod 2008). Gonium, with eight to 32 undifferentiated cells that cooperate in limited ways, such as coordinating phototaxis, might better be regarded as a simple group. Chlamydomonas represents the end of the spectrum occupied by many other single-celled organisms. Their nearest neighbours are presumably often not clonemates, and they may have little cooperation or overt conflict if they are sufficiently dispersed. However, one of the most spectacular recent developments in the field of social evolution is the growing realization of how social many unicellular microbes are (Crespi 2001; Velicer 2003; West et al. 2006; Foster in press). The pinnacles of sociality among microbes may be the curiously parallel life cycles of the eukaryote Dictyostelium (Queller et al. 2003; Shaulsky & Kessin 2003) and the prokaryote Myxococcus (Velicer & Stredwick 2002). In each, when feeding cells starve, they aggregate and go through a developmental process that results in fruiting bodies where a fraction of the cells survive as hardy spores. It is somewhat easier to make the case for organismality for Dictyostelium fruiting bodies because a fraction of the cells (approx. 25% in Dictyostelium discoideum) give up their lives to form a stalk that enhances spore dispersal. In Myxococcus xanthus, it is less clear why as many as 90 per cent of the cells die during fruiting body formation (Wireman & Dwarkin 1977). One the other hand, Dictyostelium is more solitary in the remainder of the life cycle, while Myxococcus is very social during that time. It is a swarm feeder, effectively hunting in packs (Velicer 2003). The amount of conflict in these two organisms deserves further study, but it may be minimal enough for them to qualify as organismal. Because fruiting bodies form by aggregation, there is considerable potential conflict, at least if unrelated cells commonly aggregate. In both D. discoideum and M. xanthus, we know that there is considerable genetic potential for cheaters that reap the benefits of fruiting while letting others pay the costs (Velicer et al. 2000; Santorelli et al. 2008), some of which could destroy sociality (Velicer et al. 1998; Ennis et al. 2000; Gilbert et al. 2007). But actual conflict may be rather low. In Dictyostelium, there is some separation between clones during fruiting (Mehdiabadi et al. 2006; Ostrowski 2008), but it is incomplete and chimeras do form in the laboratory. However, fruiting bodies from the wild are known to be mostly, though not exclusively, clonal. An indication of the more general importance of social cooperation is that it turns out to be significant in any microbe that is studied with sufficient intensity. Escherichia coli and Saccharomyces cerevisiae were chosen as model systems for their ease of study. We tend to think of them both as independent cells that grow nicely in broth, which they are, but they also have cooperation, which may be particularly important in more natural environments. For example, E. coli

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3146

D. C. Queller & J. E. Strassmann Organismality

often makes biofilms in which cells are held together in a common matrix (Reisner et al. 2006). Under lownutrient conditions, E. coli groups can undergo a coordinated transition to a stationary phase in which growth ceases, avoiding a tragedy of the commons, though there are mutants that cheat and grow faster, something that tends to be advantageous only when rare (Vulic & Kolter 2001). Many E. coli clones produce bacteriocin toxins that kill the producing cell and nearby non-clonemates, to the benefit of clonemates (Kerr et al. 2002). The budding yeast S. cerevisiae also has multiple cooperative behaviours. As with many microbes, some products are secreted in ways that benefit neighbours. Secreted invertase hydrolyses sucrose, part of which is captured by the secreter, but as much as 99 per cent of it goes to others (Greig & Travisano 2004; Gore et al. 2009). Under certain kinds of stress, some yeast form protective clusters called flocs, in which the cells tightly adhere, and protection is offered by both the physical barrier of the outside cells and physiological changes (Smukalla et al. 2008). With their modest array of cooperative behaviours, mixed presumably with some conflict, it seems reasonable to regard E. coli and yeast as modest societies. But, of course, the placement would depend on the kind of group. A yeast floc would be closer to organismal than yeast growing in an exponential phase in broth. An E. coli group consisting of mixed killers and victims would have to be considered competitive, but the killer clone considered by itself is an altruist that gives its life for relatives. The placement of other microbial species on our axes is even more problematic because we have an even less complete picture of the range of their behaviours. But it is clear that the kinds of cooperative behaviours we see in E. coli and yeast—secretion of public goods, biofilms, bacteriocin toxins—are quite widespread (Crespi 2001; Velicer 2003; West et al. 2006; Foster in press). Microbial groups are often dispersed and unclearly bounded, which may work against them becoming organismal. Biofilms are at least contiguous, and may sometimes be organisms, but we need more information as to their balance of cooperation and conflict (Xavier & Foster 2007). For more dispersed microbes, quorum sensing often precedes activation of cooperative pathways, and the limit of the group may be viewed as those who sense the quorum. One case where contiguity may not be necessary for organismality involves groups that live inside another organism. This gives microbes the potential for action at a distance; if they can affect the host, then they can affect each other. For example, the malaria parasite Plasmodium falciparum manipulates its mosquito host, benefiting all the parasites in the same mosquito. In the infectious stage, infected mosquitoes bite more often, mediated in part by the parasites’ interference with the enzyme apyrase that the mosquito uses to keep its victim’s blood from clotting (Koella et al. 1998). In the pre-infectious stage, at least in Plasmodium yoelli, the parasites have the opposite effect of reducing the mosquito’s propensity to bite, thus avoiding danger until the parasites are ready (Anderson et al. 1999). When you factor in Phil. Trans. R. Soc. B (2009)

suppression of the host immune system and reduction in host fecundity, which preserves resources for the parasite (Lefe`vre et al. 2006), an argument can be made for organismality. This high cooperation occurs with the high, but less than perfect, relatedness of P. falciparum within a mosquito (Razakandrainibe et al. 2005). Given the widespread incidence of host manipulation among other parasites (Thomas et al. 2004) and the fact that some of them will generally have clonal infections, we expect that such dispersed organisms are probably common. Similar effects can be achieved via beneficial effects on the host, but we will consider these later as parts of possible mutualistic organisms.

3. GROUPS OF GENES IN CELLS Replicating molecules getting together in cells was presumably one of the early steps in the evolution of life (Koonin & Martin 2005). That transition occurred so long ago and is so fixed that we hesitate to say more than that it is an important example of unrelated replicators becoming organismal. However, issues of cooperating genes remain. The general argument about Plasmodium being organismal can easily be extended to many viruses. Scientists who focus on metabolism argue that its absence in viruses means that they are not even alive. Evolutionary biologists tend to disagree, because viruses evolve by natural selection. Whether alive or not, they can be organismal by our definition. A virus contains a small set of genes, each of which performs a key task in manipulating the host into making virus copies. Although cheating is possible in viruses, particularly in mixed infections (Turner & Chao 1999), it seems likely that many function as fully cooperative units. Conflict among genes is also an issue for larger organisms. In our discussion of clonal multi-cellular organisms above, we considered only conflict among the cells. However, there is sometimes substantially more conflict among the genes within cells (Hurst 1998; Hurst & Werren 2001; Burt & Trivers 2006). With sufficient information, we could add this kind of conflict in figure 1, or alternatively construct another figure that shows cooperation and conflict at the genetic level in those organisms, but we will be content to make some general points, most of which concern sex. The first is that we should not forget what a cooperative venture sexual reproduction is. Here we are referring not to the cooperation of the parents, which we will treat later, but of the cooperation that results after two unrelated sets of genes are put together in the zygote. We think of organisms as being built by genetically identical lineages of cells, and we tend to forget that, with every sexual event, an organism is initiated by the horizontal amalgamation of two cells that have great potential conflict but little actual conflict. Clearly, high relatedness is not essential for organismality. The potential for conflict among such unrelated genes is very high, but it is normally strongly limited in several ways. The fairness of meiosis normally limits within-organism competition between alleles.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

D. C. Queller & J. E. Strassmann 3147

Organismality Selfish coalitions among alleles are limited by recombination and by the fact that genes are not usually marked by parent of origin. Nevertheless, some conflicts do arise when these conditions are violated. Meiotic-drive alleles gain by defeating the fair meiosis (Lyttle 1991). Some can impose significant costs on the organism, but spread nevertheless because of within-organism advantage. We do not know how common meiotic-drive mutants are because many may sweep to fixation, at which point they are unobservable. However, fixation is most likely when the drive imposes little cost at the organismal level, so even if these are common, they do not destroy organismal cooperation. Conflicts can also occur when parental genes are differentially marked by methylation. Maternally and paternally derived genes (matrigenes and patrigenes; Queller 2003) may be selected differently if they have different relatedness coefficients (Haig 2000). There is considerable evidence that patrigenes fight harder for their embryo than matrigenes when the resources gained come at the expense of half siblings (who share matrigenes but not patrigenes). Oddly, such within-organism conflicts are predicted to be most diverse in those paragons of cooperation at a higher level, social insect workers (Queller 2003), though these predictions remain to be tested. Perhaps the most pervasive genetic conflicts within individuals come from selfish DNA, like transposable elements. In asexual organisms, these conflicts tend to be small because they are vertically inherited. But in sexual organisms, the selfish elements can move horizontally from one lineage to another and can therefore spread more readily (Smith 2001). If we were to use a majority-rule criterion, many eukaryotes might not be considered organismal; about half the human genome is derived from transposable elements (Lander et al. 2001). However, we use actual conflict as the criterion, and most of these transposons are inactive and presumably not very costly, and some may perform useful functions (Lander et al. 2001). High costs do occur in periods when elements enter a virgin territory, as when the Drosophila melangaster p-element entered new populations, until suppressors evolve (Adams 1981). The main lesson here is that the significant conflicts occur in undoubted organisms, so we cannot use the mere existence of conflict to rule out organismality of other types. In fact, selfish DNA may pose greater problems for more complex organisms because they tend to be larger, with smaller population sizes and weaker between-organism selection. High cooperation and low conflicts do not go strictly hand-in-hand; sometimes high cooperation gives room for conflicts to operate without doing too much damage.

4. GROUPS OF MULTI-CELLULAR INDIVIDUALS Multi-cellular individuals make up the most familiar groups and societies. Figure 2 shows tentative placements of some groups of multi-cellular individuals. Most of the groups that are the topic of this symposium are societies with complex mixtures of cooperation and conflict. Polistes wasps and naked Phil. Trans. R. Soc. B (2009)

more cooperation

societies

organisms

human city human band

honeybee

Melipona bee

man of war anglerfish mates coral

Polistes wasp albatross mates Botryllus barn swallow mates naked mole rat African wild dog social aphid chimpanzee brain fluke in ant more less

conflict

conflict

Drosophila mates bedbug mates gull colony

strawberry clone

sage grouse lek aphid clone

male fig wasp

dandelion clone

competitors

less cooperation

simple groups

Figure 2. Cooperation and conflict in groups of multicellular individuals. Only conflicts between individuals are considered.

mole rats (Heterocephalus glaber) have sophisticated cooperation that includes food sharing, group defence, nest building and cooperative brood care of the progeny of one or a few group members. Yet, they are also driven by conflicts. The reproductive position is coveted and subordinates have to be kept in place, often by force or the threat of force. Other cooperative breeders have varying degrees of cooperation and conflict. Humans fall in this category. Humans are the most successful cooperators; a human city is arguably far more cooperative and integrated than groups of any other species, but that is not sufficient to make it organismal. It is far too full of conflicts. More traditional human bands cooperate in less sophisticated ways but may have less conflict. With numerous ties of both direct and indirect reciprocity, strong between-group competition and within-group homogenization by cultural norms, such bands may approach organism status, though in our view they probably still have too much conflict. Are there groups that, given our definition, ought to be considered organismal? The question is obviously not ridiculous once it is recognized that these organisms themselves evolved out of groups several times over (Buss 1987; Maynard Smith & Szathma´ry 1995). Perhaps, the easiest case to argue is one like the Portuguese man o’war (Physalia physalis). Although it is commonly viewed as a colony of polyps, it is hard to deny its organismality in any functional sense. It is a clonal unit, with polyps budding from other polyps in a regular developmental sequence, and remaining attached. The polyps are quite specialized, with some forming a sail for locomotion, others making tentacles to capture prey and others specialized for digestion. All these work on behalf of the polyps that are specialized for reproduction. The whole cannot function without the parts. No conflict is expected among the parts, and as far as we know, none exists. Somewhat less organismal are colonies of the tunicate Botryllus schlosseri, which as a chordate is a close cousin of ours. The colony is made up of perhaps 20

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3148

D. C. Queller & J. E. Strassmann Organismality

zooids, each quite like a solitary tunicate with its own gut, heart, nervous system and gonads. But the colony members share a common tunic and a common cloaca and an excurrent siphon. Moreover, there is a vascular system connecting the zooids. Again colonies form by budding, but they can also fuse with genetically similar, but not necessarily identical, colonies. When such chimeras form, there can be conflict because sometimes one partner takes over the gonadal tissue of the other. These colonies share two features—contiguity and genetic identity—that make it easy to view them as organisms, but we view neither as definitive. It has been suggested that an aphid clone or a dandelion clone ought to be considered to be individuals, but we do not consider them to be organisms. Though there is no potential conflict among members of a dandelion clone, they do little or nothing for each other. Indeed, though we have placed them among simple groups, dandelion clones may really be competitors. The units of this ‘individual’ are unattached, being derived from apomcitic seeds, and unless they have some mechanism to recognize clonemates, will compete with them just as much as with non-relatives. Plant clones that remain connected, like strawberries, probably have a greater claim to being organismal units, but unless there is considerable integration, we would argue that they are not organisms. If, for example, resource transfer is mainly limited to the establishment of new ramets, the ‘adult’ ramets are best considered separate organisms that reproduce. An aphid clone that remains bunched may be somewhat more cooperative than separated dandelions, for example in evolving warning colouration, but as the level of cooperation appears small, we would not classify such clones as organisms. In contrast, social aphids, where some individuals specialize as soldiers and defend the colony, usually inside a plant gall, could be considered organisms. But even here the cooperation seems mostly limited to defence and is less sophisticated than social insects like Polistes. Such colonies may include a small amount of conflict, as mixing with other clones occurs. The social aphids also raise the question of contiguity. Though usually confined to a gall, the aphids are not attached in the manner of a conventional organism, but we do not consider that grounds for excluding their colonies as organismal because our working definition concerns only the degrees of cooperation and conflict. However, the best cases to argue this point are not the social aphids, with their fairly rudimentary organization, but some of the highly eusocial insects, such as the honeybee (Apis mellifera). There is in fact a long tradition of recognizing certain social insect colonies as organismal (Wheeler 1911; Seeley 1989; Wilson & Sober 1989; Strassmann & Queller 2007; Ho¨lldobler & Wilson 2008). Wheeler’s (1911) use of the term ‘organism’ has been largely supplanted by ‘superorganism’, but we concur with Wheeler’s usage because we have come to learn that all of our familiar organisms are superorganisms. If superorganism is meant to highlight the common features of high cooperation, low conflict and unanimity of action, why reserve that term for the top level only? If instead Phil. Trans. R. Soc. B (2009)

the intent is to imply that these are somehow different, that they have not quite reached the level of organisms, we really ought to call them quasi-organisms. A honeybee colony includes tens of thousands of workers. Every aspect of colony life—foraging, brood care, defence, nest construction—is coordinated by communication and social feedbacks towards the end of promoting the queen’s reproduction. The glue is not adhesion molecules and intercellular signals, but attachment to a particular place, pheromones, chemical recognition cues, as well as various visual, tactile and smell signals of work done and undone. In arguing for organismal status for honeybee colonies, we are not only arguing for organisms with unattached individuals, but also that those individuals need not be genetically identical. By accepting the eukaryotic cell as an organism, we have already acknowledged that genetically distinct partners can become organismal. The genetic differences in a social insect colony lead to potential conflicts, but in honeybees, the actual conflicts appear to be very small (Ratnieks et al. 2006; Strassmann & Queller 2007). New queens fight to the death, but at little cost to the colony. Occasionally a worker will lay an egg, but this is kept rare by the effective policing of other workers who eat such eggs (Ratnieks & Visscher 1989). These seem to have as little effect on organismal function as some of the genetic conflicts in conventional organisms (see below). Although honeybees are the best studied social insect, it seems likely that many others, especially some ants and termites, approach or attain similar levels of cooperation and integration and should also be considered organismal. Some, however, have sufficient conflicts to make this status questionable. Stingless bees of the genus Melipona, among the honeybee’s closest relatives, have high degrees of cooperation but offer an interesting contrast (Engels & Imperatriz-Fonseca 1990; Peters et al. 1999). In some species, workers commonly compete to lay their own eggs, and these are not effectively policed (To´th et al. 2004). Moreover, because all larvae are given about the same amount of food, they are not forced into a worker role. As a result, 10– 20% opt to become queens, even though a new queen is only rarely needed to replace the old one or to found a new colony (Wenseleers & Ratnieks 2004). These selfish superfluous queens are ultimately killed by workers, but their production must exert a significant cost to the colony. We therefore place Melipona near the organism-society boundary. As we argued above for microbes, another category of separated organisms comes from groups of parasites. The brain fluke Dicrocoelium dendriticum parsitizes snails, ants and sheep. When an ant ingests a cyst left by a snail, the hundreds of juvenile flukes adaptively divide labour. Most encyst in the haemocoel but one invades the suboesophageal ganglion, causing the ant to climb up a blade of grass where it can be eaten by a sheep (Moore 2002). The ganglion fluke dies, but by manipulating the host, it benefits the rest. Provided there is also little or no conflict among the flukes, this level of cooperation probably qualifies as organismal. The ant of course is not part

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Organismality of this organism; its adaptations are to produce new ants, and to try to avoid being eaten. A final category that should be considered is mated pairs. Mating itself is a cooperative act, but it typically also involves conflict. The conflict is extreme in bedbugs (Cimex lectularius), where insemination takes place through the body wall of the female (Stutt & Siva-Jothy 2001), and it can take more subtle forms, such as a Drosophila melanogaster male chemically inducing his mate to increase her short-term reproduction at the expense of her lifespan (Chapman 2001). Because of the higher cooperation involved in joint parental care, we classify barn swallow (Hirundo rustica) mates as societies, but they still have considerable conflict, including infidelities and mate switching (Møller 2002). The whole tale of sexual conflict is too vast to be covered here (Arnqvist & Rowe 2005), but we should consider cases where conflict is minimal. Arguably, albatross pairs that mate for life, after an elaborate and extended courtship, could be considered organismal. We would need to see whether even the low probability of partner change or loss leads to conflict in pairs. We would also need to consider the impact of extra-pair copulations, which do occur, but which seem not to affect pair bonds—females do not seem to seek or benefit from them ( Jouventin et al. 2007). The clearest cases, however, are when mates fuse. For example, in some, but not all, species of anglerfish, a dwarf male becomes attached for life to a female (Pietsch 2005). He bites onto the female, and outgrowths from both the upper and lower jaws, which are apparently unsuitable for normal feeding, eventually fuse with the female, with apparent vascular connections to feed the male. Neither sex becomes reproductively active unless attached to the other. Such males are sometimes called ‘parasitic’ but in fact they seem to serve cooperatively as male gonads, without any known conflicts with the female, and with few expected in those species where one male is the norm.

5. MULTI-SPECIES GROUPS We do not generally think of organisms consisting of two species. But they are possible in principle if we employ a functional definition of high cooperation and low conflict. And there is the precedent that everyone accepts. The eukaryotic cell comprises the original cell and the mitochondrion, likely to have originated as an alphaproteobacterium related to Rickettsia (Margulis 1970). Plastids, including chloroplasts, came from cyanobacteria in a similar fashion. A long evolutionary history of cooperation has resulted in physical intimacy, private partnership, complete physiological interdependence and division of function. Neither exists without the other, and mitochondria and their host cells speciate together. Inheritance is not identical because mitochondria are usually inherited only through the maternal line. This difference makes some residual conflict of interest possible, particularly with regard to sex allocation. For example, mitochondrial genes cause male sterility in plants (Frank 1989), although most mitochondrial genes do things that are good for the host. Phil. Trans. R. Soc. B (2009)

D. C. Queller & J. E. Strassmann 3149 more cooperation

societies

organisms

host–mitochondrion legume–Rhizobium yucca moth–yucca

Buchnera–aphid lichen Atta–fungus fig–wasp

cleaner fish–host

plant–pollinator ant–aphid

more conflict human–helminths ant–captive worker

grass–endophyte squid–vibrio

less conflict

oxpecker ox cattle egret–cattle

malaria–mosquito

Wolbachia–arthropod warbler–cuckoo

katydid–wasp

brain fluke–ant lion–gazelle

competitors

less cooperation

simple groups

Figure 3. Cooperation and conflict in two-species groups.

This widely accepted precedent means we should ask how many other organisms have been formed from multiple species. Of course, most two-species interactions are not organismal. Some have low enough overt conflict but do not have sufficient cooperation. These are often simple byproduct mutualisms (Sachs et al. 2004). Katydids associate with wasp nests during the day, presumably gaining protection from the bellicose wasps (Downhower & Wilson 1973). Cattle egrets (Bubulcus ibis) profit from cattle movements that stir up insects and also remove ticks from the cattle (Fogarty & Hetrick 1973). Clearly, the egrets obtain more food when cattle are present, and there is little cost (Burger & Gochfeld 1982). But both can survive independently. Red-billed oxpeckers (Buphagus erythrorhynchus), by contrast, are obligate on large African mammals, but they are parasites, not mutualists, and take more blood, mucus and wax than ticks and parasites (Weeks 2000). However organismal the brain flukes may be in their manipulations of the host, the host is not part of that organism because it has not evolved to cooperate. Most host– pathogen and predator– prey relationships would fall in this category. So would socially parasitic relationships like cuckoos and their warbler hosts, or ants and the captive workers (sometimes called slaves) from other species (Brandt et al. 2005; Kru¨ger 2007). There are of course many mutualistic species pairs that perform essential services for each other. The question is how much ongoing conflict there is and which, if any, have so little conflict that they are essentially organismal. Conflicts are readily apparent in many of them (Herre et al. 1999; Bronstein et al. 2006; Douglas 2008). Cleaner fish perform the essential service of removing parasites from their clients, but also cheat by taking client tissue (Bshary & Grutter 2002; Bshary & Scha¨ffer 2002). Legumes are highly dependent on associated Rhizobia bacteria for nitrogen, supplying carbon compounds in return, but multiple bacterial genotypes associate with every plant and conflicts ensue (Sachs et al. 2004). Plant sanctions—cutting off oxygen to weak nitrogen

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3150

D. C. Queller & J. E. Strassmann Organismality

suppliers—helps keep the bacteria in line, but the conflict involved is probably enough for them not to be considered organismal, despite the intricate cooperation (Kiers & Denison 2008; Sachs & Simms 2008). Many flowering plants are completely dependent on animal pollinators to differing degrees of specificity ( Johnson & Steiner 2000). The pollinator gets food in return for transferring pollen, but there are often conflicts over how long to stay on one flower or plant, how much pollen the pollinators should take for themselves and how far the pollinator should travel (Bronstein 2001). Interestingly, it can sometimes be the very diversity of partners that stabilizes mutualisms because the optimal partners can be chosen repeatedly (Foster & Kokko 2006). However, we believe there are mutualistic associations, other than the eukaryotic cell, that should be considered organismal. At the very least, there are other endosymbiontic bacteria that live inside host cells and reproduce along with them. Some twospecies organisms involve bacteria that are housed in a small minority of the host organism’s cells: the bacteriocytes. Buchnera aphidicola produces essential amino acids for its aphid host and also migrates to ovarian cells for vertical transmission (Wernegreen & Moran 2001; Moran 2007). Buchnera aphidicola has a tiny genome, under 650 kb, specialized on what aphids cannot make, while many gene products needed by the symbiont are now made by the aphid, further binding their interests. Some potential conflicts remain over reproduction, but the aphid seems to effectively limit symbiont competition, so that little actual conflict occurs (Frank 1996). Acquiring functionality by adopting a bacterium intracellularly has happened repeatedly in insects, particularly those that ingest plant sap (Moran 2007). Many of these cases can be viewed as two-species organisms. However, some show greater signs of conflict and some endosymbionts, like Wolbachia, manipulate their arthropod hosts in various ways and do not generally provide any advantage (Charlat et al. 2003). Let us consider a range of possible organisms with decreasing physical intimacy. First, symbionts need not be intracellular. The term symbiosis was first applied to lichens (Sapp 2004), an ancient symbiosis, seen in a 600 million year old fossil (Yuan et al. 2005). Lichenized fungi have captured algae (85%), cyanobacteria (10%) or both (4%) to provide carbon (Honegger 1998), which usually grow together via coordinated meristems (Sanders 2006). The fungal partner often optimizes exposure to light, and maintains moisture for the photosynthesizing partner, a relationship that makes lichens the first colonizers in many harsh habitats and dominant in 8 per cent of habitats (Honegger 1998). The fungi at least have lost the ability for independent existence (Lutzoni et al. 2001). Sometimes lichenized fungi and their partners are codispersed as fragments of the lichen thallus, but this is not obligate (Nelson & Gargas 2007). Many different fungal species use the same species of algae, or cyanobacteria, and they have not cospeciated (Piercey-Normore & DePriest 2001; Hyva¨rinen et al. 2002; Zoller & Lutzoni 2003). Yet it is hard to argue that lichen symbioses have less than organismal levels of cooperation. Little work seems to have Phil. Trans. R. Soc. B (2009)

been done on possible conflicts, though it seems the fungus has a controlling role. Another plant –fungal association that might sometimes be organismal are certain grass–endophyte mutualisms. Endophytes confer resistance to herbivores, particularly under drought conditions (Clay et al. 2005) and are commonly transmitted vertically through seeds, though they can be lost at several different life-stage transitions (Afkhami & Rudgers 2008). Other organismal mutualisms may be even less connected. Although most pollination mutualisms are not nearly organismal, a few specialized ones may approach it. Specialization is particularly common in nursery pollination systems (Dufay¨ & Anstett 2003) where pollinators lay eggs on the plant. Moths that pollinate both senita cacti (Fleming & Holland 1998) and yucca (Pellmyr et al. 1996) provide specialized pollination services, but then exact a cost by parasitizing seeds. Fig wasp pollinators go one step further by both pollinating and having their offspring transport pollen away from the same inflorescence, thus giving the fig an incentive to raising wasps. This mutualism has persisted for at least 60 million years and has diverged into over 800 species of figs and a corresponding number of symbiotic wasp species (Silvieus et al. 2007; Rønsted et al. 2006). Cospeciation is very close for figs and pollinator wasps, though there is some evidence that the wasps speciate first, and the figs lag behind (Silvieus et al. 2007; Herre et al. 2008). By contrast, figs and parasitic wasps that are just as dependent on figs do not show evidence of cospeciation (Silvieus et al. 2007). Conflict between fig and pollinator wasps exists but is usually controlled. Each wasp larva destroys an ovule, amounting to around half of all ovules (Herre 1989). Variable style length may be the fig’s way of avoiding excessive loss of ovules, though this may be more because of the increased handling time than because they are unreachable by the wasps (Yu et al. 2004). Figs may limit access to syconia to one or a few pollinators, thus limiting competition, including the production of excess sons, which are wasteful for the fig. Experiments show that deposition of pollen increases wasp success by some mechanism not involving fruit abortion (Herre et al. 2008). Male success of the fig correlates with the number of wasps produced (Herre 1989). It may be that the interests of the figs and pollinators are sufficiently aligned to consider them organismal. Vertical cotransmission must be helpful in evolving organismality in two-species systems, but is it essential? Many highly developed mutualisms involve symbionts acquired from the environment. Bobtail squid are dependent on Vibrio fischeri bacteria for their light production, which allows them to camouflage themselves from predators lower in the water column (Nyholm & McFall-Ngai 2004). The squid are not born with their bacteria but instead take them up in a highly specific and coordinated process involving squid structures that have evolved just for this purpose, the uptake of the preferred bacterium, and not the thousands of others (Visick & McFallNgai 2000; Visick & Ruby 2006). Every morning, the squid physically expels 90 per cent of the bacteria (Visick & McFall-Ngai 2000). This appears to keep

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Organismality the bacteria in an active growth phase, which is when they best luminesce (Visick & McFall-Ngai 2000). We need further study of conflict in this and other systems that acquire their symbionts, but it is possible that these might be considered to be organismal. As with other organisms, mutualistic ones do not necessarily need to be physically cohesive. Granting that social insect colonies can be organismal, the boundaries of that organism could include other species. Atta, a fungus-growing ant, is entirely dependent on its basidiomycete fungus for food (Mueller et al. 2001) and the fungus requires dispersal via a special pouch of an Atta queen when she begins a new colony. When the ants of a colony die, the fungus is quickly overrun by bacteria and competing fungi, so the fates of fungus and ant are closely intertwined. Like the figs and fig wasps, they have partially congruent phylogenies (Mikheyev et al. 2006). Conflicts are likely to be low, though sex ratios could be contested because, like mitochondria, the fungus is maternally transmitted (Mueller 2002). Nevertheless, on our functional grounds, the interests of ants and fungi in a colony seem best viewed as organismally merged. Indeed, one might add in the bacteria that live in specialized crypts in the ant’s exoskeleton and protect the fungus (Currie et al. 2006). We by no means think that we should extend the concept of organismality further out to communities or to the biosphere in general (Lovelock 2000). But there are likely some highly cooperative multi-species assemblages with minimal conflict.

6. DISCUSSION The ‘major transitions’ tradition (Buss 1982; Maynard Smith & Szathma´ry 1995) has helped us to see that organisms could be prokaryotic groups of replicators, eukaryotic alliances with prokaryotic organelles, groups of cells and even societies. These steps have been critically important, but evolution does not work by major transitions alone. If evolution occasionally crafts new organismal alliances that are truly transformational, it seems likely that it will much more frequently craft new organismal alliances that are not necessarily revolutionary in the history of life, but organismal nevertheless. And if we want to understand the evolution of organismality, we should pay attention to the examples that are recent, to the ones that are unconventional and even to the ones that are incomplete. Our survey is a step in that direction, and it reveals a number of interesting points. Control of conflict is viewed as one of the major prerequisites for a major transition. We agree that it is important, but low conflict and high cooperation are not the same thing; that is why we gave them separate axes in figures 1 –3. Some groups have low conflict, but never become cooperative enough to be deemed organismal (clones of dandelions or nonsocial aphids, Gonium). Others have very high cooperation in spite of considerable conflict, with human societies being one familiar example. Organismality can evolve from either direction. Volvox and eusocial aphids evolved by adding cooperation in Phil. Trans. R. Soc. B (2009)

D. C. Queller & J. E. Strassmann 3151

simple groups lacking conflict, like Gonium or nonsocial aphids. Honeybees, in contrast, evolved by reducing conflicts in societies of more primitive bees. Conflict can certainly be a threat to cooperation, but the two are not incompatible. High cooperation may even sometimes be what allows significant conflict. Melipona bees are in no danger of extinction despite their internecine battles, presumably because their colonies work so well in other ways. Vertebrates can sustain a huge amount of selfish junk DNA precisely because they are such successful cooperative entities in most respects. Moreover, some conflict is not very disruptive to organismality (Travisano & Velicer 2004). The social amoeba D. discoideum has numerous cheater mutants that produce normal fruiting bodies on their own (Santorelli et al. 2008), so the spread of such cheaters would not destroy cooperation. This is one way in which our organism concept differs from a unit of selection; there can sometimes be considerable withinindividual selection favouring such facultative cheaters without much damage to adaptation at a higher level. Having defined organisms by what we consider to be their essential traits, high cooperation and very low conflict, we can now examine what is not essential to near conflict-free cooperation. Although most conventional organisms have a coherent body, contiguity is neither necessary nor sufficient for organismality. Dictyostelium and Myxococcus show that organisms can be assembled instead from formerly distinct parts. We argue further that not only can organisms come together from separate entities, but they may also be organismal without attachment. Honeybees retain their independent bodies, but a growing consensus views them, and some other social insects, as superorganisms (Seeley 1989; Wilson & Sober 1989; Strassmann & Queller 2007; Ho¨lldobler & Wilson 2008). Many microbial systems deserve similar consideration. Social insects also show that clonality is not essential. In fact, relatedness is not required for organismality, as we know from the fusion of unrelated sperm and egg to form a new organism. Employing the same logic at a higher level, there seems to be no reason to exclude a hermaphroditic anglerfish that assembles from a separate male and female. Indeed, we suggest that organismal aggregates do not even have to be of the same species. Again, conventional usage supports this, with the eukaryotic cell and some of its organelles providing the historical precedent. For consistency, we need to consider whether other mutualisms evolve to be organismal. Some, like aphid –Buchnera, seem fairly clear, particularly when there is vertical transmission to reduce conflicts. But vertical transmission does not seem necessary. Figs and their fig wasps have horizontal cotransmission (female wasp carries pollen). Though we need to probe more deeply for conflicts, it seems likely that organisms can even form using symbionts freshly acquired from the environment, as in the squid and its Vibrio bacteria or corals and the zooxanthellae. An implication of the above is that the organism does not necessarily reside in a single lineage. Two branches of the evolutionary tree can fuse to form an

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3152

D. C. Queller & J. E. Strassmann Organismality

organism, and the two components may not speciate together. This may seem odd, but it is consistent with our view of a bacterium as a good organism, even though plasmids and even chunks of chromosomal genes hop between lineages at varying rates. Though we are proposing a novel definition for organisms, there may be a place for multiple organism concepts, just as there are multiple species concepts (Wilson 1999; Pepper & Herron 2008). But it seems to us that the simplest way to include all conventionally accepted organisms is to define them in terms of extensive cooperation with little conflict. For consistency, this requires us to broaden our conception of organismality. This is more than a semantic game of deciding that X is an organism and Y is not. The scientific community could choose any name they want for entities with extensive cooperation and very little conflict, but the existence of such entities is one of the striking features of life, and explaining how they evolve should therefore be an important task. That task will be hamstrung if we restrict ourselves to those transitions that happened to have major consequences. Expanding our view beyond the major transitions suggests that there are multiple ways to achieve this degree of functional integration, and that many of the conditions that might be thought to be essential are not. We thank the US National Science Foundation for support (EF-0328455, DEB-0816690). We thank Stuart West, Andy Gardner and Max Burton-Chellew for comments on the manuscript.

REFERENCES Adams, G. 1981 Search paths of fireflies in two dimensions. Fla. Entomol. 64, 66–73. (doi:10.2307/3494601) Afkhami, M. & Rudgers, J. 2008 Symbiosis lost: imperfect vertical transmission of fungal endophytes in grasses. Am. Nat. 172, 405 –416. (doi:10.1086/589893) Anderson, R., Koella, J. & Hurd, H. 1999 The effect of Plasmodium yoelii nigeriensis infection on the feeding persistence of Anopheles stephensi Liston throughout the sporogonic cycle. Proc. R. Soc. Lond. B 266, 1729– 1733. Arnqvist, G. & Rowe, L. 2005 Sexual conflict. Princeton, NJ: Princeton University Press. Brandt, M., Foitzik, S., Fischer-Blass, B. & Heinze, J. 2005 The coevolutionary dynamics of obligate ant social parasite systems –between prudence and antagonism. Biol. Rev. 80, 251 –267. (doi:10.1017/S1464793104006669) Bronstein, J. 2001 The exploitation of mutualisms. Ecol. Lett. 4, 277– 287. (doi:10.1046/j.1461-0248.2001.00218.x) Bronstein, J., Alarco´n, R. & Geber, M. 2006 The evolution of plant –insect mutualisms. New Phytol. 172, 412 –428. (doi:10.1111/j.1469-8137.2006.01864.x) Bshary, R. & Grutter, A. 2002 Asymmetric cheating opportunities and partner control in a cleaner fish mutualism. Anim. Behav. 63, 547 –555. (doi:10.1006/anbe.2001. 1937) Bshary, R. & Scha¨ffer, D. 2002 Choosy reef fish select cleaner fish that provide a high-quality service. Anim. Behav. 63, 557 –564. (doi:10.1006/anbe.2001.1923) Burger, J. & Gochfeld, M. 1982 Host selection as an adaptation to host-dependent foraging success in the cattle egret (Bubulcus ibis). Behaviour 79, 212–229. (doi:10. 1163/156853982X00265) Burt, A. & Trivers, R. 2006 Genes in conflict: the biology of selfish genetic elements. Cambridge, MA: Belknap. Phil. Trans. R. Soc. B (2009)

Buss, L. W. 1982 Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc. Natl Acad. Sci. USA 79, 5337–5341. (doi:10.1073/pnas.79.17. 5337) Buss, L. W. 1987 The evolution of individuality. Princeton, NJ: Princeton University Press. Chapman, T. 2001 Seminal fluid-mediated fitness traits in Drosophila. Heredity 87, 511 –521. (doi:10.1046/j.13652540.2001.00961.x) Charlat, S., Hurst, G. & Merc¸ot, H. 2003 Evolutionary consequences of Wolbachia infections. Trends Genet. 19, 217 –223. (doi:10.1016/S0168-9525(03)00024-6) Clay, K., Holah, J. & Rudgers, J. 2005 Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proc. Natl Acad. Sci. USA 102, 12 465 –12 470. (doi:10.1073/pnas.0503059102) Crespi, B. J. 2001 The evolution of social behaviour in microorganisms. Trends Ecol. Evol. 16, 178 –183. (doi:10.1016/S0169-5347(01)02115-2) Currie, C. R., Poulsen, M., Mendenhall, J., Boomsma, J. J. & Billen, J. 2006 Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311, 81–85. (doi:10.1126/science.1119744) Davidson, E., Peterson, K. & Cameron, R. A. 1995 Origin of bilaterian body plans: evolution of developmental regulatory mechanisms. Science 270, 1319–1325. (doi:10.1126/ science.270.5240.1319) Dawkins, R. 1982 The extended phenotype. Oxford, UK: W. H. Freeman. Douglas, A. 2008 Conflict, cheats and the persistence of symbioses. New Phytol. 177, 849–858. (doi:10.1111/j. 1469-8137.2007.02326.x) Downhower, J. F. & Wilson, D. E. 1973 Wasps as a defense mechanism of katydids. Am. Midl. Nat. 89, 451–455. (doi:10.2307/2424050) Dufay¨, M. & Anstett, C. 2003 Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos 100, 3 –14. (doi:10.1034/j.1600-0706.2003.12053.x) Engels, W. & Imperatriz-Fonseca, V. L. 1990 Caste development, reproductive strategies and control of fertility in honey bees and stingless bees. In Social insects: an evolutionary approach to castes and reproduction (ed. W. Engels), pp. 166– 230. Berlin, Germany: Springer-Verlag. Ennis, H. L., Dao, D. N., Pukatzki, S. U. & Kessin, R. H. 2000 Dictyostelium amoebae lacking an F-box protein form spores rather than stalk in chimeras with wild type. Proc. Natl Acad. Sci. USA 97, 3292 –3297. (doi:10.1073/pnas.050005097) Fleming, T. & Holland, J. 1998 The evolution of obligate pollination mutualisms: senita cactus and senita moth. Oecologia 114, 368–375. (doi:10.1007/s004420050459) Fogarty, M. & Hetrick, W. 1973 Summer foods of cattle egrets in North Central Florida. Auk 90, 268 –280. Foster, K. In press. Social behaviour in microorganisms. In Social behaviour: genes, ecology and evolution (eds T. Szekely, A. Moore & J. Komdeur). Cambridge, UK: Cambridge University Press. Foster, K. & Kokko, H. 2006 Cheating can stabilize cooperation in mutualisms. Proc. R. Soc. B 273, 2233– 2239. (doi:10.1098/rspb.2006.3571) Frank, S. 1989 The evolutionary dynamics of cytoplasmic male sterility. Am. Nat. 133, 345–376. (doi:10.1086/ 284923) Frank, S. 1996 Host control of symbiont transmission: the separation of symbionts into germ and soma. Am. Nat. 148, 1113– 1124. Frank, S. A. & Nowak, M. A. 2004 Problems of somatic mutation and cancer. BioEssays 26, 291–299. (doi:10. 1002/bies.20000)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Organismality Gardner, A. & Grafen, A. 2009 Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659– 671. (doi:10.1111/j.1420-9101.2008. 01681.x) Gilbert, O. M., Foster, K. R., Mehdiabadi, N. J., Strassmann, J. E. & Queller, D. C. 2007 High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc. Natl Acad. Sci. USA 104, 8913– 8917. (doi:10.1073/pnas.0702723104) Gore, J., Hyuk, H. & van Oudenaarden, A. 2009 Snowdrift game dynamics and facultative cheating in yeast. Nature 459, 253 –256. (doi:10.1038/nature07921) Greig, D. & Travisano, M. 2004 The prisoner’s dilemma and polymorphism in yeast SUC genes. Proc. R. Soc. Lond. B 271, S25 –S26. (doi:10.1098/rsbl.2003.0083) Haig, D. 2000 The kinship theory of genomic imprinting. Ann. Rev. Ecol. Syst. 31, 9–32. (doi:10.1146/annurev. ecolsys.31.1.9) Herre, E. 1989 Coevolution of reproductive characteristics in 12 species of New World figs and their pollinator wasps. Experentia 45, 637–647. Herre, E., Knowlton, N., Mueller, U. & Rehner, S. 1999 The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol. Evol. 14, 49– 53. (doi:10.1016/S0169-5347(98)01529-8) Herre, E., Jande´r, K. & Machado, C. 2008 Evolutionary ecology of figs and their associates: recent progress and outstanding puzzles. Annu. Rev. Ecol. Evol. Syst. 39, 439 –358. (doi:10.1146/annurev.ecolsys.37.091305. 110232) Herron, M. & Michod, R. 2008 Evolution of complexity in the volvocine algae: transitions in individuality through darwin’s eye. Evolution 62, 436–451. (doi:10.1111/j. 1558-5646.2007.00304.x) Ho¨lldobler, B. & Wilson, E. 2008 The superorganism: the beauty, elegance, and strangeness of insect societies. New York, NY: W. W. Norton. Honegger, R. 1998 The lichen symbiosis—what is so spectacular about it? Lichenologist 30, 193 –212. Hull, D. 1980 Individuality and selection. Ann. Rev. Ecol. Syst. 11, 311 –332. (doi:10.1146/annurev.es.11.110180. 001523) Hurst, L. D. 1998 Selfish genes and meiotic drive. Nature 391, 223. (doi:10.1038/34523) Hurst, G. & Werren, J. 2001 The role of selfish genetic elements in eukaryotic evolution. Nat. Rev. Genet. 2, 597 –606. (doi:10.1038/35084545) Hyva¨rinen, M., Ha¨rdling, R. & Tuomi, J. 2002 Cyanobacterial lichen symbiosis: the fungal partner as an optimal harvester. Oikos 98, 498– 504. (doi:10.1034/j.16000706.2002.980314.x) Johnson, S. & Steiner, K. 2000 Generalization versus specialization in plant pollination systems. Trends Ecol. Evol. 15, 140 –143. (doi:10.1016/S0169-5347(99) 01811-X) Jouventin, P., Charmantier, A., Dubois, M.-P., Jarne, P. & Bried, J. 2007 Extra-pair paternity in the strongly monogamous wandering albatross Diomedea exulans has no apparent benefits for females. Ibis 149, 67–78. Kerr, B., Riley, M. A., Feldman, M. W. & Bohannan, B. J. M. 2002 Local dispersal promotes biodiversity in a real-life game of rock– scissors –paper. Nature 418, 171– 174. (doi:10.1038/nature00823) Kiers, E. & Denison, R. 2008 Sanctions, cooperation, and the stability of plant –rhizosphere mutualisms. Annu. Rev. Ecol. Evol. Syst. 39, 315 –236. Koella, J. C., Sørensen, F. L. & Anderson, R. A. 1998 The malaria parasite, Plasmodium falciparum, increases the frequency of multiple feeding of its mosquito vector Anopheles gambiae. Proc. R. Soc. Lond. B 265, 763 –768. Phil. Trans. R. Soc. B (2009)

D. C. Queller & J. E. Strassmann 3153

Koonin, E. & Martin, W. 2005 On the origin of genomes and cells within inorganic compartments. Trends Genet. 21, 647–654. (doi:10.1016/j.tig.2005.09.006) Kru¨ger, O. 2007 Cuckoos, cowbirds and hosts: adaptations, trade-offs and constraints. Phil. Trans. R. Soc. B 362, 1873–1886. (doi:10.1098/rstb.2006.1849) Lander, E. et al. 2001 Initial sequencing and analysis of the human genome. Nature 409, 860–921. (doi:10.1038/ 35057062) Lefe`vre, T., Koella, J., Renaud, F., Hurd, H., Biron, D. & Thomas, T. 2006 New prospects for research on manipulation of insect vectors by pathogens. PLoS Pathog. 2, e72. (doi:10.1371/journal.ppat.0020072) Lovelock, J. 2000 Gaia: A new look at life on earth. Oxford, UK: Oxford University Press. Lutzoni, F., Pagel, M. & Reeb, V. 2001 Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411, 937–940. (doi:10.1038/35082053) Lyttle, T. 1991 Segregation distorters. Annu. Rev. Genet. 25, 511–557. (doi:10.1146/annurev.ge.25.120191. 002455) Margulis, L. 1970 Origin of eukaryotic cells. New Haven, CT: Yale University Press. Maynard Smith, J. & Szathma´ry, E. 1995 The major transitions in evolution. Oxford, UK: W. H. Freeman. McCallum, H. & Jones, M. 2006 To lose both would look like carelessness: Tasmanian devil facial tumour disease. PLoS Biol. 4, 1671– 1674. Mehdiabadi, N. J. et al. 2006 Kin preference in a social microorganism. Nature 442, 881 –882. (doi:10.1038/ 442881a) Michod, R. 2000 Darwinian dynamics: evolutionary transitions in fitness and individuality. Princeton, NJ: Princeton University Press. Michod, R. E. & Roze, D. 1999 Cooperation and conflict in the evolution of multicellularity. Heredity 86, 1 –7. (doi:10.1046/j.1365-2540.2001.00808.x) Mikheyev, A., Mueller, U. & Abbot, P. 2006 Cryptic sex and many-to-one coevolution in the fungus-growing ant symbiosis. Proc. Natl Acad. Sci. USA 103, 10 702 –10 706. (doi:10.1073/pnas.0601441103) Møller, A. 2002 Sexual selection in the barn swallow. In Model systems in behavioural ecology: integrating conceptual, theoretical, and empirical approaches (ed. L. Dugatkin), pp. 359–377. Princeton. NJ: Princeton University Press. Moore, J. 2002 Parasites and the behaviour of animals. Oxford, UK: Oxford University Press. Moran, N. 2007 Symbiosis as an adaptive process and source of phenotypic complexity. Proc. Natl Acad. Sci. USA 104, 8627–8633. (doi:10.1073/pnas. 0611659104) Mueller, U. 2002 Ant versus fungus versus mutualism: antcultivar conflict and the deconstruction of the attine ant–fungus symbiosis. Am. Nat. 160, S67–S98. (doi:10. 1086/342084) Mueller, U., Schultz, T., Currie, C., Adams, R. & Malloch, D. 2001 The origin of the attine ant –fungus mutualism. Q. Rev. Biol. 76, 169–197. (doi:10.1086/ 393867) Nelson, M. & Gargas, A. 2007 Dissociation and horizontal transmission of codispersing lichen symbionts in the genus Lepraria (Lecanorales: Stereocaulaceae). New Phytol. 177, 264– 275. Nyholm, S. & McFall-Ngai, M. 2004 The winnowing: establishing the squid–Vibrio symbiosis. Nat. Rev. Microbiol. 2, 632–643. (doi:10.1038/nrmicro957) Ostrowski, E. 2008 Kin discrimination increases with genetic distance in a social amoeba. PLoS Biol. 6, 2376–2382.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3154

D. C. Queller & J. E. Strassmann Organismality

Pellmyr, O., Thompson, J., Brown, J. & Harrison, R. 1996 Evolution of pollination and mutualism in the yucca moth lineage. Am. Nat. 148, 827 –847. (doi:10.1086/ 285958) Pepper, J. & Herron, M. 2008 Does biology need an organism concept? Biol. Rev. 83, 621 –627. Peters, J. M., Queller, D. C., Imperatriz-Fonseca, V. L., Roubik, D. W. & Strassmann, J. E. 1999 Mate number, kin selection and social conflicts in stingless bees and honey bees. Proc. R. Soc. Lond. B 266, 379 –384. (doi:10.1098/rspb.1999.0648) Piercey-Normore, M. & DePriest, P. 2001 Algal switching among lichen symbioses. Am. J. Bot. 88, 1490–1498. (doi:10.2307/3558457) Pietsch, T. 2005 Dimorphism, parasitism, and sex revisited: modes of reproduction among deep-sea ceratoid anglerfishes (Teleostei: Lophiiformes). Ichthy. Res. 52, 207 –236. (doi:10.1007/s10228-005-0286-2) Pineda-Krch, M. & Lehtila, K. 2004 Costs and benefits of genetic heterogeneity within organisms. J. Evol. Biol. 17, 1167–1177. Queller, D. 1997 Cooperators since life began. Book review of: The major transitions in evolution, by J. Maynard Smith and E. Szathmary. Q. Rev. Biol. 72, 184 –188. (doi:10.1086/419766) Queller, D. C. 2003 Theory of genomic imprinting conflict in social insects. BMC Evol. Biol. 3, 15. (doi:10.1186/ 1471-2148-3-15) Queller, D. C., Foster, K. R., Fortunato, A. & Strassmann, J. E. 2003 Cooperation and conflict in the social amoeba, Dictyostelium discoideum. In Social insects and sociogenetics (eds T. Kikuchi, T. Kubo & S. Higashi), pp. 173 –200. Sapporo, Japan: Hokkaido University Press. Ratnieks, F. L. W. & Visscher, P. K. 1989 Worker policing in the honeybee. Nature 342, 796–797. (doi:10.1038/342796a0) Ratnieks, F., Foster, K. R. & Wenseleers, T. 2006 Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581–608. (doi:10.1146/annurev.ento.51.110104.151003) Razakandrainibe, F. G., Durand, P., Koella, J. C., De Meeu¨s, T., Rousset, F., Ayala, F. J. & Renaud, F. 2005 ‘Clonal’ population structure of the malaria agent Plasmodium falciparum in high-infection regions. Proc. Natl Acad. Sci. USA 102, 17 388 –17 393. (doi:10.1073/ pnas.0508871102) Reisner, A., Ho¨ller, B., Molin, S. & Zechner, E. 2006 Synergistic effects in mixed Escherichia coli biofilms: conjugative plasmid transfer drives biofilm expansion. J. Bacteriol. 188, 3582–3588. (doi:10.1128/JB.188.10. 3582-3588.2006) Rønsted, N., Weiblen, G., Clement, W., Zerega, N. & Savolainen, V. 2006 Reconstructing the phylogeny of figs (Ficus, Moraceae) to reveal the history of fig pollination mutualism. Symbiosis 45, 45–56. Ross, C., French, J. A. & Orti, G. 2007 Germ-line chimerism and paternal care in marmosets (Callithrix kuhlii). Proc. Natl Acad. Sci. USA 104, 6278–6282. (doi:10. 1073/pnas.0607426104) Sachs, J. & Simms, E. 2008 The origins of uncooperative bacteria. Oikos 117, 961–966. (doi:10.1111/j.00301299.2008.16606.x) Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull, J. J. 2004 The evolution of cooperation. Q. Rev. Biol. 79, 135 –160. (doi:10.1086/383541) Sanders, W. 2006 A feeling for the superorganism: expression of plant form in the lichen thallus. Bot. J. Linn. Soc. 150, 89–99. (doi:10.1111/j.1095-8339.2006.00497.x) Santelices, B. 1999 How many kinds of individual are there? Trends Ecol. Evol. 14, 152 –155. (doi:10.1016/S01695347(98)01519-5) Phil. Trans. R. Soc. B (2009)

Santorelli, L. et al. 2008 Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451, 1107 –1110. (doi:10.1038/ nature06558) Sapp, J. 2004 The dynamics of symbiosis: an historical overview. Can. J. Bot. 82, 1046– 1056. (doi:10.1139/b04-055) Seeley, T. D. 1989 The honey bee colony as a superorganism. Am. Sci. 77, 546 –553. Shaulsky, G. & Kessin, R. 2003 The cold war of the social amoebae. Curr. Biol. 17, R684 –R692. (doi:10.1016/j. cub.2007.06.024) Silvieus, S., Clement, W. & Weiblen, G. 2007 Cophylogeny of figs, pollinators, gallers, and parasitoids. In Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects (ed. K. Tilmon), pp. 225–239. Berkeley, CA: University of California Press. Smith, J. 2001 The social evolution of bacterial pathogenesis. Proc. R. Soc. Lond. B 268, 61–69. (doi:10.1098/rspb.2000. 1330) Smukalla, S. et al. 2008 FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell 135, 726 –737. (doi:10.1016/j.cell.2008.09.037) Strassmann, J. & Queller, D. 2007 Insect societies as divided organisms: the complexities of purpose and crosspurpose. Proc. Natl Acad. Sci. USA 104, 8619– 8626. (doi:10.1073/pnas.0701285104) Stutt, A. D. & Siva-Jothy, M. T. 2001 Traumatic insemination and sexual conflict in the bed bug Cimex lectularius. Proc. Natl Acad. Sci. USA 98, 5683–5687. (doi:10. 1073/pnas.101440698) Thomas, F., Adamo, S. & Moore, J. 2004 Parasitic manipulation: where are we and where should we go? Behav. Proc. 68, 185 –189. (doi:10.1016/j.beproc.2004. 06.010) To´th, E., Queller, D. C., Dollin, A. & Strassmann, J. E. 2004 Conflict over male parentage in stingless bees. Insect Soc. 51, 1–11. (doi:10.1007/s00040-003-0707-z) Travisano, M. & Velicer, G. J. 2004 Strategies of microbial cheater control. Trends Microbiol. 12, 72–78. (doi:10. 1016/j.tim.2003.12.009) Turner, P. E. & Chao, L. 1999 Prisoner’s Dilemma in an RNA virus. Nature 398, 441–443. (doi:10.1038/18913) Velicer, G. J. 2003 Social strife in the microbial world. Trends Microbiol. 11, 330 –337. (doi:10.1016/S0966842X(03)00152-5) Velicer, G. & Stredwick, K. 2002 Experimental social evolution with Myxococcus xanthus. Antonie Van Leeuwenhoek 81, 155–164. (doi:10.1023/A:1020546130033) Velicer, G. J., Kroos, L. & Lenski, R. E. 1998 Loss of social behaviours by Myxococcus xanthus during evolution in an unstructured habitat. Proc. Natl Acad. Sci. USA 95, 12 376 –12 380. (doi:10.1073/pnas.95.21.12376) Velicer, G. J., Kroos, L. & Lenski, R. E. 2000 Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404, 598–601. (doi:10.1038/35007066) Visick, K. & McFall-Ngai, M. 2000 An exclusive contract: specificity in the Vibrio fischeri –Euprymna scolopes partnership. J. Bacteriol. 182, 1779–1787. (doi:10.1128/JB. 182.7.1779-1787.2000) Visick, K. & Ruby, E. 2006 Vibrio fischeri and its host: it takes two to tango. Curr. Opin. Microbiol. 9, 1 –7. Weeks, P. 2000 Red-billed oxpeckers: vampires or tickbirds? Behav. Ecol. 11, 154–160. (doi:10.1093/beheco/11.2.154) Wenseleers, T. & Ratnieks, F. L. W. 2004 Tragedy of the commons in Melipona bees. Proc. R. Soc. Lond. B 271, S310 –S312. (doi:10.1098/rsbl.2003.0159) Wernegreen, J. & Moran, N. 2001 Vertical transmission of biosynthetic plasmids in aphid endosymbionts (Buchnera). J. Bacteriol. 183, 785–790. (doi:10.1128/ JB.183.2.785-790.2001)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Organismality West, S. A., Griffin, A. S., Gardner, A. & Diggle, S. P. 2006 Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4. (doi:10.1038/nrmicro1461) Wheeler, W. M. 1911 The ant colony as organism. J. Morph. 22, 307–325. (doi:10.1002/jmor.105022 0206) Wilson, J. 1999 Biological individuality: the identity and persistence of living entities. Cambridge, UK: Cambridge University Press. Wilson, J. 2000 Ontological butchery: organism concepts and biological generalizations. Phil. Sci. 67, S301 –S311. (doi:10.1086/392827) Wilson, D. S. & Sober, E. 1989 Reviving the superorganism. J. Theor. Biol. 136, 337 –356. (doi:10.1016/S00225193(89)80169-9) Wireman, J. & Dwarkin, M. 1977 Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. J. Bacteriol. 129, 798 –802.

Phil. Trans. R. Soc. B (2009)

D. C. Queller & J. E. Strassmann 3155

Woese, C. & Olsen, G. 1986 Archaebacterial phylogeny: perspectives on the urkingdoms. Syst. Appl. Microbiol. 7, 161–177. Xavier, J. & Foster, K. 2007 Cooperation and conflict in microbial biofilms. Proc. Natl Acad. Sci. USA 104, 876– 881. (doi:10.1073/pnas.0607651104) Yu, D., Ridley, J., Jousselin, E., Herre, E., Compton, S., Cook, J., Moore, J. & Weiblen, G. 2004 Oviposition strategies, host coercion and the stable exploitation of figs by wasps. Proc. R. Soc. Lond. B271, 1185–1195. (doi:10.1098/rspb.2003.2630) Yuan, X., Xiao, S. & Taylor, T. 2005 Lichen-like symbiosis 600 million years ago. Science 308, 1017–1020. (doi:10. 1126/science.1111347) Zoller, S. & Lutzoni, F. 2003 Slow algae, fast fungi: exceptionally high nucleotide substitution rate differences between lichenized fungi Omphalina and their symbiotic green algae Coccomyxa. Mol. Phylogenet. Evol. 29, 629–640. (doi:10.1016/S1055-7903(03)00215-X)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3157–3168 doi:10.1098/rstb.2009.0055

Review

Social evolution in micro-organisms and a Trojan horse approach to medical intervention strategies Sam P. Brown1, Stuart A. West1, Stephen P. Diggle2 and Ashleigh S. Griffin1,* 1

Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK School of Molecular Medical Sciences, Centre for Biomolecular Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK

2

Medical science is typically pitted against the evolutionary forces acting upon infective populations of bacteria. As an alternative strategy, we could exploit our growing understanding of population dynamics of social traits in bacteria to help treat bacterial disease. In particular, population dynamics of social traits could be exploited to introduce less virulent strains of bacteria, or medically beneficial alleles into infective populations. We discuss how bacterial strains adopting different social strategies can invade a population of cooperative wild-type, considering public good cheats, cheats carrying medically beneficial alleles (Trojan horses) and cheats carrying allelopathic traits (anti-competitor chemical bacteriocins or temperate bacteriophage viruses). We suggest that exploitation of the ability of cheats to invade cooperative, wild-type populations is a potential new strategy for treating bacterial disease. Keywords: altruism; bacteriocins; cheat; cooperation; spite; virulence

1. INTRODUCTION Bacteria and other micro-organisms exhibit a wide range of social behaviours. Technological advances made by microbiologists have overturned the long held assumption that micro-organisms live relatively independent, unicellular lives. Instead, it appears that individual cells can communicate and cooperate to perform activities such as dispersal, foraging, construction of biofilms, reproduction, chemical warfare and signalling (reviewed by Crespi 2001; Velicer 2003; Webb et al. 2003; Keller & Surette 2006; Kolter & Greenberg 2006; West et al. 2006; Diggle et al. 2007a; Foster 2007; Hense et al. 2007; West et al. 2007a; Williams et al. 2007; Brown & Buckling 2008; MacLean 2008; Popat et al. 2008). These social behaviours are comparable to the more familiar patterns of sociality in metazoans such as social insects and cooperative breeding vertebrates, discussed in the other articles in this volume. Furthermore, these social traits are critical to determining the damage caused by microbial parasites to their hosts (virulence) due to their importance for microbial growth. However, evolutionary theory shows how cooperation is easily lost in competition against selfish strategies (Hamilton 1964; Trivers 1971). Consider a population of unconditional cooperators in which an uncooperative,

* Author for correspondence ([email protected]). One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

relatively selfish cheater arises through mutation or migration. In the absence of any mechanism to punish non-cooperators, the cheater benefits from the cooperative behaviour of its social partners, without paying any cost. Consequently, genes for cheating have greater fitness than the genes for cooperation, and spread through the population, even though this will lead to a decline in population fitness (figure 1). A large body of theoretical and empirical work has examined the conditions under which cooperation can be favoured, via direct or indirect (kin selected) benefits (reviewed by Sachs et al. 2004; Lehmann & Keller 2006; West et al. 2007b), and how this may be applied to microbes (West et al. 2006). Experimental studies using microbes show how cheats can invade populations of wild-type cooperators (Strassmann et al. 2000; Velicer et al. 2000; Greig & Travisano 2004; Griffin et al. 2004; Harrison et al. 2006; Diggle et al. 2007b; Ross-Gillespie et al. 2007; Sandoz et al. 2007; Ku¨mmerli et al. 2009a,b; Rumbaugh et al. 2009). The most common way for microbes to cooperate with one another is by the release of exoproducts, such as proteases and toxins, that facilitate bacterial growth (West et al. 2007a). Exoproducts can benefit any individual in the local group and so can be considered as public goods, which can be exploited by cheats that do not produce the exoproduct. Possibly, the best studied exoproducts from a evolutionary perspective are iron-scavenging siderophore molecules in Pseudomonas aeruginosa (West & Buckling 2003). Mutants (cheats or

3157

This journal is # 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3158

S. P. Brown et al.

W

W WWW WW

Review. Trojan horse mutation or migration

W W WWc

selection

W

c

W W

c c

selection

c c

c c

declining average fitness Figure 1. Natural selection favours selfish individuals who do not cooperate. Consider a population of wild-type cooperators (‘W’) in which an uncooperative, selfish cheater (‘c’) arises through mutation or migration. In a mixed population, the selfish cheater benefits from the cooperative behaviour of the cooperators, without paying the cost. Consequently, the selfish cheater has a higher fitness than the cooperators and spreads through the population, despite the fact that this leads to a decline in mean fitness (redrawn from Nowak 2006; West et al. 2007b). This figure illustrates the problem of cooperation—our main aim in this paper is to discuss how this problem can be exploited for medical intervention strategies.

free-riders) that do not produce siderophores are able to exploit those produced by others, and hence increase in frequency in mixed populations that contain both cooperators and cheats (Griffin et al. 2004; Harrison et al. 2006). Another layer of complexity is that the release of many exoproducts is regulated in a cell density-dependent manner via diffusible signal molecules by a process that has been termed quorum sensing (QS). Experimental studies in both laboratory cultures and mouse hosts have shown that QSdefective mutants, that do not signal or respond to signal, are able to benefit from public goods produced by others and increase in frequency, even in conditions where they would normally show only very limited growth (Diggle et al. 2007b; Sandoz et al. 2007; Rumbaugh et al. 2009). Cooperative behaviours in bacteria are of particular interest because they are fundamental to the success and virulence of bacterial infections. Exoproducts are commonly referred to as ‘virulence factors’ because their production is associated with virulence, either through direct damage to the host, or through aiding bacterial growth (West et al. 2007a). Infections containing mutants that do not produce exoproducts are often characterized by lower virulence. For example, QS has been demonstrated to be important for virulence in several species of bacteria including P. aeruginosa (Rumbaugh et al. 1999, 2009), Burkholderia pseudomallei (Ulrich et al. 2004), Vibrio cholerae (Lin et al. 2007) and Staphylococcus aureus (Fleming et al. 2006). In nature, we do not see cheats dominate because infections that contain few cooperators will be less productive and relatively poor in transmission and initiating new colonies (Brown & Johnstone 2001; Diggle 2007a; Diggle et al. 2007b; Rumbaugh et al. 2009; see figure 2 and discussion). However, the population structure of pathogen populations that favours the evolution of cooperative, virulence traits (figure 2) presents an opportunity for the artificial introduction of social cheats, and consequent disruption of microbial-cooperative virulence traits (Andre´ & Godelle 2005). We review the possibility of exploiting the ability of cheater strains to invade cooperative, wild-type populations in medical intervention strategies. Firstly, the introduction of an invasive cheat can lead to direct reduction in parasite virulence, as well as a reduced Phil. Trans. R. Soc. B (2009)

bacterial population size, that may make the infection more susceptible to other intervention strategies (Harrison et al. 2006; West et al. 2006; Diggle et al. 2007b; Kurzban & Egreth 2008; Rumbaugh et al. 2009). A second possibility is that cheats could act as ‘Trojan horses’, vehicles for the introduction of alleles such as sensitivity to antibiotics, into a population that was previously antibioticresistant (figure 3). Another possible use for the Trojan horse approach would be to introduce a lethal toxin under the control of an inducible promoter, which when activated, would eliminate both cooperators and cheats. We present a number of heuristic models to formally illustrate the possibilities as simply as possible.

2. POPULATION DYNAMICS OF SOCIAL TRAITS In this section, we show how social traits may be exploited as part of a medical intervention strategy. We first focus on cooperative social traits, such as the production of exoproducts (cooperative public goods). In §2a we show how a cheat that does not produce some exoproduct can invade a wild-type population, consisting of cooperative individuals who do produce the exoproduct. This can lead to a direct decrease in parasite virulence (due to loss of exoproduct production), as well as a smaller population size that may be more susceptible to other intervention strategies (e.g. antibiotic treatment). In §2b we extend this, by showing how such traits can also be used to hitch-hike useful traits (e.g. antibiotic vulnerabilities) into the population. In §2c we examine the complications that can occur when within-host populations are spatially structured, which will reduce the ability of non-cooperative cheats to spread. We then consider how harmful, or spiteful, social traits may be exploited, such as anti-competitor chemicals, bacteriocins and temperate bacteriophage viruses. In §2d, we show that the addition of bacteriocin production to a cheat or Trojan horse lineage can favour the engineered strain’s invasion, particularly in spatially structured host compartments. We then discuss how related forms of microbial spite involving the production of temperate phages can generate distinct invasion advantages to an engineered strain,

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

S. P. Brown et al.

Review. Trojan horse (a)

3159

natural population W C C C

W WW W WWW

W WW C WW

W WW W WWW

W WW W WWW

C C

W WW W WWW

W WW W WWW

W WW W WWW

W WW W WWW

manipulated population

(b) W C C C

C

C

W WW W WWW

C

C

W WW W WWW

C C

C

C C W

C

C WW C CW

W WW W WWW

C

W C C

Figure 2. Manipulation of natural population dynamics of social behaviour to reduce virulence of bacterial infection. The top row of mice represents the initial population of hosts which are infected with either wild-type (W in green) or cheat (C in red) strains of bacteria. The arrows represent transmission to new hosts, represented by the lower row of mice. (a) Illustrates the fact that wild-type strains are more productive and better at transmission and colonization of new hosts. This promotes the maintenance of cooperative behaviour in the global population: even though cheats can outcompete wild-type strains within hosts, groups containing only wild-type will be more productive and more likely to spread to new hosts (this requires that wildtype and cheats tend to be in different hosts—high relatedness). (b) Illustrates how inoculation of hosts containing wild-type infections with cheater strains can counteract the natural population dynamics of cooperators and cheats.

in particular, allowing rapid invasion from rare into relatively unstructured foci of infection.

(a) A cheat that does not produce exoproducts ( public goods) Possibly, the most common form of social behaviour in microbes is the production of exoproducts. Exoproducts are manufactured by an individual, but can then be used by the individual and its neighbours. For example, bacteria produce numerous factors that are released into the environment beyond the cell membrane, such as siderophores to scavenge iron, proteases to digest proteins and b-lactamases to inactivate antibiotics (see table 1 of West et al. 2007a). Exoproducts lead to the problem of cooperation because they are metabolically costly to the individual to produce but provide a benefit to all the individuals Phil. Trans. R. Soc. B (2009)

in the local group or population, as well as the individual that produced them, and hence can be thought of as public goods (West et al. 2006). Such exoproducts are often termed ‘virulence factors’, because their production is linked with damage to the host, either through some direct effect, or through facilitating parasite growth. We begin with a simple ecological model of withinhost competition between a cooperative, resident wild-type lineage that produces a certain exoproduct, and an invading cheat lineage that does not produce the exoproduct, but can profit equally from its presence within the host. Such cheats can be genetically engineered, artificially selected for and are found in natural populations. For illustration, we assume no within-host population structuring—this assumption is relaxed below. The within-host cell densities of the wild-type and cheat are W and C, respectively, and

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3160

S. P. Brown et al.

Review. Trojan horse

(a)

(b) W W W W W W W

W W W W W W W

T C

C

T

infected hosts

inoculation with cheater strains

C

C

treatment with antibiotics

C C

Trojan cheat

cheat

Figure 3. Introducing antibiotic resistance with a Trojan horse approach. (a) This panel shows a host infected with wild-type strains (W in green) inoculated with a strain of cheats (C in red) that are able to invade and outcompete the wild-type infection. The resulting population of bacteria is less virulent, less productive and more vulnerable to eradication by the host’s immune system. However, this cheat strain (C) is still resistant to antibiotics. (b) This panel represents a host inoculated with a cheater strain (T in red) that has also been genetically engineered to have antibiotic sensitivity restored, allowing the infection to be eradicated by antibiotic treatment. We have called this kind of strain a Trojan horse cheat: host ¼ Troy; cheat ¼ wooden horse; antibiotic sensitive gene ¼ Greeks. This representation shows the best possible outcome: in all likelihood, the cheats will not completely eradicate the wild-type cells and so, following antibiotic treatment, the resistant population could recover. Even if resistant strains survive, the infective population may be reduced to levels that can be eradicated by immune system of the host and there is theoretically no limit to the number of times antibiotic-sensitive strains could be inoculated.

we describe their change in time via the following ordinary differential equations: dW ¼ W ðð1 NÞ x þ bW =NÞ; dt dC ¼ Cðð1 NÞ þ bW =NÞ: dt

ð2:1Þ

Here, x is the cost of exoproduct production, b the benefit (weighted by frequency of wild-type, W/N) and N total population within the host (N ¼ W þ C). In the absence of any exoproduct production (x ¼ b ¼ 0), we have a simple pair of Lotka – Volterra competition equations (Otto & Day 2007) with carrying capacity and maximum growth rate normalized to 1 (and the remaining parameters are scaled appropriately). In contrast, a pure cooperative wild-type lineage expends resources on enhancing both its net growth rate and carrying capacity, given b . x (e.g. through the secretion of shared exoproducts). Despite gains to both growth rate and carrying capacity, a stability analysis (Otto & Day 2007) demonstrates that a population of pure cooperators (at carrying capacity, W* ¼ 1 þ b 2x) is vulnerable to invasion by rare cheats, and that the only stable equilibrium in model one is pure Phil. Trans. R. Soc. B (2009)

cheats, at C* ¼ 1 and extinction of the wild-type, W* ¼ 0 (see also Andre´ & Godelle 2005). From a therapeutic perspective, the replacement of W by C leads to a reduction of bacterial density, and potentially more significantly, the cessation of cooperative virulence factor production (figure 4a). This predicted invasion of cheats, with a subsequent reduction of virulence has been observed with QS of cheats in the bacterium P. aeruginosa when infecting mice (Rumbaugh et al. 2009).

(b) Trojan horse cheats The ability of a cheat lineage to invade a patch (i.e. a host) of cooperators opens the potential for hitchhiking useful traits (e.g. antibiotic vulnerabilities) along with the socially dominant cheat strategy into the microbial pathogen population—a Trojan horse cheat. This is analogous in some ways to the suggestion that selfish genetic elements can be used to genetically engineer natural populations (Turelli & Hoffman 1999; Burt 2003). We modify our above model by inserting an engineered vulnerability into the cheat lineage, imposing a direct growth cost q (if the engineered trait provides a direct growth benefit, this would be

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Trojan horse 2.0

(a)

(b)

(c)

(d)

(e)

(f)

S. P. Brown et al.

3161

1.5 1.0

cell density, virulence intensity

0.5

2.0 1.5 1.0 0.5

2.0 1.5 1.0 0.5 0

50

100 150 time (arb. units)

200

0

50

100 150 time (arb. units)

200

Figure 4. Invasion of cheats and Trojan horses into an established resident infection and consequent virulence (model 4). Black lines, wild-type (W ). Blue lines, cheats or Trojan horses (C or T ). Dotted lines, virulence (a weighted sum of wild-type and cheat density). (a,c,e) No within-host spatial structure (r ¼ 0). (b,d,f ) Limited within-host spatial structure (r ¼ 0.3). (a,b) Cheats versus wild-type (model 4 with a ¼ q ¼ 0); virulence is a weighted combination of the two lineage densities, here virulence equals 2W þ C. (c,d) Trojan horse cheats versus wild-type (model 4 with a ¼ 0.5, q ¼ 0.01), virulence equals 2W þ T. (e,f ) Trojan horse cooperators versus wild-type (model 4 with a ¼ 20.3, q ¼ 0.01), virulence equals 2WþT. Other parameters: x ¼ 0.1, b ¼ 0.2. Initial densities: W(0) ¼ 1.1, C(0) ¼ 0.001, T(0) ¼ 0.001.

represented by a negative q), yielding. dW ¼ W ðð1 NÞ x þ bW =NÞ; dt dT ¼ T ðð1 NÞ q þ bW =NÞ: dt

ð2:2Þ

In the case of an engineered susceptibility to a specific antibiotic treatment, it is important to delay use of the antibiotic treatment until the Trojan horse cheat has established within the host, otherwise the costs imposed on the Trojan horse cheat by the antibiotic would overwhelm the gains via social cheating, and the Trojan horse would fail to invade. While any remaining wild-type are likely to enjoy a competitive advantage once the Trojan horse controlling antibiotic is administered, at this point the wild-type is reduced in density following the earlier Trojan horse invasion. This reduction in parasite density could aid any other intervention strategy, emphasizing that such Trojan horse cheats could be useful as part of a larger strategy. An alternate class of Trojan horse traits could bring more immediate therapeutic advantages to Trojan horse invasion, if the Trojan horse directly sows the Phil. Trans. R. Soc. B (2009)

seeds of destruction for both the wild-type and itself. For example, a Trojan horse lineage engineered to produce an antimicrobial toxin that kills when at sufficient density (i.e. the toxin is under QS-dependent regulation), both W and T. In this case, the Trojan horse lineage generates a socially mediated cost, proportionate to its population share (T/N ), thus when the Trojan horse is initially rare, it can largely escape this social cost, and still invade. Alternatively, a Trojan horse could be engineered to produce an antimicrobial toxin upon addition of a certain chemical. In this case, a toxin gene would be placed under the control of an inducible promoter and only activated when the promoter is activated by the inducer chemical. In this case it would be advantageous to allow the Trojan horse to significantly invade the population before activating its deadly cargo. Weighing the socially mediated cost by a, in the case of a constitutive toxin-producer, we have dW ¼ W ðð1 NÞ x þ bW =N aT =NÞ; dt dT ¼ T ðð1 NÞ q þ bW =N aT =NÞ: dt

ð2:3Þ

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3162

S. P. Brown et al.

Review. Trojan horse

In this non-spatial model, the outcome of competition is entirely defined by the relative magnitudes of the direct effects x and q. If x . q (if the cost of wild-type cooperation is greater than the cost of the Trojan horse engineered vulnerability), then the cheat lineage will again invade and dominate within the host (tending to a carrying capacity of T* ¼ 1 2 q 2 a; figure 4c) driving the wild-type to extinction, otherwise the cheat will fail to invade. The Trojan horse cheat offers potentially multiple therapeutic gains. Given a ¼ 0 (equation (2.2)), Trojan horse invasion leads to a reduction of total bacterial density (tending to T* ¼ 1 2 q, from W * ¼ 1 þ b 2 x), the loss of virulence factor production associated with wild-type cooperation, and the fixation of an engineered vulnerability (e.g. antibiotic susceptibility) within the bacterial population (figure 4a). The generation of a socially mediated cost by the Trojan horse lineage (a . 0; equation (2.3)) offers the additional benefit of further depressing the remaining Trojan horse bacterial lineage (figure 4c), potentially to extinction (if a . 1 2 q). (c) Trojan horse cheat in a spatially structured host The above model is very favourable to our basic argument, as cheats that produce no or less exoproducts can readily invade an unstructured population of cooperators (e.g. Griffin et al. 2004; Brockhurst et al. 2007; Diggle et al. 2007b; Ross-Gillespie et al. 2007; Sandoz et al. 2007; Ku¨mmerli et al. 2009a,b). However, while unstructured populations occur in shaken laboratory cultures, infections in hosts are likely to be spatially structured (Rumbaugh et al. 2009). In order to consider the additional challenge of cheat invasion into a spatially structured host, we assume that within-host interactions are non-random. Specifically, we assume that individual pathogens interact with their kin with probability r, and otherwise interact with individuals drawn at random from the entire within-host population (e.g. Ross-Gillespie et al. 2007), yielding dW ¼ W ðð1 NÞ x þ bWw aTw Þ; dt dT ¼ T ðð1 NÞ q þ bWt aTt Þ; dt

ð2:4Þ

where Ww and Tw refer to the average local density of W and T, in the neighbourhood of a wild-type, and Wt and Tt refer to the average local density of W and T, in the neighbourhood of a Trojan horse. Specifically, we have Ww ¼ r þ (1 2 r) W/N; Wt ¼ (1 2 r) W/N; Tw ¼ (1 2 r)T/N and Tt ¼ r þ (1 2 r)T/N. When r ¼ 0, we recover the well-mixed model 1, with Ww ¼ Wt ¼ W/N and Tw ¼ Tt ¼ T/N, and when r ¼ 1 we have complete separation of the strains, with Ww ¼ Tt ¼ 1 and Tw ¼ Wt ¼ 0. Note the demographic term (1 2 N ) remains global (unmodified by r), reflecting constraints on the remaining ‘host space’. We can interpret N in the spatial model as the proportion of distinct potential infection sites within a host that are infected, and r as a measure of within-site relatedness (where social interactions take place). Phil. Trans. R. Soc. B (2009)

When a ¼ q ¼ 0, we recover a structured version of equation (2.1), wild-type versus cheats C. Given sufficiently low r, the sole stable equilibrium remains pure C (with W* ¼ 0), however if rb . x (cf. Hamilton’s Rule (Hamilton 1963, 1964)); then pure W (at W* ¼ 1 þ b 2 x) becomes the sole attractor, highlighting a standard result of social evolution theory that spatial structure promotes cooperation (figure 4b illustrates an intermediate case, where limited within-host structuring slows invasion of the cheat; reviewed by West et al. 2002; Lehmann & Keller 2006). Given that this result runs counter to our goal of developing a therapeutic cheat agent, how can we proceed? Turning to the full Trojan horse model (equation (2.4)), we see that the condition for wild-type vulnerability to invasion (and for Trojan horse stability) becomes r(b þ a) , x2q, again favoured by low within-host structure r. The Trojan horse cheat’s invasive ability is further weakened by its direct costs q, and also any socially mediated costs a, as these costs are now more heavily felt by the invasive Trojan horse lineage (figure 4d). Hamilton’s rule also shows how ‘ultra-cooperators’ could theoretically be used to invade a population, although this is unlikely to be a practical option. If the Trojan horse delivers sufficient social benefits (i.e. if 2a . b, the Trojan horse is more cooperative than the wild-type), then increasing population structure r will favour invasion of the Trojan horse lineage. In this scenario, we have a negative a (for example the Trojan horse produces a growth-enhancing exoproduct) and the Trojan horse would lead to an increase in the within-host microbial density (from W* ¼ 1 þ b 2 x to T* ¼ 1 2 a 2 q and W* ¼ 0; figure 4e, f ), but the remaining therapeutic gains would still stand: loss of virulence factor production (extinction of the wild-type strain), fixation of engineered vulnerability (e.g. antibiotic sensitivity). If a is negative, the Trojan horse becomes a cooperative lineage and therefore we are exploring a reversal of our original premise, here proposing a cooperator to invade a structured social population, and consequently we find that increasing within-host structure enhances the invisibility of the Trojan horse cooperator (figure 4e, f ). While this demonstrates the theoretical plausibility of using an ultra-cooperator to invade a structured population (of cooperators), we note that there are likely to be practical problems that make this much less useful than the scenario of a cheat invading. In particular, natural selection is likely to have led to the wild-type producing exoproducts at a rate that cannot be invaded (i.e. if greater cooperation was favoured, then lineages would already be doing it), or it may be hard to genetically engineer such cooperators.

(d) Bacteriocinogen cheat invasion The above models have considered the invasion of individuals that differ in their rate of production of a cooperative exoproduct. Another possibility is to exploit a different type of social trait—the production of anti-competitor chemicals or bacteriocins (Riley & Gordon 1999; Riley & Wertz 2002).

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Trojan horse Bacteriocin-producing lineages carry two tightly linked traits. First, they carry genes coding for a small peptide anti-competitor toxin, a bacteriocin. Second, they carry genes conferring immunity to this bacteriocin, ensuring that the toxicity is experienced preferentially by non-kin. A broad strand of experimental and theoretical work on the ecology of bacteriocin-mediated competition highlights the importance of spatial structure in mediating the outcome of competition, with the consensus recognizing that structured environments promote the invasion of rare killers by increasing the local density of chemical weapons to an effective dose (Chao & Levin 1981; Levin 1988; Frank 1994; Durrett & Levin 1997; Gordon & Riley 1999; Gardner et al. 2004). Gardner et al. (2004) go on to illustrate that the production of anti-competitor chemical weapons can be understood as an example of microbial spite. A spiteful trait imposes costs on both actor and recipient, and is favoured when it is preferentially directed at non-relatives, because this has the indirect benefit of freeing-up resources for relatives (Hamilton 1970; Lehmann et al. 2006; Gardner et al. 2007a). Bacteriocin production can be considered a spiteful trait as it has a negative fitness impact on the actor cell producing the toxin (suicidal cell lysis to release the toxins), imposes a clear cost on recipient cells that are sensitive to the action of the toxin, while freeingup resources for resistant relatives (Gardner & West 2004; Gardner et al. 2004; Inglis et al. 2009). Note that the indirect benefit of freeing-up resources is greatest when populations are structured, with local competition for resources. We begin with a non-spatial treatment of competition between a bacteriocinogenic cheat and wild-type. Consider a cheat lineage B that is also bacteriocinogenic, producing (at a cost q) an anti-wild-type compound with efficacy e (scaled by density of bacteriocinogen, B/N ). In a well-mixed host, we have wild-type: dW ¼ W ðð1 NÞ x þ bW =N eB=NÞ; dt bacteriocinogen cheat: dB ¼ Bðð1 NÞ q þ bW =NÞ: dt

ð2:5Þ

We again assume b . x (investment in public goods increases carrying capacity) and additionally that e . q (investment in bacteriocin gives relative advantage when dominant). Note when x ¼ b ¼ 0 (no public goods interaction), we recover classic bacteriocinmediated competition models with frequency threshold to invasion at B/N ¼ q/e (Frank 1994; Durrett & Levin 1997; Brown et al. 2006). A stability analysis illustrates that pure wild-type is locally stable (at W* ¼ 1 þ b 2 x) if q . x (i.e. if bacteriocin is expensive relative to public good of W lineage). Pure cheat B is stable (at B* ¼ 1 2 q) if x þ e . q (killing compensates for costs) and q , 1 (B* is sustainable). Note that if x þ e . q . x, then both pure equilibria are stable (bistability, with threshold defined by unstable equilibrium {W*, B*}, where B*/N* ¼ Phil. Trans. R. Soc. B (2009)

S. P. Brown et al.

3163

(q2x)/e). Note that this threshold frequency of invaders (q 2 x)/e simplifies to the classic threshold frequency of q/e when x ¼ 0. Increasing x (increasing the additional cheat benefit to B) decreases the threshold to disappearance when x . q: i.e. given a sufficient cheating advantage, the rarity threshold to bacteriocin-mediated invasion can be overcome (i.e. the cheating and spiteful traits interact synergistically, see also Brown & Taylor submitted). Figure 5a,b illustrates the frequency-dependent fate of bacteriocinogen invasion when the invading B lineage pays a significant direct cost, q . x (e.g. B carries a costly Trojan horse trait. A similar and classic result would hold for the case where B and W are identical with respect to their public goods provision). In this particular illustration, the unstable equilibrium is at B*/N ¼ 0.1; below this frequency, invasion fails (figure 5a), above this frequency the invader dominates (figure 5b). In contrast, figure 5c,d illustrates the more favourable case, where the direct costs to the bacteriocinogenic lineage are small (q , x), and consequently the killer lineage can invade from any frequency. Figure 5 illustrates that modifying multiple social traits in conjunction (here, public goods and bacteriocin production) can generate more favourable outcomes (here, invasion from rare due to public goods cheating, and accelerating exclusion of wild-type due bacteriocin production). Modelling structured within-host (or within-patch) ecological dynamics of bacteriocin-mediated competition is more complex than the previous structured social interactions in §2c, and is usually addressed via simulations (Frank 1994; Durrett & Levin 1997; Cza´ra´n et al. 2002) or a heuristic approach (Gardner et al. 2004). Across these models we find consensus with the experimental findings that spatial structuring allows bacteriocinogen invasion from rare (Chao & Levin 1981). The effect of spatial structuring on the invisibility of a cooperative wild-type by a bacteriocinogenic cheat remains an open question. On the one hand, invasibility via bacteriocin production will be enhanced by spatial structuring (see above), while on the other hand, invasibility via social cheating will be reduced by within-host structuring (figure 4a,b). It is worth noting that there are other mechanisms of microbial spite, with qualitatively different invasion dynamics (Brown et al. 2009), which could be engineered into a Trojan horse therapeutic strain. In particular, a strategy of coupling a Trojan horse with a temperate phages may offer significant advantages for the invasion of unstructured foci of infection (Brown et al. 2006). Temperate phages are viruses of bacteria that can be transmitted either vertically or horizontally. Infection of susceptible bacteria by temperate phages can result in two possible outcomes; the most common is the lytic cycle (rapid host lysis and production of numerous horizontally transmissible viral particles). Very rarely, however, the phage can lysogenize the host, persisting in a dormant state while allowing the survival of the infected bacteria. This dormant phage is then replicated with the bacterial genome, and thus vertically transmitted upon bacterial division. Furthermore, this vertically transmitted carried-phage provides immunity to its

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3164

S. P. Brown et al.

Review. Trojan horse

2.0 (a)

(b)

cell density, virulence intensity

1.5 1.0 0.5

2.0 (c)

(d)

1.5 1.0 0.5

0

20

40

60 80 100 120 140 time (arb. units)

0

20

40

60 80 100 120 140 time (arb. units)

Figure 5. Invasion of bacteriocinogen cheats into an established resident infection and consequent virulence (equation (2.5)). Black lines, wild-type (W ). Blue lines, bacteriocinogenic (B). Dotted lines, virulence (a weighted sum of wild-type and cheat density). (a,b) Bacteriocinogen has higher direct costs (x ¼ 0.1, q ¼ 0.15). (c,d) Bacteriocinogen has lower direct costs, and is an effective social cheat (x ¼ 0.1, q ¼ 0.05). (a,c) Bacteriocinogen is initially rare (W(0) ¼ 1.1, B(0) ¼ 0.001). (b,d) Bacteriocinogen is initially more common (W(0) ¼ 1.1, B(0) ¼ 0.13). Virulence ¼ 2W þ T. Other parameters: b ¼ 0.2; e ¼ 0.5.

carrier-bacteria against further horizontal infection by this phage (Adams 1959; Campbell 1996). Upon rare spontaneous induction of the carried-phage, viral progeny are released through host lysis. Temperate phages have been demonstrated to function analogously to bacteriocins (Bossi et al. 2003; Brown et al. 2006; Joo et al. 2006), by differentially killing susceptible (non-lysogen) bacteria. Brown et al. (2006) further demonstrated experimentally that unlike bacteriocinogenic lineages (see above), lysogenic bacteria can invade rapidly from rare into unstructured environments, due to the ability of the released phage to amplify on susceptibles. Here, we consider the fate of a candidate theraputic cheat lineage, that carries an additional temperate phage weapon that is active against the target resident bacteria. We begin with a simple non-spatial treatment tracking the densities of wild-type W, lysogen cheat C and free viral propagules V, dW ¼ W ðð1 NÞ x þ bW =N aV Þ; dt dC ¼ Cðð1 NÞ q þ bW =NÞ; dt dV ¼ yqC þ yaWV aVN: dt

ð2:6Þ

Following Brown et al. (2006), we find that pure wild-type is always unstable (so long as burst size y is greater than 1), and that pure C and V are stable if q , 1 and y . 1, therefore we have a simple general outcome in the non-spatial case of extinction of the wild-type W, irrespective of the social behaviour (governed by x and b) of the resident wild-type. Understanding how microbial competition mediated by temperate phage is modified by within-host spatial Phil. Trans. R. Soc. B (2009)

structure is an open question, however it is likely that in contrast to the bacteriocin case, spatial structuring will act to dampen invasion by slowing the viral epidemic, due to the separation of susceptibles from free virus.

3. DISCUSSION We have applied social evolution theory to suggest novel intervention strategies in the treatment of bacterial infection: (i) the introduction of an invasive cheat that does not contribute to the production of a virulence factor can lead to a reduction in parasite virulence, as well as a reduced bacterial population size, that may make the infection more susceptible to other intervention strategies (§2a, figure 2); (ii) cheats could be used as Trojan horses to introduce useful traits such as antibiotic sensitivity into the population (§2b, figure 3); (iii) social dominance by a more benign and controllable microbe could be achieved by harnessing allelopathic traits to the therapeutic strain, that are active against the resident pathogen (e.g. bacteriocins, temperate phages; §2d,e). These different possibilities may interact synergistically (e.g. a bacteriocin-producing cheat), or with other strategies in a larger intervention plan (see also Brown & Taylor submitted). We have used a few simple examples to illustrate the general points, and there are a range of other social behaviours that could be exploited, including lower levels of persistence (Gardner et al. 2007b), cell death (Ackermann et al. 2008) as well as cheats defective in multiple social traits. Furthermore, this approach could also be useful in other areas such as industry (e.g. problems with biofilms) or agriculture (e.g. treating plant pathogens).

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Trojan horse Table 1. A classification of social strategies by their conjectured strengths. strategy

favoured by

cheat

unstructured populations, more highly diffusible exoproducts, more costly exoproducts, lower specificity in exoproduct uptake as above, and with low cost or high benefit associated with Trojan horse trait structured populations, less diffusible exoproducts, less costly exoproducts, higher specificity in exoproduct uptake structured populations (if low cheat advantage), more diffusible bacteriocins, higher specificity in bacteriocin immunity, low cost or high benefit associated with any Trojan horse trait unstructured populations, durable phage propagules, low cost or high benefit associated with any Trojan horse trait

Trojan horse cheat Trojan horse cooperator

bacteriocin cheat

lysogen cheat

All the different scenarios that we have suggested have advantages and disadvantages, which should be considered for specific cases (table 1). Invasion of an exoproduct cheat is more likely when microbial populations are relatively unstructured within-hosts (§2c) where the exoproduct diffuses over larger distances (lower r), and when the cost of exoproduct production is high (higher x). Note that the degree of within-host structuring can be temporarily reduced to favour cheat invasion through the use of a sufficiently diffuse mechanism of inoculation, for example using an aerosol spray. As the invasion of cheats proceeds, within-host structuring is liable to increase (with cheats and cooperators increasingly segregated in distinct foci), however, by this time a significant theraputic gain in overall virulence factor reduction may have been achieved. A potential complication is that some exoproducts show specificity in their uptake: different strains of P. aeruginosa produce different forms of pyoverdine, and strains are best able to take up their form of pyoverdine (Meyer et al. 1997; Smith et al. 2005). Exoproducts that did not involve such specificity (e.g. proteases) would be more useful, because it would not be necessary to match the ‘type’ of the cheat and the cooperator that they are to invade. Another complication that we have not considered is that the genes for many social traits can be on plasmids that are horizontally transmitted between cells (Smith 2001). For example, one of the most virulent strains of bacteria to be reported recently is the strain of MRSA USA300, in which the gene responsible for antibiotic resistance is located on a horizontally transmissible plasmid. Plasmids may represent another avenue for the Trojan horse approach. Given that cheats producing less or no exoproducts can invade infections, why are cheats not more common in natural infections? It is important here to distinguish between within-host and between-host Phil. Trans. R. Soc. B (2009)

S. P. Brown et al.

3165

(patch) dynamics (Ku¨mmerli et al. 2009a). Within hosts, cheats can potentially invade (Rumbaugh et al. 2009). However, this leads to reduced bacterial growth (Rumbaugh et al. 2009) and hence a lower transmission to future hosts—transmission success will depend on the proportion of cooperator cells in an infection (figure 2). The overall balance of these two opposing forces will depend upon the extent to which cheats and cooperators can occur in the host (Brown et al. 2002; West & Buckling 2003; West et al. 2006). If the population dynamics lead to mixed infections with both types (high strain diversity within hosts), then within-host dynamics will favour cheats. In contrast, if infections tend to be only cheats or cooperators (low strain diversity within hosts), then the between-host dynamics will favour cooperators. These two conditions correspond to relatedness being relatively low or high, respectively, and are another way of conceptualizing the familiar result that altruistic cooperation is favoured by high relatedness (Hamilton 1964). Even when natural population dynamics lead to high relatedness that favours cooperative virulence traits, it is still possible that a cheat could invade. In chronic infections, where there is a relatively low level of transmission between hosts, we predict that cheater strains could invade in natural populations. There is some evidence to support this prediction: biofilm formation is relatively poor in strains from older infections (Lee et al. 2005) and mutations occurring post-colonization are found in genes controlling social behaviours, such as public good production and QS (Smith et al. 2006). The introduction of cheats into these infections may be less effective in the ways described in this paper, as there may not be a sufficient amount of cooperation going on in the infective population for the introduced cheats to exploit. Another general point is that we assume throughout that the mechanics of host exploitation are inherently cooperative, and therefore, that the introduction of cheats will reduce virulence. For pathogens that do not engage in cooperative virulence mechanisms, social cheats are predicted to be more virulent (Frank 1996) and our theraputic approach would not work. With any new class of anti-infective therapy, it is essential to consider the potential risk of resistance evolution—see discussions of phage therapy (Levin & Bull 2004) and antimicrobial peptides (Bell & Gouyon 2003; Perron et al. 2006). Andre´ & Godelle (2005) have also argued that by attacking social traits directly (for example, by disrupting QS regulation), the selective pressure driving the emergence of resistance traits to social perturbations can be dramatically reduced relative to classic antimicrobials, because it is hard for rare cooperators to invade populations of cheaters. Selection will be unlikely to favour the restoration of cooperative function in individuals that have evolved resistance to cheats. While the same argument holds for our particular brand of social perturbation, the emergence of resistance is still conceivable. Natural anti-cheat resistance traits are widespread, for example mechanisms of specificity (discussed above) effectively remove cheats from the pool of shared goodies produced by a focal cooperative

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3166

S. P. Brown et al.

Review. Trojan horse

lineage. For lineages without inbuilt mechanisms of cheater resistance (most likely reflecting a transmission ecology characterized by high bottlenecking and consequently a dominance of single-genotype infections), we anticipate the greatest initial success for our strategy, and also the greatest long-term risk of resistance evolution. Another point of departure from classic chemical mechanisms of microbial control concerns the within-host dynamics of our control agent. In this regard, our proposed cheat therapy most closely resembles phage therapy, where a live natural enemy is administered to control an infection (rather than a live social parasite). In both cases, the control agent is able, in principle, to replicate at the site of interest, within infection, therefore offering significant gains over a chemical agent that must be introduced en masse, often at damagingly high doses, at a remote site of entry. However, the slow development of phage therapy over many decades offers further notes of caution (Levin & Bull 2004): replication of the control agent may only be possible under certain physiological states of both resident and control agent, and the ability of the control agent to reach infection sites (the ‘pharmacokinetics’ of social parasites) may be severely limited, relative to classic chemical control agents (although see Rumbaugh et al. 2009). A further cause for advantage—and cause for concern—shared by phage and social parasite therapy is the potential ability of the control agent to co-evolve with its target, potentially prolonging efficacy, but also raising the spectre of unintended consequences. This paper was inspired by an interview about gene therapy for the treatment of cystic fibrosis with Andrew Bush, Professor of Paediatric Respirology at the Royal Brompton Hospital and Imperial College London, broadcast on the BBC Radio 4 programme Case Notes, with Dr Mark Porter. We thank: Jean-Baptiste Andre´, Andrew Bourke, Heikki Helantera¨, Francis Ratnieks and Adin Ross-Gillespie for comments; the Royal Society, Leverhulme Trust and Wellcome Trust for funding.

REFERENCES Ackermann, M., Stecher, B., Freed, N. E., Songher, P., Hard, W.-D. & Doebeli, M. 2008 Self-destructive cooperation mediated by phenotypic noise. Nature 454, 987 –990. (doi:10.1038/nature07067) Adams, M. H. 1959 Bacteriophages. London, UK: Interscience Publishers Ltd. Andre´, J.-B. & Godelle, B. 2005 Multicellular organization in bacteria as a target for drug therapy? Ecol. Lett. 8, 800 –810. (doi:10.1111/j.1461-0248.2005.00783.x) Bell, G. & Gouyon, H. 2003 Arming the enemy: the evolution of resistance to self-proteins. Microbiology 149, 1367–1375. (doi:10.1099/mic.0.26265-0) Bossi, L., Fuentes, J. A., Mora, G. & Figueroa-Bossi, N. 2003 Prophage contribution to bacterial population dynamics. J. Bacteriol. 185, 6467–6471. (doi:10.1128/ JB.185.21.6467-6471.2003) Brockhurst, M. A., Buckling, A. & Gardner, A. 2007 Cooperation peaks at intermediate disturbance. Curr. Biol. 17, 761–765. (doi:10.1016/j.cub.2007.02.057) Brown, S. P. & Buckling, A. 2008 A social life for discerning microbes. Cell 135, 600–603. (doi:10.1016/j.cell.2008. 10.030) Phil. Trans. R. Soc. B (2009)

Brown, S. P. & Johnstone, R. A. 2001 Cooperation in the dark: signalling and collective action in quorum-sensing bacteria. Proc. R. Soc. Lond. B 268, 961–965. (doi:10. 1098/rspb.2001.1609) Brown, S. P. & Taylor, P. D. Submitted. Joint evolution of multiple social traits—an inclusive fitness analysis. Brown, S. P., Hochberg, M. E. & Grenfell, B. T. 2002 Does multiple infection select for raised virulence? Trends Microbiol. 10, 401–405. (doi:10.1016/S0966842X(02)02413-7) Brown, S. P., Le Chat, L., De Paepe, M. & Taddei, F. 2006 Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare. Curr. Biol. 16, 2048–2052. (doi:10.1016/j.cub.2006.08.089) Brown, S. P., Inglis, R. F. & Taddei, F. 2009 Evolutionary ecology of microbial wars: within-host competition and (incidental) virulence. Evol. Appl. 2, 32–39. Burt, A. 2003 Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. R. Soc. Lond. B 270, 1471 –2954. (doi:10.1098/ rspb.2002.2319) Campbell, A. M. 1996 Cryptic prophages. In Escherichia coli and Salmonella (ed. F. C. Neidhardt), pp. 2325 –2338. Washington, DC: ASM Press. Chao, L. & Levin, B. R. 1981 Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc. Natl Acad. Sci. USA 78, 6324–6328. (doi:10.1073/pnas.78.10.6324) Crespi, B. J. 2001 The evolution of social behavior in microorganisms. Trends Ecol. Evol. 16, 178 –183. (doi:10.1016/ S0169-5347(01)02115-2) Cza´ra´n, T. L., Hoekstra, H. & Pagie, L. 2002 Chemical warfare between microbes promotes biodiversity. Proc. Natl Acad. Sci. USA 99, 786–790. (doi:10.1073/pnas.012399899) Diggle, S. P., Gardner, A., West, S. A. & Griffin, A. S. 2007a Evolutionary theory of bacterial quorum sensing: when is a signal not a signal? Phil. Trans. R. Soc. B 362, 1241– 1249. (doi:10.1098/rstb.2007.2049) Diggle, S. P., Griffin, A. S., Campbell, G. S. & West, S. A. 2007b Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411– 414. (doi:10. 1038/nature06279) Durrett, R. & Levin, S. 1997 Allelopathy in spatially distributed populations. J. Theoret. Biol. 165 –171. (doi:10. 1006/jtbi.1996.0292) Fleming, V., Feil, E., Sewell, A. K., Day, N., Buckling, A. & Massey, R. C. 2006 Agr interference between clinical Staphylococcus aureus strains in an insect model of virulence. J. Bacteriol. 188, 7686– 7688. (doi:10.1128/JB. 00700-06) Foster, K. R. 2007 What can microbial genetics teach sociobiology? Trends Genet. 23, 74–80. (doi:10.1016/j.tig. 2006.12.003) Frank, S. A. 1994 Spatial polymorphism of bacteriocins and other allelopathic traits. Evol. Ecol. 8, 369– 386. (doi:10. 1007/BF01238189) Frank, S. A. 1996 Models of parasite virulence. Q. Rev. Biol. 71, 37–78. (doi:10.1086/419267) Gardner, A. & West, S. A. 2004 Spite and the scale of competition. J. Evol. Biol. 17, 1195–1203. (doi:10.1111/j. 1420-9101.2004.00775.x) Gardner, A., West, S. A. & Buckling, A. 2004 Bacteriocins, spite and virulence. Proc. R. Soc. Lond. B 271, 1529– 2535. (doi:10.1098/rspb.2004.2756) Gardner, A., Hardy, I. C. W., Taylor, P. D. & West, S. A. 2007a Spiteful soldiers and sex ratio conflict in polyembryonic parasitoid wasps. Am. Nat. 169, 519–533. (doi:10.1086/512107) Gardner, A., West, S. A. & Griffin, A. S. 2007b Is bacterial persistence a social trait? PLOS One 2, e752. (doi:10. 1371/journal.pone.0000752)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Trojan horse Gordon, D. M. & Riley, M. A. 1999 A theoretical and empirical investigation of the invasion dynamics of colicinogeny. Microbiology 145, 655–661. (doi:10.1099/ 13500872-145-3-655) Greig, D. & Travisano, M. 2004 The Prisoner’s Dilemma and polymorphism in yeast SUC genes. Biol. Lett. 271, S25 –S26. Griffin, A. S., West, S. A. & Buckling, A. 2004 Cooperation and competition in pathogenic bacteria. Nature 430, 1024– 1027. (doi:10.1038/nature02744) Hamilton, W. D. 1963 The evolution of altruistic behaviour. Am. Nat. 97, 354–356. (doi:10.1086/497114) Hamilton, W. D. 1964 The genetical evolution of social behaviour, I & II. J. Theor. Biol. 7, 1–52. (doi:10.1016/ 0022-5193(64)90038-4) Hamilton, W. D. 1970 Selfish and spiteful behaviour in an evolutionary model. Nature 228, 1218– 1220. (doi:10. 1038/2281218a0) Harrison, F., Browning, L. E., Vos, M. & Buckling, A. 2006 Cooperation and virulence in acute Pseudomonas aeruginosa infections. BMC Biol. 4, 21. (doi:10.1186/17417007-4-21) Hense, B. A., Kuttler, C., Mu¨ller, J., Rothballer, M., Hartmann, A. & Kreft, H. 2007 Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5, 230 –239. (doi:10.1038/nrmicro1600) Inglis, R. F., Gardner, A., Cornelis, P. & Buckling, A. 2009 Spite and virulence in the bacterium Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 106, 5703–5707. Joo, J., Gunny, M., Cases, M., Hudson, P., Albert, R. & Harvill, E. 2006 Bacteriophage-mediated competition in Bordetella bacteria. Proc. R. Soc. B 273, 1843–1848. (doi:10.1098/rspb.2006.3512) Keller, L. & Surette, M. G. 2006 Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4, 249– 258. (doi:10.1038/nrmicro1383) Kolter, R. & Greenberg, E. P. 2006 The superficial life of microbes. Nature 441, 300–302. (doi:10.1038/441300a) Ku¨mmerli, R., Gardner, A., West, S. A. & Griffin, A. S. 2009a Limited dispersal, budding dispersal and cooperation: an experimental study. Evolution 63, 939 –949. (doi:10.1111/j.1558-5646.2008.00548.x) Ku¨mmerli, R., Jiricny, N., Clarke, L. S., West, S. A. & Griffin, A. S. 2009b Phenotypic plasticity of a cooperative behaviour in bacteria. J. Evol. Biol. 22, 589– 598. Kurzban, R. & Egreth, M. 2008 Applied Darwinian medicine: artificial selection for less-harmful parasites. Med. Hypotheses 71, 976– 977. (doi:10.1016/j.mehy.2008.07. 019) Lee, B., Haagensen, J. A. J., Ciofu, O., Andersen, J. B., Høiby, N. & Molin, S. 2005 Heterogeneity of biofilms formed by nonmucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. J. Clin. Microbiol. 43, 5247– 5255. (doi:10.1128/JCM.43.10.5247-5255.2005) Lehmann, L. & Keller, L. 2006 The evolution of cooperation and altruism. A general framework and classification of models. J. Evol. Biol. 19, 1365 –1378. (doi:10.1111/j.1420-9101.2006.01119.x) Lehmann, L., Bargum, K. & Reuter, M. 2006 An evolutionary analysis of the relationship between spite and altruism. J. Evol. Biol. 19, 1507–1516. (doi:10.1111/j. 1420-9101.2006.01128.x) Levin, B. R. 1988 Frequency-dependent selection in bacterial populations. Phil. Trans. R. Soc. Lond. B 319, 459 –472. (doi:10.1098/rstb.1988.0059) Levin, B. R. & Bull, J. J. 2004 Population and evolutionary dynamics of phage therapy. Nat. Rev. Microbiol. 2, 166 –173. (doi:10.1038/nrmicro822) Lin, W., Kovacikova, G. & Skorupski, K. 2007 The quorum sensing regulator HapR downregulates the expression of Phil. Trans. R. Soc. B (2009)

S. P. Brown et al.

3167

the virulence gene transcription factor AphA in Vibrio cholerae by antagonizing Lrp- and VpsR-mediated activation. Mol. Microbiol. 64, 953– 967. (doi:10.1111/j. 1365-2958.2007.05693.x) MacLean, R. C. 2008 The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies. Heredity 100, 233–239. (doi:10.1038/sj.hdy.6801073) Meyer, J.-M., Stintzi, A., Vos, D. D., Cornellis, P., Tappe, R., Taraz, K. & Budzikiewicz, H. 1997 Use of siderophores to type pseudomonads: the three Pseudomonas aeruginosa pyoverdine systems. Microbiology 143, 35–43. (doi:10. 1099/00221287-143-1-35) Nowak, M. A. 2006 Five rules for the evolution of cooperation. Science 314, 1560 –1563. (doi:10.1126/ science.1133755) Otto, S. P. & Day, T. 2007 A biologist’s guide to mathematical modeling in ecology and evolution. Princeton, USA: Princeton University Press. Perron, G. G., Zasloff, M. & Bell, G. 2006 Experimental evolution of resistance to an antimicrobial peptide. Proc. R. Soc. B 273, 251–256. (doi:10.1098/rspb.2005.3301) Popat, R., Crusz, S. A. & Diggle, S. P. 2008 The social behaviours of bacterial pathogens. Br. Med. J. 87, 63–75. Riley, M. A. & Gordon, D. M. 1999 The ecological role of bacteriocins in bacterial cooperation. Trends Microbiol. 7, 129–133. (doi:10.1016/S0966-842X(99)01459-6) Riley, M. A. & Wertz, J. E. 2002 Bacteriocins: evolution, ecology and application. A Rev. Microbiol. 56, 117– 137. (doi:10.1146/annurev.micro.56.012302.161024) Ross-Gillespie, A., Gardner, A., West, S. A. & Griffin, A. S. 2007 Frequency dependence and cooperation: theory and a test with bacteria. Am. Nat. 170, 331 –342. (doi:10. 1086/519860) Rumbaugh, K. P., Griswold, J. A., Iglewski, B. H. & Hamood, A. N. 1999 Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect. Immun. 67, 5854–5862. Rumbaugh, K. P., Diggle, S. P., Watters, C. M., Ross-Gillespie, A., Griffin, A. S. & West, S. A. 2009 Quorum sensing and the social evolution of bacterial virulence. Curr. Biol. 19, 341 –345. (doi:10.1016/j.cub. 2009.01.050) Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull, J. J. 2004 The evolution of cooperation. Q. Rev. Biol. 79, 135 –160. (doi:10.1086/383541) Sandoz, K. M., Mitzimberg, S. M. & Schuster, M. 2007 Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl Acad. Sci. USA 104, 15 876 –15 881. (doi:10.1073/pnas.0705653104) Smith, J. 2001 The social evolution of bacterial pathogenesis. Proc. R. Soc. Lond. B 268, 61–69. (doi:10.1098/ rspb.2000.1330) Smith, E. E., Sims, E. H., Spencer, D. H., Kaul, R. & Olson, M. V. 2005 Evidence for diversifying selection at the pyoverdine locus of Pseudomonas aeruginosa. J. Bacteriol. 187, 2138–2147. (doi:10.1128/JB.187.6.2138-2147.2005) Smith, E. E. et al. 2006 Genetic adaptation by Pseudomonas aeruginosa to the airways of cyctic fibrosis patients. Proc. Natl Acad. Sci. USA 103, 8487–8492. (doi:10.1073/ pnas.0602138103) Strassmann, J. E., Zhu, Y. & Queller, D. C. 2000 Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408, 965 –967. (doi:10.1038/35050087) Trivers, R. L. 1971 The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57. (doi:10.1086/406755) Turelli, M. & Hoffman, A. A. 1999 Microbe-induced cytoplasmic incompatibility as a mechanism for introducing transgenes into arthropod populations. Insect Mol. Biol. 8, 243 –255. (doi:10.1046/j.1365-2583.1999.820243.x)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3168

S. P. Brown et al.

Review. Trojan horse

Ulrich, R. L., Deshazer, D., Brueggemann, E. E., Hines, H. B., Oyston, P. C. & Jeddeloh, J. A. 2004 Role of quorum sensing in the pathogenicity of Burkholderia pseudomallei. J. Med. Microbiol. 53, 1053– 1064. (doi:10. 1099/jmm.0.45661-0) Velicer, G. J. 2003 Social strife in the microbial world. Trends Microbiol. 11, 330 –337. (doi:10.1016/S0966842X(03)00152-5) Velicer, G. J., Kroos, L. & Lenski, R. E. 2000 Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404, 598 –601. (doi:10.1038/35007066) Webb, J. S., Givskov, M. & Kjelleberg, S. 2003 Bacterial biofilms: prokaryotic adventures in multicellularity. Curr. Opin. Microbiol. 6, 578–585. (doi:10.1016/j.mib.2003.10.014) West, S. A. & Buckling, A. 2003 Cooperation, virulence and siderophore production in bacterial parasites. Proc. R. Soc. Lond. B 270, 37–44. (doi:10.1098/rspb.2002.2209)

Phil. Trans. R. Soc. B (2009)

West, S. A., Pen, I. & Griffin, A. S. 2002 Cooperation and competition between relatives. Science 296, 72–75. (doi:10.1126/science.1065507) West, S. A., Griffin, A. S., Gardner, A. & Diggle, S. P. 2006 Social evolution theory for microbes. Nat. Rev. Microbiol. 4, 597 –607. (doi:10.1038/nrmicro1461) West, S. A., Diggle, S. P., Buckling, A., Gardner, A. & Griffin, A. S. 2007a The social lives of microbes. Ann. Rev. Ecol. Evol. Syst. 38, 53–77. (doi:10.1146/annurev. ecolsys.38.091206.095740) West, S. A., Griffin, A. S. & Gardner, A. 2007b Evolutionary explanations for cooperation. Curr. Biol. 17, R661–R672. (doi:10.1016/j.cub.2007.06.004) Williams, P., Winzer, K., Chan, W. & Ca´mara, M. 2007 Look who’s talking: communication and quorum sensing in the bacterial world. Phil. Trans. R. Soc. B 362, 1119– 1134. (doi:10.1098/rstb.2007.2039)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3169–3179 doi:10.1098/rstb.2009.0129

Review

The evolution of extreme altruism and inequality in insect societies Francis L. W. Ratnieks1 and Heikki Helantera¨1,2,* 1

Laboratory of Apiculture and Social Insects, Department of Biological and Environmental Science, University of Sussex, Falmer, Brighton BN1 9QG, UK 2 Department of Biological and Environmental Sciences, University of Helsinki, PO Box 65, 00014 Helsinki, Finland

In eusocial organisms, some individuals specialize in reproduction and others in altruistic helping. The evolution of eusociality is, therefore, also the evolution of remarkable inequality. For example, a colony of honeybees (Apis mellifera) may contain 50 000 females all of whom can lay eggs. But 100 per cent of the females and 99.9 per cent of the males are offspring of the queen. How did such extremes evolve? Phylogenetic analyses show that high relatedness was almost certainly necessary for the origin of eusociality. However, even the highest family levels of kinship are insufficient to cause the extreme inequality seen in e.g. honeybees via ‘voluntary altruism’. ‘Enforced altruism’ is needed, i.e. social pressures that deter individuals from attempting to reproduce. Coercion acts at two stages in an individual’s life cycle. Queens are typically larger so larvae can be coerced into developing into workers by being given less food. Workers are coerced into working by ‘policing’, in which workers or the queen eat worker-laid eggs or aggress fertile workers. In some cases, individuals rebel, such as when stingless bee larvae develop into dwarf queens. The incentive to rebel is strong as an individual is the most closely related to its own offspring. However, because individuals gain inclusive fitness by rearing relatives, there is also a strong incentive to ‘acquiesce’ to social coercion. In a queenright honeybee colony, the policing of worker-laid eggs is very effective, which results in most workers working instead of attempting to reproduce. Thus, extreme altruism is due to both kinship and coercion. Altruism is frequently seen as a Darwinian puzzle but was not a puzzle that troubled Darwin. Darwin saw his difficulty in explaining how individuals that did not reproduce could evolve, given that natural selection was based on the accumulation of small heritable changes. The recognition that altruism is an evolutionary puzzle, and the solution was to wait another 100 years for William Hamilton. Keywords: eusociality; worker policing; inclusive fitness theory; voluntary altruism; enforced altruism; acquiescence

1. INTRODUCTION The year 2009 is a double anniversary in the life of Charles Darwin, marking 200 years since his birth and 150 years since the publication of On the origin of species by means of natural selection (Darwin 1859). With hindsight, it is clear that this book was a turning point in biology, which revolutionized both our understanding of the living world and our place within it. The Origin also represents one of the greatest advances in scientific theory ever made by a single individual in a single publication. This article begins by briefly putting the social insects in the context of the Origin. Although social insects were discussed at length and presented great difficulties to Darwin’s theory of natural selection, Darwin was not primarily troubled by what we would now refer to as the evolution of eusociality or altruism.

* Author for correspondence ([email protected]). One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

Darwin’s difficulty was in a sense greater than this, as he had to explain how natural selection could act on individuals—worker insects—that did not have offspring. Although altruism is frequently referred to as a Darwinian puzzle, the puzzle was not brought squarely to attention until over 100 years later by William Hamilton, who also provided the solution with his theory of inclusive fitness (Hamilton 1964). Hamilton’s theory of inclusive fitness is a major extension of Darwinian theory (Grafen 2006, 2009). Using theoretical ideas from inclusive fitness theory combined with empirical evidence and tests, this article provides an overview of how social evolution in insects has proceeded to the point that some modern-day insect societies, such as the honeybee Apis mellifera, are both supremely unequal and harmonious. From a human perspective, extreme inequality and harmony would seem to be incompatible. This illustrates that social evolution can reach diverse outcomes, which in large part arise from the fact that human society is based on cooperation among unrelated individuals while insect societies are based on

3169

This journal is # 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3170

F. L. W. Ratnieks & H. Helantera¨ Review. Inequality in insect societies

altruism among family members (Ratnieks 2006; Ratnieks & Wenseleers 2008).

2. THE EVOLUTION OF EUSOCIALITY (a) Darwin (1859): social insect difficulties and the evolution of altruism in insect workers Darwin (1859) makes frequent reference to social insects. In chapter 6 (Instinct), two of the three examples of ‘how instincts in a state of nature have become modified by selection’ that he chooses are from social insects—slave making in ants and comb building in honeybees. Social insects also provided difficulties to his theory and may even have delayed publication (Prete 1990). In chapter 7 (Difficulties of the theory), he writes ‘so wonderful an instinct as that of the hive-bee making its cells will probably have occurred to many readers, as a difficulty sufficient to overthrow my whole theory’. By drawing on evidence from bumblebees and stingless bees, Darwin presents possible intermediate stages to building combs of hexagonal cells. Chapter 7 (pp. 236–237) discusses ‘ . . . one special difficulty, which at first appeared to me insuperable, and actually fatal to my whole theory. I allude to the neuters or sterile females in insect-communities: for these neuters often differ widely in instinct and in structure from both the males and fertile females, and yet, from being sterile, they cannot propagate their kind’. Although this is often (Starr 1979; Thorne 1997), but not always (Hunt 2007; Herbers 2009), taken by social insect researchers to refer to what we would now call the evolution of altruism or eusociality, this seems not to have been Darwin’s main concern given that he also writes ‘ . . . How the workers have been rendered sterile is a difficulty; but not much greater than that of any other striking modification of structure’. In terms of the workings of natural selection, Darwin (1859) typically explains traits via their benefit to the individual. Without attempting to justify the change of beneficiary, he variously explains worker traits as being due to benefits to colony or parents. Thus, in reference to the sting of the worker honeybee, which becomes detached during stinging and so results in the worker’s death, Darwin writes ‘if on the whole the power of stinging be useful to the community, it will fulfil all the requirements of natural selection, though it may cause the death of some few members’ (ch. 7). And in reference to worker ants he writes ‘ . . . natural selection, by acting on the fertile parents, could form a species which should regularly produce neuters, either all of large size with one form of jaw, or all of small size with jaws having a widely different structure’ (ch. 7, pp. 236 – 237). Darwin’s (1859) theory was about evolution, not social evolution. Darwin’s theory of evolution by natural selection was built on a foundation of small heritable changes, and his ‘special difficulty’ was in explaining how individuals that had no offspring could evolve body shapes that were radically different from their fertile parents. He did not specifically try to explain how natural selection could cause the origin of altruistic workers in the first place, which he basically dismissed as a problem. But he did not Phil. Trans. R. Soc. B (2009)

need to. Only much later was this seen as an important evolutionary puzzle in its own right. (b) Altruism: an evolutionary puzzle The altruism of worker insects if often referred to as a Darwinian puzzle or paradox. How can natural selection, which normally favours the evolution of traits that increase an organism’s reproduction, favour the reverse—foregoing reproduction. But it seems to have been an inconsistency that for a century worried few evolutionary biologists. The evolution of altruism makes brief appearances in the work of both Haldane and Fisher, two of the founders of the ‘modern synthesis’ in evolutionary biology (Dugatkin 2006). But it was evidently not considered a major problem as both only made brief reference to it, even though both were on what proved to be the right track and certainly had the necessary mathematical abilities to make a formal theory (Dugatkin 2006). Altruism was recognized as an important evolutionary puzzle by Hamilton (1964) and solved by him in a general way. Natural selection can favour altruistic acts provided that the interacting individuals are related. Specifically, Hamilton’s rule c , rb, states that, for a social act to favoured by natural selection, the cost to the actor should be lower than the benefit to the recipient times their relatedness. (c) Altruism: the basis of eusocial insect societies Eusocial insects, the bees, wasps, ants and termites that live in colonies with a queen and workers, are one of the pinnacles of social evolution (Wilson 1975). The key characteristic of eusociality is reproductive division of labour, in which some society members specialize in reproduction (queens, and also kings in termites) while others (workers) carry out the other tasks such as foraging, building and defending the nest and caring for the brood. Workers have reduced or even zero direct reproduction. The evolution of eusociality is, therefore, both the evolution of altruism and the evolution of inequality. In some modern-day social insects, reproductive inequality has reached remarkable levels with a single female (and her mate or mates) exclusively or almost exclusively monopolizing reproduction. For example, a colony of honeybees, A. mellifera, may contain 50 000 females all of whom have developed ovaries and can lay eggs. But 100 per cent of the females and 99.9 per cent of the males are offspring of just one female, the queen, who is the mother of the other females—the workers (Visscher 1989; Ratnieks & Wenseleers 2008). (d) Kinship and the origin of eusociality Hamilton (1964) proposed an attractive explanation for the fact that eusociality is especially frequent in the Hymenoptera (bees, wasps, ants), which comprise the majority of eusocial species and which represent approximately nine independent origins of eusociality. Because Hymenoptera are haplodiploid, this leads to a female being more related to full-sisters (0.75) than to daughters (0.5). Although this explanation was convincing at the time, because it seemed to show that

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Inequality in insect societies hymenopteran females would have higher inclusive fitness if they worked to rear their mother’s offspring rather than their own, it overlooked the fact that haplodiploidy also leads to a female being less related to brothers (0.25) than to sons (0.5). On average, therefore, hymenopteran females are not more related to siblings than to offspring (Trivers & Hare 1976). Nevertheless, recent evidence shows that high levels of relatedness almost certainly played a critical role in the evolution of eusociality in the Hymenoptera. A phylogenetic analysis of the mating systems of 267 species of ants, bees and wasps in eight eusocial lineages shows that the mating of queens to multiple males is a derived trait (Hughes et al. 2008). When eusociality evolved in the Hymenoptera, it was in the context of the highest family levels of kinship possible: a colony headed by a single queen mated to a single male (Hughes et al. 2008). Under these circumstances, a daughter helper is as related to siblings as to offspring. Hamilton (1964) pointed out that multiple mating by queens would reduce relatedness and that this would lower the incentive to helping and suggested, therefore, that multiple mating evolved after eusociality. The contention that high kinship may have evolved after eusociality (Wilson & Holldobler 2005; Wilson 2008) is rejected. Although single mating by females does not provide any special kinship incentive towards working versus breeding alone from the perspective of an incipient worker, it also provides no disincentive provided that a helper’s efforts are as productive in rearing siblings as in rearing offspring when nesting independently. High relatedness is certainly not a sufficient condition for the evolution of eusociality but it appears to be necessary. When relatedness is high, even small asymmetries in costs versus benefits that favour rearing siblings instead of offspring can select for helping. In addition, offspring are not selected to resist manipulation and coercion from parents or siblings that increase the probability of helping instead of nesting independently (Charnov 1978; Stubblefield & Charnov 1986; Linksvayer & Wade 2005). A favourable benefit-to-cost ratio may arise in a simple way via a reproductive head start (Queller 1989), extended parental care (Queller 1994) or ecological factors that make it hard for offspring to nest independently. There must also be a way of providing aiding and directing the aid to kin, such as by defending the natal nest and feeding the young there. Thus, in addition to high relatedness, factors such as nest building and the need for brood care or defence are necessary for eusociality to evolve (Queller 1989, 1994; Strassmann & Queller 1989; Gadagkar 1990). Boomsma (2007, 2009) also addresses the importance of kinship in the evolution of eusociality versus cooperative breeding, which he views as two alternative social outcomes, rather than as a continuum. High levels of kinship over the life of the parents arise from lifetime pairing in termites and the absence or remating in ants, bees and wasps. In contrast, changing partners is frequent in vertebrate societies and leads to a reduction in kinship among offspring (Boomsma 2007). As a result, where helping Phil. Trans. R. Soc. B (2009)

F. L. W. Ratnieks & H. Helantera¨ 3171

occurs in vertebrates, it is usually on a temporary basis and has never led to a morphologically specialized worker caste (Clutton-Brock 2009). (e) Kinship and the origin of distinct queen and worker castes The most familiar and abundant eusocial insects do not merely have working and reproducing colony members. They have morphologically distinct castes in which the workers have reduced reproductive abilities and the queens have increased reproductive abilities. The evolution of distinct castes has not occurred in all lineages, but is characteristic of termites and three groups of eusocial Hymenoptera: ants, Vespinae wasps (hornets and yellowjackets) and Apidae bees (honeybees, stingless bees and bumble bees) and also occurs in allodapine bees (Schwarz et al. 2007) and Epiponini wasps. Queens in some of these species can have amazing egg-laying abilities, and in the Hymenoptera, the ability to store, keep alive and eke out the millions of sperm needed to fertilize up to millions of female eggs over up to 20 years of egg laying following the nuptial flight (Ho¨lldobler & Wilson 2008). Workers in these groups of Hymenoptera have typically lost the ability to mate and so can only lay unfertilized, haploid, male eggs. (In a few genera of ants and stingless bees, the workers are completely sterile.) Workers of these species have lost the ability to nest independently—they cannot ‘opt out’ of social life. Interestingly, it is only in groups with non-totipotent workers that we see high levels of multiple mating by queens (Hughes et al. 2008). It may be restricted to these species because multiple mating in species with totipotent workers may lead to workers opting out. Opting out could select against multiple mating in one of two ways. First, queens that mated multiply would be disadvantaged relative to queens that mated singly if their daughters facultatively adjusted their probability of helping versus nesting independently based on queen-mating frequency. Nesting independently would be a relatively better option for daughters in a colony headed by a multiple-mated versus a single-mated queen. (Social insect workers are capable of detecting the mating frequency of their queen, probably through assessing the diversity of her offspring, and adjusting their helping behaviour (Sundstrom 1994; Sundstro¨m et al. 1996; Ratnieks et al. 2007).) Second, even if workers do not facultatively respond to the mating frequency of their mother queen, species with multiple mating by queens might revert back to non-eusociality as an evolved response by offspring over many generations to reduced average relatedness. Reversions to noneusociality have occurred in Halictidae bees (Danforth et al. 2003; Schwarz et al. 2007), but probably not for this reason. 3. THE EVOLUTION OF EXTREME ALTRUISM AND INEQUALITY IN MODERN-DAY SPECIES (a) To reproduce or to help others reproduce? A female bee, ant or wasp in a species with morphologically distinct queens and workers, makes two life-history decisions that determine whether she will

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3172

F. L. W. Ratnieks & H. Helantera¨ Review. Inequality in insect societies (a) life history decisions leading to reproductive division of labour reproductive morphology totipotent individual

active ovaries do little or no work worker morphology (altruist) inactive ovaries (altruist) work for good of colony

(b) actual decisions made by honeybee females queen, 0.01% larva

coercion

worker, 99.99%

egg-laying worker, <0.1% coercion

working worker, >99.9%

(c) predicted decisions based on voluntary altruism alone queen, ca 50% larva

no coercion

egg-laying worker, ca 50%

worker, ca 50% no coercion

working worker, ca 50%

(d ) acquiescence in decisions made by honeybee females queen, r = 0.5 larva

acquiescence to coercion

worker, r = 0.3 (0.25 to 0.75)

egg-laying worker, r = 0.5 acquiescence to coercion

working worker, r = 0.25 Figure 1. Working versus reproducing. (a) In insect societies with morphologically distinct queens and workers, a female makes two life history decisions that determine whether it will reproduce or work. (b) In the honeybee, A. mellifera, owing to social coercion, most females become altruists at both these decision points. (c) In the honeybee, a species with low relatedness (r ¼ 0.3) among female offspring owing to multiple mating by the mother queen, the proportions becoming altruists are much higher than expected based on ‘voluntary’ altruism alone, as would occur in the absence of coercion. (d) Individuals acquiesce to coercion by becoming altruists because they rear kin and so gain inclusive fitness. Worker honeybees are related to the queen’s female and male offspring (r ¼ 0.3, 0.25) even though this is not as high as the relatedness of a queen or an egg-laying worker to its own offspring (r ¼ 0.5).

reproduce or help (figure 1a). Early in life, females in most species are totipotent and can develop into either a queen or a worker depending on environmental factors, and in particular on how they are treated as larvae (Wilson 1971). In the larval stage, the individual commits to developing either as a queen or as a worker. In the adult stage, an individual that has developed into a worker can activate its ovaries and lay eggs or not. At both decision points, almost all honeybee females take the non-reproductive option (figure 1b). From an inclusive fitness perspective this is puzzling because we expect a large proportion to try to reproduce (Bourke & Ratnieks 1999; Ratnieks 2001; Wenseleers et al. 2004a). If individual honeybee females were free to choose their own caste fate, approximately 50 per cent should develop into queens, given that honeybee queens mate with approximately 10 – 20 males, which reduces relatedness among the female offspring to 0.3 – 0.275 (figure 1c). Even in species with high relatedness, in Phil. Trans. R. Soc. B (2009)

which the mother queen is mated to a single male, a large proportion, up to 20 per cent, are expected to develop into queens. Similar results are obtained when analysing the proportion of workers that lay eggs (Wenseleers et al. 2004b). These proportions are calculated by determining the critical proportion at which the inclusive fitness benefit from helping is equal to that of attempting to reproduce (by a larva developing into a queen or a worker activating its ovaries and laying eggs) under the assumption that reproducing individuals do not do any work and that the productivity of the colony is in direct proportion to the proportion of working individuals. If these assumptions are relaxed (Wenseleers et al. 2004a,b), the general result that a substantial proportion of individuals should attempt to reproduce instead of work remains, but the proportions change. Family levels of relatedness are simply not high enough to eliminate potential conflict over reproduction. Relatedness of 1, as occurs in a

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Inequality in insect societies clonal group, would be needed (Ratnieks & Reeve 1992; Gardner & Grafen 2009).

(b) Social coercion: the cause of extreme altruism and inequality There is a bad fit between the theoretical prediction (figure 1c) and the empirical data (figure 1b) because the model leaves out social coercion. The model’s prediction is based on ‘voluntary’ altruism alone (Ratnieks & Wenseleers 2008). That is, on the assumption that an individual’s options are not affected by social interactions. In fact, both reproductive decisions are greatly affected by coercion imposed by adult workers and sometimes the mother queen. In most social insects, queens are considerably larger than workers. Although nests may contain abundant food stores, larvae lack mobility and can normally eat only what they are given by the adult workers. In the honeybee, for example, queens are reared in special royal cells that are larger than the small hexagonal cells used to rear workers and receive special food known as royal jelly. As a result, female larvae are normally powerless to determine their own caste fate because they cannot obtain the additional food needed to develop into a queen if the adult workers do not provide it. Melipona stingless bees are a telling exception. In stingless bees, each larva is reared in a sealed cell on a food mass placed there by the workers before the queen lays an egg. Each cell is sealed by a worker immediately after egg laying. Melipona queens are not larger than workers, although they are morphologically distinct. Queens and workers are reared side by side in identical sealed cells. Far more queens are reared than required by the colony, which would normally need just a few ‘spare’ queens in the event that the mother queen dies or the colony is swarming (Ratnieks 2001). Excess queens are executed shortly after emerging as adults from their cells (Wenseleers & Ratnieks 2004). The Melipona situation is a clear example of individual colony members being able to make decisions about whether or not to be altruists in the absence of coercion. Self-interest causes more to develop as queens than is needed for the colony to function effectively. In the case of male production by workers, in many species worker-laid eggs are eaten by other workers (worker policing) or by the queen (queen policing) (Ratnieks 1988; Wenseleers & Ratnieks 2006a). As a result, a worker that lays eggs does not necessarily have offspring. In the honeybee, worker policing is approximately 98 per cent effective in killing workerlaid eggs. Egg-laying workers can also be subject to physical aggression (Visscher & Dukas 1995; Monnin & Ratnieks 2001), and in some ants, this is known to cause the victim’s ovaries to regress (Monnin & Ratnieks 2001). In the honeybee, worker policing is normally (Miller & Ratnieks 2001) but not always (Chaˆline et al. 2004) switched off in queenless colonies and a batch of males is reared before the colony dies out through dwindling of the work force. In a honeybee colony with a queen, egg laying by workers is not needed for the colony to function effectively. The queen has sufficient fecundity to lay all the Phil. Trans. R. Soc. B (2009)

F. L. W. Ratnieks & H. Helantera¨ 3173

eggs, both male and female, that the colony can rear into adults. In queenless colonies, far more workers activate their ovaries than are needed to allow a batch of males to be reared. Each male cell can only be used to rear one larva at a time, but typically has many eggs laid in it. (c) Beating the system by evading coercion Why do not individuals rebel against social coercion? In some cases, they do. Evasion is predicted by inclusive fitness theory because an individual is generally more related to its own offspring. In the case of male production, a worker is more related to sons (0.5) than to nephews (other workers’ sons, maximum of 0.375) or brothers (0.25). Thus, there is a strong relatedness incentive to rebel. Similarly, in caste fate conflict, a female larva will be more related to its own offspring (0.5) than to a sister queen’s offspring (maximum of 0.375). So even if actual conflict over whether or not to reproduce is reduced through coercion, potential conflict still exists. A good example of evasion is provided by dwarf queens in trigonine stingless bees. Unlike Melipona stingless bees, trigonine queens are larger than workers and are normally reared in larger sealed cells. But in some species, a female larva being reared in a worker cell develops into a small-sized queen. These dwarf queens can mate and head colonies (Ribeiro et al. 2006). In some trigonine bees, a larva may be able to break into a neighbouring cell to obtain additional food, and thereby develop into a queen (Faustino et al. 2002; Ribeiro et al. 2006). In the honeybee, A. mellifera, some workers are able to lay eggs that evade egg policing (Barron et al. 2001; Martin et al. 2002). In some Asian species of honeybees, workers can adopt a parasitic strategy of joining queenless colonies and laying eggs (Nanork et al. 2005, 2007). As workers in queenless honeybee colonies stop policing worker-laid eggs (Miller & Ratnieks 2001), the chance that eggs laid by a joining worker will be reared is greater in a queenless colony. (d) Comparative tests of the effects of kinship and coercion The above examples make sense from an inclusive fitness perspective. Melipona bees are a particularly compelling case showing how the absence of coercion can allow individuals to attempt to reproduce even when this is against the best interest of their colony as a whole. But a good theory should ideally provide quantitative tests and predictions. Because levels of kinship and coercion vary across species, a comparative approach provides a powerful way of testing theory. In terms of voluntary altruism, inclusive fitness theory predictions are supported by a comparison of queenless colonies in nine species of wasps and the honeybee (Wenseleers & Ratnieks 2006b). Among these 10 species, there is great variation in relatedness among the female offspring, from 0.75 to 0.3 owing to variation in queen mating frequency, and in the proportion of egg-laying workers, from ca 8 per cent to 37 per cent. As predicted, there is a strong positive

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3174

F. L. W. Ratnieks & H. Helantera¨ Review. Inequality in insect societies

relationship between the proportion of altruists (nonlaying workers) and relatedness. For example, the species with the lowest relatedness, the honeybee, has the highest proportion of egg-laying workers. When colonies with a queen are studied, the relationship in the same 10 species is reversed (Wenseleers & Ratnieks 2006b). The honeybee is now the species with the lowest proportion of egglaying workers (less than 0.1%). Here the prediction based on voluntary altruism is not relevant because kinship is not the only factor influencing levels of altruism in queenright colonies. A second factor is coercion in the form of egg policing. In the 10 species, the proportion of worker-laid eggs that are killed, either by the queen or by the workers or by both, varies from approximately 40 to 100 per cent. The proportion of egg-laying workers declines significantly as the effectiveness of policing increases. Policing has long been known to kill worker-laid eggs and to be highly effective in doing so (Ratnieks & Visscher 1989; Ratnieks 1993; Visscher 1996; Foster & Ratnieks 2001a). The comparative study shows that it also deters workers from attempting to lay eggs in the first place (Wenseleers & Ratnieks 2006b). Although egg policing does not directly punish egg-laying workers, when most of their eggs are killed it is better in terms of inclusive fitness to work to rear relatives than to lay eggs few of which will be reared into offspring. However, policing by aggression against workers who are activating their ovaries is punishment (Monnin & Ratnieks 2001).

(e) Application of inclusive fitness theory The above examples show that making predictions from inclusive fitness theory is relatively complex. In particular, it is necessary to consider how the theory influences both attempted reproduction and coercion (figure 2, table 1). In some circumstances, the effects of kinship work in opposite directions (table 1). Thus, a colony headed by a single mother queen mated to a single male gives high relatedness among the female offspring and, in the absence of coercion, causes a higher level of altruism (i.e. a lower proportion of individuals attempting to reproduce instead of working). Multiple mating by queens leads to lower relatedness among the workers and reduces the expected level of voluntary altruism. But it also increases the incentive for workers to police the reproduction (production of males) of other workers (Ratnieks 1988; Wenseleers & Ratnieks 2006a). Counter-intuitively, therefore, low relatedness can lead to greater levels of altruism than high relatedness (Ratnieks 1988). This is because family levels of relatedness cannot reach the value (1) necessary to eliminate all potential conflicts over reproduction versus working based on voluntary altruism alone. But social coercion, via the policing of worker-laid eggs, can be sufficiently effective to reduce the benefits of attempted reproduction to a level at which very few or even zero workers should attempt to lay eggs (Wenseleers et al. 2004b). The resolution of conflict due to coercion does not depend on removing the source of the conflict—potential conflict still exists. Phil. Trans. R. Soc. B (2009)

kinship and relatedness in social group

direct effect

indirect effect

coercion of individuals in social group

level of altruism in social group Figure 2. Direct and indirect effects on the level of altruism in a social group, as affected by kinship and relatedness. Kinship has a direct effect (voluntary altruism) but also a wide range of indirect effects via its effect on coercion (enforced altruism). In applying inclusive fitness theory, it is necessary to integrate these multiple effects. See table 1 and the text for examples of indirect effects.

Rather, effective policing reduces actual conflict by making working relatively more worthwhile than attempting to reproduce, given that few of the eggs laid by a worker will be reared and egg-laying workers do less work. In terms of Hamilton’s rule, policing reduces the cost of altruism. Many inclusive fitness factors influence coercion (figure 2, table 1). Thus, worker policing of workerlaid male eggs can be favoured on relatedness grounds (Ratnieks 1988), sex allocation grounds (Foster & Ratnieks 2001b) and colony efficiency grounds (Ratnieks 1988). In addition, queen policing and selfish worker policing (the situation in which egg-laying workers also kill eggs laid by other workers (Wenseleers et al. 2005)) are both based on the inclusive fitness benefit that arises from the fact that a female is more related to her sons (0.5) than her grandsons (0.25) (queen policing) and to her sons than her nephews (full nephews 0.375). In addition, theory is only part of the picture. In a situation where coercers have one optimum and individuals that have the potential to reproduce have another optimum, what is the outcome? Is there an outright winner or is there some intermediate stalemate or balance? The outcome cannot be predicted by theory because it depends on a wide range of biological factors, which are often highly idiosyncratic and vary among groups at all taxonomic levels from subspecies to order (Beekman & Ratnieks 2003; Ratnieks et al. 2006). One obvious difference in the biology of honeybees and stingless bees is that honeybees rear brood progressively in open cells while stingless bees rear brood in sealed cells. This difference has profound effects on the outcome of reproductive conflicts. In particular, it has given individual female larvae more power over their caste fate because it limits the power of the adult workers to check the development of larvae. In Melipona stingless bees, mass provisioning combined with the fact that

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Inequality in insect societies

F. L. W. Ratnieks & H. Helantera¨ 3175

Table 1. Challenges in applying inclusive fitness theory to the alternative individual strategies of reproduction versus altruism in insect societies. challenge in applying inclusive fitness theory

empirical example in relation to reproduction versus altruism

must consider both direct and indirect effects of kinship

in queenless colonies, only the direct effect applies in relation to worker egg laying (production of males). In queenright colonies, indirect effects, via coercion (e.g. killing of worker-laid eggs, aggression of egg laying workers), also occur but vary in importance among species worker policing (coercion) is more strongly selected for when relatedness among female offspring is low due to multiple mating by the queen. Self-restraint/ acquiescence is more strongly selected when relatedness is high or when coercion is effective egg policing, for example, can be carried out by the queen or by workers. Worker policing of eggs may be carried out either by egg-laying workers (selfish policing) or by non-reproducing workers brood-rearing method of stingless bees versus honeybees. When each larva is reared in a sealed cell (mass provisioning) individual larvae have more power over their own caste fate than in the honeybee, in which each larva is reared progressively in an open cell egg policing requires policing individuals to be able to discriminate between queen-laid and worker-laid eggs individuals have an incentive to evade social coercion. Dwarf queens in trigonine stingless bees develop in a worker cell. Honeybee workers may lay eggs that evade worker policing, or enter a nearby queenless colony in which worker policing has been switched off worker policing of worker-laid eggs can be selected for on sex allocation grounds. This may account for the occurrence of worker policing in species with queens mated to a single male policing on colony efficiency grounds. Insurance and head start benefits in the origin of eusociality. Ecological factors that affect the ease or difficulty of founding a nest independently

must consider both reproducing and coercing individuals

must take into account all relevant parties

must consider idiosyncracies that affect power relations among colony members

must consider information

evasion

must consider interactions with other conflicts

must consider also benefits and costs

queens are not larger than workers has resulted in almost complete power being in the hands of individual larvae. Brood rearing in sealed cells may also give stingless bee queens more power over colony sex ratio, as this will make it difficult for workers to manipulate the sex ratio during brood rearing as occurs in ants (Sundstro¨m et al. 1996).

4. CONSEQUENCES AND WHY DOES IT MATTER? (a) Enforced altruism and acquiescence An important consequence of the fact that eusocial insect societies are families is acquiescence (Wenseleers et al. 2004a,b) by coerced individuals. As noted above, there is a strong incentive for evasion given that individuals are more related to their own sons than to the queen’s sons (incentive to evade control over worker production of males) and to their own offspring versus their sister’s offspring (incentive to evade caste-fate control and incentive to evade control over worker Phil. Trans. R. Soc. B (2009)

selected references Wenseleers & Ratnieks (2006b)

Ratnieks (1988), Wenseleers et al. (2004b)

Wenseleers & Ratnieks (2006a)

Bourke & Ratnieks (1999), Wenseleers & Ratnieks (2004)

Beekman & Ratnieks (2003)

Beekman & Oldroyd (2008), Ribeiro et al. (2006)

Foster & Ratnieks (2001b)

Ratnieks (1988), Queller (1989)

production of males). But living in a family also means that individuals who are coerced into a nonreproductive role do not have zero inclusive fitness. In the honeybee, for example, workers are approximately half as related to the female and male offspring being reared in the colony as the queen (figure 1d). The relative significance of coercion and relatedness vary considerably at different stages in the origin and elaboration of eusociality and inequality (figure 3) (Bourke 1999). Coercion probably played a minor role compared to high relatedness at the origin of eusociality (Ratnieks & Wenseleers 2008). Once eusociality has evolved, coercion (especially by the mother queen) may then evolve, with high relatedness helping to select for acquiescence in the offspring for working at the parental nest versus nesting independently. When workers and queens are morphologically different, such that workers have lost the ability to nest independently, high relatedness is not necessary to prevent offspring from opting out to nest independently. In the majority of species, the evolution of distinct worker

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3176

F. L. W. Ratnieks & H. Helantera¨ Review. Inequality in insect societies occasional association of mother and daughter or daughters totipotent individuals high relatedness no coercion Helper daughters have not been selected for a helping role. High relatedness, and a favourable cost : benefit ratio via ‘insurance’, ‘head start’, etc. result in this unselected helping behaviour not being selected against.

×

colony of mother/queen and daughters totipotent individuals high relatedness coercion by mother/queen Selection favours specialized queen and worker roles with physiological and behavioural differences.

×

×

×

colony of morphologically distinct queen and workers workers not totipotent high relatedness coercion by workers and also by queen Morphologically distinct worker caste evolves, with coercion of larvae by adult workers and larval acquiescence to coercion; increased fecundity of queen. colony of queen and workers workers not totipotent reduced relatedness via multiple paternity or polygyny coercion by workers Once caste fate conflict has been resolved via coercion of larvae, relatedness may decrease through multiple mating or polygyny. Decreased relatedness selects more strongly for worker policing of worker-laid male eggs. in some ants: unicoloniality/many queens workers not totipotent very low relatedness via unicoloniality/many queens coercion by workers Ecological factors may favour increased queen number and breakdown of distinct colonies. Coercion and acquiescene initially maintain working/helping despite very low relatedness. However, this may select against acquiescence making low relatedness eusociality unstable over evolutionary time.

Figure 3. How relatedness and coercion interact in the evolution of insect societies. At the origin of eusociality, relatedness is high but coercion is low or non-existent. As eusociality evolves further, the role of coercion and acquiescence increases and workers become morphologically distinct from queens. This allows relatedness to decrease via multiple mating by queens and/or polygyny. Extreme polygyny, as in some ants which are shown without wings, can cause relatedness to drop almost to zero. This may be an evolutionary dead end.

and queen castes will also result in female larvae being subject to effective coercion via food control so that excess offspring queens are not reared. At this stage, a large diversity of social structures with a wide range of relatedness values (Bourke & Franks 1995) may evolve. But even in highly derived eusocial species where conflicts seem extremely well resolved through enforced altruism, relatedness still plays a major role in determining potential conflicts (Ratnieks & Reeve 1992) and, through its effect on coercion, on actual conflict. The lower the relatedness in a colony, the stronger the incentive for evasion. This may explain why species where colony relatedness approaches zero, such as unicolonial ants, seem to be evolutionary dead ends (Helantera¨ et al. 2009). Very low-relatedness societies may be successful in the short term, such as for invasive Phil. Trans. R. Soc. B (2009)

unicolonial ants, but not in the long term if selection favouring selfishness predominates over selection favouring working for the colony via acquiescence. One analogy sometimes used to describe an insect society is that of a factory (Oster & Wilson 1978). To extend the analogy, it is a factory in which the working individuals are not as well paid as the boss or owner (the queen). But neither are they badly paid. There are few human businesses or organizations in which the highest salary is only twice the lowest, as occurring in the honeybee. (b) Creating a better society: building an organism made of many individuals Why does it matter that many insect societies, including the honeybee, seem to have almost entirely

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Inequality in insect societies resolved their internal conflicts over reproduction via coercion? On the one hand, it matters because the understanding of this issue shows the explanatory power of Hamilton’s (1964) theory and is important in the study of social evolution. But it also matters in that it shows how natural selection can cause societies to become more organism like, so that the actions of all or most individuals serve colony rather than individual interests (Ratnieks & Reeve 1992; Seeley 1995; Ratnieks et al. 2006; Gardner & Grafen 2009; Queller & Strassmann 2009; see also Wilson & Ho¨lldobler 2005; Ho¨lldobler & Wilson 2008; Wilson 2008 for alternative viewpoints). Many insect societies have high levels of actual conflict. Melipona bees are a good example. They have the highest possible levels of family relatedness (a single queen mated to a single male), and their colonies show remarkable levels of internal organization. But they also show one of the most glaring examples of an unresolved conflict that can be seen in social insects. Colonies rear and execute many excess queens, and this clearly comes at a cost to the colony as every queen executed takes up exactly the same resources as needed to produce a worker—a cell provisioned with food. Complete or almost complete resolution of these conflicts requires coercion to play an additional role. In contrast to Melipona, honeybee societies have almost zero actual conflict due to effective coercion of individuals at the two critical decision points in an individual’s life (figure 1).

5. DISCUSSION The examples, theory and evidence presented above make it clear that many modern-day insect societies, as exemplified by the honeybee, are harmonious because of effective social coercion. Coercion has evolved after eusociality and acts to prevent individuals attempting to reproduce instead of working. Without coercion, more insect societies would be like colonies of Melipona or queenless honeybees, in which a large proportion of colony resources and individual lives are directed into intra-colony competition over reproduction rather than into working to increase the colony’s total reproduction. Insect societies are not the only type of social group in which the interests of different individuals vary and in which social coercion plays a role in reducing conflict (West et al. submitted; Ratnieks & Wenseleers 2008). In insect societies, this has led to extreme inequality. But in other social groups, the outcome may be greater equality or fairness. In interspecies mutualisms, for example, the partners are completely unrelated and coercion often serves to prevent one partner overexploiting the other (Kiers et al. 2003; Foster & Wenseleers 2006). Human society at the family level involves interaction among kin and the possibility of extreme altruism (Foster & Ratnieks 2005). But at the wider level, relatedness is low. Human society is based mainly on the benefits of mutual cooperation (Ratnieks 2006). As in insect societies, coercion is prevalent in human society (West et al. submitted). We are all constantly subject to subtle and sometimes Phil. Trans. R. Soc. B (2009)

F. L. W. Ratnieks & H. Helantera¨ 3177

not so subtle forms of coercion from the people we interact with. Coercion of this type exists even in primitive societies (Henrich et al. 2006) and is probably a very long-established part of human life and that of the ancestors of Homo sapiens. Advanced societies, such as the modern-day nation states, typically have elaborate ways of coercing group members including institutionalized police forces, taxation, punishment and surveillance. Opting out (except by migrating to another nation, which probably has similar restrictions) is not permitted. Coercion is well known for enforcing inequality, such as when it serves to promote the advantage of an elite. One encouraging trend in human political development in the use of coercion is that it is increasingly used to promote greater equality and cooperation. In a modern nation state, no one is supposed to be above the law and extremes of wealth and poverty are reduced via redistribution through the tax system and the provision of education, healthcare, pensions, social safety nets, etc. Although such attempts at creating greater equality are inevitably contentious, and in the extreme have proved to be unworkable, the elimination of extreme inequality is surely a worthwhile objective. In regard to equality, therefore, the current endpoints in human and insect social evolution are almost exactly opposite, with human society moving towards greater equality and insect societies to greater inequality. But in some other respects, such as in achieving greater social complexity, size and ecological importance, the current endpoints have much in common. We thank Stuart West, Claire El Mouden and an anonymous referee for helpful comments. H.H. was funded by the Academy of Finland (grant number 121078).

REFERENCES Barron, A. & Oldroyd, B. 2001 Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review. Behav. Ecol. Sociobiol. 50, 199 –208. (doi:10.1007/ s002650100362) Beekman, M. & Oldroyd, B. P. 2008 When workers disunite: intraspecific parasitism by eusocial bees. Ann. Rev. Entomol. 53, 19– 37. (doi:10.1146/annurev.ento.53.103106. 093515) Beekman, M. & Ratnieks, F. L. W. 2003 Power over reproduction in social Hymenoptera. Phil. Trans. R. Soc. Lond. B 358, 1741–1753. (doi:10.1098/rstb.2002.1262) Boomsma, J. J. 2007 Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17, R673– R683. (doi:10.1016/j.cub.2007.06.033) Boomsma, J. J. 2009 Lifetime monogamy and the evolution of eusociality. Phil. Trans. R. Soc. B 364, 3191–3207. (doi:10.1098/rstb.2009.0101) Bourke, A. F. G. 1999 Colony size, social complexity and reproductive conflict in social insects. J. Evol. Biol. 12, 245–257. (doi:10.1046/j.1420-9101.1999.00028.x) Bourke, A. F. G. & Franks, N. R. 1995 Social evolution in ants. Princeton, NJ: Princeton University Press. Bourke, A. F. G. & Ratnieks, F. L. W. 1999 Kin conflict over caste determination in social Hymenoptera. Behav. Ecol. Sociobiol. 46, 287– 297. (doi:10.1007/s002650050622) Chaˆline, N., Martin, S. J. & Ratnieks, F. L. W. 2004 Worker policing persists in a hopelessly queenless honey bee

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3178

F. L. W. Ratnieks & H. Helantera¨ Review. Inequality in insect societies

colony (Apis mellifera). Insectes Sociaux 51, 113 –116. (doi:10.1007/s00040-003-0708-y) Charnov, E. L. 1978 Evolution of eusocial behavior—offspring choice or parental parasitism. J. Theor. Biol. 75, 451 –465. (doi:10.1016/0022-5193(78)90356-9) Clutton-Brock, T. 2009 Structure and function in mammalian societies. Phil. Trans. R. Soc. B 364, 3229– 3242. (doi:10.1098/rstb.2009.0120) Danforth, B. N., Conway, L. & Ji, S. 2003 Phylogeny of eusocial Lasioglossum reveals multiple losses of eusociality within a primitively eusocial clade of bees (Hymenoptera: Halictidae). Syst. Biol. 52, 23– 36. (doi:10.1080/ 10635150390132687) Darwin, C. 1859 On the origin of species by means of natural selection. London, UK: John Murray. Dugatkin, L. A. 2006 The altruism equation. Princeton, NJ: Princeton University Press. Faustino, C. D., Silva-Matos, E. V., Mateus, S. & Zucchi, R. 2002 First record of emergency queen rearing in stingless bees (Hymenoptera, Apinae, Meliponini). Insectes Sociaux 49, 111 –113. (doi:10.1007/s00040-002-8287-x) Foster, K. R. & Ratnieks, F. L. W. 2001a Convergent evolution of worker policing by egg eating in the honeybee and common wasp. Proc. R. Soc. Lond. B 268, 169–174. (doi:10.1098/rspb.2000.1346) Foster, K. R. & Ratnieks, F. L. W. 2001b The effect of sexallocation biasing on the evolution of worker policing in hymenopteran societies. Am. Nat. 158, 615–623. Foster, K. R. & Ratnieks, F. L. W. 2005 A new eusocial vertebrate? Trends Ecol. Evol. 20, 363–364. (doi:10.1016/j. tree.2005.05.005) Foster, K. R. & Wenseleers, T. 2006 A general model for the evolution of mutualisms. J. Evol. Biol. 19, 1283–1293. (doi:10.1111/j.1420-9101.2005.01073.x) Gadagkar, R. 1990 Evolution of eusociality—the advantage of assured fitness returns. Phil. Trans. R. Soc. Lond. B 329, 17–25. (doi:10.1098/rstb.1990.0146) Gardner, A. & Grafen, A. 2009 Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659 –671. (doi:10.1111/j.1420-9101.2008.01681.x) Grafen, A. 2006 Optimization of inclusive fitness. J. Theor. Biol. 238, 541 –563. (doi:10.1016/j.jtbi.2005.06.009) Grafen, A. 2009 Formalizing Darwinism and inclusive fitness theory. Phil. Trans. R. Soc. B 364, 3135– 3141. (doi:10.1098/rstb.2009.0056) Hamilton, W. D. 1964 Genetical evolution of social behaviour I. J. Theor. Biol. 7, 1 –16. (doi:10.1016/00225193(64)90038-4) Helantera¨, H., Strassmann, J. E., Carrillo, J. & Queller, D. C. 2009 Unicolonial ants: where do they come from, what are they, and where are they going? Trends Ecol. Evol. 24, 341 –349. (doi:10.1016/j.tree.2009.01.013) Henrich, J. et al. 2006 Costly punishment across human societies. Science 312, 1767–1770. (doi:10.1126/science. 1127333) Herbers, J. H. 2009 Darwin’s ‘one special difficulty’: celebrating Darwin 200. Biol. Lett. 5, 214–217. (doi:10. 1098/rsbl.2009.0014) Ho¨lldobler, B. & Wilson, E. O. 2008 The superorganism. New York, NY: WW Norton & Company Inc. Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. 2008 Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213– 1216. (doi:10.1126/science.1156108) Hunt, J. 2007 The evolution of social wasps. Oxford, UK: Oxford University Press. Kiers, E. T., Rousseau, R. A., West, S. A. & Denison, R. F. 2003 Host sanctions and the legume –rhizobium mutualism. Nature 425, 78–81. (doi:10.1038/ nature01931) Phil. Trans. R. Soc. B (2009)

Linksvayer, T. A. & Wade, M. J. 2005 The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony. Q. Rev. Biol. 80, 317–336. (doi:10.1086/432266) Martin, S. J., Beekman, M., Wossler, T. C. & Ratnieks, F. L. W. 2002 Parasitic worker honey bees, Apis mellifera capensis, evade policing. Nature 415, 163–165. Miller, D. G. & Ratnieks, F. L. W. 2001 The timing of worker reproduction and breakdown of policing behaviour in queenless honey bee (Apis mellifera L.) societies. Insectes Sociaux 48, 178–184. (doi:10.1007/PL00001762) Monnin, T. & Ratnieks, F. 2001 Policing in queenless ponerine ants. Behav. Ecol. Sociobiol. 50, 97–108. (doi:10.1007/ s002650100351) Nanork, P., Paar, J., Chapman, N. C., Wongsiri, S. & Oldroyd, B. P. 2005 Asian honeybees parasitize the future dead. Nature 437, 829– 829. (doi:10.1038/ 437829a) Nanork, P., Chapman, N. C., Wongsiri, S., Lim, J., Gloag, R. S. & Oldroyd, B. P. 2007 Social parasitism by workers in queenless and queenright Apis cerana colonies. Mol. Ecol. 16, 1107–1114. (doi:10.1111/j.1365-294X.2006. 03207.x) Oster, G. F. & Wilson, E. O. 1978 Caste and ecology in the social insects. Princeton, NJ: Princeton University Press. Prete, F. 1990 The conundrum of the honeybees: one impediment to the publication of Darwin’s theory. J. Hist. Biol. 23, 271–290. (doi:10.1007/BF00141472) Queller, D. C. 1989 The evolution of eusociality: reproductive head starts of workers. Proc. Natl Acad. Sci. USA 86, 3224– 3226. (doi:10.1073/pnas.86.9.3224) Queller, D. C. 1994 Extended parental care and the origin of eusociality. Proc. R. Soc. Lond. B 256, 105 –111. (doi:10. 1098/rspb.1994.0056) Queller, D. C. & Strassmann, J. E. 2009 Beyond society: the evolution of organismality. Phil. Trans. R. Soc. B 364, 3143– 3155. (doi:10.1098/rstb.2009.0095) Ratnieks, F. L. W. 1988 Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132, 217 –236. Ratnieks, F. 1993 Egg-laying, egg-removal, and ovary development by workers in queenright honey bee colonies. Behav. Ecol. Sociobiol. 32, 191 –198. Ratnieks, F. L. W. 2001 Heirs and spares: caste conflict and excess queen production in Melipona bees. Behav. Ecol. Sociobiol. 50, 467 –473. (doi:10.1007/s002650100388) Ratnieks, F. L. W. 2006 Can humans learn from insect societies? Nova Acta Leopoldina 345, 97–116. Ratnieks, F. L. W. & Reeve, H. K. 1992 Conflict in singlequeen hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species. J. Theor. Biol. 158, 33– 65. (doi:10.1016/S00225193(05)80647-2) Ratnieks, F. L. W. & Visscher, P. K. 1989 Worker policing in the honeybee. Nature 342, 796 –797. (doi:10.1038/ 342796a0) Ratnieks, F. L. W. & Wenseleers, T. 2008 Altruism in insect societies and beyond: voluntary or enforced? Trends Ecol. Evol. 23, 45–52. (doi:10.1016/j.tree.2007.09.013) Ratnieks, F. L. W., Wenseleers, T. & Foster, K. R. 2006 Conflict resolution in insect societies. Ann. Rev. Entomol. 51, 581 –608. (doi:10.1146/annurev.ento.51.110104. 151003) Ratnieks, F. L. W., Helantera¨, H. & Foster, K. R. 2007 Are mistakes inevitable? Sex allocation specialization by workers can reduce the genetic information needed to assess queen mating frequency. J. Theor. Biol. 244, 470– 477. (doi:10.1016/j.jtbi.2006.09.003) Ribeiro, M. d. F., Wenseleers, T., Santos Filho, P. d. S. & Alves, D. d. A. 2006 Miniature queens in stingless bees:

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Inequality in insect societies basic facts and evolutionary hypotheses. Apidologie 37, 191 –206. (doi:10.1051/apido:2006023) Schwarz, M. P., Richards, M. H. & Danforth, B. N. 2007 Changing paradigms in insect social evolution: Insights from halictine and allodapine bees. Ann. Rev. Entomol. 52, 127–150. (doi:10.1146/annurev.ento.51.110104.150950) Seeley, T. D. 1995 The wisdom of the hive. Cambridge, MA: Harvard University Press. Starr, C. 1979 Origin and evolution of insect sociality: a review of modern theory. In Social Insects vol. 1 (ed. H. Hermann), pp. 35– 79. New York, NY: Academic Press Inc. Strassmann, J. E. & Queller, D. C. 1989 Ecological determinants of social evolution. In The genetics of social evolution (eds M. Breed & R. Page), pp. 81–101. Boulder, CO: Westview Press. Stubblefield, J. W. & Charnov, E. L. 1986 Some conceptual issues in the origin of eusociality. Heredity 57, 181–187. (doi:10.1038/hdy.1986.108) Sundstrom, L. 1994 Sex-ratio bias, relatedness asymmetry and queen mating frequency in ants. Nature 367, 266– 267. (doi:10.1038/367266a0) Sundstro¨m, L., Chapuisat, M. & Keller, L. 1996 Conditional manipulation of sex ratios by ant workers: a test of kin selection theory. Science 274, 993 –995. (doi:10. 1126/science.274.5289.993) Thorne, B. 1997 Evolution of eusociality in termites. Ann. Rev. Ecol. Syst. 28, 27–54. (doi:10.1146/annurev. ecolsys.28.1.27) Trivers, R. L. & Hare, H. 1976 Haplodiploidy and evolution of social insects. Science 191, 249–263. (doi:10.1126/ science.1108197) Visscher, P. K. 1989 A quantitative study of worker reproduction in honey bee colonies. Behav. Ecol. Sociobiol. 25, 247– 254. (doi:10.1007/BF00300050) Visscher, P. K. 1996 Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing. Behav. Ecol. Sociobiol. 39, 237–244. (doi:10.1007/s00265 0050286)

Phil. Trans. R. Soc. B (2009)

F. L. W. Ratnieks & H. Helantera¨ 3179

Visscher, K. P. & Dukas, R. 1995 Honey bees recognize development of nestmates’ ovaries. Anim. Behav. 49, 542–544. (doi:10.1006/anbe.1995.0074) Wenseleers, T. & Ratnieks, F. L. W. 2004 Tragedy of the commons in Melipona bees. Proc. R. Soc. Lond. B 271, S310– S312. (doi:10.1098/rsbl.2003.0159) Wenseleers, T. & Ratnieks, F. L. W. 2006a Comparative analysis of worker reproduction and policing in eusocial Hymenoptera supports relatedness theory. Am. Nat. 168, E163–E179. Wenseleers, T. & Ratnieks, F. L. W. 2006b Enforced altruism in insect societies. Nature 444, 50– 50. (doi:10.1038/ 444050a) Wenseleers, T., Hart, A. G. & Ratnieks, F. L. W. 2004a When resistance is useless: policing and the evolution of reproductive acquiescence in insect societies. 164, E154–E167. Wenseleers, T., Helantera¨, H., Hart, A. & Ratnieks, F. L. W. 2004b Worker reproduction and policing in insect societies: an ESS analysis. J. Evol. Biol. 17, 1035–1047. (doi:10.1111/j.1420-9101.2004.00751.x) Wenseleers, T., Tofilski, A. & Ratnieks, F. L. W. 2005 Queen and worker policing in the tree wasp Dolichovespula sylvestris. Behav. Ecol. Sociobiol. 58, 80–86. (doi:10.1007/ S00265-004-0892-4) West, S. A., El Mouden, C. & Gardner, A. Submitted. Social evolution theory and its application to the evolution of cooperation in humans. See http://www.zoo.ox.ac.uk/ group/west/pdf/West_etal.pdf. Wilson, E. O. 1971 Insect societies. Cambridge, MA: Harvard University Press. Wilson, E. O. 1975 In Sociobiology: the new synthesis. Cambridge, MA: Harvard University Press. Wilson, E. O. 2008 One giant leap: how insects achieved altruism and colonial life. Bioscience 58, 17–25. (doi:10. 1641/B580106) Wilson, E. O. & Ho¨lldobler, B. 2005 Eusociality: origin and consequences. Proc. Natl Acad. Sci. USA 102, 13 367–13 371. (doi:10.1073/pnas.0505858102)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3181–3189 doi:10.1098/rstb.2009.0110

Social stability and helping in small animal societies Jeremy Field1,* and Michael A. Cant2 1

Department of Biology and Environmental Science, John Maynard Smith Building, University of Sussex, Brighton BN1 9QG, UK 2 Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Tremough, Penryn TR10 9EZ, UK

In primitively eusocial societies, all individuals can potentially reproduce independently. The key fact that we focus on in this paper is that individuals in such societies instead often queue to inherit breeding positions. Queuing leads to systematic differences in expected future fitness. We first discuss the implications this has for variation in behaviour. For example, because helpers nearer to the front of the queue have more to lose, they should work less hard to rear the dominant’s offspring. However, higher rankers may be more aggressive than low rankers, even if they risk injury in the process, if aggression functions to maintain or enhance queue position. Second, we discuss how queuing rules may be enforced through hidden threats that rarely have to be carried out. In fishes, rule breakers face the threat of eviction from the group. In contrast, subordinate paper wasps are not injured or evicted during escalated challenges against the dominant, perhaps because they are more valuable to the dominant. We discuss evidence that paper-wasp dominants avoid escalated conflicts by ceding reproduction to subordinates. Queuing rules appear usually to be enforced by individuals adjacent in the queue rather than by dominants. Further manipulative studies are required to reveal mechanisms underlying queue stability and to elucidate what determines queue position in the first place. Keywords: social queues; social aggression; helping; group stability; Polistes; reproductive skew

1. INTRODUCTION In primitively eusocial insect societies, some individuals, known as subordinates or helpers, sacrifice their own reproduction and help to rear the offspring of other individuals known as the queen or dominant. The defining feature of primitively eusocial societies, however, is that all individuals, including the helpers, are potentially capable of mating and independent reproduction. The key fact that we focus on in this paper is that the individuals in such societies are often in a queue to inherit breeding positions. The individuals in the queue inherit breeding positions in a predictable order. This leads to systematic differences in waiting times, which means that individuals differ in their future prospects. The differences are most marked in the short queues typical of the taxa we discuss. We first summarize the consequences of queuing for behavioural variation between individuals in the society. We then discuss evidence for behavioural mechanisms that might stabilize the queue. The organisms we focus on are primitively eusocial wasps in two subfamilies, Stenogastrinae (hover wasps) and Polistinae (paper wasps), but where relevant we draw comparisons with social queues in other Hymenoptera and vertebrates.

* Author for correspondence ([email protected]). One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

(a) Natural history of primitively eusocial wasps Paper wasps and hover wasps probably represent independent origins of eusociality (Hines et al. 2007). In temperate populations of Polistes, females, known as foundresses, start building their characteristic open paper nests in spring after overwintering as mated adults. In some species, each nest has only a single foundress, but founding by multiple females is common in other species. In this paper, we discuss species in which some nests have multiple foundresses. On such nests, one of the foundresses, known as the dominant or rank 1, lays most of the eggs. The other foundresses, which are often, but not always, relatives of the dominant, act as helpers and carry out tasks such as foraging to feed the larvae. When the larvae reach adulthood, many of the newly matured females stay and become helpers on their natal nests, but here we will discuss studies of populations during the pre-worker phase, when only foundresses are present. The most recent general review of Polistes nesting biology is by Reeve (1991). Whereas Polistes has an almost cosmopolitan distribution, hover wasps are restricted to the tropics of southeast Asia and New Guinea. We discuss studies of the hairy-faced hover wasp Liostenogaster flavolineata in which, unlike temperate Polistes, brood rearing continues all year. Nests are usually initiated by a single female, and multiple-female nests arise mainly through some adult offspring remaining on their natal nests as helpers. Other offspring leave to follow alternative

3181

This journal is q 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3182

J. Field & M. A. Cant

Social queues

strategies such as founding nests of their own. Groups never become very large, in this respect resembling the pre-worker nests of Polistes, with group sizes of typically one to four females, very rarely more than 10. Turillazzi (1991) and Field (2008) are two recent reviews of hover wasp nesting biology. Reproductive skew is generally high at any one time in primitively eusocial wasps (Field & Cant 2009). However, when the dominant female dies, one of the other females in the group inherits the egg-laying position, so that skew is lower when viewed across the group’s entire lifespan.

2. CONSEQUENCES OF QUEUING: INDIVIDUAL VARIATION IN BEHAVIOUR One of the most noticeable features of primitively eusocial societies is behavioural variation between the different individuals in a group. Some individuals are more aggressive than others, some work harder than others, and some are more likely than others to defend the group against outside threats (e.g. Clutton-Brock et al. 2000; Cant & Field 2001; Field et al. 2006; Cant et al. 2006a,b; Cronin & Field 2007b). Little of this variation is correlated with within-group variation in genetic relatedness, although further work, particularly manipulative experiments, is needed to confirm this (e.g. Queller et al. 2000; Griffin & West 2003; Cant et al. 2006b; Field et al. 2006). There is, however, good evidence that much of the variation in behaviour is caused by variation in expected future fitness. Life-history theory suggests that helpers in primitively eusocial societies face a fundamental trade-off between helping effort and future fitness (Cant & Field 2001, 2005). By working harder to rear the offspring of their dominant relative, they can increase the indirect component of their fitness. But this comes only at a cost of reduced personal survival, and reduced fecundity if they survive to inherit the dominant position themselves. A major prediction from this life-history framework is that because individuals with greater expected future fitness have more to lose, they should invest less in working to rear the dominant’s offspring. In primitively eusocial insects, foraging is probably the costliest activity performed by helpers because it involves energy-expensive flight and an increased risk of predation away from the safety of the nest (Cant & Field 2001). We can therefore make two clear predictions. First, helpers nearer to the front of the queue should forage less because they have more to lose. Second, helpers at a given position in the queue should forage less if they are part of a larger group. This second prediction relies on the fact that in most primitively eusocial societies, the reproductive payoff from inheriting the dominant position is greater in larger groups because there are more helpers available to rear the dominant’s offspring in such groups. Thus, a helper has more to lose if the group she stands to inherit is larger, assuming that her chance of inheritance from a given rank is independent of group size (Field & Cant 2006). Consistent with these predictions, the expected correlations between foraging effort and both group size Phil. Trans. R. Soc. B (2009)

and queue position are found in Polistes cofoundress associations and in the hairy-faced hover wasp (Cant & Field 2001; Field et al. 2006). Note that the correlation with group size is unlikely to result simply from the larger number of helpers available to feed offspring in larger groups, as may be the case in some cooperatively breeding vertebrates (Field & Cant 2006). In primitively eusocial insects, clutch size is typically not fixed, so that the number of dependent offspring per helper is roughly constant across group sizes (e.g. Field et al. 2000; reviewed in Shreeves & Field 2002). In addition to these correlations, manipulation of expected future fitness has been carried out in the hairy-faced hover wasp (Field et al. 2006). These manipulations took advantage of the fact that queueing is strictly age-based in this species, so that by knowing the relative ages of the individuals in the group, we know the order in which they will inherit the dominant position. It is therefore possible to experimentally promote focal individuals up the queue by removing higher ranking nest-mates. The group size that a focal subordinate stands to inherit can also be reduced by removing lower ranking nest-mates. The results of these manipulations were that focal individuals worked less hard than unmanipulated controls when they were promoted, but harder than controls when their group size was reduced (Field & Cant 2006; Field et al. 2006). Both results supported the theoretical predictions. The life-history perspective outlined above does not mean that high-ranked individuals should necessarily always be the ones that take the fewest risks. For example, Cant et al. (2006a) developed a kin selection model of aggression in social queues. It turns out that if aggression functions to challenge the status of individuals further up the queue, high-ranking individuals should be the most aggressive, even though they risk injury in the process (figure 1a). This is because high rankers have the most to gain by jumping the queue, in terms of increasing their probability of inheriting the rank 1 position. Probability of inheritance declines exponentially with decreasing rank, so that the effect of moving one place up the queue is larger for an individual nearer the front (Field et al. 1999). Thus, the predicted correlation with rank will differ for different behaviours, depending on the pattern of costs and benefits. High rankers should take the fewest risks with foraging, but may be more likely to risk injury via aggression (figure 1b). The important general point, however, is that variation in future fitness may be the hidden factor that explains much of the previously unexplained variation in behaviour within social queues. The data reviewed above imply that variation in costs and benefits, rather than variation in genetic relatedness, primarily determines variation in behaviour within groups of primitively eusocial wasps. We emphasize, however, that we cannot conclude from this that kin selection is unimportant in general. Most groups of primitively eusocial wasps comprise relatives, so that helpers gain indirect fitness through boosting the reproductive success of the dominant. The reason that behavioural fine-tuning reflects variation in costs and benefits is probably that there are

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Social queues

0.35

0.030 sub’s aggression rate

(b) 0.035

challenger’s payoff

(a) 0.40

0.30 0.25 0.20 0.15 0.10

J. Field & M. A. Cant

3183

0.025 0.020 0.015 0.010 0.005

0.05 0

0 2

3

4 rank

5

6

2

3

4 rank

5

6

Figure 1. (a) Theoretical payoff to a subordinate of challenging the individual ahead of it in the queue to inherit dominant status, versus inheritance rank. In this model (model 1 of Cant et al. 2006a), a successful challenge leads to a reversal in dominance rank, but incurs a cost to group productivity. (b) Observed rates of aggression by subordinate Polistes dominulus to their immediate dominant as a function of their inheritance rank. Ranks were revealed by repeatedly removing rank 1 individuals and allowing the next individual in the queue to inherit (see Cant et al. 2006a for details). Points show means + s.e.

informational constraints. Cues such as rank or group size, which are correlated with an individual’s future fitness, may be more easily detected than cues correlated with relatedness (Keller 1997; Field et al. 2006). It is possible, however, that in other situations where cues correlated with within-group variation in relatedness are readily available, relatedness could be a determinant of within-group variation in behaviour. For example, if it was systematically correlated with rank or group size, relatedness could reinforce or oppose the effects of rank or group size on behaviour. Relatedness is not strongly correlated with rank or group size in the wasp populations reviewed above (Bridge & Field 2007; Zanette & Field 2008, 2009), but is likely to be correlated with rank in other social queues (e.g. Dierkes et al. 2005).

3. QUEUE STABILITY (a) The queue should be stable The foregoing results imply that at least in primitively eusocial wasps, the queuing rule must be adhered to reasonably closely. In the hairy-faced hover wasp, for example, if relative age was only a weak predictor of inheritance payoff, variation in behaviours such as helping effort would not be expected to map so well onto queue position. Experimental removal of dominants from groups of individuals of known relative age suggests that age is indeed a good predictor of inheritance order (Bridge & Field 2007). After 90 per cent of removals (n ¼ 69), the oldest subordinate was the one to inherit. Wasps that inherited naturally were the oldest in a similar fraction of cases. Bridge & Field (2007) identified seven out of 69 individuals that jumped the queue, in the sense that they inherited ahead of one or more older individuals. Before they inherited, these queue jumpers had worked significantly less hard than expected for their rank, suggesting that their accession might not simply be the result of winning a fight with an older wasp at the moment when the previous dominant was removed. The sample size was small, but there Phil. Trans. R. Soc. B (2009)

was no indication that queue jumpers were larger than the individuals supplanted, or that they had an especially large incentive to jump the queue because they were unrelated to their nest-mates (Bridge & Field 2007). It is possible that the queuing system can support a small proportion of ‘cheats’ that break the rules, perhaps by mimicking cues associated with age. However, an obvious question then is why more individuals do not cheat, unless mimicry is costly. Alternatively, perhaps there are no cheats: the queueing rules may just be more complex than we realize. Instead of being based purely on age, the rule might be that the oldest wasp inherits unless another unknown variable takes particular values. (b) What behavioural mechanisms stabilize the queue? In an inheritance queue, individuals wait their turn, and so risk dying before they inherit. This begs the question of how the queuing rules are enforced. All else being equal, each individual should prefer itself to produce the offspring reared by the group. Yet reproductive skew is often high in primitively eusocial wasps, perhaps especially in hover wasps (Field & Cant 2009). Why do low-ranked individuals not challenge those ranked above them? One kind of explanation for queue stability is that even after successfully challenging for reproductive status, a former subordinate might end up with a larger slice of a smaller ‘cake’. In other words, there could be group-level costs of violating the queueing rules, paralleled in several well-known scenarios such as the tug-of-war model of reproductive skew (Reeve et al. 1998). These costs would translate into reduced group productivity, perhaps because group-mates are injured or leave the group following their demotion, and more generally because time and energy were wasted in competition. In social insects, precious time can be wasted when a new dominant takes over, simply because she must often mate and develop physiologically before attaining full reproductive capacity (e.g. Strassmann et al. 2004).

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3184

J. Field & M. A. Cant

Social queues

By definition, group-level costs are paid by all members of the group. A potentially more potent disincentive against breaking the queuing rules would be the existence of personal costs involved in doing so. In meerkat (Suricata suricatta) social groups, such costs are suggested by observations of dominants temporarily expelling pregnant subordinates from the group. Such subordinates, which might otherwise kill the dominant’s own pups or produce competing litters, lose weight and fertility while they are away from the group, and usually abort their litters (Clutton-Brock et al. 1998; Young et al. 2006). The ideal way to measure costs, however, is to manipulate individuals into breaking the rules and then measuring the consequences. Some of the best work in this area has involved queues of fishes in which, as in the hairyfaced hover wasp, only the dominants breed (Buston 2003a; Heg et al. 2004; Wong et al. 2007, 2008). In these queues, there is a breeding pair rather than just a breeding female, and the queue appears to be based primarily on size (although size is perfectly correlated with age in natural queues). The breeding pair are typically the largest fish in the group, and a young fish joins the end of the queue because it is the smallest. More interestingly, there tends to be a constant size ratio between pairs of individuals that occupy adjacent positions in the queue, and if one individual is removed experimentally, the individuals ranked below start to grow (Buston 2003a; Heg et al. 2004; Buston & Cant 2006). As in the hairy-faced hover wasp, knowing the queuing rule means that we can predict the order of inheritance. But size-based queueing provides the added advantage that individuals can be manipulated into breaking the rules. Wong et al. (2008) achieved this by giving a lowranked goby (Paragobiodon) extra food in each of nine social groups in laboratory aquaria. The result was that five of the nine manipulated gobies, having grown by eating the supplementary food, were evicted from the group. Wong et al.’s (2008) interpretation of these results was that by growing, food-supplemented fish approached the size of those ranked above them, and so became a threat to their status. The hidden threat that normally maintains queue stability was then revealed: the threat of eviction for rule breakers. Eviction is likely to be costly, at least in nature, because an evicted goby probably has only a small chance of finding a new breeding site (Wong et al. 2007). Normally, subordinates avoid eviction through exhibiting self-restraint: by starving themselves, they avoid becoming a threat to higher ranked individuals. Direct interference in feeding by higher ranked individuals could also help to maintain size ratios, at least in other fish queues (Heg et al. 2004). In the hairy-faced hover wasp, because queue position is based on age rather than size, it is less obvious how to manipulate subordinates into breaking the rules of the queue. Cant et al. (2006b) instead induced subordinates to challenge the dominant breeder physically, this time in natural spring cofoundress associations of the paper wasp Polistes dominulus. Polistes dominulus foundresses again appear to queue for egg-laying positions: the subordinates that will inherit earliest are also the laziest subordinates, Phil. Trans. R. Soc. B (2009)

implying that there are detectable cues correlated with inheritance rank (Cant & Field 2001). In P. dominulus, however, the rules that determine inheritance rank are not known (Zanette & Field 2009). Although there is frequent low-level aggression between foundresses, escalated conflicts are rarely observed ( J. Field & M. A. Cant 2006, unpublished observations of video recordings). Yet, molecular parentage data suggest that there are at least occasional role reversals in Polistes, in which a previously dominant wasp has become a subordinate (e.g. Peters et al. 1995; Field et al. 1998a). In order to induce escalated conflicts, Cant et al. (2006b) placed the dominant (rank 1) female temporarily in a refrigerator and allowed rank 2 to begin establishing herself as the new dominant. After a few days, rank 1 was released and, on her return to the nest, her interaction with rank 2 recorded. Two kinds of interaction were observed. In 11 cases, rank 2 simply submitted to the returning rank 1 without a fight. In another 17 cases, however, there was a serious escalated contest, sometimes lasting several minutes, involving biting, grappling and sometimes attempted stinging. At the end of all but one of these contests, however, rank 2 submitted to rank 1 without any obvious signs of injury and without being expelled from the group. To the extent that these contests in Polistes mimic challenges that subordinates could mount naturally, they suggest that subordinates do not queue peacefully because they risk serious injury or expulsion during a challenge. Nevertheless, escalated challenges presumably are costly, and may not be worth mounting simply because the dominant usually wins them. The contrast with Wong et al.’s (2008) results, in which subordinates were expelled from the group if they became a threat, may reflect idiosyncratic differences between the two study systems—perhaps it is harder to expel or injure a wasp than a fish, for example. The difference could also reflect the lower value of subordinate gobies to dominants: mean relatedness is lower in gobies than in wasps, perhaps close to zero. And subordinate gobies, unlike subordinate wasps, do not enhance the fitness of the dominant (Shreeves et al. 2003; Wong et al. 2007). However, expulsion has also been observed when subordinate Neolamprologus fishes were manipulated so that they appeared to be lazy. Relatedness is comparable in Neolamprologus and Polistes, and Neolamprologus helpers may increase breeder fitness (Balshine-Earn et al. 1998; Dierkes et al. 2005; but see Bergmu¨ller & Taborsky 2005). How closely the contests induced by Cant et al. (2006b) resemble natural challenges to the dominant is less clear than in the case of Wong et al.’s (2008) gobies. In nature, a rank 1 P. dominulus rarely leaves the nest for more than a few minutes at a time (e.g. Cant & Field 2001). After a long, artificially enforced absence, rank 2 might need to seriously test rank 1 to check that she can still hold her position. That P. dominulus subordinates rarely win escalated contests with dominants raises the question of whether they have any leverage at all in the group. Must they simply wait in the hope of one day inheriting the dominant position? Or can they somehow induce the dominant to grant them at least a small share of

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Social queues

Phil. Trans. R. Soc. B (2009)

3185

2.5 subordinate ovarian score

the current reproduction? This question is particularly pertinent in P. dominulus, in which a large proportion of subordinates are unrelated to the dominant and so cannot obtain indirect fitness benefits through rearing her offspring (Queller et al. 2000; Zanette & Field 2008). One possibility is that subordinates might threaten to leave the group if no reproduction is ceded to them, as in the concessions model of reproductive skew (Vehrencamp 1983; Reeve & Ratnieks 1993). Especially if subordinates normally boost the dominant’s fitness by helping, this might be an effective sanction. In the allodapine bee Exoneura, and in the cichlid fish Neolamprologus, both of which have subordinates that provide help, the payoff through leaving has been experimentally increased by providing vacant breeding sites for subordinates to use. In both cases, however, although some individuals did leave their groups to take up the vacancies provided, there was no effect on the reproductive share obtained by subordinates that stayed (Langer et al. 2004; Heg et al. 2006). Thus, even though leaving was clearly an option—some individuals did leave—a greater payoff through leaving did not enable subordinates to extract a larger share of reproduction from the dominant. One possible explanation for these results is that unlike subordinates, dominants could not reliably assess the threat of leaving for themselves (Field & Cant 2009). Indeed, in Heg et al.’s (2006) experiment, only subordinates had access to the vacancies provided. In most wasps and bees, the dominant leaves the nest infrequently and only briefly, and so may be unable to track changes in the social environment very effectively. Thus, subordinates that can benefit by leaving may do so, while those that stay are those that do better to accept the prevailing reproductive skew. In analogous experiments on the hairy-faced hover wasp, and another experiment on the same species of Exoneura, provision of vacancies induced few or no extra subordinates to leave their groups (Bull & Schwarz 1996; Field et al. 1998b). In these cases, it would seem that leaving is not even a credible threat, probably because a subordinate on her own is unlikely to survive long enough to rear offspring through to adulthood (e.g. Field et al. 2000; Shreeves et al. 2003). In such situations, there would be no need for the dominant to cede reproduction to the subordinate in order to retain her in the group (Reeve & Ratnieks 1993). An alternative source of leverage for subordinates might be the threat of aggression. This could take the form of low-level harassment (e.g. ‘lunges’ in Polistes) or escalated fights. In either case, the potential cost might be enough to induce appeasement in the form of reproductive concessions from the dominant. This is similar to the idea of ‘peace incentives’, where it was postulated that a dominant might cede some reproduction to a subordinate in order to reduce her motivation to risk a challenge in the form of a fatal fight (Reeve & Ratnieks 1993). Cant et al. (2006b) tested the counterpart of this argument, that high skew will lead to more aggression by subordinates, using data from the contests that they induced in P. dominulus. Rank 2s appeared to control whether an escalated contest occurred, because a contest

J. Field & M. A. Cant

2.0 1.5 1.0 0.5 0 2

3 4 5 6 7 group size (productivity)

8

Figure 2. Results of a dominant removal –reintroduction experiment designed to induce contests over the rank 1 position in P. dominulus (Cant et al. 2006b). Rank 1 foundresses were removed for several days to allow rank 2 foundresses to inherit and establish themselves as replacement dominants. Mean ovarian development of rank 2s is plotted as a function of group size, which is an index of productivity. The line shows the significant least-squares regression of ovarian development on group size. Filled circles represent trials in which these newly promoted rank 2 individuals entered into an escalated fight with reintroduced rank 1 individuals; open circles represent trials in which rank 2s immediately submitted to reintroduced rank 1s. Both ovarian development and group size had significant effects on the probability of escalated conflict.

ended when rank 2 exhibited stereotyped submissive behaviour (Cant et al. 2006b). Cant et al. (2006b) predicted that if rank 2s were granted little or no direct reproduction (high skew), so that they had more to gain from reversing roles with the dominant, they should be more likely to engage in escalated contests with her. This prediction was supported by the data (figure 2). What rank 2 stood to inherit if she could maintain her newly dominant position was estimated by the group size: larger groups with more helpers are more productive. As expected, rank 2s were more likely to engage in escalated conflict with the returning rank 1 when the winner stood to inherit a more valuable group (figure 2). But more interestingly, rank 2s that had less ovarian development—suggesting a smaller share of the direct reproduction—were also more likely to escalate (figure 2). This suggests that the threat of escalation could give subordinates a way of extracting reproduction: by ceding reproduction, the dominant might avoid escalation. The underlying cause of variation in the rank 2s’ ovarian development is only partially clear. Rank 2s in larger groups had better developed ovaries (figure 2). This could again be consistent with rank 2s being able to extract more reproduction when they had more incentive to overthrow the dominant, although other explanations are possible (Cant et al. 2006b). But the variation in ovarian development that was correlated with the decision to escalate was present after controlling for group size. It seems unlikely that subordinates with betterdeveloped ovaries were simply subordinates of better quality: better quality subordinates should also be

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3186

J. Field & M. A. Cant

Social queues

more likely to win an escalated contest, yet were less likely to initiate one (figure 2). It is interesting to note that the correlation between low-level aggression and reproductive skew in two other Polistes species was in the reverse direction to the one found by Cant et al. (2006b) for escalated aggression: subordinate Polistes bellicosus and Polistes carolina exhibited less low-level aggression when skew was high (Field et al. 1998a; Seppa¨ et al. 2002). Manipulative studies are needed, but these contrasting results may indicate that different kinds of aggression have different functions.

4. DISCUSSION Accumulating evidence suggests that the individuals in small animal societies typically queue to inherit reproductive positions. This is implied by the repeated finding that individual behaviour is correlated with queue position (e.g. Monnin & Peeters 1999; Cant & Field 2001; Deshpande et al. 2006; Field & Cant 2006; Field et al. 2006). One apparent exception to this pattern was the primitively eusocial wasp Ropalidia marginata, in which it has so far proved impossible to identify rank 2 female before her accession to rank 1. However, recent experiments suggest that even though humans cannot identify rank 2, the wasps themselves can (Bhadra & Gadagkar 2008). Social queues create asymmetries in expected future fitness, which appear to strongly influence individual behaviour, perhaps facilitating cooperation (Innocent & West 2006). Nevertheless, each individual would still prefer to be nearer the front of the queue. The stability of these social hierarchies may result more from hidden threats that rarely have to be carried out than from direct, all-out competition of the kind seen in a tug-of-war. This has an obvious efficiency advantage. If threats are rarely carried out, both group-level and personal costs are rarely paid. We expect strong selection to avoid triggering hidden threats because an individual that does so suffers a sudden drop in fitness (or fitness ‘cliff-edge’; Kokko 2003) as a result. For example, a dominant that monopolizes reproduction to the extent that it triggers a subordinate’s departure suddenly loses all future help from that subordinate. In order to avoid triggering threats unnecessarily, individuals must gain information about the nature of the threat and the location of the threshold beyond which a threat will be triggered, either by trial-and-error learning or by communicating. In the goby Paragobiodon xanthosomus, for example, subordinates must know the minimum size difference that will be tolerated if they are to avoid triggering eviction unnecessarily. Dominants could signal to growing subordinates that they are approaching the threshold, but here there is considerable scope for deception because a dominant will benefit from exaggerating its willingness to exercise a threat, while a subordinate will be selected to ignore warning signals unless there is some way to evaluate their credibility. One way to guarantee credibility is to use warning signals that are costly to the signaller, such as direct aggression or costly displays. This raises the intriguing possibility that dominance displays and acts of social Phil. Trans. R. Soc. B (2009)

aggression may function to support the credibility of threats to destabilize the group (e.g. by eviction or departure) so that these threats do not, in the end, have to be carried out (Cant & Johnstone 2009). Which individuals enforce the queuing rules, given that enforcement itself may have personal costs? At one extreme, a single individual such as the dominant might be able to police the entire queue in a small society. Unless relatedness varies systematically with rank, rank reversals among subordinates might have little effect on the dominant’s fitness, but the dominant might police the queue because she stands to lose most if within-group conflict leads to a decline in group productivity. Alternatively, each individual might be policed primarily by the individual just ahead of it in the queue—the individual that will lose rank if queue jumping occurs. Consistent with the latter scenario, Cant et al. (2006a) found that the vast majority of low-level aggressive interactions among P. dominulus foundresses were between wasps at adjacent positions in the queue (but see Cronin & Field 2007a,b in the hairy-faced hover wasp). Similarly, dominants that were returned to their nests after temporary removal interacted only with rank 2s that stood to be displaced by them. An exception was after the single escalated contest where a rank 1 submitted to a rank 2: rank 3 then immediately submitted to the defeated rank 1. Parallel observations exist for queues of fishes. In anemonefish, it is the smallest, lowest-ranking subordinates that are most aggressive towards potential joiners to the end of the queue, and subordinates occasionally attempt to evict the individual ranked immediately below them (Elliott et al. 1995; Mitchell 2005; Buston 2003b). Wong et al. (2008) state that rank 4 gobies that had been manipulated into breaking the queuing rules were evicted by their immediate dominants, the individuals at rank 3, rather than by the breeding pair. Similarly, manipulated Neolamprologus cichlid helpers were attacked by other subordinates, not by the dominant, when they were returned to their groups (Balshine-Earn et al. 1998). Overall, these observations suggest that each individual interacts primarily with the individual adjacent to it in the queue. An interesting exception is the ant Dinoponera quadriceps, in which a challenger may be chemically marked by the adjacent rank 1 female. However, marking causes lower ranking females to restrain the challenger physically (‘immobilization’), which in turn can lead to a loss of rank for the challenger (Monnin & Peeters 1999; Monnin et al. 2002). The approach that we have taken in this paper and previously (Cant & Field 2001, 2005) implies that variation between individuals in future fitness, as embodied by factors such as group size and queue position, has important consequences for variation in behaviours such as helping effort and aggression. Particularly in the case of aggression, this somewhat reverses the traditional argument that it is resourceholding potential that determines access to resources and hence position in the hierarchy. Could it be that queue position is initially determined by individual variation in resource-holding potential, expressed through aggression, so that resource-holding potential

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Social queues is what ultimately determines variation in behaviours such as helping effort in primitively eusocial wasps? For example, do individuals nearer to the end of the queue carry out most of the risky foraging because higher ranked individuals are physically stronger and can force them into doing so, rather than because low-ranked individuals have little expected future fitness? In the hairy-faced hover wasp, this seems unlikely. The term ‘gerontocracy’, in which older individuals are ranked above younger ones, means that the highest-ranked wasps may sometimes be the smallest in the group. Indeed, to the extent that size reflects resource-holding potential, there is no evidence that rank is correlated with quality (Field et al. 1999; Sumner et al. 2002). There could plausibly be selection on other attributes of quality during the queuing process, so that only higher quality individuals tend to survive to reach the highest ranks. But it seems unlikely that mortality, which probably acts largely stochastically during foraging, could lead to the oldest individual, which inherits 90 per cent of the time, consistently being the individual of highest quality. Furthermore, variation in quality would not explain the results of Field et al. (2006), where future fitness was experimentally manipulated. For example, individual helpers worked harder after their group sizes were reduced, even though the same individuals still occupied the ranks above them. Helping effort was measured only 2 days after the manipulation, so that it is also unlikely that individual condition had changed significantly in the interim. In P. dominulus, what determines an individual’s position in the queue is less clear. The dominant individual tends to be larger than rank 2 in an Italian population (Cervo et al. 2008), but in the population studied by Cant et al. (2006a,b), queue position was not correlated with body size (Cant & Field 2001; Zanette & Field 2009). Correlations between queue position and order of arrival at the nest in spring, genetic relatedness or the presence of black facial marks (another potential indicator of quality; Tibbetts & Dale 2004) are also either weak or nonexistent (Zanette & Field 2009). Cant et al. (2006a,b) found no evidence that body size determines rates of aggression between wasps of adjacent rank, or the occurrence and duration of escalated contests. If rank is not correlated with body size, why were 16/17 escalated contests won by rank 1 female? Cant et al. (2006b) attribute the asymmetry in outcomes to an ownership effect. The nest may be more valuable to rank 1 female because it contains mainly her offspring, so that she may be prepared to fight harder to retain control of it. Nevertheless, it remains possible that rank is somehow influenced by individual quality: aggressive interactions characterize the initial stages of group formation in Polistes (Reeve 1991). Alternatively, higher ranked individuals may eventually attain better condition through priority of access to resources and reduced energy expenditure, even if rank was initially established independent of individual quality. A positive feedback loop might then result. Queue position, determined by whatever mechanism, could lead low-ranked individuals to work harder, so that they lose condition. This in turn might further Phil. Trans. R. Soc. B (2009)

J. Field & M. A. Cant

3187

reduce their life expectancy and chance of inheritance, further increasing their incentive to work and further reducing their condition. Variation in resource-holding potential, whether intrinsic or occurring via variation in condition, could then reinforce the effect of variation in future fitness in influencing behaviours such as helping effort. Further work to investigate what ultimately determines queue position in primitively eusocial wasps, especially Polistes, is needed to resolve this issue. We thank A. Bourke, H. Helantera¨ and F. Ratnieks for constructive comments on the manuscript. J.F. thanks T. H. Clutton-Brock, R. A. Foley, F. L. W. Ratnieks and S. West for inviting him to take part in the Royal Society’s ‘Evolution of Society’ Discussion Meeting.

REFERENCES Balshine-Earn, S., Neat, F. C., Reid, H. & Taborsky, M. 1998 Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish. Behav. Ecol. 9, 432 –438. (doi:10.1093/ beheco/9.5.432) Bergmu¨ller, R. & Taborsky, M. 2005 Experimental manipulation of helping in a cooperative breeder: helpers ‘pay to stay’ by pre-emptive appeasement. Anim. Behav. 69, 19–28. (doi:10.1016/j.anbehav.2004.05.009) Bhadra, A. & Gadagkar, R. 2008 We know that the wasps ‘know’: cryptic successors to the queen in Ropalidia marginata. Biol. Lett. 4, 634 –637. (doi:10.1098/rsbl. 2008.0455) Bridge, C. & Field, J. 2007 Queuing for dominance: gerontocracy and queue-jumping in the hover wasp Liostenogaster flavolineata. Behav. Ecol. Sociobiol. 61, 1253–1259. (doi:10.1007/s00265-007-0355-9) Bull, N. J. & Schwarz, M. P. 1996 The habitat saturation hypothesis and sociality in an allodapine bee: cooperative nesting is not ’making the best of a bad situation’. Behav. Ecol. Sociobiol. 39, 267 –274. (doi:10.1007/ s002650050289) Buston, P. 2003a Forcible eviction and prevention of recruitment in the clown anemonefish. Behav. Ecol. 14, 576–582. (doi:10.1093/beheco/arg036) Buston, P. 2003b Social hierarchies: Size and growth modification in clownfish. Nature 424, 145 –146. (doi:10.1038/ 424145a) Buston, P. M. & Cant, M. A. 2006 A new perspective on size hierarchies in nature: patterns, causes, and consequences. Oecologia 149, 362 –372. (doi:10.1007/ s00442-006-0442-z) Cant, M. A. & Field, J. 2001 Helping effort and future fitness in cooperative animal societies. Proc. R. Soc. Lond. B 268, 1959–1964. (doi:10.1098/rspb.2001.1754) Cant, M. A. & Field, J. 2005 Helping effort in a dominance hierarchy. Behav. Ecol. 16, 708 –715. (doi:10.1093/ beheco/ari051) Cant, M. A. & Johnstone, R. A. 2009 How threats influence the evolutionary resolution of within-group conflict. Am. Nat. 173, 759–771. (doi:10.1086/598489) Cant, M. A., Llop, J. B. & Field, J. 2006a Individual variation in social aggression and the probability of inheritance: Theory and a field test. Am. Nat. 167, 837–852. (doi:10.1086/503445) Cant, M. A., English, S., Reeve, H. K. & Field, J. 2006b Escalated conflict in a social hierarchy. Proc. R. Soc. B 273, 2977–2984. (doi:10.1098/rspb.2006.3669) Cervo, R., Dapporto, L., Beani, L., Strassmann, J. E. & Turillazzi, S. 2008 On status badges and quality signals

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3188

J. Field & M. A. Cant

Social queues

in the paper wasp Polistes dominulus: body size, facial colour patterns and hierarchical rank. Proc. R. Soc. B 275, 1189–1196. (doi:10.1098/rspb.2007.1779) Clutton-Brock, T. H., Brotherton, P. N. M., Smith, R., McIlrath, G. M., Kansky, R., Gaynor, D., O’Riain, M. J. & Skinner, J. D. 1998 Infanticide and expulsion of females in a cooperative mammal. Proc. R. Soc. Lond. B 265, 2291–2295. (doi:10.1098/rspb.1998.0573) Clutton-Brock, T. H., Brotherton, P. N. M., O’Riain, M. J., Griffin, A. S., Gaynor, D., Sharpe, L., Kansky, R., Manser, M. B. & McIlrath, G. M. 2000 Individual contributions to babysitting in a cooperative mongoose, Suricata suricatta. Proc. R. Soc. Lond. B 267, 301 –305. (doi:10.1098/rspb.2000.1000) Cronin, A. L. & Field, J. 2007a Rank and colony defense against conspecifics in a facultatively eusocial hover wasp. Behav. Ecol. 18, 331–336. (doi:10.1093/beheco/arl091) Cronin, A. L. & Field, J. 2007b Social aggression in an age-dependent dominance hierarchy. Behaviour 144, 753 –765. (doi:10.1163/156853907781476436) Deshpande, S. A., Sumana, A., Surbeck, M. & Gadagkar, R. 2006 Wasp who would be queen: a comparative study of two primitively eusocial species. Curr. Sci. 91, 332 –336. Dierkes, P., Heg, D., Taborsky, M., Skubic, E. & Achmann, R. 2005 Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid. Ecol. Lett. 8, 968– 975. (doi:10.1111/j.14610248.2005.00801.x) Elliott, J. K., Elliott, J. M. & Mariscal, R. N. 1995 Host selection, location, and association behaviors of anemonefishes in field settlement experiments. Mar. Biol. 122, 377 –389. (doi:10.1007/BF00350870) Field, J. 2008 The ecology and evolution of helping in hover wasps (Hymenoptera: Stenogastrinae). In Ecology of social evolution (eds J. Korb & J. Heinze), pp. 85–107. Berlin, Germany: Springer. Field, J. & Cant, M. A. 2006 Helping effort in primitively eusocial wasps. Ann. Zool. Fenn. 43, 481– 487. Field, J. & Cant, M. A. 2009 Reproductive skew in primitively eusocial wasps: how useful are current models? In Reproductive skew in vertebrates, vol. 20 (eds R. Hager & C. Jones), pp. 773 – 780. Cambridge, UK: Cambridge University Press. Field, J., Solis, C. R., Queller, D. C. & Strassmann, J. E. 1998a Social and genetic structure of paper wasp cofoundress associations: tests of reproductive skew models. Am. Nat. 151, 545–563. (doi:10.1086/286140) Field, J., Foster, W., Shreeves, G. & Sumner, S. 1998b Ecological constraints on independent nesting in facultatively eusocial hover wasps. Proc. R. Soc. Lond. B 265, 973 –977. (doi:10.1098/rspb.1998.0386) Field, J., Shreeves, G. & Sumner, S. 1999 Group size, queuing and helping decisions in facultatively eusocial hover wasps. Behav. Ecol. Sociobiol. 45, 378 –385. (doi:10. 1007/s002650050574) Field, J., Shreeves, G., Sumner, S. & Casiraghi, M. 2000 Insurance-based advantage to helpers in a tropical hover wasp. Nature 404, 869– 871. (doi:10.1038/35009097) Field, J., Cronin, A. & Bridge, C. 2006 Future fitness and helping in social queues. Nature 441, 214 –217. (doi:10. 1038/nature04560) Griffin, A. S. & West, S. A. 2003 Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302, 634 –636. (doi:10.1126/science.1089402) Heg, D., Bender, N. & Hamilton, I. 2004 Strategic growth decisions in helper cichlids. Proc. R. Soc. Lond. B 271, S505 –S508. (doi:10.1098/rsbl.2004.0232) Heg, D., Bergmu¨ller, R., Bonfils, D., Otti, O., Bachar, Z., Burri, R., Heckel, G. & Taborsky, M. 2006 Cichlids do not adjust reproductive skew to the availability of Phil. Trans. R. Soc. B (2009)

independent breeding options. Behav. Ecol. 17, 419 – 429. (doi:10.1093/beheco/arj056) Hines, H. M., Hunt, J. H., O’Connor, T. K., Gillespie, J. J. & Cameron, S. A. 2007 Multigene phylogeny reveals eusociality evolved twice in vespid wasps. Proc. Natl Acad. Sci. USA 104, 3295–3299. (doi:10.1073/ pnas.0610140104) Innocent, T. M. & West, S. A. 2006 Social evolution: cooperation by conflict. Curr. Biol. 16, R365 –R367. (doi:10.1016/j.cub.2006.04.009) Keller, L. 1997 Indiscriminate altruism: unduly nice parents and siblings. Trends Ecol. Evol. 12, 99–103. (doi:10.1016/ S0169-5347(96)10065-3) Kokko, H. 2003 Are reproductive skew models evolutionarily stable. Proc. R. Soc. Lond. B 270, 265–270. (doi:10. 1098/rspb.2002.2238) Langer, P., Hogendoorn, K. & Keller, L. 2004 Tug-of-war over reproduction in a social bee. Nature 428, 844–847. (doi:10.1038/nature02431) Mitchell, J. 2005 Queue selection and switching by false clown anemonefish, Amphiprion ocellaris. Anim. Behav. 69, 643 –652. (doi:10.1016/j.anbehav.2004. 05.017) Monnin, T. & Peeters, C. 1999 Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behav. Ecol. 10, 323 –332. (doi:10. 1093/beheco/10.3.323) Monnin, T., Ratnieks, F. L. W., Jones, G. R. & Beard, R. 2002 Pretender punishment induced by chemical signalling in a queenless ant. Nature 419, 61– 65. (doi:10. 1038/nature00932) Peters, J. M., Queller, D. C., Strassmann, J. E. & Solis, C. R. 1995 Maternity assignment and queen replacement in a social wasp. Proc. R. Soc. Lond. B 260, 7 –12. (doi:10. 1098/rspb.1995.0052) Queller, D. C., Zacchi, F., Cervo, R., Turillazzi, S., Henshaw, M. T., Santorelli, L. A. & Strassmann, J. E. 2000 Unrelated helpers in a social insect. Nature 405, 784 –787. (doi:10.1038/35015552) Reeve, H. K. 1991 Polistes. In The Social biology of wasps (eds K. G. Ross & R. W. Mathews), pp. 99–148. Ithaca, NY: Cornell University Press. Reeve, H. K. & Ratnieks, F. L. W. 1993 Queen – queen conflicts in polygynous societies: mutual tolerance and reproductive skew. In Queen number and sociality in insects (ed. L. Keller), pp. 45– 85. Oxford, UK: Oxford University Press. Reeve, H. K., Emlen, S. T. & Keller, L. 1998 Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? Behav. Ecol. 9, 267 –278. (doi:10.1093/beheco/9.3.267) Seppa¨, P., Queller, D. C. & Strassmann, J. E. 2002 Reproduction in foundress associations of the social wasp, Polistes carolina: conventions, competition, and skew. Behav. Ecol. 13, 531–542. (doi:10.1093/beheco/13.4.531) Shreeves, G. & Field, J. 2002 Group size and direct fitness in social queues. Am. Nat. 159, 81–95. Shreeves, G., Cant, M. A., Bolton, A. & Field, J. 2003 Insurance-based advantages for subordinate co-foundresses in a temperate paper wasp. Proc. R. Soc. Lond. B 270, 1617– 1622. (doi:10.1098/rspb.2003.2409) Strassmann, J. E., Fortunato, A., Cervo, R., Turillazzi, S., Damon, J. M. & Queller, D. C. 2004 The cost of queen loss in the social wasp Polistes dominulus (Hymenoptera: Vespidae). J. Kans. Entomol. Soc. 77, 343 –355. (doi:10. 2317/E-15.1) Sumner, S., Casiraghi, M., Foster, W. & Field, J. 2002 High reproductive skew in tropical hover wasps. Proc. R. Soc. Lond. B 269, 179 –186. (doi:10.1098/rspb.2001. 1884)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Social queues Tibbetts, E. A. & Dale, J. 2004 A socially enforced signal of quality in a paper wasp. Nature 432, 218 –222. (doi:10. 1038/nature02949) Turillazzi, S. 1991 The Stenogastrinae. In The social biology of wasps (eds K. G. Ross & R. W. Matthews), pp. 74–98. Ithaca, NY: Cornell University Press. Vehrencamp, S. L. 1983 A model for the evolution of despotic versus egalitarian societies. Anim. Behav. 31, 667 –682. (doi:10.1016/S0003-3472(83)80222-X) Wong, M. Y. L., Buston, P. M., Munday, P. L. & Jones, G. P. 2007 The threat of punishment enforces peaceful cooperation and stabilizes queues in a coral-reef fish. Proc. R. Soc. B 274, 1093–1099. (doi:10.1098/rspb.2006.0284) Wong, M. Y. L., Munday, P. L., Buston, P. M. & Jones, G. R. 2008 Fasting or feasting in a fish social hierarchy.

Phil. Trans. R. Soc. B (2009)

J. Field & M. A. Cant

3189

Curr. Biol. 18, R372–R373. (doi:10.1016/j.cub.2008. 02.063) Young, A. J., Carlson, A. A., Monfort, S. L., Russell, A. F., Bennett, N. C. & Clutton-Brock, T. 2006 Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc. Natl Acad. Sci. USA 103, 12 005–12 001. (doi:10.1073/pnas. 0510038103) Zanette, L. R. S. & Field, J. 2008 Genetic relatedness in early associations of Polistes dominulus: from related to unrelated helpers. Mol. Ecol. 17, 2590–2597. (doi:10. 1111/j.1365-294X.2008.03785.x) Zanette, L. R. S. & Field, J. 2009 Cues, concessions and inheritance: dominance hierarchies in the paper wasp Polistes dominulus. Behav. Ecol. 20, 773 –780.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3191–3207 doi:10.1098/rstb.2009.0101

Review

Lifetime monogamy and the evolution of eusociality Jacobus J. Boomsma* Centre for Social Evolution, Department of Biology, University of Copenhagen, 2100 Copenhagen, Denmark All evidence currently available indicates that obligatory sterile eusocial castes only arose via the association of lifetime monogamous parents and offspring. This is consistent with Hamilton’s rule (brs . roc), but implies that relatedness cancels out of the equation because average relatedness to siblings (rs) and offspring (ro) are both predictably 0.5. This equality implies that any infinitesimally small benefit of helping at the maternal nest (b), relative to the cost in personal reproduction (c) that persists throughout the lifespan of entire cohorts of helpers suffices to establish permanent eusociality, so that group benefits can increase gradually during, but mostly after the transition. The monogamy window can be conceptualized as a singularity comparable with the single zygote commitment of gametes in eukaryotes. The increase of colony size in ants, bees, wasps and termites is thus analogous to the evolution of multicellularity. Focusing on lifetime monogamy as a universal precondition for the evolution of obligate eusociality simplifies the theory and may help to resolve controversies about levels of selection and targets of adaptation. The monogamy window underlines that cooperative breeding and eusociality are different domains of social evolution, characterized by different sectors of parameter space for Hamilton’s rule. Keywords: Hamilton’s rule; insect societies; kin selection; levels of selection; germ line

‘Hence I can see no real difficulty in any character having become correlated with the sterile condition of certain members of insect-communities: the difficulty lies in understanding how such correlated modifications of structure could have been slowly accumulated by natural selection’. (Darwin 1859, p. 258) ‘I here suggest that the burden of proof may be upon the investigator who argues that sterile castes have evolved other than within broods of single mothers’. (Alexander 1974, p. 359) ‘Monogamy and especially monogamy outside the breeding season, is the rare exception’ . . . . ‘In the animal world, fidelity is a special condition that evolves when the Darwinian advantage of cooperation in rearing offspring outweighs the advantage of either partner of seeking extra mates’. (Wilson 1975, pp. 315, 330)

1. INTRODUCTION Extensive clades characterized by societies with obligatorily sterile members evolved in the ants, bees, wasps and termites (Wilson 1971, 1975). These eusocial forms of life have been associated with a major transition in organic evolution (Maynard Smith & Szathma´ry 1995), and some of them have been singled out as spectacularly sophisticated superorganisms (Ho¨lldobler & Wilson 1990, 2008; Moritz & * Author for correspondence ([email protected]). One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

Southwick 1992; Seeley 1995), but the fundamental nature of their evolutionary origins remains the subject of considerable debate (for recent contributions see Crozier 2008; Wilson 2008). This is remarkable, as Darwin had already provided the outline of an answer by suggesting that selection at the family level could explain why workers gave up personal reproduction and came to express different traits than queens and males. As the first quote above illustrates, a major issue for Darwin was to explain the evolution of worker sterility syndromes as a gradual directional process without any sudden leaps. As he writes, ‘Natura non facit saltum’ is an old canon in natural history that every experienced naturalist of his days adhered to. Re-reading the seventh ‘Instinct’ chapter in ‘The origin’ makes it clear that Darwin’s understanding of the problem was straightforward: insect workers lose their reproductive totipotency because of selection at the level of the close relatives around them and not merely any randomly formed group. William Morton Wheeler (1928) echoes Darwin’s insight by considering the transition to full sociality as a mere final step of increased family coherence in which ‘The progeny are not only protected and fed by the mother, but eventually cooperate with her in rearing additional broods of young, so that parent and offspring live together in an annual or perennial society’. A more pluralistic spectrum of hypothetical origins of eusociality arose in the second half of the twentieth century. The Darwin – Wheeler scenario was questioned because some eusocial bees mass-provision their cells before egg-laying, which precludes direct interaction between mother and offspring during the

3191

This journal is # 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3192

J. J. Boomsma

Review. Lifetime monogamy and eusociality

larval stage. Because of this apparent difficulty, Michener (1958) proposed that there might have been two precursor states for eusociality: The association between parents and offspring (the subsocial route) and the association between same generation breeders (the parasocial or semisocial route; see also Lin & Michener 1972; West Eberhard 1975). Although direct positive evidence for the parasocial route towards obligate eusociality has not been obtained (even 50 years after this hypothesis was conceived Bourke & Franks 1995; Boomsma 2007), this alternative paradigm was provisionally accepted by many (e.g. West Eberhard 1975; Wilson 1975) and appears to have retained some prevalence until the present day. This may be partly due to Hamilton’s (1964, 1972) inclusive fitness concept leaving open the possibility of multiple pathways towards eusociality, as his inequality condition for the evolution of altruism (Hamilton’s rule) can be fulfilled by a range of relatedness values. However, he also stressed that it is difficult if not impossible to conceptualize how sufficiently high relatedness in groups of same-generation females can be maintained across enough generations to make subordinates irreversibly lose their reproductive totipotency (Hamilton 1964, 1972; Wilson 1971), points that were reinforced by Alexander (1974) (see quote above) and Alexander et al. (1991). The main theme of the first part of the present review will be to refute the parasocial route towards eusociality more firmly, as being both conceptually untenable and inconsistent with empirical evidence, and to reinforce the subsocial scenario by explicitly connecting it to lifetime parental monogamy. I will argue that parasocial arrangements apply only to cooperative breeders and to those facultatively eusocial groups that are, in reality, cooperative breeders because they never realized the transition to having obligately eusocial helper castes. Ambiguity about the selection forces that ultimately caused individuals to irreversibly lose most or all of their reproductive potential has recently expanded into an extensive debate on the relative importance of kin selection and group selection (Wilson & Ho¨lldobler 2005; Fletcher et al. 2006; Foster et al. 2006a; Helantera¨ & Bargum 2007; West et al. 2007, 2008; Wilson & Wilson 2007; Gardner & Grafen 2009), and on the necessity of high relatedness to pass the eusociality threshold (Wilson 2005, 2008; Foster et al. 2006b; Crozier 2008). I hope to contribute to the resolution of the eusociality part of this debate by proposing a relatively simple and parsimonious scenario based on the notion that sexual partners commit for life in all presently known obligately eusocial ants, bees, wasps and termites. I will use the term ‘obligate eusociality’ to indicate situations where caste is irreversibly determined early in development (before pupation in the Hymenoptera), and to such extent that no individuals of predestined worker cohorts retain the behavioural, and often also physiological, option to disperse and found their own colonies (Crespi & Yanega 1995). Rather than focusing on Hamilton’s rule, I will concentrate on the lifetime monogamous mating system conditions that must have characterized lineages at the very origin of these eusocial clades. It was these Phil. Trans. R. Soc. B (2009)

conditions of ‘dying with the only sexual partner you ever have’ that gave Hamilton’s rule the most optimal conditions for forging the sweep towards eusociality without any leaps, or ‘salta’, because they implied that relatedness to siblings was no longer a variable, but a predictable equivalent of relatedness towards own offspring (Charnov 1978). When that is so, the relatedness terms cancel out of Hamilton’s rule when the actual transition towards obligate eusociality takes place. In the later sections of this review, I will briefly explore some of the implications, novel predictions and perspectives that this approach to the evolution of eusociality allows. I will argue that lifetime monogamy makes the evolution of obligate eusociality analogous to the evolution of multicellularity and that both types of development happened at roughly equal frequencies over evolutionary time. I will outline the kind of phenotypic and genetic predictions that can be derived from the lifetime monogamy idea and conclude that the obligatorily eusocial lineages are best considered as a separate domain of social evolution relative to the solitary and cooperative breeders. Finally, I will return to the analogy with multicellularity and briefly explore how the conceptualization of colony-level analogues of germ line and soma may further enhance our understanding of collective adaptations of eusocial colonies.

2. LIFETIME SEXUAL COMMITMENT OF PARENTS The parents of most eusocial insects (queens and males, the latter are sometimes referred to as drones or kings) produce only full sibling offspring throughout their lives (Boomsma & Ratnieks 1996; Strassmann 2001). They have a single brief period of irreversible mate choice as newly emerged adults and the ensuing monogamous relationship persists until they die (Boomsma et al. 2005). Physical lifetime monogamy is the default in termites, but queens of ants, bees and wasps have a functional equivalent of this in that their mates die without ever participating in colony founding, but have their sperm stored (Wilson 1971). These hymenopteran queens never re-mate even though they may survive and reproduce for years or decades (Ho¨lldobler & Bartz 1985; Boomsma et al. 2005; Kronauer & Boomsma 2007). The complete absence of re-mating promiscuity (Boomsma 2007) not only imposes extraordinary selection for maintaining viability of stored sperm (Ho¨lldobler & Bartz 1985; Baer et al. 2006; Den Boer et al. 2008), but also implies that altruism (as soldiers or workers) benefits siblings with an average relatedness (r) of 0.5 when queens are singly inseminated and there is equal Fisherian sex allocation. For haplodiploid Hymenoptera this average is between 0.75 relatedness towards sisters and 0.25 relatedness towards brothers, whereas the diploid termites are related to siblings of both genders by 0.5 (see also Queller 2000). Multiple queen-mating arose in many clades of eusocial Hymenoptera (Boomsma & Ratnieks 1996; Boomsma et al. 2009) but, as predicted by Hamilton (1964): ‘ . . . if the trend to multiple insemination occurs after the firm establishment of the worker

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Lifetime monogamy and eusociality caste, its threat to colonial discipline is a rather remote one’. This was recently confirmed by a formal comparative analysis (Hughes et al. 2008), which showed that all presently known clades of eusocial ants, bees and wasps with multiple queen-mating are derived from ancestors with single queen-mating. Multiple mating therefore neither complicates the early evolution of eusociality nor its later elaborations. As worked out in more detail in a previous review (Boomsma 2007), every ancestor of an extant independent eusocial lineage can be predicted to have passed through a monogamy window. This prediction has been—and will be below—primarily elaborated for the four classical examples of advanced eusociality (ants, most corbiculate bees, vespine wasps, higher termites), but should equally apply to thrips, bark beetles, sphecid wasps, shrimps, naked mole-rats (Heterocephalus glaber) and aphids (with due consideration of clonality), if they were to be considered as eusocial lineages or advanced cooperative breeders on the brink towards making the transition (Crespi 1996). The rationale of this prediction is that only the lifetime exact equivalence (in average relatedness terms) between offspring and sibling production is a parsimonious universal condition to start and maintain consistent directional selection for the loss of reproductive totipotency of entire cohorts of offspring. Once this average r ¼ 0.5 condition is fulfilled, there may be (but often will not be) cost–benefit factors that push a species into the eusocial state (Bourke & Franks 1995; Crespi 1996; Crozier & Pamilo 1996; Gadagkar 1996; Queller 1996) in the gradual accumulative way envisaged by Darwin (1859) and with the necessary genetic changes as hypothesized by West Eberhard (1996) and Linksvayer & Wade (2005). When parents commit their lifetime reproductive success to a single sexual partner, any infinitesimal cost–benefit advantage (c/b sensu Hamilton’s rule) would suffice to make the irreversible transition towards obligate eusociality. Lifetime monogamy would make such advantage last a helper’s lifetime, where it would not in cooperatively breeders where sexual partners do get exchanged. Thus, entire cohorts of offspring would be selected to give up the ability to mate and reproduce in the former, but not in the latter social setting. Any minute degree of parental coercion (Charnov 1978) would suffice to achieve the same result, and could easily trigger an increased dependence on indirect fitness benefits in offspring (cf. Linksvayer & Wade 2005), because the transition towards eusociality is neutral in terms of offspring inclusive fitness and unambiguously favourable for direct parental fitness (Bourke & Franks 1995; Crozier & Pamilo 1996). To see this, it is important to realize that for the evolution of eusociality, Hamilton’s rule is not written as: br . c, but as br . 0.5c, because the cost is paid as a reduction in offspring to which the actor is related by 0.5, rather than in the survival probability of self to whom the actor is related by 1 (as is, for example, the case for vertebrate alarm calls). Lifetime monogamy thus implies that the relatedness term cancels out of Hamilton’s rule when the average relatedness to siblings is predictably 0.5, so that becoming a sterile helper should merely be a matter of time when b.c is fulfilled throughout the lifetime of cohorts of offspring. Any other mating Phil. Trans. R. Soc. B (2009)

J. J. Boomsma

3193

system that would not necessitate that you die with the single mate that you found early in life would produce a less favourable scenario for the evolution of obligate reproductive altruism as it would probably require leaps in the Hamiltonian b/c ratio for making the transition (figure 1; see also Boomsma 2007, fig. 2).

3. EVIDENCE FOR ANCESTRAL LIFETIME MONOGAMY IN EUSOCIAL LINEAGES Termite queens normally produce full sibling offspring throughout their lives, because they commit to a single male when founding a colony. The only difference with the ants, bees and wasps is that males have similarly long lifespans to queens and that mating continues throughout life. Exceptions to this rule may occur in evolutionarily derived termite lineages where multiple breeders are sometimes found (Thorne 1983, 1985; Roisin 1987; Darlington 1988; Atkinson & Adams 1997; Thompson & Hebert 1998; Brandl et al. 2001; Hacker et al. 2005; Atkinson et al. 2008), but no cases of effective re-mating promiscuity followed by successful colony continuation appear to have been documented with genetic markers. Issues of matechoice and sexual selection during swarming (e.g. courtship, sex pheromone communication, display) and society building therefore appear to be as fully separated in the termites as they are in the eusocial Hymenoptera (Boomsma et al. 2005). The crucial point is that, as a rule, no ‘new blood’ ever seems to enter an existing termite colony (Boomsma 2007; see below for an evaluation of apparent exceptions). In spite of lifetime parental monogamy at colony founding, the lower termites remained cooperative breeders in a functional sense (Korb 2008; Lo et al. 2009). This may be related to most of them having life histories of ‘one piece’ (‘single-site’) nesting, which implies that they gradually excavate their nest in the log that they feed on. Larger and older colonies thus become more likely to lose their local nesting and feeding monopoly, as the probability of being confronted with neighbouring colonies in the same log increases when less of the food and nest substrate remains. This maintains selection for reproductive totipotency in offspring, as dispersal will remain the ultimately superior solution when nestmate relatedness stands to become diluted by joining non-relative breeders, re-assortment of parentage and finally, starvation. This is consistent with the first eusocial castes in termites arising as soldiers rather than workers, as the former are more effective in maintaining the integrity of a monogamous family against assaults of neighbouring conspecifics (Shellman-Reeve 1997; Roisin 1999; Korb 2008). Reproductively altruistic workers apparently only evolved after termites had reached the derived state of having both a nest and an external foraging range (multiple site nesters and central place foragers), as envisaged by Abe (1991) and Higashi et al. (1991). It is still unclear how often these nesting habits and worker castes evolved (Thompson et al. 2000; Inward et al. 2007), but the correlation between the presence of true workers and foraging beyond the boundaries of the nest is apparently a perfect one (Inward et al. 2007). Both the cost of

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3194

J. J. Boomsma

Review. Lifetime monogamy and eusociality 1.5

likely transition

unlikely transition

0.5 auxiliary colony founders and/or re-mating promiscuity

elaborations of eusociality via polyandry or polygyny 0.5

monogamy window

0

Hamiltonian b/c ratio

relatedness to nestmates

1.0

0 evolutionary time

Figure 1. Evolving obligate eusociality via a monogamy window, with nestmate relatedness to the left and the per capita Hamiltonian b/c ratio to the right (both lifetime averages as in Boomsma 2007, fig. 3). Given that promiscuity and some degree of multiple breeder aggregation are the default settings of most breeding systems, nestmate relatedness (lower curves) is typically low but positive in distant ancestors and has to increase to 0.5 (either shallowly via a cooperative breeding system, or steeply from a polygamous solitary ancestor—the hatched area towards the left illustrates the likely ranges of relatedness). However, when lifetime monogamy has been established (i.e. the monogamy window has been reached), infinitesimally small but consistent group benefits (b/c . 1) will be sufficient to make the transition towards eusociality (short vertical arrow). Once obligate non-matedness (complete or partial sterility) of helper cohorts has been established, polyandry (multiple queen-mating) or (secondary) polygyny may re-evolve (but would not necessarily do so) and will reduce nestmate relatedness (hatched area towards the right). With the possible exception of inquiline social parasites, and the poneroid ants where adult workers may later become mated to assume dominant breeder roles, this has never led to the abandonment of obligately eusocial phenotypes. This must have been because the group-size benefit curve b/c increases more sharply than the relatedness curve decreases. Inbreeding is not considered here because there seem to be no examples where inbreeding has been associated with the evolution of eusociality without parents also being lifetime monogamous (Pamilo 1991). Any transition that could conceivably take place at, say, r ¼ 0.4, would require a per capita group size (b/c) benefit .1.25 to be consistent with Hamilton’s rule. Given that b/c cannot be expected to exceed 1 before group-living is established, this would require a step-wise transition in the b/c curve, which makes this scenario (long vertical arrow) unlikely.

foraging (Korb 2008) and disease pressure (Thorne & Traniello 2003) probably increased significantly when colonies came to extend beyond the confinements of a single log, which may have gradually increased the group-wise benefits from task partitioning and mutual grooming, so that obligate altruism evolved in combination with increased rates of senescence of the now more exposed helpers (Alexander et al. 1991; Bourke 1999, 2007; Crespi 2007). However, the decisive selection force for evolving lifetime sterile worker phenotypes may well have been that inescapable mergers of mature colonies no longer occurred so that the risk of sudden drops in relatedness towards nestmates due to remaining parents finding new mates had disappeared. The fact that colony boundaries became defined by foraging ranges rather than nest space thus implied that the inclusive fitness benefits owing to parental monogamy became guaranteed across the lifetime of any entire cohort of helpers. Phil. Trans. R. Soc. B (2009)

All free-living ants have (had ancestors with) an obligatorily eusocial worker caste, whereas rather few derived lineages with large colonies also have soldiers (Wilson 1971; Ho¨lldobler & Wilson 1990). This is consistent with the early evolution of the ants being characterized by foraging beyond the nests boundaries, which was unavoidable as primitive ants were predators, so they could not live within their food as the ancestral termites could. The subsocial origin of the ants appears to be generally accepted as the most likely scenario from Wheeler (1928) onwards, and lifetime monogamy of the ancestral ant is consistent with the comparative data available (Boomsma & Ratnieks 1996; Boomsma 2007; Hughes et al. 2008). A unique feature of the ants is that they have a large basal branch, the poneroid complex, that retained an exclusively predatory lifestyle and realized relatively little further elaboration of eusociality compared with the formicoid ants (Brady et al. 2006; Moreau et al. 2006;

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Lifetime monogamy and eusociality Ho¨lldobler & Wilson 2008; Rabeling et al. 2008). Some of these ants have workers that may become mated after having gained single breeder status, whereas others have lost the queen caste, either in part of the colony or altogether (Peeters 1997; Ho¨lldobler & Wilson 2008). The latest phylogenetic reconstructions seem to imply that the poneroid ants and a few other lineages might have lost a number of key eusocial traits that probably characterized the ancestor of all ants, e.g. queen castes were lost in some clades, whereas others have many workers that mate and compete with queens for full reproduction. These ants have thus reverted to advanced forms of cooperative breeding comparable to, for example, naked mole-rats (Peeters 1997; Hart & Ratnieks 2005; Ho¨lldobler & Wilson 2008). The crucial trait that makes them cooperative breeders is that females with a morphologically distinct worker phenotype can mate later in life to become the dominant breeder in the same colony in which they hatched (Ho¨lldobler & Wilson 2008). The recent discovery of the sister group of all previously known ants (Rabeling et al. 2008) suggests that many early ants lived as hidden soil-dwellers (also the next branch, the Leptanillinae, have such a lifestyle). As Hamilton (1978) argued, life under the bark of dead trees (or its equivalent in the soil under decaying logs) may have imposed consistent selection for wing polymorphism and facultative non-dispersal of offspring. At the same time, the spaced-out and hidden nest cavities that he describes may have provided many of the conditions favouring lifetime parental monogamy. Likewise, nesting in or under decaying logs may have selected for a long lifespan because of low extrinsic mortality after colony establishment (Keller & Genoud 1997), which would explain that all ants (and termites to which the same selection forces must have applied) have perennial colonies in contrast to all but the most evolutionary derived eusocial wasps and bees. This inference is not necessarily in conflict with the oldest known fossil ant having large eyes (Wilson 1971; Grimaldi & Engel 2005), as many ants combine deep soil nesting with diurnal surface or arboreal foraging. However, clades combining these traits may have been more prone to extinction than those specialized for a completely underground lifestyle, so that only the latter are extant. The early social evolution pathways in the vespid wasps were characterized by cooperative breeding rather than eusocial commitment and it seems that open nesting may have prevented single females from creating full sibling colonies. Whether related or not, if females compete for nests or nestsites, full sibling families will arise only if one female can exclude all nest-founding competitors until the first offspring cohort hatches. The prevalence of primary polygyny (following pleometrosis) in the tropical stenogastrine and polistine wasps is therefore consistent with the maintenance of individual totipotency, as options for direct fitness benefits either in a co-founded nest or elsewhere remain a realistic option. The stenogastrine clade never evolved obligate eusociality, whereas the sister clade consisting of the polistine and vespine wasps has a single transition towards obligate Phil. Trans. R. Soc. B (2009)

J. J. Boomsma

3195

eusociality in the ancestor of the vespines that adopted single queen breeding (Hines et al. 2007). This scenario was already conceptualized by Wheeler (1928), and by Wilson (1971) who wrote: ‘The life cycle of the vespines is basically similar to that of Polistes, except that the queen is not joined by auxiliaries during nest founding in spring’. Thus, although single mating as a precondition for eusociality was fulfilled in all basal wasp lineages (Hughes et al. 2008) it was only after obligate monogyny arose in the ancestor of the vespine wasps that the transition to obligate eusociality happened, as predicted by the monogamy window hypothesis. The arguments above illustrate that social systems like Polistes, and their close relatives such as Ropalidia, are best considered as cooperative breeders, because they have no permanent castes as defined in the introduction of this review (Gadagkar 1994, 1996), as broods tend to have at least some individuals that become early diapausing queens rather than helpers at the nest (Reeve et al. 1998). Just like many poneroid ants, these social systems are characterized by most individuals ‘queuing’ for possible future reproductive dominance (i.e. direct fitness benefits). Similar to vertebrate cooperative breeders, relatedness-based inclusive fitness benefits may or may not be found, as both the ability to recognize kin and the (in)direct benefits from helping vary across species so that each of these parameters needs to be explicitly considered (Griffin & West 2003). The data are noisy, but Polistes gynes in spring tend to voluntarily associate only with those natal nestmates of the previous season that are relatives. Later in the season interactions between unrelated females increase in frequency, but females that join at this stage behave quite differently than related cofoundresses. They are highly likely to have lost their own nests to predators and usurp nests for direct fitness benefits rather than indirect ones (Strassmann 1996). In addition, colonies that suffer a sudden reduction in relatedness due to usurpation events will tend to have more female larvae developing into dispersing gynes (aiming for direct future fitness benefits) than into staying workers (continuing to rely on indirect fitness benefits) (Strassmann 1996). The epiponine (polybiine) wasps, which puzzled Hamilton (1964, 1972) as odd enigmas for inclusive fitness theory, have since been shown to produce males when colony relatedness is low, but gynes later in the colony cycle when relatedness is high because the number of egg-layers has been reduced to one (Queller et al. 1993). This implies that largely totipotent helpers (Strassmann et al. 2002) reap considerable indirect fitness benefits through sex ratio biasing (Boomsma & Grafen 1991) in a social system that is cyclically monogamous (Queller et al. 1993; Hastings et al. 1998). This highly successful clade of wasps with perennial nests even managed to decouple swarm production from queen production (Strassmann et al. 1998). Yet, although the collective worker interests are largely met—in contrast to what is generally found in Polistes (Hastings et al. 1998)— it seems doubtful whether the epiponine wasps crossed the threshold towards obligate eusociality in the sense of evolving a worker caste that is uniformly determined

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3196

J. J. Boomsma

Review. Lifetime monogamy and eusociality

before larval pupation (Strassmann et al. 2002). This is consistent with founding new colonies by multiple females (swarm founding), which precludes lifetime monogamous parenting (Boomsma 2007). Interpreting the early evolution of eusociality in bees as a straightforward subsocial transition has been hampered by the apparent absence of progressive larval provisioning (adults continuing to actively feed larvae until pupation), which is one of the crucial brood-care traits of eusociality, in the stingless bees. This seemed to imply that the ancestor of the corbiculate bees, which also include the largely solitary euglossine bees and the eusocial bumble-bees and honeybees that have progressive provisioning, might have had a different family structure (Michener 1958; Lin & Michener 1972). Also the origins of incipient, facultative forms of eusociality in the halictid bees did not seem to depend on progressive provisioning. However, recent work has indicated that all eusocial halictid bees that have been studied do in fact have regular brood inspection by a single mother bee, which is likely to be adaptive for reasons of sanitation and adjustment of the quality and quantity of the pollen provision masses (Plateaux-Que´nu 2008). The most parsimonious explanation for the three emergences of facultative eusociality (in the sense that worker broods contain at least some early diapausing individuals) in halictid bees (Danforth 2002) would therefore now appear to be the subsocial route. As all corbiculate bees are monogynous (Wheeler 1928) and have a singly mated ancestor (Hughes et al. 2008), this must also apply to the origin of obligate eusociality in this clade. A universal explanation of eusocial evolution via the monogamy window hypothesis would therefore imply that the extant practice of mass provisioning (adults completing provisioning of brood cells before egg-laying and capping cells shortly afterwards) in stingless bees is a secondary development that arose after the ancestor of the corbiculate bees had become obligately eusocial. It is tempting to speculate that increased disease pressure on perennial colonies of these tropical bees, relative to their annual temperate zone bumble-bee sister clade (Kawakita et al. 2008), may have selected for capping cells immediately after provisioning, and that this was not required in honeybees because they evolved genetically more diverse colonies via multiple queen-mating (Boomsma & Ratnieks 1996). As in the polistine and stenogastrine wasps, it is essential for comparative evaluations of sociality in bees to be precise on whether eusocial helping is obligate, i.e. whether individual caste fate is irreversibly determined before pupation. Even though females often remain wholly or largely sterile, this is not a universal trait for entire cohorts of same-age offspring in clades such as the halictids and allodapines that have been called ‘eusocial’ (cf. Crespi & Yanega 1995). Workers have maintained their spermathecae and many are mated and have the option to express full breeding potential elsewhere, either alone or with other females. The halictid and allodapine bees are therefore best considered to be cooperative breeders, where individuals can facultatively adjust their helping and dominance behaviour to the particular mixture of Phil. Trans. R. Soc. B (2009)

direct and indirect fitness opportunities that they encounter. Even a very low frequency of early diapausing individuals in worker cohorts implies that the social system has not passed the point of no return towards obligate eusociality. Deviations from lifetime monogamy in lineages that are likely to still have such early diapausers (Soro et al. 2009) therefore do not refute the monogamy window hypothesis, but rather assert that such a lineage will not make the transition in the future either. Not having passed the threshold towards obligate eusociality does not imply that worker roles do not allow considerable indirect fitness benefits to be obtained. Similar to the epiponine wasps, Augochlorella bees have been shown to capitalize on relative relatedness asymmetries by producing adaptive split sex ratios based on colony-level variation in relatedness asymmetry (Mueller 1991). It thus appears that the monogamy window hypothesis is consistent with most if not all evidence available, which is satisfying as it lends credit to the most general and parsimonious explanation for the convergent origins of eusociality, without any of them requiring sudden step-wise leaps (figure 1) in the b/c ratio of Hamilton’s rule (see Darwin’s quote at the start of this essay). The seeming absence of countervailing evidence is also somewhat surprising, as it might be argued that the monogamy window hypothesis may be a rather crude oversimplification. It has, for example, been shown that a fraction of unmated, male producing foundresses and partial bivoltinism may both select for female biased sex ratios so that Hamilton’s rule is fulfilled at sibling relatednesses that are somewhat below 0.5 on average (Seger 1983; Godfray & Grafen 1988). A similar effect has been shown to apply when a newly evolved worker caste produces some of the males (Pamilo 1991). This implies that low frequencies of double-mating or foundress association would theoretically be compatible with the gradual evolution of obligate eusociality. Yet, there is nothing in the available data that suggests that scenarios like this were likely to have applied. Clarifying why this is so is beyond the scope of this paper and would require formal modelling. I assume though that such models will vindicate the monogamy window hypothesis, when they make reasonable assumptions on the additional costs of cofoundressconflict, sexual selection and ejaculate competition, when they assume that there is a cost of discriminating between the haploid eggs to be replaced versus the diploid eggs to be left alone, when they consider geometric mean fitness rather than arithmetic mean fitness, and when they allow for realistic amounts of stochasticity. Inbreeding might be included as a factor in such models, although it seems unlikely that this would have a significant effect (Pamilo 1991).

4. IMPLICATIONS One could argue that the monogamy hypothesis makes the evolution of eusociality too easy. However, where previous authors (Stubblefield & Charnov 1986; Maynard Smith & Szathma´ry 1995) used this argument when discussing a rather unspecified form of monogamy, it does make a difference that the lifetime type

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Lifetime monogamy and eusociality of monogamy considered here is a very rare condition (e.g. E. O. Wilson quote at the start of this review), particularly when it would have to be maintained over thousands of generations to reshape entire gene expression networks, as would be required for the evolution of permanent helper castes (cf. Linksvayer & Wade 2005). At least two further factors would also hamper the evolution of obligate eusociality. First, the monogamy window hypothesis requires that the ‘point of no return’ transition towards eusociality (Wilson & Ho¨lldobler 2005; Wilson 2008) can only be passed when the b/c ratio remains .1 (if only just) throughout the life of entire helper cohorts. When this is not completely met, social evolution will remain stalled in an advanced form of cooperative breeding where at least some helpers can move on to breed independently as, for example, in halictid and allodapine bees, stenogastrine and polistine wasps, lower termites, social spiders, and naked and Damaraland mole-rats (Cryptomys damarensis) (cf. Hart & Ratnieks 2005). Second, there may be many factors that enhance the Hamiltonian benefits of group living (b), but there are also many (e.g. temporal variation in food availability) that constrain such benefits relative to the direct fitness gains of personal reproduction (c), thus effectively precluding anything other than solitary breeding (e.g. Bourke & Franks 1995; Crespi 1996; Crozier & Pamilo 1996; Gadagkar 1996; Queller 1996). This may explain why lineages may be life-time monogamous for a long time before eusociality evolves. A striking benefit of group living is improved nest defence (fortress defence sensu Strassmann & Queller 2007), but the other side of this coin is that nest predation has probably been a major general factor that precluded eusocial breeding, as high family-level mortality will maintain selection for dispersal and solitary breeding. Closed and easily defendable nests, often with a single entrance, may thus have provided both protection from conspecific female auxiliaries and usurpers (preventing dilution of sibling relatedness) and protection against nest predators (providing consistent b/c benefits) when lineages were passing through the monogamy window towards eusociality. When the 0.5 relatedness term cancels out of Hamilton’s rule, the conditions for the evolution of eusociality become equivalent to those that apply for the evolution of clonal multicellularity (Queller 2000). This is because the relatedness ratio of siblings versus offspring is equal to the relatedness ratio of adhering cell copies versus dispersing ones, in spite of the twofold difference in absolute values of relatedness (0.5 versus 1.0). Similar to lifetime monogamy not always leading to eusociality (e.g. the lower termites and many solitary wasps and bees), clonal kinship is an essential condition for making the transition to multicellularity, but there are many clonal eukaryotes that never achieved this. The respective statistics between origins of eusociality and multicellularity are remarkably similar: There have been at least 25 independent transitions towards multicellularity (plus a number of secondary reversals), but only approximately three to five of these concerned eukaryotes and produced extensive radiations of complex organisms (Grosberg & Strathmann 2007). These Phil. Trans. R. Soc. B (2009)

J. J. Boomsma

3197

figures are unlikely to be significantly different from the still increasing number of shallow origins of facultative eusociality relative to the four ‘classic’ deep origins of obligate eusociality (Crespi 1996, 2007). Thus, if there is a problem in obligate eusociality having evolved rather rarely (Stubblefield & Charnov 1986), there is an analogous problem in the scattered evolution of multicellularity. In this perspective, it is not surprising that three of these four deep evolutionary origins occurred in the haplodiploid Hymenoptera, as the ancestors of the ants, the vespine wasps and the corbiculate bees must have had lifetime sperm storage by females, which makes it easier to maintain lifetime monogamy. The selective advantages that drove the evolution of multicellularity were size-related returns to scale and benefits from functional specialization and division of labour (Grosberg & Strathmann 2007), analogous to the advantages that must have accompanied the origins and early elaborations of eusociality (Pamilo 1991; Bourke & Franks 1995; Crespi 1996; Crozier & Pamilo 1996; Queller 1996) (cf. the accelerating b/c curve in figure 1). When partners commit for life, their ‘triploid’ (Hymenoptera) or ‘tetraploid’ (termites) union is analogous to the diploid zygote that initiates every individual of a multicellular sexually reproducing species (figure 2). The origin of the zygote is generally considered to have been a crucial bottlenecking singularity that reduced conflict by starting each individual as a merger of the minimal number of independent nuclear genomes to allow recombination and a single clone of uniparentally transmitted cytoplasmic symbionts that became organelles while contributing, and ultimately retaining some of their own genomes (Buss 1987; Maynard Smith & Szathma´ry 1995; Queller 2000; Grosberg & Strathmann 2007; Michod 2007). Just like life-time monogamous pairs, the sexual zygote allowed transitions towards lifetime-committed group-living based on the predictable production equivalence of vertical (adhering) versus horizontal (dispersing) gene copies in the next generation (see also Queller 2000). It is useful, therefore, to distinguish them as each having initiated their own domains of social evolution, the zygote by establishing the individual as unit of selection and target of adaptation and the lifetime monogamous parents of insect societies by offering the same potential to the eusocial colony (table 1). However, while the clonal nature of multicellular bodies allowed them to become inclusive fitness maximizing vehicles for their gene replicators (Dawkins 1982), the evolution of explicitly eusocial colony-level adaptations was constrained—in spite of the importance of colony level selection—because internal conflict repression is difficult in non-clonal groups (Wenseleers et al. 2004; Ratnieks et al. 2006) and a higher degree of such repression appears needed for the evolution of superorganismality (Gardner & Grafen 2009) than previously thought (e.g. Reeve & Ho¨lldobler 2007). The evolution of anisogamous sex itself that preceded the origins of multicellularity in eukaryotes could only happen after a twofold disadvantage was overcome (e.g. Williams 1985; Maynard Smith & Szathma´ry

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3198

J. J. Boomsma

Review. Lifetime monogamy and eusociality evolutionary transition

singularity

transition to (clonal) eukaryote multicellularity

zygote

r = 1.0

royal ant pair

transition to (haplodiploid) eusociality ‘triploid zygote’ r = 0.5

royal termite pair

transition to (diploid) eusociality

‘tetraploid zygote’ r = 0.5

Figure 2. Schematic comparison of the evolutionary transition from unicellularity to multicellularity and the evolution of eusociality in the haplodiploid ants (the same applies to bees and wasps) and diploid termites. The diploid zygote that originates when syngamous haploid gametes commit for life is an analogous singularity to the permanent ‘triploid’ or ‘tetraploid’ unit that is created by lifetime monogamous mates when they co-found a eusocial colony. Zygotes create multiple, genetically identical (r ¼ 1) copies when making multicellular bodies, whereas lifetime monogamous mating pairs create genetically variable offspring that are on average 50 per cent (r ¼ 0.5) identical. All three examples are fully equivalent for the transmission of maternally inherited cytoplasmatic organelles. When multiple queen-mating evolves secondarily in the eusocial Hymenoptera, the ‘ploidy’ of the founding unit may increase considerably (up to approx. 50 haplotypes in army ants and honeybees). This implies that relatedness asymptotically drops to 0.25, but it does not change the principle of lifetime commitment. Parental (chromosomal) haplotype contributions are marked with different colours; the female cytoplasmatic background is kept in white, whereas the non-transmitted male one is marked in light green. For the eusocial colonies, a sample of their sexual production is plotted, assuming Fisherian sex allocation with 50 per cent haploid males in the Hymenoptera. The workers of such colonies are all females (diploid). No such asymmetries apply in the diploid termites.

Table 1. A partial reappraisal of the major eukaryote transitions in evolutionary complexity (cf. Maynard Smith & Szathma´ry 1995), emphasizing the singularities that initiated them, the main selection drivers that pushed ancestors through these singularities, and the major threats that might have prevented the transition and that needed further evolutionary elaboration to be sufficiently controlled for the higher level of selection to prevail. The three classes represent different domains of social evolution, characterized (roughly) by outbred sex as the only cooperative social interaction (1); a combination of (usually outbred) sex and (possibly) social interactions between relatives (the latter in case of cooperative breeding) that normally overlap in space and time (2); a strict separation between solitary sexual behaviour and family-based social interactions in time, and usually also in space (3). Because of these fundamental differences and the presence/absence of a committed worker caste, secondary developments towards cooperative breeding in the eusocial domain 3 (e.g. poneroid ants; secondary polygynous formicoid ants) are often not directly comparable with non-eusocial cooperative-breeding systems that belong (together with all solitary breeding) to domain 2. The integrity of the domains is threatened by genetically distinct elements that themselves represent different levels of organization. Those relevant for domain 1 are reviewed in Burt & Trivers (2006) and those relevant for domain 2 in Buss (1987) and Michod (2005). Threats of domain 3 may include workers that reproduce in the presence of the queen and socially parasitic additional queens that may ultimately give rise to inquiline species (Buschinger 1990) and selfish patrilines (Hughes & Boomsma 2008).

singularity

transition

drivers

threats

prevailing level of selection

1. haploid symbiotic cell 2. life-time committed zygote 3. life-time committed parents

sexuality multicellularity eusociality

recombination/repair group selection group selectiona

selfish genetic elements selfish cell lineages selfish individuals

cell individual colony

a

In contrast to domain 2 where group selection leads to individual adaptation, group selection in domain 3 does not necessarily lead to group adaptation.

1995; Cavalier-Smith 2006), so it is not surprising that this only happened once at the base of the eukaryote tree. The monogamy window hypothesis makes a sharp distinction between cooperative breeding and Phil. Trans. R. Soc. B (2009)

eusociality, and thus explicitly sides with the restricted definition of eusociality formulated by Crespi & Yanega (1995). It makes their definition more precise by merging the facultative eusociality and cooperative

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Lifetime monogamy and eusociality breeding categories. This is based on the notion that expressing facultative, context-dependent caste phenotypes is something fundamentally different from expressing irreversible physical caste phenotypes. Linksvayer & Wade (2005) have outlined a three-step hypothetical scenario for the genetic mechanisms mediating transitions towards eusociality that is consistent with this distinction. First, they assume that maternal care genes start being pre-reproductively expressed for sibling-rearing functions (cf. West Eberhard 1996) in association with nutritional state or other environmental factors (e.g. Hunt 1994; Wheeler et al. 2006; Patel et al. 2007), which themselves may have been influenced by parental manipulation. Second, these phenotypically plastic reaction norms of optimal performance as a breeder or helper may then become associated with the expression of additional genes that specifically produce good queens or good workers. Third, the transition to obligate eusociality requires further evolution or elaboration of caste-specific gene expression, for example through gene duplications, to reduce the relative significance of the original pleiotropic genes that affect both helper and breeder performance. Whereas it is easy to see how the first two steps apply to cooperative breeders such as Polistes wasps, step 3 requires a long process of directional selection for decoupling the expression of genes coding for maternal and sibling care and for these alternative phenotypes to become associated with an early developmental bifurcation and correlated with the expression of novel mutations at other loci so that permanent morphological castes emerge (Hunt 1994; West Eberhard 1996; Abouheif & Wray 2002; Linksvayer & Wade 2005; Wilson 2008). Recent evidence has demonstrated the key significance of nutrition for caste determination (Hunt 2007), providing direct insights into the proximate factors that characterize transitions to obligate eusociality. However, it is important to separate this type of explanations from the ultimate causes, i.e. the notion that selection is only likely to work consistently and directionally on these mechanisms to forge transitions to obligate eusociality when lifetime parental monogamy is ensured (figure 1). I conclude that all extant obligatorily eusocial clades appear to have in common that their distant ancestral mother became a lone nest founder and stopped mating with additional males, so that entire cohorts of her offspring could give up mating at all. This notion is consistent with a general trade-off between parental effort and mating effort (West Eberhard 1983; Boomsma 2007; Crespi 2007) and with Yanega’s (1997) conclusion that (non-)mating is the main correlate across halictid bees of helping and dying in the same year versus early diapause and breeding the following year. The loss of a functional spermatheca in hymenopteran workers is a much later development and has only been documented for the honeybees and most of the ants (Gotoh et al. 2008). This implies that many groups that have passed the no-return threshold towards obligate eusociality have workers with spermathecae although these workers never mate (Gotoh et al. 2008). This would explain that some exceptions to this rule, for example Phil. Trans. R. Soc. B (2009)

J. J. Boomsma

3199

in the poneroid ants, could resume worker mating even though they likely had ancestors with behaviourally sterile workers (Gobin et al. 2006; Rabeling et al. 2008). This underlines the notion already expressed by Wheeler (1928) that most traits that characterize extant crown groups of obligatorily eusocial insects are secondary elaborations that cannot shed light on the early evolution of eusociality.

5. PREDICTIONS OF THE MONOGAMY WINDOW HYPOTHESIS The lifetime monogamy hypothesis is a bold generalization that implies strong inferences about the parasocial route towards obligate eusociality being incorrect and Hamilton’s rule being applicable in a general, but uniquely restricted manner. Neither of these restrictions should apply to cooperative breeding, including many facultatively eusocial forms, where associations between same-generation females are often relevant and where relatedness towards nestmates or siblings may vary freely without jeopardizing the evolutionary stability of these breeding systems (e.g. Griffin & West 2003; see also Hamilton 1964, 1972; Alexander 1974; Alexander et al. 1991). Although the monogamy window hypothesis at present appears to be compatible with the available data (see above and also Boomsma 2007; Hughes et al. 2008), its predictions need to be made more quantitative by explicit modelling and be tested by further empirical work. A general qualitative prediction is that the secondary evolution of polygyny and polyandry in the eusocial higher termites (Termitidae) should be constrained, because their worker and soldier caste determination systems are likely to have remained more reversible than in the ants (e.g. Roisin & Pasteels 1987). Parental promiscuity would introduce sexual conflict into existing societies and instigate selection on helper castes to express selfish rather than altruistic traits, developments that would tend to destabilize the eusocial breeding system. Such constraints would not apply to any of the eusocial Hymenoptera, because sexually conflictual re-mating promiscuity is precluded by early male death and life-time sperm storage by females. This appears consistent with the data as multiple breeders, although reported from tens of termite species, are almost always a rare and facultative phenomenon at the population level (Thorne 1985; Roisin 1987). Given these interesting differences between the ants and the termites, it would be of paramount importance to critically evaluate the sparse records on multiple breeders in colonies of the higher termites (Thorne 1983, 1985; Roisin 1987; Darlington 1988; Atkinson & Adams 1997; Thompson & Hebert 1998; Brandl et al. 2001; Hacker et al. 2005; Atkinson et al. 2008) to ascertain that: 1. They are derived from unrelated co-founders for each of the sexes, rather than being secondary reproductives produced by a single founding pair; 2. The combination of breeders does indeed allow re-mating promiscuity, which would require that there are both multiple unrelated kings and queens in a single colony. If only one of the sexes is found as multiple breeders, the principle of life-time

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3200

J. J. Boomsma

Review. Lifetime monogamy and eusociality

commitment would probably be upheld, so that the breeding system is analogous with multiple queen mating in the eusocial Hymenoptera (e.g. records of multiple kings per colony are rare and these colonies might be monogynous); and 3. All multiple reproductives do indeed contribute to the offspring of the colony. The overall expectation would be that occasional cases of sexual partner shift can occur in the lower termites where helper castes have in any case maintained the possibility to develop into staying or dispersing (winged) breeder phenotypes, although documentation of the reproductive fitness of such novel parental combinations is needed. However, in the higher termites early caste determination should have evolved a high degree of irreversibility for remating promiscuity to be evolutionarily stable. Somewhat less precise qualitative tests would be possible in the advanced cooperative breeders for which developments towards eusociality have been documented: haplodiploid thrips, bark beetles and sphecid wasps, the clonal aphids and the diploid social Crustacea and naked and Damaraland molerats. All of these have well-defendable nests, galls or sponges and overlapping generations that extend tenure of the colonies (Crespi 1996) and all of them should be expected to have very low promiscuity. However, it is important to realize that many of them are lineages of recent origin with slight radiations at best and with close relatives that have lost or never gained eusocial traits (e.g. Stern & Foster 1997; Duffy 2003; Chapman et al. 2002), so that they will not fit the strict obligate eusociality definition of Crespi & Yanega (1995) that I adhered to in Boomsma (2007) and the present review. I expect that even the naked mole-rat, with its social system based on sterile foragers and nurses rather than soldiers, will turn out not to be obligatorily eusocial, because its helpers are not sufficiently differentiated in lifespan (in captivity, Sherman & Jarvis 2002) and at least some of them can shift to a breeder phenotype when the dominant of the same gender disappears. This underlines another prediction that has already been hinted at. As long as obligate lifetime non-matedness of helper cohorts has not been established, it cannot be inferred that the threshold towards obligate eusociality has been passed and that the species in question should thus necessarily be lifetime monogamous (e.g. Soro et al. 2009). The rapidly increasing availability of genomic databases will provide a good test bed for the lifetime monogamy hypothesis. When every extant eusocial lineage has a series of lifetime monogamous ancestors, antagonistic genes involved in interlocus sexual conflicts inherited from earlier promiscuous ancestors are expected to have been lost or become dysfunctional. This implies that such genes had to re-evolve in lineages of ants, bees and wasps that later evolved multiple queen-mating to regulate novel types of male – female conflict over sperm survival or sperm storage. Extant gene networks of the latter kind are therefore expected to be convergent and lineagespecific. The same prediction would apply for genes that are expressed to mediate issues of dominance and reproductive skew (Reeve & Keller 2001). Phil. Trans. R. Soc. B (2009)

A parasocial route towards eusociality would predict that genetic mechanisms have remained similar and homologous, so that for example polistine wasps and poneroid ants should share some of them. However, punctuation by a long-lasting monogamy singularity in the common ancestor of the ants should imply that novel gene expression networks had to evolve to regulate novel conflicts when polygyny re-emerged in the poneroid ants. Finally, I would expect that—as far as they are genetic—the kin-recognition systems of clades that represent independent evolutionary contrasts of cooperative breeding versus eusociality (e.g. the polistine and vespine wasps, and the halictid and corbiculate bees) may well be based on non-homologous genes, as only nestmate versus non-nestmate recognition was required in the full sibling colonies that characterized the monogamy window. When eusocial lineages secondarily evolved genetically more variable colonies, owing to multiple queen-mating or polygyny, the (re)establishment of any nepotistic recognition cues via random mutation was highly constrained, because of increased group selection for colony-level productivity and significant erosion of informative genetically determined cues (Crozier 1987). This inference matches an emerging consensus that nepotistic recognition cues are absent in the multiply mated ants, bees and wasps, and rare in the polygynous ants (Keller 1997; Boomsma et al. 2003; Gardner & West 2007) and seems to provide an interesting contrast with at least a few documented cases of recognition of degree of kin in non-eusocial insects (Greenberg 1979; Lihoreau & Rivault 2009). This is consistent with Wilson & Ho¨lldobler’s (2005) view that this form of nepotistic kin selection is a disruptive force in obligatorily eusocial systems, but a potentially binding force in cooperative breeders. As long as a species breeds cooperatively, it may pay (but not necessarily always; cf. Griffin & West 2003) to be able to estimate the degree of relatedness of cobreeders because focal individuals are likely to have retained alternative, dispersal-based reproductive options. However, obligatorily eusocial systems are mostly characterized by unconditional rather than conditional altruism and by the rejection of individuals that deviate from a colony Gestalt, rather than acceptance or preferential treatment of individuals according to their degree of similarity with such a recognition template (Guerrieri et al. 2009).

6. PERSPECTIVES Looking back, the history of explaining the evolution of eusociality has been confusing. Although the simplest (r ¼ 0.75) predictions of the haplodiploidy hypothesis were quickly corrected (Trivers & Hare 1976), the search for relatednesses higher than 0.5 continued focusing, among others, on mechanisms associated with partial bivoltinism, partial unmatedness, inbreeding and chromosomal idiosyncrasies (Bourke & Franks 1995; Crozier & Pamilo 1996; Shellman-Reeve 1997; Crozier 2008). At the same time, the bees seemed to require a separate explanation (Michener 1958), multiple queen-mating was

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Lifetime monogamy and eusociality considered a problem because early origins and later evolutionary elaborations of mating systems were insufficiently distinguished (Boomsma & Ratnieks 1996), and a number of new instances of phylogenetically shallow and facultative eusocial helping were discovered in both diploid and haplodiploid taxa (Crespi 1996) and given similar status to the four classic eusocial lineages. Ambiguity was further enhanced by controversies over the definitions of eusociality (e.g. Gadagkar 1994; Crespi & Yanega 1995; Sherman et al. 1995; Keller & Perrin 1995; Costa & Fitzgerald 1996) and finally led to challenges of the merits of kin-selection theory (Wilson 2005, 2008; Wilson & Ho¨lldobler 2005; Fletcher et al. 2006; Wilson & Wilson 2007) that had insufficient connection with the insights that had already gained unambiguous mathematical support in the early days of sociobiology (Foster et al. 2006a,b; Helantera¨ & Bargum 2007; West et al. 2007, 2008; Crozier 2008; Gardner & Grafen 2009). During the almost five decades that discussions about the origin of eusociality have been ongoing, William D. Hamilton, Richard D. Alexander, Eric L. Charnov, Richard Dawkins, David Queller, Mary Jane West Eberhard, Edward O. Wilson and many others have realized that monogamy provided very special conditions for the evolution of reproductive altruism, but the crucial significance of lifetime monogamous parental commitment and complete absence of re-mating promiscuity failed to surface as possibly the most fundamental principle of all. The theory has therefore remained unnecessarily complex and has precluded seeing the wood for the trees. The present review aims to rectify this situation and outlines the contours of a research agenda that: (i) Removes some of the obstacles that appear to prevent some ‘advocates’ of group selection and kin selection language to understand each other’s agenda. (ii) Emphasizes the need to recognize different domains of social evolution that are separated by singularities such as the monogamy window. In the paragraphs below, I will outline some further perspectives of this approach, which will hopefully stimulate more unified directions in future research. As Queller (2000) noticed, a single cell or singly mated queen bottleneck in each generation prevents the expression of most selfish genetic traits that could burden a new organism or colony. This notion is consistent with, and becomes more precise when applying the ‘triploid’ or ‘tetraploid’ zygote analogies (figure 2), as this demonstrates that transitions towards eusociality require kin selection (precisely r ¼ 0.5 to siblings on average) to be achieved, but are ultimately driven by benefits obtained from group(colony)-level selection (table 1). This illustrates that the largely semantic debate on the relative merits of kin selection and group selection for the evolution of eusociality had best be abandoned. Both approaches were shown to be mathematically equivalent by Hamilton (1975), when he reformulated his ‘rule’ in the more general notation allowed by the Price equation (see also Wade 1980; Queller 1992; West et al. 2007, 2008; Wilson & Wilson 2007). Group-selection approaches are a shortcut for levels-of-selection models on processes of genetic change (Reeve & Keller 1998; Phil. Trans. R. Soc. B (2009)

J. J. Boomsma

3201

Linksvayer & Wade 2005), whereas kin-selection models address the adaptive evolutionary endpoints of such processes. This complementarity implies that levels-of-selection models by themselves cannot decide whether superorganismal properties of colonies reflect colony-level adaptation or inclusive fitness maximization of the individuals within such colonies (Gardner & Grafen 2009). Rather, it appears that complete resolution of internal conflict is required before colony processes can become colony adaptations (Ratnieks & Reeve 1992; Gardner & Grafen 2009). In this perspective, non-conflict behaviours and communication processes that relate to resource acquisition can easily become supercolonial, whereas it is almost impossible to achieve this for traits involved in reproductive resource allocation (Boomsma & Franks 2006). As long as a social system is defined as cooperative breeding, group selection is likely to be of variable significance as it will be over-ruled by individual selection for anything between 1 and 80 per cent of the subordinate individuals who end-up reproducing in each generation (Brockmann 1997). After the transition towards obligate eusociality has been made, not a single helper will realize full reproductive potential, so that colony-level selection has become the leading determinant of inclusive fitness. The instalment of eusociality thus implies that a new level of organization has become decisive for both parental and offspring fitness, but also that new conflicts of interest come to challenge the arrangement as the interests of the generations are only partly aligned. For example, parent– offspring conflict over who reproduces is replaced by parent– offspring conflict over who to invest in (Alexander 1974). As illustrated in figure 2, the reproductive conflict load of newly emerged obligate eusociality is relatively severe in the haplodiploid Hymenoptera, because parents contribute unequally to the triploid zygote analogue setting the stage for the classic worker – queen conflicts over sex allocation and worker reproduction (Trivers & Hare 1976) and the interaction between these conflicts (Foster & Ratnieks 2001; Reuter & Keller 2001). Termite societies lack this fundamental parental asymmetry, so that only conflict over caste fate can be expressed, a conflict that they share with the eusocial Hymenoptera (Bourke & Ratnieks 1999). What characterizes any current supercolonial endpoints of evolutionary developments that started with passing through a monogamy window is that virtually all potential conflicts have been resolved or carefully regulated to ensure minimal damage to society (Bourke 1999; Ratnieks et al. 2006). However, these conflict regulations can normally be explained as having evolved to maximize inclusive fitness of individuals and not as a colony-level adaptation (Gardner & Grafen 2009). The most fruitful way to progress in understanding the evolution of eusociality would seem to concentrate research efforts on a further conceptual unification with already developed theory on the origin of multicellularity (Korb & Heinze 2004). Models have shown that the shape of a crucial trade-off between survival and fecundity changes when cell number increases, so that the cost of unicellular reproduction gradually increases with the benefits of joint

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3202

J. J. Boomsma

Review. Lifetime monogamy and eusociality

‘soma’

modular reproduction ‘germ line’

unitary reproduction Figure 3. The ‘soma’ and ‘germ line’ analogues of a eusocial colony of ants, bees or wasps. Symbols are the same as in figure 1. The small ellipse in the centre is the founding pair, which for simplicity has been depicted as a singly mated queen. The diagram would be similar for a multiply mated queen, in which case her multiple unrelated mates and their offspring could be depicted as having different shades of dark green. The box at the bottom represents the queen-produced gynes and males, i.e. the fraction of the colony’s reproduction that is derived from the analogue of the unitary ‘germ line’ (assuming 50/50 Fisherian sex allocation in this example, but female biased sex ratios would not make a principal difference for the argument). The inner circle at the top represents the collective ‘soma’ of all the colony’s workers and the larger circle the fraction of modular (‘germ line’ independent) reproduction that the ‘soma’ pursues in the form of worker-produced haploid males. Active coercion via policing (Ratnieks et al. 2006) and self restraint due to decreasing pay-offs of ‘somatic’ reproduction when colony size increases (Bourke 1999; Wenseleers et al. 2004) tend to remove most of the modular outer circle in the more advanced societies. Superorganismic societies such as colonies of Atta leafcutter ants or honeybees have lost the outer circle of modular worker reproduction completely (except when queenless in the case of honeybees), but most eusocial Hymenoptera have retained some of this modular reproduction mode over which the queen ‘germ line’ and the worker ‘soma’ are in conflict as long as the queen is alive. Termite colonies have a modular reproduction ellipse when replacement reproductives become established in the existing colonies, although they are in reality an extension of the existing germ line when they mate with full siblings.

reproduction (Michod 2005, 2006). This process, which is reminiscent of the synergistic benefits of increasing colony size in insect societies (Bourke 1999; see also figure 1) results in a significant increase in the heritability of fitness at the collective level (Michod & Roze 1997) and is connected to the emergence of a totipotent germ line and a majority of cells that have been terminally determined to serve somatic functions. The emergence of individual germ lines has been hypothesized to be either parentally enforced or voluntarily altruistic (Queller 2000). Also, this is similar to the concepts of parental manipulation and Phil. Trans. R. Soc. B (2009)

offspring choice that dominated discussions on the origin of eusociality, until both were shown to be consistent with the same force of kin-selection (Craig 1979; Bourke & Franks 1995, but see Linksvayer & Wade 2005 for differences when taking a level of selection approach). Comparisons of this kind show that extant multicellular organisms differ 13 orders of magnitude in cell number, but only two orders of magnitude in the number of cell types, whereas insect societies vary five orders of magnitude in the number of individuals and less than one order of magnitude in the number of castes (Strassmann & Queller 2007).

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Lifetime monogamy and eusociality Both relationships show similar positive correlations but there are roughly an order of magnitude fewer castes than cell types throughout the ranges of cell numbers and colony nestmates (Strassmann & Queller 2007). Comparative explorations of this kind ought to include explicit considerations on the analogues of the multicellular germ line and soma that characterize eusociality. Bourke & Franks (1995) established that the growth of insect societies is modular in the sense that a colony can remain viable even after half of the workers are removed. However, it is also clear that a colony of Atta leafcutter ants with five million sterile workers has all but completed the unitary superorganism analogy of having a fully separated ‘germ line’ for reproductive purposes, except perhaps for the final step of raising new cohorts of dispersing queens from genetically predisposed eggs of superior quality (Dijkstra & Boomsma 2006). However, as illustrated in figure 3, there are many stages in between the early monogamy window origin of obligate eusociality and this advanced superorganism state where the ‘germ line’ is only partly sequestered and where a significant part of the colony’s total reproductive effort is based on an equivalent of modular ‘somatic’ reproduction. As long as workers still have functional ovaries, hymenopteran colonies partly reproduce like plants rather than animals, in particular when they become queenless so that male production by workers has become the only option for future inclusive fitness. It is this modular form of reproduction that is institutionalized in ants that evolved secondary polygyny, as re-adopted newly inseminated daughter-queens facilitate unconstrained ‘somatic’ reproduction, relative to unmated workers that can only produce males. When such adoption cycles are repeated within the same long-lived nest, colonies may lose their founding ‘germ line’ entirely and become modular chimaeras that mostly reproduce by vegetative budding (Keller 1993; Bourke & Franks 1995; Crozier & Pamilo 1996). Termite societies can also be interpreted in this manner, although some of the details differs, as replacement reproductives in termites are merely extensions of the colony’s germ line when their partners are full siblings (e.g. Thorne 1985). As noted above, the monogamy window separates eusociality, which evolves only when Hamilton’s rule is fulfilled throughout the lives of entire helper cohorts, from cooperative breeding (including facultative eusociality), which is maintained when Hamilton’s rule applies during some period of life. During the transition towards obligate eusociality, within-colony selection proceeds from being a major force of gradually waning significance (when cooperative breeders converge on monogamous mating systems; cf. figure 1) to being a subordinate force that has been surpassed by colony-level selection but keeps threatening colony productivity (table 1). Re-mating promiscuity is compatible with cooperative breeding and solitary breeding, but not with becoming eusocial (Boomsma 2007) and most likely not with remaining eusocial either, unless secondary partner shifts become documented in some higher termites. This is analogous to promiscuous exchange of genetic Phil. Trans. R. Soc. B (2009)

J. J. Boomsma

3203

elements being compatible with prokaryote reproduction, but not with eukaryote reproduction based on life-time commitment of gametes to a single zygote (figure 2 and table 1). Cooperative breeding is not separated from solitary breeding by a transition singularity comparable to the monogamy window, consistent with cooperative breeding often being as optional as facultative eusociality. The major transition between facultative and obligate eusociality rather than between cooperative breeding and facultative eusociality has been noted by many but has, paradoxically, resulted in arguments in favour of lumping social categories (e.g. Gadagkar 1994; Sherman et al. 1995) to stress that the same Hamiltonian principles apply throughout. The overview provided here maintains this commonality of principle, but highlights the necessity of recognizing obligate eusociality as a separate domain of social evolution (table 1). This logic implies that it was not the origins of social groups per se that triggered major transitions in evolution (Maynard Smith & Szathma´ry 1995), but rather the multiple passings through monogamy windows. The latter allowed entries into the novel domain of permanent eusociality, whereas the former were less fundamental extensions of solitary life. The evolutionary ecology of cooperative breeding and facultative eusociality is often richer and more complicated than the study of obligate eusociality, because all three parameters in Hamilton’s rule are continuous variables, whereas relatedness tends to be a class variable (e.g. in haplodiploidy 0.75 to full sisters, 0.25 to half sisters, etc.) in obligatorily eusocial systems. In addition, sexual behaviour or the consequences of matedness always interact with other social behaviours in cooperative breeders, whereas these fundamental activities are completely separated in time (and often also space) in eusocial breeders (Boomsma 2007; see also table 1). This implies that biological idiosyncrasy and ecological contingency, although important, are less overwhelming across the obligatorily eusocial clades than across the cooperatively breeding clades, so that an overall synthetic theory for the evolution and maintenance of stable cooperation and altruism may be reached earlier for the eusociality domain than for cooperative breeding. I thank Tim Clutton-Brock, Francis Ratnieks and Stuart West for the opportunity to present a summary of this review at the Royal Society discussion meeting on the Evolution of Society in January 2009, the Danish National Research Foundation for funding, and Joao Alpedrinha, Trine Bilde, Ross Crozier, Raghavendra Gadagkar, Tamara Hartke, Bert Ho¨lldobler, Luke Holman, Daniel Kronauer, Tim Linksvayer, Steve Stearns and Stuart West for comments on an earlier version of the manuscript.

REFERENCES Abe, T. 1991 Ecological factors associated with the evolution of worker and soldier castes in termites. Ann. Entomol. 9, 101–107. Abouheif, E. & Wray, G. A. 2002 Evolution of the gene network underlying wing polyphenism in ants. Science 297, 249–252. (doi:10.1126/science.1071468) Alexander, R. D. 1974 The evolution of social behavior. Annu. Rev. Ecol. Syst. 5, 325 –383. (doi:10.1146/ annurev.es.05.110174.001545)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3204

J. J. Boomsma

Review. Lifetime monogamy and eusociality

Alexander, R. D., Noonan, K. M. & Crespi, B. J. 1991 In The biology of the naked mole rat (eds P. W. Sherman, J. U. M. Jarvis & R. D. Alexander), pp. 3 –44. Princeton, NJ: Princeton University Press. Atkinson, L. & Adams, E. S. 1997 The origins and relatedness of multiple reproductives in colonies of the termite Nasutitermes corniger. Proc. R. Soc. Lond. B 264, 1131–1136. (doi:10.1098/rspb.1997.0156) Atkinson, L., Teschendorf, G. & Adams, E. S. 2008 Lack of evidence for nepotism by workers tending queens of the polygynous termite, Nasutitermes corniger. Behav. Ecol. Sociobiol. 62, 805–812. (doi:10.1007/S00265-007-0506-z) Baer, B., Armitage, S. A. O. & Boomsma, J. J. 2006 Sperm storage induces an immunity cost in ants. Nature 441, 872 –875. (doi:10.1038/nature04698) Boomsma, J. J. 2007 Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17, R673 –R683. (doi:10.1016/j.cub.2007.06.033) Boomsma, J. J. & Grafen, A. 1991 Colony-level sex ratio selection in the eusocial Hymenoptera. J. Evol. Biol. 4, 383 –407. (doi:10.1046/j.1420-9101.1991.4030383.x) Boomsma, J. J. & Ratnieks, F. L. W. 1996 Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. Lond. B 351, 947 –975. (doi:10.1098/rstb.1996.0087) Boomsma, J. J., Nielsen, J., Sundstro¨m, L., Oldham, N. J., Tentschert, J., Petersen, H. C. & Morgan, E. D. 2003 Informational constraints on optimal sex allocation in ants. Proc. Natl Acad. Sci. USA 100, 8799– 8804. (doi:10.1073/pnas.1430283100) Boomsma, J. J., Baer, B. & Heinze, J. 2005 The evolution of male traits in social insects. Ann. Rev. Entomol. 50, 395–420. (doi:10.1146/annurev.ento.50.071803.130416) Boomsma, J. J., Kronauer, D. J. C. & Pedersen, J. S. 2009 The evolution of social insect mating systems. In Organization of insect societies—from genomes to sociocomplexity (eds J. Gadau & J. Fewell), pp. 3– 25. Cambridge, MA: Harvard University Press. Bourke, A. F. G. 1999 Colony size, social complexity and reproductive conflict in social insects. J. Evol. Biol. 12, 245 –257. (doi:10.1046/j.1420-9101.1999.00028.x) Bourke, A. F. G. 2007 Kin selection and the evolutionary theory of aging. Annu. Rev. Ecol. Evol. Syst. 38, 103–128. (doi:10.1146/annurev.ecolsys.38.091206.095528) Bourke, A. F. G. & Franks, N. R. 1995 Social evolution in ants. Princeton, NJ: Princeton University Press. Bourke, A. F. G. & Ratnieks, F. L. W. 1999 Kin conflict over caste determination in social Hymenoptera. Behav. Ecol. Sociobiol. 46, 287 –297. (doi:10.1007/ s002650050622) Brady, S., Schultz, T., Fisher, B. & Ward, P. 2006 Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc. Natl Acad. Sci. USA 103, 18172–18177. (doi:10.1073/pnas.0605858103) Brandl, R., Hacker, M., Bagine, R. K. N. & Kaib, M. 2001 Geographic variation of polygyny in the termite Macrotermes michaelseni (Sjostedt). Insectes Soc. 48, 134 –137. (doi:10.1007/PL00001755) Brockmann, H. J. 1997 Cooperative breeding in wasps and vertebrates: the role of ecological constrains. In The evolution of social behavior in insects and arachnids (eds J. C. Choe & B. J. Crespi), pp. 347 –371. Cambridge, UK: Cambridge University Press. Burt, A. & Trivers, R. 2006 Genes in conflict. Cambridge, MA: The Belknap Press of Harvard University Press. Buschinger, A. 1990 Sympatric speciation and radiative evolution of socially parasitic ants—heretic hypotheses and their factual background. Zeitschr. Zool. Syst. Evolutionsforsch. 28, 241 –260. Buss, L. W. 1987 The evolution of individuality. Princeton, NJ: Princeton University Press. Phil. Trans. R. Soc. B (2009)

Cavalier-Smith, T. 2006 Cell evolution and Earth history: stasis and revolution. Phil. Trans. R. Soc. B 361, 969 –1006. (doi:10.1098/rstb.2006.1842) Chapman, T. W., Kranz, B. D., Bejah, K. L., Morris, D. C., Schwarz, M. P. & Crespi, B. J. 2002 The evolution of soldier reproduction in social thrips. Behav. Ecol. 13, 519 –525. (doi:10.1093/beheco/13.4.519) Charnov, E. L. 1978 Evolution of eusocial behavior: offspring choice or parental parasitism? J. Theor. Biol. 75, 451 –465. (doi:10.1016/0022-5193(78)90356-9) Costa, J. T. & Fitzgerald, T. D. 1996 Developments in social terminology: semantic battles in a conceptual war. Trends Ecol. Evol. 11, 285 –289. (doi:10.1016/0169-5347(96) 10035-5) Craig, R. 1979 Parental manipulation, kin selection, and the evolution of altruism. Evolution 33, 319 –334. (doi:10. 2307/2407622) Crespi, B. J. 1996 Comparative analysis of the origins and losses of eusociality: causal mosaics and historical uniqueness. In Phylogenetics and the comparative method in animal behavior (ed. E. P. Martins), pp. 253–287. New York, NY: Oxford University Press. Crespi, B. J. 2007 Comparative evolutionary ecology of social and sexual systems: water-breathing insects come of age. In Evolutionary ecology of social and sexual systems: crustaceans as model organisms (eds J. E. Duffy & M. Thiel), pp. 442–460. Oxford, UK: Oxford University Press. Crespi, B. J. & Yanega, D. 1995 The definition of eusociality. Behav. Ecol. 6, 109 –115. (doi:10.1093/beheco/6.1.109) Crozier, R. H. 1987 Genetic aspects of kin recognition: concepts, models, and synthesis. In Kin recognition in animals (eds D. J. C. Fletcher & C. D. Michener), pp. 55–73. New York, NY: John Wiley and Sons. Crozier, R. H. 2008 Advanced eusociality, kin selection and male haploidy. Aust. J. Entomol. 47, 2– 8. (doi:10.1111/ j.1440-6055.2007.00621.x) Crozier, R. H. & Pamilo, P. 1996 Evolution of social insect colonies. Oxford, UK: Oxford University Press. Danforth, B. N. 2002 Evolution of sociality in a primitively eusocial lineage of bees. Proc. Natl Acad. Sci. USA 99, 286 –290. (doi:10.1073/pnas.012387999) Darlington, J. 1988 Multiple reproductives in nests of Macrotermes herus (Isoptera: Termitidae). Sociobiology 14, 347–351. Darwin, C. 1859 On the origin of species by means of natural selection, 1st edn. London, UK: John Murray. (Published by Penguin Books in 1968.) Dawkins, R. 1982 The extended phenotype. Oxford, UK: Oxford University Press. Den Boer, S. P. A., Boomsma, J. J. & Baer, B. C. 2008 Seminal fluid ensures high sperm viability in the leafcutter ant Atta colombica. Behav. Ecol. Sociobiol. 62, 1843 –1849. (doi:10.1007/s00265-008-0613-5) Dijkstra, M. B. & Boomsma, J. J. 2006 Are workers of Atta leafcutter ants capable of reproduction? Insectes Soc. 53, 136 –140. (doi:10.1007/s00040-005-0848-3) Duffy, J. E. 2003 The ecology and evolution of eusociality in sponge-dwelling shrimp. In Genes, behavior and evolution in social insects (eds T. Kikuchi, N. Azuma & S. Higashi), pp. 217–252. Sapporo, Japan: Hokkaido University Press. Fletcher, J. A., Zwick, M., Doebeli, M. & Wilson, D. S. 2006 What’s wrong with inclusive fitness? Trends Ecol. Evol. 21, 597 –598. (doi:10.1016/j.tree.2006.08.008) Foster, K. R. & Ratnieks, F. L. W. 2001 The effect of sex allocation biasing on the evolution of worker policing in hymenopteran societies. Am. Nat. 158, 615–623. (doi:10.1086/323588) Foster, K. R., Wenseleers, T. & Ratnieks, F. L. W. 2006a Kin selection is the key to altruism. Trends Ecol. Evol. 21, 57–60. (doi:10.1016/j.tree.2005.11.020)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Lifetime monogamy and eusociality Foster, K. R., Wenseleers, T., Ratnieks, F. L. W. & Queller, D. C. 2006b There is nothing wrong with inclusive fitness. Trends Ecol. Evol. 21, 599 –600. (doi:10.1016/ j.tree.2006.08.010) Gadagkar, R. 1994 Why the definition of eusociality is not helpful to understand its evolution and what should we do about it. Oikos 70, 485–488. (doi:10.2307/3545789) Gadagkar, R. 1996 The evolution of eusociality, including a review of the social status of Ropalidia marginata. In Natural history and evolution of paper-wasps (eds S. Turillazzi & M. J. West Eberhard), pp. 248– 271. Oxford, UK: Oxford University Press. Gardner, A. & Grafen, A. 2009 Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659– 667. Gardner, A. & West, S. A. 2007 Social evolution: The decline and fall of genetic kin recognition. Curr. Biol. 17, R810– R812. (doi:10.1016/j.cub.2007.07.030) Gobin, B., Ito, F., Peeters, C. & Billen, J. 2006 Queen–worker differences in spermatheca reservoir of phylogenetically basal ants. Cell Tissue Res. 326, 169–178. (doi:10.1007/ s00441-006-0232-2) Godfray, H. C. J. & Grafen, A. 1988 Unmatedness and the evolution of eusociality. Am. Nat. 131, 303–305. (doi:10.1086/284791) Gotoh, A., Billen, J., Hashim, R. & Ito, F. 2008 Comparison of spermatheca morphology between reproductive and non-reproductive females in social wasps. Arthropod Struct. Dev. 37, 199–209. (doi:10.1016/j.asd.2007.11.001) Greenberg, L. 1979 Genetic component of bee odor in kin recognition. Science 206, 1095– 1097. (doi:10.1126/ science.206.4422.1095) Griffin, A. S. & West, S. A. 2003 Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302, 634– 636. (doi:10.1126/science.1089402) Grimaldi, D. & Engel, M. S. 2005 Evolution of the insects. Cambridge, UK: Cambridge University Press. Grosberg, R. K. & Strathmann, R. R. 2007 The evolution of multicellularity: a minor major transition? Annu. Rev. Ecol. Evol. Syst. 38, 621 –654. (doi:10.1146/annurev. ecolsys.36.102403.114735) Guerrieri, F. J., Nehring, V., Jørgensen, C. G., Nielsen, J., Galizia, C. G. & d’Ettorre, P. 2009 Ants recognize foes and not friends. Proc. R. Soc. B. 276, 2461–2468. (doi:10.1098/rspb.2008.1860) Hacker, M., Kaib, M., Bagine, R. K. N., Epplen, J. T. & Brandl, R. 2005 Unrelated queens coexist in colonies of the termite Macrotermes michaelseni. Mol. Ecol. 14, 1527– 1532. (doi:10.1111/j.1365-294X.2005.02507.x) Hamilton, W. D. 1964 The genetical evolution of social behaviour, I & II. J. Theor. Biol. 7, 1–52. (doi:10.1016/ 0022-5193(64)90038-4) Hamilton, W. D. 1972 Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3, 193 –232. (doi:10.1146/annurev.es.03.110172.001205) Hamilton, W. D. 1975 Innate social aptitudes of man: an approach from evolutionary genetics. In Biosocial anthropology (ed. R. Fox), pp. 133–155. London, UK: Malaby Press. Hamilton, W. D. 1978 Evolution and diversity under bark. In Diversity of insect faunas, vol. 9 (eds L. A. Mound & N. Waloff), pp. 154– 175. Oxford, UK: Blackwell. Symposia of the Royal Entomological Society of London. Hart, A. G. & Ratnieks, F. L. W. 2005 Crossing the taxonomic divide: conflict and its resolution in societies of reproductively totipotent individuals. J. Evol. Biol. 18, 383 –395. (doi:10.1111/j.1420-9101.2004.00832.x) Hastings, M. D., Queller, D. C., Eischen, F. & Strassmann, J. E. 1998 Kin selection, relatedness, and worker control of reproduction in a large-colony epiponine wasp, Phil. Trans. R. Soc. B (2009)

J. J. Boomsma

3205

Brachygastra mellifica. Behav. Ecol. 9, 573– 581. (doi:10. 1093/beheco/9.6.573) Helantera¨, H. & Bargum, K. 2007 Pedigree relatedness, not greenbeard genes, explains eusociality. Oikos 116, 217–220. (doi:10.1111/j.0030-1299.2007.15411.x) Higashi, M., Yamamura, N., Abe, T. & Burns, T. P. 1991 Why don’t all termite species have a sterile worker caste? Proc. R. Soc. Lond. B 246, 25–30. (doi:10.1098/ rspb.1991.0120) Hines, H. M., Hunt, J. H., O’Connor, T. K., Gillespie, J. J. & Cameron, S. A. 2007 Multigene phylogeny reveals eusociality evolved twice in vespid wasps. Proc. Natl Acad. Sci. USA 104, 3295–3299. (doi:10.1073/pnas.0610140104) Ho¨lldobler, B. & Bartz, S. H. 1985 Sociobiology of reproduction in ants. In Experimental behavioral ecology and sociobiology (eds B. Ho¨lldobler & M. Lindauer), pp. 237–257. Stuttgart, Germany; New York, NY: Gustav Fischer. Ho¨lldobler, B. & Wilson, E. O. 1990 The ants. Cambridge, MA: Harvard University Press. Ho¨lldobler, B. & Wilson, E. O. 2008 The super-organism. New York, NY: Norton. Hughes, W. O. H. & Boomsma, J. J. 2008 Genetic royal cheats in leaf-cutting ant societies. Proc. Natl Acad. Sci. USA 105, 5150– 5153. (doi:10.1073/pnas.0710262105) Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. 2008 Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216. (doi:10.1126/science.1156108) Hunt, J. H. 1994 Nourishment and evolution in wasps sensu lato. In Nourishment and evolution in insect societies (eds J. H. Hunt & C. A. Nalepa), pp. 211 –244. Boulder, CO: Westview Press. Hunt, J. H. 2007 The evolution of social wasps. New York, NY: Oxford University Press. Inward, D., Beccaloni, G. & Eggleton, P. 2007 Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol. Lett. 3, 331 –335. (doi:10.1098/rsbl.2007.0102) Kawakita, A., Ascher, J. S., Sota, T., Kato, M. & Roubik, D. W. 2008 Phylogenetic analysis of the corbiculate bee tribes based on 12 nuclear protein-coding genes (Hymenoptera: Apoidea: Apidae). Apidologie 39, 163–175. (doi:10.1051/apido:2007046) Keller, L. (ed.) 1993 Queen number and sociality in insects. Oxford, UK: Oxford University Press. Keller, L. 1997 Indiscriminate altruism: unduly nice parents and siblings. Trends Ecol. Evol. 12, 99–103. (doi:10.1016/ S0169-5347(96)10065-3) Keller, L. & Genoud, M. 1997 Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389, 958–960. (doi:10.1038/40130) Keller, L. & Perrin, N. 1995 Quantifying the level of eusociality. Proc. R. Soc. Lond. B 260, 311 –315. (doi:10.1098/ rspb.1995.0097) Korb, J. 2008 The ecology of social evolution in termites. In Ecology of social evolution (eds J. Korb & J. Heinze), pp. 151–174. Berlin, Germany: Springer. Korb, J. & Heinze, J. 2004 Multilevel selection and social evolution of insect societies. Naturwissenschaften 91, 291–304. Kronauer, D. J. C. & Boomsma, J. J. 2007 Do army ant queens re-mate later in life? Insectes Soc. 54, 20–28. (doi:10.1007/s00040-007-0904-2) Lihoreau, M. & Rivault, C. 2009 Kin recognition via cuticular hydrocarbons shapes cockroach social life. Behav. Ecol. 20, 46–53. (doi:10.1093/beheco/arn113) Linksvayer, T. A. & Wade, M. J. 2005 The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony. Q. Rev. Biol. 80, 317 –336. (doi:10.1086/432266)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3206

J. J. Boomsma

Review. Lifetime monogamy and eusociality

Lin, N. & Michener, C. D. 1972 Evolution of sociality in insects. Q. Rev. Biol. 47, 131– 159. (doi:10.1086/407216) Lo, N., Hayashi, Y. & Kitade, O. 2009 Should environmental caste determination be assumed for termites? Am. Nat. 173, 848 –853. Maynard Smith, J. & Szathma´ry, E. 1995 The major transitions in evolution. Oxford, UK: Freeman. Michener, C. D. 1958 The evolution of social behavior in bees. Proc. Tenth Int. Cong. Entomol. 2, 441– 447. Michod, R. E. 2005 On the transfer of fitness from the cell to the multicellular organism. Biol. Philos. 20, 967 –987. Michod, R. E. 2006 The group covariance effect and fitness trade-offs during evolutionary transitions in individuality. Proc. Natl Acad. Sci. USA 103, 9113–9117. (doi:10. 1073/pnas.0601080103) Michod, R. E. 2007 Evolution of individuality during the transition from unicellular to multicellular life. Proc. Natl Acad. Sci. USA 104, 8613 –8618. (doi:10.1073/ pnas.0701489104) Michod, R. E. & Roze, D. 1997 Transitions in individuality. Proc. R. Soc. Lond. B 264, 853– 857. (doi:10.1098/rspb. 1997.0119) Moreau, C., Bell, C., Vila, R., Archibald, S. & Pierce, N. 2006 Phylogeny of the ants: diversification in the age of angiosperms. Science 312, 101–104. (doi:10.1126/ science.1124891) Moritz, R. F. A. & Southwick, E. E. 1992 Bees as superorganisms: an evolutionary reality. Berlin, Germany: Springer. Mueller, U. G. 1991 Haplodiploidy and the evolution of facultative sex ratios in a primitively eusocial bee. Science 254, 442 –444. (doi:10.1126/science.254.5030.442) Pamilo, P. 1991 Evolution of the sterile caste. J. Theor. Biol. 149, 75–95. (doi:10.1016/S0022-5193(05)80073-6) Patel, A., Fondrk, M. K., Kaftanoglu, O., Emore, C., Hunt, G., Frederick, K. & Amdam, G. V. 2007 The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS ONE 2, e509. (doi:10.1371/journal. pone.0000509) Peeters, C. 1997 Morphologically ‘primitive’ ants: comparative review of social characters, and the importance of queen –worker dimorphism. In The evolution of social behavior in insects and arachnids (eds J. C. Choe & B. J. Crespi), pp. 372–391. Cambridge, UK: Cambridge University Press. Plateaux-Que´nu, C. 2008 Subsociality in halictine bees. Insectes Soc. 55, 335– 346. (doi:10.1007/s00040-0081028-z) Queller, D. C. 1989 The evolution of eusociality: reproductive head starts of workers. Proc. Natl Acad. Sci. USA 86, 3224–3226. (doi:10.1073/pnas.86.9.3224) Queller, D. C. 1992 Quantitative genetics, inclusive fitness, and group selection. Am. Nat. 139, 540 –558. (doi:10. 1086/285343) Queller, D. C. 1996 The origin and maintenance of eusociality: the advantage of extended parental care. In Natural history and evolution of paper-wasps (eds S. Turillazzi & M. J. West Eberhard), pp. 218 –234. Oxford, UK: Oxford University Press. Queller, D. C. 2000 Relatedness and the fraternal major transitions. Proc. R. Soc. Lond. B 355, 1647– 1655. (doi:10.1098/rstb.2000.0727) Queller, D. C., Strassmann, J. E., Solis, C. R., Hughes, C. R. & DeLoach, D. M. 1993 A selfish strategy of social insect workers that promotes social cohesion. Nature 365, 639 –641. (doi:10.1038/365639a0) Rabeling, C., Brown, J. M. & Verhaagh, M. 2008 Newly discovered sister lineage sheds light on early ant evolution. Proc. Natl Acad. Sci. USA 105, 14913–14917. (doi:10.1073/pnas.0806187105) Phil. Trans. R. Soc. B (2009)

Ratnieks, F. L. W. & Reeve, H. K. 1992 Conflict in singlequeen hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species. J. Theor. Biol. 158, 33– 65. (doi:10.1016/S00225193(05)80647-2) Ratnieks, F. L. W., Foster, K. R. & Wenseleers, T. 2006 Conflict resolution in insect societies. Ann. Rev. Entomol. 51, 581–608. (doi:10.1146/annurev.ento.51.110104.151003) Reeve, H. K. & Keller, L. 1998 Levels of selection: burying the units-of-selection debate and unearthing the crucial new issues. In Levels of selection in evolution (ed. L. Keller), pp. 3 –14. Princeton, NJ: Princeton University Press. Reeve, H. K. & Keller, L. 2001 Tests of reproductive-skew models in social insects. Annu. Rev. Entomol. 46, 347 –385. (doi:10.1146/annurev.ento.46.1.347) Reeve, H. K., Peters, J. M., Nonacs, P. & Starks, P. T. 1998 Dispersal of first ‘workers’ in social wasps: causes and implications of an alternative reproductive strategy. Proc. Natl Acad. Sci. USA 95, 13737–13742. (doi:10.1073/ pnas.95.23.13737) Reeve, H. K. & Ho¨lldobler, B. 2007 The emergence of a superorganism through intergroup competition. Proc. Natl Acad. Sci. USA 104, 9736–9740. (doi:10.1073/ pnas.0703466104) Reuter, M. & Keller, L. 2001 Sex ratio conflict and worker production in eusocial Hymenoptera. Am. Nat. 158, 166 –177. (doi:10.1086/321311) Roisin, Y. 1987 Polygyny in Nasutitermes species: field data and theoretical approaches. Experientia 54(Suppl.), 379 –404. Roisin, Y. 1999 Philopatric reproduction, a prime mover in the evolution of termite sociality? Insectes Soc. 46, 297 –305. (doi:10.1007/s000400050149) Roisin, Y. & Pasteels, J. M. 1987 Caste developmental potentialities in the termite Nasutitermes novarumhebridarum. Entomol. Exp. Appl. 44, 277– 287. Seeley, T. D. 1995 The wisdom of the hive. Cambridge, MA: Harvard University Press. Seger, J. 1983 Partial bivoltinism may cause alternating sex ratio biases that favour eusociality. Nature 301, 59–62. (doi:10.1038/301059a0) Shellman-Reeve, J. S. 1997 The spectrum of eusociality in termites. Social behavior in insects and arachnids (eds J. C. Choe & B. J. Crespi), pp. 52–93. Cambridge, UK: Cambridge University Press. Sherman, P. W. & Jarvis, J. U. W. 2002 Extraordinary life spans of naked mole-rats (Heterocephalus glaber). J. Zool. Lond. 258, 307 –311. (doi:10.1017/S0952836902001437) Sherman, P. W., Lacey, E. A., Reeve, H. K. & Keller, L. 1995 The eusociality continuum. Behav. Ecol. 6, 102 –108. (doi:10.1093/beheco/6.1.102) Soro, A., Ayasse, M., Zobel, M. U. & Paxton, R. J. 2009 Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee Lasioglossum malachurum. Insectes Soc. 56, 55–63. (doi:10.1007/ s00040-008-1037-y) Stern, D. L. & Foster, W. A. 1997 The evolution of sociality in aphids: a clone’s-eye view. In Social behavior in insects and arachnids (eds J. C. Choe & B. J. Crespi), pp. 150 –165. Cambridge, UK: Cambridge University Press. Strassmann, J. E. 1996 Selective altruism towards closer over more distant relatives in colonies of the primitively eusocial wasp, Polistes. In Natural history and evolution of paper-wasps (eds S. Turillazzi & M. J. West Eberhard), pp. 190–201. Oxford, UK: Oxford University Press. Strassmann, J. E. 2001 The rarity of multiple mating by females in the social Hymenoptera. Insectes Soc. 48, 1 –13. (doi:10.1007/PL00001737)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Lifetime monogamy and eusociality Strassmann, J. E. & Queller, D. C. 2007 Insect societies as divided organisms: the complexities of purpose and cross-purpose. Proc. Natl Acad. Sci. USA 104, 8619– 8626. (doi:10.1073/pnas.0701285104) Strassmann, J. E., Goodnight, K. F., Klingler, C. J. & Queller, D. C. 1998 The genetic structure of swarms and the timing of their production in the queen cycles of neotropical wasps. Mol. Ecol. 7, 709– 718. (doi:10. 1046/j.1365-294x.1998.00381.x) Strassmann, J. E., Sullender, B. W. & Queller, D. C. 2002 Caste totipotency and conflict in a large-colony social insect. Proc. R. Soc. Lond. B 269, 263 –270. (doi:10. 1098/rspb.2001.1880) Stubblefield, J. W. & Charnov, E. L. 1986 Some conceptual issues in the origin of eusociality. Heredity 57, 181–187. (doi:10.1038/hdy.1986.108) Thompson, G. J. & Herbert, P. D. N. 1998 Population genetic structure of the Neotropical termite Nasutitermes nigriceps (Isoptera: Termitidae). Heredity 80, 48–55. (doi:10.1046/j.1365-2540.1998.00277.x) Thompson, G. J., Kitate, O., Lo, N. & Crozier, R. H. 2000 Phylogenetic evidence for a single, ancestral origin of a ‘true’ worker caste in termites. J. Evol. Biol. 13, 869 –881. (doi:10.1046/j.1420-9101.2000.00237.x) Thorne, B. L. 1983 Alate production and sex ratio in colonies of the Neotropical termite Nasutitermes corniger (Isoptera; Termitidae). Oecologia 58, 103–109. (doi:10. 1007/BF00384548) Thorne, B. L. 1985 Termite polygyny: the ecological dynamics of queen mutualism. In Experimental behavioural ecology and sociobiology (eds B. Ho¨lldobler & M. Lindauer), pp. 325– 341. Stuttgart, Germany; New York, NY: Gustav Fischer. Thorne, B. L. & Traniello, J. F. A. 2003 Comparative social biology of basal taxa of ants and termites. Annu. Rev. Entomol. 48, 283– 306. (doi:10.1146/annurev.ento. 48.091801.112611) Trivers, R. L. & Hare, H. 1976 Haplodiploidy and the evolution of the social insects. Science 191, 249 –263. (doi:10. 1126/science.1108197) Wade, M. J. 1980 Kin selection: its components. Science 210, 665 –667. (doi:10.1126/science.210.4470.665) Wenseleers, T., Hart, A. G. & Ratnieks, F. L. W. 2004 When resistance is useless: policing and the evolution of reproductive acquiescence in insect societies. Am. Nat. 164, 154 –167.

Phil. Trans. R. Soc. B (2009)

J. J. Boomsma

3207

West, S. A., Griffin, A. S. & Gardner, A. 2007 Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415– 432. (doi:10. 1111/j.1420-9101.2006.01258.x) West, S. A., Griffin, A. S. & Gardner, A. 2008 Social semantics: how useful has group selection been? J. Evol. Biol. 21, 374 –385. West Eberhard, M. J. 1975 The evolution of social behavior by kin selection. Q. Rev. Biol. 50, 1 –33. West Eberhard, M. J. 1983 Sexual selection, social competition, and speciation. Q. Rev. Biol. 58, 155– 183. (doi:10.1086/413215) West Eberhard, M. J. 1996 Wasp societies as microcosms for the study of development and evolution. In Natural history and evolution of paper-wasps (eds S. Turillazzi & M. J. West Eberhard), pp. 290– 317. Oxford, UK: Oxford University Press. Wheeler, D. E., Buck, N. & Evans, J. D. 2006 Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Mol. Biol. 15, 597–602. (doi:10.1111/j.1365-2583.2006.00681.x) Wheeler, W. M. 1928 The social insects. New York, UK: Harcourt, Brace & co. Williams, G. C. 1985 Sex and evolution. Princeton, NJ: Princeton University Press. Wilson, E. O. 1971 The insect societies. Cambridge, MA: Belknap Press of Harvard University Press. Wilson, E. O. 1975 Sociobiology, the new synthesis. 2nd edn (2000). Cambridge, MA: Belknap Press of Harvard University Press. Wilson, E. O. 2005 Kin selection as the key to altruism: its rise and fall. Soc. Res. 72, 159 –166. Wilson, E. O. 2008 One giant leap: how insects achieved altruism and colonial life. BioScience 58, 17–25. (doi:10.1641/B580106) Wilson, E. O. & Ho¨lldobler, B. 2005 Eusociality: origin and consequences. Proc. Natl Acad. Sci. USA 102, 13367–13371. (doi:10.1073/pnas.0505858102) Wilson, D. S. & Wilson, E. O. 2007 Rethinking the theoretical foundation of sociobiology. Q. Rev. Biol. 82, 327 –348. (doi:10.1086/522809) Yanega, D. 1997 Demography and sociality in halictine bees. In The evolution of social behavior in insects and arachnids (eds J. C. Choe & B. J. Crespi), pp. 293 –315. Cambridge, UK: Cambridge University Press.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3209–3216 doi:10.1098/rstb.2009.0108

Review

Adaptation and the genetics of social behaviour Laurent Keller* Department of Ecology and Evolution, University of Lausanne, Biophore, Lausanne 1015, Switzerland In recent years much progress has been made towards understanding the selective forces involved in the evolution of social behaviour including conflicts over reproduction among group members. Here, I argue that an important additional step necessary for advancing our understanding of the resolution of potential conflicts within insect societies is to consider the genetics of the behaviours involved. First, I discuss how epigenetic modifications of behaviour may affect conflict resolution within groups. Second, I review known natural polymorphisms of social organization to demonstrate that a lack of consideration of the genetic mechanisms involved may lead to erroneous explanations of the adaptive significance of behaviour. Third, I suggest that, on the basis of recent genetic studies of sexual conflict in Drosophila, it is necessary to reconsider the possibility of within-group manipulation by means of chemical substances (i.e. pheromones). Fourth, I address the issue of direct versus indirect genetic effects, which is of particular importance for the study of behaviour in social groups. Fifth, I discuss the issue of how a genetic influence on dominance hierarchies and reproductive division of labour can have secondary effects, for example in the evolution of promiscuity. Finally, because the same sets of genes (e.g. those implicated in chemical signalling and the responses that are triggered) may be used even in species as divergent as ants, cooperative breeding birds and primates, an integration of genetic mechanisms into the field of social evolution may also provide unifying ideas. Keywords: genetics of behaviour; adaptation; conflict; altruism; indirect genetic effects; pleiotropy

1. INTRODUCTION The success and increased complexity of organisms in the course of evolution is thought to have depended on a small number of major transitions in how information is transmitted from one generation to the next (Maynard Smith & Szathma´ry 1995). One such transition was the shift from solitary organisms to societies with a marked reproductive division of labour (eusociality). This transition has led to the tremendous ecological success of social insects, which are now dominant in many terrestrial ecosystems. This success stems from the benefits conferred by sociality, which allows individuals in a group to more efficiently modify their environment and conduct tasks that could not be performed by single individuals (Ho¨lldobler & Wilson 1990). Over recent years much progress has been made in understanding the selective forces involved in the evolution of social behaviour. There is currently no doubt that kin selection has been the all important selective force for the evolution of reproductive altruism (Bourke & Franks 1995; Queller & Strassmann 1998; Foster et al. 2006; Lehmann & Keller 2006). Numerous genetic studies in insects, other

*[email protected] One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

invertebrates and vertebrates have shown that eusociality with reproductive division of labour evolved in groups of highly related individuals, such as those formed by a mother and her offspring (Reeve & Keller 1996; Hughes et al. 2008). However, kin selection theory also predicts that groups of cooperating individuals should be the scene of potential conflicts, because, in contrast to cells of an organism, group mates are not genetically identical. Over the last decade much attention has focussed on within-group conflicts, in particular in social Hymenoptera. While these studies have revealed striking cases of conflicts being modulated by variation in kin structure (e.g. Trivers & Hare 1976; Bourke & Franks 1995; Sundstro¨m et al. 1996; Ratnieks & Helantera¨ in press), there are also many situations where variation in relatedness does not, or only to a very small extent, influence the dynamics of conflicts (Hammond & Keller 2004; Langer et al. 2004; Ratnieks et al. 2006). This has lead to the realization that the proximate mechanisms affecting the relative power of parties need to be considered if one is to understand the resolution of potential conflicts (e.g. Beekman & Ratnieks 2003; Helms et al. 2005). In this essay, I argue that an important need for further progress is the inclusion of genetic mechanisms, in particular those underlying intraspecific variation in behaviour and social organization. I also suggest that a lack of understanding of the genetic basis of traits under

3209

This journal is # 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3210

L. Keller

Review. Genetics of behaviour

investigation may lead to erroneous conclusions about their adaptive significance.

2. THE GENETIC PATHWAYS TO SOCIAL EVOLUTION The first basic question, which is starting to attract attention, is to what extant changes in social behaviour are due to changes in gene regulation rather than to sequence differences at genes influencing behaviour (Robinson & Ben-Shahar 2002). That differences in gene expression can lead to major behavioural differences and even marked morphological differences is well illustrated by the differences between queens and workers. In many social insects, queens and workers have extremely divergent morphologies and behaviour. However, usually these differences do not stem from genetic differences but rather from environmental factors triggering differential gene expression during development. At the adult stage, queens and workers typically have thousands of differently expressed genes (Miura et al. 1999; Evans & Wheeler 2001; Whitfield et al. 2002; Gra¨ff et al. 2007; Goodisman et al. 2008) just as different tissues or cell types in a multicellular organism. A major challenge will be to identify the mechanisms involved in the developmental switch, in particular the causal environmental and social factors and how they mediate changes in gene regulation. A first step in this direction has come from a pioneering study in the honeybee Apis mellifera where the experimental decrease in the methylation level of worker-destined larvae has been shown to result in the production of many larvae with queen-like phenotypic characteristics (Kucharski et al. 2008). This suggests that the specific food (i.e. the addition of royal jelly, pollen and worker glandular secretions in addition to honey) provided to queen-destined larvae may affect the level of methylation and thereby alter the processes of gene expression and caste determination. Interestingly, a recent study in humans also suggested a role of nutrition on patterns of methylation. Individuals who were prenatally exposed to famine during the Dutch Hunger Winter in 1944– 1945 had, six decades later, less DNA methylation of the imprinted IGF2 gene than their unexposed siblings (Heijmans et al. 2008). The suggestion that early-life environmental conditions can cause epigenetic changes that persist throughout life has important implications for our understanding of the dynamics of within-group conflicts. It has been proposed that, in addition to kin selection, parental manipulation could be another mechanism favouring altruism in social insects (Alexander 1974; Michener & Brothers 1974). For example, the reproduction of workers may be prevented if they are physically dominated by the queen or if they are underfed (making them poor potential reproductive individuals). However, it was pointed out that the parental manipulation hypothesis contained a flaw because a gene causing an adult to act against the interests of an offspring will be counterselected when it is present in juveniles, through these juveniles having a parent bearing the gene (Dawkins 1976; Parker & Macnair 1978; Bourke & Franks Phil. Trans. R. Soc. B (2009)

1995; see also Smiseth et al. 2008 for a review of models of parent– offspring conflict). Importantly, however, these arguments are based on simple genetic or game-theoretical models and the conclusion might be altered if the expression of the trait is conditional and/or if imprinting mechanisms are involved in parental manipulation. While some theoretical work has been conducted on the potential role of differential expression of genes inherited from the mother and father (Haig 2000; Queller 2003; Kronauer 2008), it remains to be investigated how imprinting and epigenetic trans-generational effects on behaviour may affect conflict resolution.

3. GENETIC ARCHITECTURE, HETEROZYGOTE ADVANTAGE, PLEIOTROPY AND ADAPTATION Adaptation, including in social life, can never be perfect because of constraints in the genetic system, including mutation, drift, inbreeding, selection, pleiotropy, linkage disequilibrium, heterozygote advantage and gene flow (Crespi 2000). The fire ant Solenopsis invicta provides a good example to illustrate how these effects can lead to surprising and unexpected behaviours. This species exhibits a fundamental social polymorphism with a monogyne form in which colonies have a single queen and a polygyne form where colonies contain several queens. As in many other ants, this difference in queen number is associated with differences in a wide range of reproductive and social traits, including queen phenotype and breeding strategy and the mode of colony reproduction (Ross & Keller 1995). In the polygyne form, the probability that a queen will be accepted in an established colony is strongly associated with their genotypes at the locus Gp-9 (General protein-9). All homozygous Gp-9BB queens are killed by workers when they initiate reproduction (Keller & Ross 1993, 1998). Intriguingly, Gp-9BB queens are heavier and more fecund than queens with alternate genotypes (Gp-9Bb and Gp-9bb), raising the question of why workers selectively eliminate queens with apparently the ‘best’ phenotype. To resolve this paradox, it was suggested (Keller & Ross 1998) that the execution of reproductively superior queens may represent a mechanism selected to maintain multiple queens within a colony if, as has been demonstrated in some ants, polygyny is advantageous under some ecological conditions. However, further genetic and behavioural studies revealed unexpected twists to the story and a completely different explanation for the workers’ behaviour. This is because the Gp-9b allele was found to be a kind of green beard gene inducing workers carrying one copy of that allele to selectively kill queens lacking the same allele (Keller & Ross 1998). In addition to these effects, the locus Gp-9 is also strongly associated with queen behaviour. After their mating flight, Gp-9BB queens typically attempt to start a new colony independently by feeding their progeny from their body reserves. By contrast, queens of the two other genotypes do not fly far and try to enter established colonies rather than starting a new one on their own. Interestingly, these behavioural differences are tightly correlated with an important

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Genetics of behaviour physiological difference as only Gp-9BB queens accumulate sufficient fat reserves before their mating flight to raise a first cohort of workers alone (Ross & Keller 1995; DeHeer et al. 1999; Keller & Ross 1999). The strong association between the genotype at Gp-9 and all these behavioural, morphological and physiological differences most likely results from the combined effect of several linked genes in the genomic region marked by Gp-9. This region is expected to have many of the unusual properties of regions containing the sex-determining genes in species with sex chromosomes because the b haplotype is found only in the polygyne social form, just as the Y chromosome is found only in males in species with male heterogamety. As a result, the Gp-9b region is predicted to (i) accumulate genes beneficial in the polygyne social environment (as the Y chromosome accumulates genes beneficial to male function; Rice 1987); (ii) evolve reduced recombination to preserve associations of genes advantageous for polygyny (as occurs for genes advantageous to males on the Y chromosome; Charlesworth et al. 2005); and (iii) accumulate deleterious alleles and transposable elements (because of reduced recombination; Charlesworth et al. 2005). Consistent with these expectations, the Gp-9 genomic region is characterized by low recombination (Ross 1997; Krieger & Ross 2005; Wang et al. 2008), the b allele behaves as a homozygous lethal allele (Ross 1997; Keller & Ross 1999; Hallar et al. 2007), and two transposons are preferentially expressed on the b haplotype (evidence suggests that at least one of them likely reflects a single insertion in the b haplotype; Wang et al. 2008). This example illustrates the danger of searching for adaptive explanations without a clear understanding of the genetic basis of the behaviour. The consideration of selection at the individual or colony levels only would have led to an erroneous explanation of why workers eliminate the heavier and more fecund queens in polygyne colonies. This is an important point, in particular because of the current confusion by many scientists in how selection works at the different levels of biological organization. Similarly, it is likely that the interpretation of the social behaviours of many other organisms would change if one had information on their genetic bases. In this respect, it should be mentioned that pleiotropy is probably the rule rather than the exception for many traits, particularly for behaviours which are the product of many sensory, integrative, motivational and motor processes. For example, a recent study (Ducrest et al. 2008) predicted that, and provided evidence for, the widespread association between the degree of melanin-based coloration and many physiological and behavioural traits in vertebrates stems from the melanocortins binding to the melanocortin-1-receptor (regulating the eumelanin synthesis), also binding to five other melanocortin receptors with very different functions. Similarly, it has been suggested that the pleiotropic linkage of a gene in stalk and spore formation might be an important component stabilizing cooperation in the social amoeba Dyctiostelium discoideum (Foster et al. 2004). A big challenge will be to determine how commonly suites of behavioural Phil. Trans. R. Soc. B (2009)

L. Keller

3211

differences in social organisms are similar due to pleiotropic effects and also determine to what extent pleiotropy affects the adaptive values of traits.

4. GENES, COOPERATION AND MANIPULATION In insect societies with strong queen– worker dimorphism, it was thought that queens could manipulate workers into pursuing actions that are contrary to their inclusive fitness through ‘pheromonal queen control’, whereby chemicals exuded by the queen(s) replace physical intimidation in forcing workers to behave in ways that increase queen fitness (e.g. Wilson 1971; Fletcher & Ross 1985; Ho¨lldobler & Wilson 1990). However, this view was challenged on the basis that pheromonal queen control had never conclusively been demonstrated and was evolutionarily difficult to justify (Keller & Nonacs 1993). The main arguments proposed against the pheromonal queen control hypothesis was that, if workers have their fitness significantly reduced, there would be strong selection to escape control by building up tolerance or immunity to the queen pheromone. To retain strong control, queens would therefore be required to continually produce new compounds to stay one step ahead of the workers, and/or to invest more and more resources in producing larger quantities of the pheromone as effective dosage levels increase. As both of these solutions would eventually lose costeffectiveness, queens would probably gain more overall fitness by allowing workers to win in some respects rather than indulge in an escalating arms race that would eventually decrease overall colony productivity. Later experimental studies have indeed concluded that queen pheromones are more likely to be honest signals to which workers respond in a way that generally increases their own inclusive fitness (e.g. Cuvillier-Hot et al. 2004; Endler et al. 2006; Bhadra & Gadagkar 2008; Smith et al. 2009). Interestingly, a similar type of argument has also been made with regard to male – female conflict between mating partners. However, given that recent studies of sexual conflicts in Drosophila are revealing unexpected sophistication in the males’ ability to manipulate females, the theoretical and empirical basis of queen control in social insects needs to be re-evaluated. During mating, Drosophila males have been shown to transfer more than 100 proteins (e.g. Findlay et al. 2008), causing a wide variety of fitnessrelated effects in females, including decreased sexual receptivity, increased egg production, altered morphology of the reproductive tract, increased production of immune-related peptides and the liberation of juvenile hormone ( JH) (reviewed in Wolfner 2002; Ravi Ram & Wolfner 2007). While some of these changes are beneficial to both sexes, others are costly to females. Information on the role of seminal proteins in sexual conflict, including whether they mediate physiological and behavioural changes against the females’ interest, can be gained by the analyses of the tissues that are targeted by the protein (McGraw et al. 2004; Ravi Ram & Wolfner 2007). For example, proteins binding to receptors in the reproductive tract are

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3212

L. Keller

Review. Genetics of behaviour

unlikely to permit males to force females to behave contrary to their interest. By contrast, proteins acting through neuroendocrine pathways after having entered the female circulatory system (haemolymph) may allow chemical manipulation. Interestingly, at least 10 of the proteins transferred during mating have been shown to pass from the reproductive tract into the circulation system of Drosophila females (Ravi Ram & Wolfner 2005), some probably even reaching the brain where they could directly affect the female’s behaviour. Further evidence for seminal proteins being implicated in sexual conflict (Rice 2000) comes from their very rapid evolution, the expected pattern if there is antagonistic coevolution between molecules in males and females (Swanson et al. 2001; Begun & Lindfors 2005; Findlay et al. 2008). The apparent ability of males to chemically manipulate females during the process of mating re-opens the question of whether pheromonal queen control really does not occur in social insects. In contrast to the conflict between males and females, an additional issue that needs to be considered in the case of social insects is that chemicals are generally distributed among all colony members. Thus, a queen producing a chemical aimed at preventing workers from reproducing may suffer herself from the effect of the chemical (Keller & Nonacs 1993). Chemical manipulation would thus require the queen to be much less sensitive than workers to pheromone produced. It is necessary, therefore, to precisely identify the pheromones involved and their target in workers. Most current studies consist of searching for an association between the fertility of queens and their chemical signature. Ultimately, it will be important to determine whether queenproduced pheromones exclusively bind to antennal receptors (which would support the view that they are honest signals) or whether they also enter the worker circulatory system and mediate hormonal changes directly affecting reproduction (which would be consistent with pheromonal queen control). If pheromones entering the circulatory system of workers are to be identified, it will also be interesting to determine if they also affect queen physiology or whether queens evolved immunity to their own chemicals.

5. DIRECT AND INDIRECT EFFECTS All behaviours are modulated by interactions between genes and the environment. In social organisms, social interactions are a key component of the environment. To understand the link between genotypes and phenotypes, therefore, requires determining how an individual’s phenotype is influenced by its own genes (direct genetic effects) and those expressed in social partners (indirect effects) (e.g. Moore et al. 1997; Linksvayer & Wade 2005). While indirect effects are increasingly being recognized as an important component of the genetic architecture of species (e.g. Moore et al. 1997; Linksvayer & Wade 2005), there are still almost no empirical data on such effects. One of the social systems where indirect effects have been studied is the fire ant Solenopsis invicta, where the behaviour of Gp-9BB workers was shown to depend on the ratio of Gp-9Bb workers in their Phil. Trans. R. Soc. B (2009)

colony (Ross & Keller 1998, 2002). When this ratio is lower than 5– 10 per cent, Gp-9BB workers accept only a single queen per colony that must also bear the genotype Gp-9BB (i.e. they exhibit a typical monogyne behaviour). However, when there are more than 5– 10 per cent of Gp-9Bb workers, Gp-9BB workers will accept many additional queens (up to hundreds), but only Gp-9Bb queens. Thus Gp-9 exerts indirect genetic effects, in that a threshold ratio of Gp-9Bb workers induce changes in the social behaviour of all colony members (even those lacking the b allele) and determines a fundamental aspect of social organization (monogyne versus polygyne social organization). Microarray experiments (Wang et al. 2008) revealed that differences at the genomic region marked by Gp-9 have direct effects on the level of expression of 39 genes in workers (i.e. these genes are differentially expressed between Gp-9Bb and Gp-9BB workers, irrespective of their social environment) and indirect effects on the level of expression of 91 genes (i.e. the level of expression of these genes in Gp-9BB workers depends on the presence or absence of GP-9Bb workers, possibly as a result of changes in the processes of within-colony chemical communication). Remarkably, there is almost no overlap between the genes whose level of expression is influenced by the focal workers’ Gp-9 genotypes and genes whose expression is influenced by the social environment, with only one of the 129 differentially expressed genes appearing in both categories. There have been very few other studies of indirect genetic effects within social groups. In Drosophila melanogaster, the genotypic composition of social groups (single versus mixed genotypes) was shown to affect behaviours and gene expression (i.e. the transcription of the clock gene, pheromonal profile on the cuticle and mating frequency) (Kent et al. 2008). Similarly, the mixing within colonies of individuals coming from honeybee strains selected for high and low pollen hoarding revealed that the ovariole number and dry mass of workers produced was influenced by interactions between their genotypes and those of other colony members (Linkvayer et al. 2009). In another study with European honey bees, the defensive behaviour of workers was increased when they were in colonies containing Africanized honeybees (Guzma´n-Novoa & Page 1994). It will be of great interest to investigate the consequences of such indirect genetic effects on social evolution. For example, it remains to be studied whether variation in within-group genetic diversity may mediate changes in worker behaviour via indirect effects and, if so, whether it might have favoured multiple mating in some species.

6. GENES, DIVISION OF LABOUR AND PHENOTYPIC PLASTICITY While it used to be thought that the morphological and physiological differences between castes in social insects stem only from environmental effects influencing developmental processes, several exceptional cases of genetic caste determination have recently been discovered (Helms Cahan et al. 2002, 2004;

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Genetics of behaviour Julian et al. 2002; Volny & Gordon 2002; Helms Cahan & Keller 2003; Helms Cahan & Vinson 2003; Fournier et al. 2005; Ohkawara et al. 2006). In many of these examples, populations contain two distinct genetic lineages and the developmental fate of female brood depends on the genetic origin of the parents; the inter-lineage eggs develop into workers while intralineage eggs develop into queens (Helms Cahan & Keller 2003). This system of caste determination has important implications on mating behaviour and social organization. In monogyne species with such a mode of reproduction (e.g. some Pogonomyrmex ants), queens have to mate multiply (Gadau et al. 2003) to ensure matings with males of both lineages and the production of both worker-destined and queen-destined eggs. In another similar system in the genus Solenopsis, some queens mate with males of the same species and others with males of another species (Helms Cahan & Vinson 2003). The presence of many queens in the same nest ensures the production of both queens (conspecific matings) and workers (interspecific matings). Finally, in two other ants (Wasmannia, Fournier et al. 2005; Vollenhovia, Ohkawara et al. 2006), the problem of producing both queen- and worker-destined eggs has been resolved by the conditional use of sexual and asexual reproduction. As males and females are from different lineages, queens produce workers by laying fertilized eggs and queens by reproducing clonally. Although these systems of reproduction are highly unusual, I believe that they are much more common than realized. My prediction is that maybe as many as 10 per cent of social insects have such unusual modes of reproduction. This is based on three lines of evidence. First, there is an increasing number of examples of new ant reproductive systems (see Heinze 2008). Second, I know of several unpublished population genetic studies having data inconsistent with conventional modes of reproduction; yet these studies make no reference to the unusual mode of reproduction that must be involved. Finally, controlled mating experiments revealed genetic compatibility effects on caste differentiation in Pogonomyrmex rugosus, an ant thought to have an environmental system of caste determination. In this species, the viability of queens and workers depends on genetic interactions between the parental genomes with some parental combinations being mostly compatible with queen development and others with worker development (Schwander & Keller 2008). Because similar controlled mating experiments have never been conducted in other social insects, it is impossible to determine how common such genetic compatibility effects are. Intriguingly, however, many observations are suggestive of incompatibility effects in other social insects. In several social insects where queens mate multiply, patrilines are differently represented in queens and workers (Osborne & Oldroyd 1999; Chaline et al. 2003; Moritz et al. 2005). The explanations proposed so far include nepotism (the preference of closest relatives over less-related individuals) and royalty genes (i.e. alleles increasing the likelihood of their bearers to develop into queens) (Osborne & Oldroyd 1999; Moritz et al. 2005; Hughes et al. 2008). However, Phil. Trans. R. Soc. B (2009)

L. Keller

3213

nepotism between patrilines or matrilines is rare or absent in social insects (Keller 1997) and royalty genes are unlikely because they would rapidly go to fixation. Thus, it is likely that, as in Pogonomyrmex rugosus, the different representation of patrilines in queens and workers of many social insects reflects incompatibility effects. Unequal distribution of patrilines has also been reported between morphologically divergent worker castes in the leaf-cutting ants (Acromyrmex echinatior; Hughes & Boomsma 2008) and three ant species (Camponotus consobrinus, Fraser et al. 2000; Pogonomyrmex badius, Rheindt et al. 2005; Eciton burchellii, Jaffe et al. 2007). Given that discrete worker morphologies also stem from different developmental pathways (Wilson 1971), the unequal distribution of patrilines among worker castes and between queens and workers might also be simply due to larval development being affected by genetic compatibility effects. Finally, incompatibility effects may also explain the frequently observed association between patrilines and division of labour, whereby particular tasks are preferentially performed by workers of a given patriline (see Smith et al. 2008). In the same line, it would be interesting to determine whether incompatibility effects play a role in the establishment of dominance hierarchies in vertebrate societies and small insect colonies.

7. CONCLUSION In this review I have selected a few examples to illustrate why knowledge of the genetics of behaviour should be of interest not only to those with a proximal or mechanistic interest in behaviour but also to those interested in ultimate questions. In fact, I would go as far as to say that, in many cases, a compelling demonstration of behaviour being adaptive requires one to have a clear understanding of its genetic basis. This is of course a challenging task because the identification of genes involved in social behaviour is still in its early phases (e.g. Robinson et al. 2008), and functional analyses are still impossible in most social insects. However, there is no doubt that many new genes will soon be identified setting up the possibility of studies of social behaviour and adaptation from both an evolutionary and mechanistic perspective. Most of the known genetic polymorphisms influencing social behaviour have been discovered serendipitously during the course of population genetic studies of social insects. In the future it would be helpful to also use a candidate gene approach, for example by investigating genes known to be involved in orchestrating the perception and processing of sensory information or genes known to affect behaviour as for example the vasopressin receptor 1a (avpr1a) gene, which is involved in interspecific differences in social and mating behaviour in voles (Young et al. 1999; Lim et al. 2004) and possibly individual behavioural difference in humans (e.g. Knafo et al. 2008; Walum et al. 2008). Because these genes are likely to figure prominently in social evolution it would be very interesting to conduct population genetic studies to identify natural polymorphisms affecting behaviour and social organization.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3214

L. Keller

Review. Genetics of behaviour

Finally, an integration of genetics may also contribute to bridging of the gap between studies conducted in invertebrate and vertebrate societies. Until recently, studies in these two taxa have typically proceeded independently and, in fact, there has been too little interaction between students of social vertebrates and of social insects. As the same set of genes (e.g. those implicated in chemical signalling and the responses that are triggered) are likely to be implicated in species as divergent as ants, cooperative breeding birds and primates, an integration of genetics in social evolution should provide a general framework helping in bridging the different communities. My work has been continuously supported by grants from the Swiss NSF. I thank Andrew Bourke, Philippe Christe, Heikki Helantera¨, Rob Page and Francis Ratnieks for useful comments on the manuscript.

REFERENCES Alexander, R. D. 1974 The evolution of social behavior. Annu. Rev. Ecol. Syst. 5, 325–383. (doi:10.1146/ annurev.es.05.110174.001545) Begun, D. J. & Lindfors, H. A. 2005 Rapid evolution of genomic Acp complement in the melanogaster subgroup of Drosophila. Mol. Biol. Evol. 22, 2010–2202. (doi:10. 1093/molbev/msi201) Bhadra, A. & Gadagkar, R. 2008 We know that the wasps ‘know’: cryptic successors to the queen in Ropalidia marginata. Biol. Lett. 4, 634–637. (doi:10.1098/rsbl. 2008.0455) Beekman, M. & Ratnieks, F. L. W. 2003 Power over reproduction in social Hymenoptera. Phil. Trans. R. Soc. Lond. B 358, 1741–1753. (doi:10.1098/rstb.2002.1262) Bourke, A. F. G. & Franks, N. R. 1995 Social evolution in ants. Princeton, USA: Princeton University Press. Chaline, N., Arnold, G., Papin, C. & Ratnieks, F. L. W. 2003 Patriline differences in emergency queen rearing in the honey bee Apis mellifera. Insect. Soc. 50, 234 –236. (doi:10.1007/s00040-003-0664-6) Charlesworth, D., Charlesworth, B. & Marais, G. 2005 Steps in the evolution of heteromorphic sex chromosomes. Heredity 95, 118 –128. (doi:10.1038/sj.hdy. 6800697) Crespi, B. J. 2000 The evolution of maladaptation. Heredity 84, 623 –629. (doi:10.1046/j.1365-2540.2000.00746.x) Cuvillier-Hot, V., Lenoir, A. & Peeters, C. 2004 Reproductive monopoly enforced by sterile police workers in a queenless ant. Behav. Ecol. 15, 970– 975. (doi:10.1093/ beheco/arh072) Dawkins, R. 1976 The selfish gene. Oxford, UK: Oxford University Press. DeHeer, C. J., Goodisman, M. A. D. & Ross, K. G. 1999 Queen dispersal strategies in the multiple-queen form of the fire ant Solenopsis invicta. Am. Nat. 153, 660 –675. (doi:10.1086/303205) Ducrest, A.-L., Keller, L. & Roulin, A. 2008 Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol. Evol. 23, 502–510. (doi:10. 1016/j.tree.2008.06.001) Endler, A., Liebig, J. & Ho¨lldobler, B. 2006 Queen fertility, egg marking and colony size in the ant Camponotus floridanus. Behav. Ecol. Sociobiol. 59, 490–499. (doi:10. 1007/s00265-005-0073-0) Evans, J. D. & Wheeler, D. E. 2001 Expression profiles during honeybee caste determination. Genome Biol. 2, 0001.1–0001.6. Phil. Trans. R. Soc. B (2009)

Findlay, G. D., Yi, X., MacCoss, M. J. & Swanson, W. J. 2008 Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. PLoS Biol. 6, e178. (doi:10.1371/journal.pbio.0060178) Fletcher, D. J. C. & Ross, K. G. 1985 Regulation of reproduction in social Hymenoptera. Annu. Rev. Entomol. 30, 319 –343. (doi:10.1146/annurev.en.30.010185.001535) Foster, K. R., Shaulsky, G., Strassmann, J. E., Queller, D. C. & Thompson, C. R. L. 2004 Pleiotropy as a mechanism to stabilise cooperation. Nature 431, 693–969. (doi:10.1038/ nature02894) Foster, K. R., Wenseleers, T. & Ratnieks, F. L. W. 2006 Kin selection is the key to altruism. Trends Ecol. Evol. 21, 57–60. (doi:10.1016/j.tree.2005.11.020) Fournier, D., Estoup, A., Orivel, J., Foucaud, J., Jourdan, H., Le Breton, J. & Keller, L. 2005 Clonal reproduction by males and females in the little fire ant. Nature 435, 1230–1234. (doi:10.1038/nature03705) Fraser, V. S., Kaufmann, B., Oldroyd, B. P. & Crozier, R. H. 2000 Genetic influence on caste in the ant Camponotus consobrinus. Behav. Ecol. Sociobiol. 47, 188 –194. (doi:10. 1007/s002650050010) Gadau, J., Strehl, C.-P., Oettler, J. & Ho¨lldobler, B. 2003 Determinants of intracolonial relatedness in Pogonomyrmex rugosus (Hymenoptera; Formicidae): mating frequency and brood raids. Mol. Ecol. 12, 1931– 1938. (doi:10.1046/j.1365-294X.2003.01853.x) Goodisman, M. A. D., Kovacs, J. L. & Hunt, B. G. 2008 Functional genetics and genomics in ants (Hymenoptera: Formicidae): The interplay of genes and social life. Myrmecol. News 11, 107 –117. Gra¨ff, J., Jemielity, S., Parker, J. D., Parker, K. M. & Keller, L. 2007 Differential gene expression between adult queens and workers in the ant Lasius niger. Mol. Ecol. 16, 675–683. (doi:10.1111/j.1365-294X.2007.03162.x) Guzma´n-Novoa, E. & Page Jr, R. E. 1994 Genetic dominance and worker interactions affect honeybee colony defense. Behav. Ecol. 5, 91–97. (doi:10.1093/beheco/5.1.91) Haig, D. 2000 The kinship theory of genomic imprinting. Ann. Rev. Ecol. Syst. 31, 9–32. (doi:10.1146/annurev. ecolsys.31.1.9) Hallar, B. L., Krieger, M. J. B. & Ross, K. G. 2007 Potential cause of lethality of an allele implicated in social evolution in fire ants. Genetica 131, 69–79. (doi:10.1007/s10709006-9114-5) Hammond, R. L. & Keller, L. 2004 Conflict over male parentage in social insects. PLoS Biol. 2, e248. 1472– 1482. (doi:10.1371/journal.pbio.0020248) Heijmans, B. T., Tobia, E. W., Steinb, A. D., Putterc, H., Blauwd, G. J., Sussere, E. S., Slagbooma, P. E. & Lumeye, L. H. 2008 Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl Acad. Sci. USA 105, 17 046 –17 049. (doi:10. 1073/pnas.0806560105) Heinze, J. 2008 The demise of the standard ant (Hymenoptera: Formicidae). Myrmecol. News 11, 9 –20. Helms Cahan, S. & Keller, L. 2003 Complex hybrid origin of genetic caste determination in harvester ants. Nature 424, 306 –309. (doi:10.1038/nature01744) Helms Cahan, S. & Vinson, B. S. 2003 Reproductive division of labor between hybrid and nonhybrid offspring in a fire ant hybrid zone. Evolution 57, 1562–1570. Helms Cahan, S., Parker, J. D., Rissing, S. W., Johnson, R. A., Polony, T. S., Weiser, M. D. & Smith, D. R. 2002 Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants. Proc. R. Soc. Lond. B 269, 1871 –1877. (doi:10.1098/ rspb.2002.2061) Helms Cahan, S., Julian, G. E., Rissing, S. W., Schwander, T., Parker, J. D. & Keller, L. 2004 Loss of phenotypic

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Genetics of behaviour plasticity generates genotype –caste association in harvester ants. Curr. Biol. 14, 2277– 2282. (doi:10.1016/ j.cub.2004.12.027) Helms, K. R., Reuter, M. & Keller, L. 2005 Sex-ratio conflict between queens and workers in eusocial Hymenoptera: mechanisms, costs, and the evolution of split colony sex ratios. Evolution 59, 2626 –2638. Ho¨lldobler, B. & Wilson, E. O. 1990 The ants. Cambridge, UK: Belknap Press of Harvard University Press. Hughes, W. O. H. & Boomsma, J. J. 2008 Genetic royal cheats in leaf-cutting ant societies. Proc. Natl Acad. Sci. USA 105, 5150–5153. (doi:10.1073/pnas.0710262105) Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. 2008 Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213– 1216. (doi:10.1126/science.1156108) Jaffe, R., Kronauer, D. J. C., Kraus, F. B., Boomsma, J. J. & Moritz, R. F. A. 2007 Worker caste determination in the army ant Eciton burchellii. Biol. Lett. 3, 513 –516. (doi:10. 1098/rsbl.2007.0257) Julian, G. E., Fewell, J. H., Gadau, J., Johnson, R. A. & Larrabee, D. 2002 Genetic determination of the queen caste in an ant hybrid zone. Proc. Natl Acad. Sci. USA 99, 8157–8160. (doi:10.1073/pnas.112222099) Keller, L. 1997 Indiscriminate altruism: unduly nice parents and siblings. Trends Ecol. Evol. 12, 99–103. (doi:10.1016/ S0169-5347(96)10065-3) Keller, L. & Nonacs, P. 1993 The role of queen pheromones in colonies of social insects: queen control or queen signal? Anim. Behav. 45, 787 –794. (doi:10.1006/anbe. 1993.1092) Keller, L. & Ross, K. G. 1993 Phenotypic basis of reproductive success in a social insect: genetic and social determinants. Science 260, 1107–1110. (doi:10. 1126/science.260.5111.1107) Keller, L. & Ross, K. G. 1998 Selfish genes: a green beard in the red fire ant. Nature 394, 573–575. (doi:10.1038/ 29064) Keller, L. & Ross, K. G. 1999 Major gene effects on phenotype and fitness: the relative roles of Pgm-3 and Gp-9 in introduced populations of the fire ant Solenopsis invicta. J. Evol. Biol. 12, 672–680. (doi:10.1046/j.14209101.1999.00064.x) Kent, C., Azanchi, R., Smith, B., Formosa, A. & Levine, J. D. 2008 Social context influences chemical communication in Drosophila melanogaster males. Curr. Biol. 18, 1384– 1389. (doi:10.1016/j.cub.2008.07.088) Knafo, A. et al. 2008 Genes Brain Behav. 7, 266–275. (doi:10.1111/j.1601-183X.2007.00341.x) Krieger, M. J. B. & Ross, K. G. 2005 Molecular evolutionary analyses of the odorant-binding protein gene Gp-9 in fire ants and other Solenopsis species. Mol. Biol. Evol. 22, 2090– 2103. (doi:10.1093/molbev/msi203) Kronauer, D. C. 2008 Genomic imprinting and kinship in the social Hymenoptera: what are the predictions? J. Theor. Biol 254, 737–740. (doi:10.1016/j.jtbi.2008. 06.019) Kucharski, R. J., Maleszka, J., Foret, S. & Maleszka, R. 2008 Nutritional control of reproductive status in honeybees via DNA methylation. Science 319, 1827–1830. (doi:10. 1126/science.1153069) Langer, P., Hogendoorn, K. & Keller, L. 2004 Tug-of-war over reproduction in a social bee. Nature 428, 844–847. (doi:10.1038/nature02431) Lehmann, L. & Keller, L. 2006 The evolution of cooperation and altruism—a general framework and a classification of models. J. Evol. Biol. 19, 1365 –1376. (doi:10.1111/j.1420-9101.2006.01119.x) Lim, M. M., Wang, Z., Olaza´bal, D. E., Xianghui, R., Terwilliger, E. F. & Young, L. J. 2004 Enhanced partner Phil. Trans. R. Soc. B (2009)

L. Keller

3215

preference in a promiscuous species by manipulating the expression of a single gene. Nature 429, 754 –757. (doi:10.1038/nature02539) Linksvayer, T. A. & Wade, M. J. 2005 The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony. Q. Rev. Biol. 80, 317 –336. (doi:10.1086/ 432266) Linksvayer, T. A., Fondrk, M. K. & Page Jr, R. E. 2009 Honeybee social regulatory networks are shaped by colony level selection. Am. Nat. 173, E99–E107. (doi:10.1086/596527) Maynard Smith, J. & Szathma´ry, E. 1995 The major transitions in evolution. Oxford, UK: Oxford University Press. McGraw, L. A., Gibson, G., Clark, A. G. & Wolfner, M. F. 2004 Genes regulated by mating, sperm or seminal proteins in mated female Drosophila melanogaster. Curr. Biol. 14, 1509–1514. (doi:10.1016/j.cub.2004.08.028) Michener, C. D. & Brothers, D. J. 1974 Were workers of eusocial Hymenoptera initially altruistic or oppressed? Proc. Natl Acad. Sci. USA 68, 1242–1245. Miura, T., Kamikouchi, A., Sawata, M., Takeuchi, H., Natori, S., Kubo, T. & Matsumoto, T. 1999 Soldier caste-specific gene expression in the mandibular glands of Hodotermopsis japonica (Isoptera: Termopsidae). Proc. Natl Acad. Sci. USA 96, 13874–13879. (doi:10.1073/ pnas.96.24.13874) Moore, A. J., Brodie III, E. D. & Wolf, J. B. 1997 Interacting phenotypes and the evolutionary process I. Direct and indirect genetic effects of social interactions. Evolution 51, 1352–1362. (doi:10.2307/2411187) Moritz, R. F. A., Lattorff, H. M., Neumann, P., Kraus, F. B., Radloff, S. E. & Hepburn, H. R. 2005 Rare royal families in honeybees, Apis mellifera. Naturwissenschaften 92, 488–491. (doi:10.1007/s00114-005-0025-6) Ohkawara, K., Nakayama, M., Sato, A., Trindl, A. & Heinze, J. 2006 Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi. Biol. Lett. 2, 359–363. (doi:10.1098/rsbl.2006.0491) Osborne, K. E. & Oldroyd, B. P. 1999 Possible causes of reproductive dominance during emergency queen rearing by honeybees. Anim. Behav. 58, 267 –272. (doi:10.1006/ anbe.1999.1139) Parker, G. A. & MacNair, M. R. 1978 Models of parent– offspring conflict. I. Monogamy. Anim. Behav. 26, 97–110. (doi:10.1016/0003-3472(78)90009-X) Queller, D. C. 2003 Theory of genomic imprinting conflict in social insects. BMC Evol. Biol. 3, 15. (doi:10.1186/ 1471-2148-3-15) Queller, D. C. & Strassmann, J. E. 1998 Kin selection and social insects. Bioscience 48, 165– 175. (doi:10.2307/ 1313262) Ratnieks, F. L. W. & Helantera¨, H. In press. The evolution of extreme altruism and inequality in insect colonies. Phil. Trans. R. Soc. B. (doi:10.1098/rstb.2009.0129) Ratnieks, F. L. W., Foster, K. R. & Wenseleers, T. 2006 Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581– 608. (doi:10.1146/annurev.ento.51.110104.151003) Ravi Ram, K. R. & Wolfner, M. F. 2005 Fates and targets of male accessory gland proteins in mated female Drosophila melanogaster. Insect Biochem. Mol. Biol. 35, 1059–1071. (doi:10.1016/j.ibmb.2005.05.001) Ravi Ram, K. R. & Wolfner, M. F. 2007 Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Int. Comp. Biol. 47, 427 –445. (doi:10.1093/icb/icm046) Reeve, H. K. & Keller, L. 1996 Relatedness asymmetry and reproductive sharing in animal societies. Am. Nat. 148, 764–769. (doi:10.1086/285954)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3216

L. Keller

Review. Genetics of behaviour

Rheindt, F. E., Strehl, C. P. & Gadau, J. 2005 A genetic component in the determination of worker polymorphism in the Florida harvester ant Pogonomyrmex badius. Insectes Soc. 52, 163–168. (doi:10.1007/s00040-004-0787-4) Rice, W. R. 1987 Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116, 161 –167. Rice, W. R. 2000 Dangerous liaisons. Proc. Natl Acad. Sci. USA 97, 12953–12955. (doi:10.1073/pnas.97.24. 12953) Robinson, G. E. & Ben-Shahar, Y. 2002 Social behavior and comparative genomics: new genes or new gene regulation? Genes Brain Behav. 1, 197– 203. (doi:10.1034/j. 1601-183X.2002.10401.x) Robinson, G. E., Fernald, R. D. & Clayton, D. F. 2008 Genes and social behavior. Science 322, 896 –900. (doi:10.1126/science.1159277) Ross, K. G. 1997 Multilocus evolution in fire ants: effects of selection, gene flow and recombination. Genetics 145, 961 –974. Ross, K. G. & Keller, L. 1995 Ecology and evolution of social organization: insights from fire ants and other highly eusocial insects. Annu. Rev. Ecol. Syst. 26, 631 –656. (doi:10.1146/annurev.es.26.110195.003215) Ross, K. G. & Keller, L. 1998 Genetic control of social organization in an ant. Proc. Natl Acad. Sci. USA 95, 14232–14237. (doi:10.1073/pnas.95.24.14232) Ross, K. G. & Keller, L. 2002 Experimental conversion of colony social organization by manipulation of worker genotype composition in fire ants (Solenopsis invicta). Behav. Ecol. Sociobiol. 51, 287 –295. Schwander, T. & Keller, L. 2008 Genetic compatibility affects queen and worker caste determination. Science 322, 552. (doi:10.1126/science.1162590) Smiseth, P. T., Wright, J. & Ko¨lliker, M. 2008 Parent – offspring conflict and co-adaptation: behavioural ecology meets quantitative genetics. Proc. R. Soc. B 275, 1823–1830. (doi:10.1098/rspb.2008.0199) Smith, C. R., Toth, A. L., Suarez, A. V. & Robinson, G. E. 2008 Genetic and genomic analyses of the division of labour in insect societies. Nat. Rev. Genet. 9, 735 –748. (doi:10.1038/nrg2429) Smith, A. A., Ho¨lldobler, B. & Liebig, J. 2009 Cuticular hydrocarbons reliably identify cheaters and allow

Phil. Trans. R. Soc. B (2009)

enforcement of altruism in a social insect. Curr. Biol. 19, 78–81. (doi:10.1016/j.cub.2008.11.059) Sundstro¨m, L., Chapuisat, M. & Keller, L. 1996 Conditional manipulation of sex ratios by ant workers—a test of kin selection theory. Science 274, 993–995. (doi:10.1126/science.274.5289.993) Swanson, W. J., Clark, A. G., Waldrip-Dail, H. M., Wolfner, M. F. & Aquadro, C. F. 2001 Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc. Natl Acad. Sci. USA 98, 7375– 7379. (doi:10.1073/pnas.131568198) Trivers, R. L. & Hare, H. 1976 Haplodiploidy and the evolution of the social insects. Science 191, 249–263. (doi:10.1126/science.1108197) Volny, V. P. & Gordon, D. M. 2002 Genetic basis for queen –worker dimorphism in a social insect. Proc. Natl Acad. Sci. USA 99, 6108–6111. (doi:10.1073/pnas. 092066699) Walum, H. et al. 2008 Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc. Natl Acad. Sci. USA 105, 14 153 –14 156. (doi:10.1073/pnas.080308 1105) Wang, J., Ross, K. G. & Keller, L. 2008 Genome-wide expression patterns and the genetic architecture of a fundamental social trait. PLoS Genet. 7, e1000127. (doi:10.1371/journal.pgen.1000127) Whitfield, C. W., Band, M. R., Bonaldo, M. F., Kumar, C. G., Liu, L., Pardinas, J. R., Robertson, H. M., Soares, M. B. & Robinson, G. E. 2002 Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee. Genome Res. 12, 555–566. (doi:10.1101/gr.5302) Wilson, E. O. 1971 The insect societies. Cambridge, UK: Belknap Press of Harvard University Press. Wolfner, M. F. 2002 The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88, 85–93. (doi:10.1038/sj.hdy.6800017) Young, L. J., Nilsen, R., Waymire, K. G., MacGregor, G. R. & Insel, T. R. 1999 Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400, 766–768. (doi:10.1038/ 23475)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3217–3227 doi:10.1098/rstb.2009.0109

Review

The evolution of cooperative breeding in birds: kinship, dispersal and life history Ben J. Hatchwell* Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK The evolution of cooperation among animals has posed a major problem for evolutionary biologists, and despite decades of research into avian cooperative breeding systems, many questions about the evolution of their societies remain unresolved. A review of the kin structure of avian societies shows that a large majority live in kin-based groups. This is consistent with the proposed evolutionary routes to cooperative breeding via delayed dispersal leading to family formation, or limited dispersal leading to kin neighbourhoods. Hypotheses proposed to explain the evolution of cooperative breeding systems have focused on the role of population viscosity, induced by ecological/demographic constraints or benefits of philopatry, in generating this kin structure. However, comparative analyses have failed to generate robust predictions about the nature of those constraints, nor differentiated between the viscosity of social and non-social populations, except at a coarse level. I consider deficiencies in our understanding of how avian dispersal strategies differ between social and nonsocial species, and suggest that research has focused too narrowly on population viscosity and that a broader perspective that encompasses life history and demographic processes may provide fresh insights into the evolution of avian societies. Keywords: cooperative breeding; helping; avian sociality; ecological constraints; dispersal; avian phylogeny

1. INTRODUCTION The evolution of cooperation has been a fundamental and persistent problem for evolutionary biologists for the past 150 years. Darwin (1859) recognized the paradox of apparently altruistic behaviour among individuals subject to natural selection, but the full extent of the problem of cooperation and its ubiquity in biological systems from the level of genes to our own complex society has been appreciated only recently. Indeed, the last few years have seen a plethora of theoretical studies and synthetic reviews that seek to consolidate the diverse theoretical and empirical approaches and solutions to this long-standing puzzle (West et al. 2007). The cooperative breeding systems of birds have been a fertile testing ground for ideas on the evolution of societies, resulting in some of the most intensive studies of natural populations in ecology (e.g. Stacey & Koenig 1990). As the number of studies has grown, coupled with developments in molecular genetics, so has the realization that vertebrate societies are extremely diverse in their social organization and mating system (Cockburn 2004). This diversity presents significant problems in defining what is meant by ‘cooperative breeding’. ‘Helper-at-the-nest’ systems where grown offspring remain on their natal territory and help their parents to raise subsequent broods are

*[email protected] One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

easily classified, but in many species there are multiple breeders of either sex within social groups, in addition to non-breeding helpers. These ‘plural’ breeding systems are also universally included as cooperative breeders. More contentious are those species in which all individuals within social groups are potential breeders and there are no non-breeding helpers, e.g. dunnocks Prunella modularis (Davies 1992). Cockburn (2006) used a broad definition that considered a species to be cooperative when more than 10 per cent of nests in one or more populations are attended by more than two birds, thereby including such systems. Others have used more restrictive definitions that differentiate between cooperative polygamy and cooperation based on collateral kinship (e.g. Hartley & Davies 1994) or care by non-breeders (Ligon & Burt 2004). However, there is no clear distinction between cooperative polygamy and systems with helpers (Cockburn 1998) and in many cases, it is unknown whether ‘helpers’ are non-breeders or potential breeders. In this article, I first follow Cockburn’s (2006) definition in reviewing the importance of family formation and kinship in avian cooperative breeding systems. Another problem arises over obligate and facultative cooperation, terms that have been used in various senses by different authors (e.g. DuPlessis et al. 1995; Cockburn 1998). In reality, a tiny minority of avian cooperative breeding systems are truly obligate in the sense that successful reproduction is impossible without helpers, e.g. white-winged chough Corcorax melanorhamphos (Heinsohn 1992). In principle, at

3217

This journal is # 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3218

B. J. Hatchwell

Review. Avian cooperative breeding

least, the facultative nature of the vast majority of their cooperative societies makes birds an ideal group in which to study the conditions that promote cooperative behaviour, but our understanding of the ecological, demographic and phylogenetic factors that have resulted in the evolution of cooperation is still far from comprehensive. In this article, I consider the problems that may have contributed to this failure to fully explain social evolution in birds, and suggest areas of research that may contribute to achieving that goal. First, I consider the phylogenetic distribution of cooperative breeding and describe likely evolutionary routes to cooperative breeding, emphasizing the important role that the kinship of cooperators has played. Next, I discuss the evidence that constraints on dispersal are responsible for the development of kin-structured populations, highlighting our relatively poor knowledge of dispersal strategies in both social and non-social species. Finally, I suggest that explanations have focused too closely on population viscosity, and that a broader perspective on the processes generating kin-structured populations would be profitable.

2. PHYLOGENETIC DISTRIBUTION OF COOPERATIVE BREEDING Cockburn (2006) recently compiled a remarkable dataset that included the breeding systems of 9456 extant bird species, of which 9268 (98%) were assigned to 188 families, the remainder having uncertain affinities. The pattern of parental care has been described, in more or less detail, for over half of these species (5143/9456; 54%) and patterns of parental care for the rest were inferred from phylogenetic relationships. Cockburn (2006) assigned 852 species (9%) as cooperative breeders, which represents a substantial increase on the 2.5 – 3% recognized in previous studies (Brown 1987; Arnold & Owens 1998; Ligon & Burt 2004). This increase is not simply a consequence of Cockburn’s (2006) use of a broad definition of cooperative breeding, but is attributable to the use of phylogenetic inference in the assignment of a breeding system, rather than relying on direct evidence (which is inevitably patchy even for a well-studied taxon, such as the birds) and the assumption of biparental care as the default pattern. Given the lack of detailed studies of the avifaunas of tropical regions, where cooperative breeding is particularly prevalent, this approach is likely to give a closer approximation than previous treatments, despite the likely errors in some assignments (Cockburn 2006). As in previous studies, Cockburn (2006) found a patchy phylogenetic distribution of cooperative breeding and evidence that it has evolved multiple times (Russell 1989; Peterson & Burt 1992; Edwards & Naeem 1993; Cockburn 1996). Assuming that biparental care is ancestral, Ligon & Burt (2004) estimated that there had been at least 28 independent transitions to cooperative breeding. Furthermore, although several bird families have cooperative breeding as an ancestral state, and many may have experienced a single transition to cooperation in their evolutionary history, Cockburn (2006) lists 35 bird families in Phil. Trans. R. Soc. B (2009)

which there have been multiple transitions to or from cooperative breeding. Of course, the number of evolutionary transitions identified is dependent on phylogenetic relationships and even in a well-studied group like the birds, the affinities of many species remain obscure, with some high-level relationships still a matter of debate (e.g. Hackett et al. 2008). Therefore, although the patchy distribution of cooperation within the avian phylogeny and the multiple evolutionary transitions to and from cooperative breeding are robust, the finer details of the phylogenetic distribution and relationships of some cooperative breeders remain to be resolved. A key point that emerges from this analysis is that avian breeding systems offer an excellent opportunity to understand the evolutionary origins of cooperative behaviour in vertebrates. Three features are important in this regard: (i) our relatively good knowledge of avian breeding systems; (ii) the fact that the great majority of cooperative species exhibit facultative cooperation allowing observational and experimental tests within species; and (iii) the multiple transitions to and from cooperation provide ample opportunity to test evolutionary hypotheses through comparative methods.

3. EVOLUTIONARY ROUTES TO COOPERATIVE BREEDING Ligon & Burt (2004) argued that the evolution of altriciality in birds, which is likely to be an ancestral trait for most extant bird lineages (Ricklefs & Starck 1998), played a key role in the evolution of cooperative breeding because altriciality and the high level of parental investment it requires provides the opportunity of helping as an adaptive strategy. This view is supported by the observation that there have been more transitions to cooperation in altricial lineages than expected if developmental mode and cooperative breeding were randomly associated (Ligon & Burt 2004). Nevertheless, cooperative brood care is found in 4 per cent (n ¼ 789) of precocial species, in many of which parental investment may also be high. Therefore, while less frequent than in altricial species (11% of 7698 species), cooperation still occurs in a substantial number of precocial species (Cockburn 2006). It is also important to note that the cooperatively breeding precocial species include helper-at-the-nest systems, such as members of the Psophiidae and Rallidae (del Hoyo et al. 1996), although in other precocial families the system is more precisely described as cooperative polygamy, e.g. in the Rheidae and Anseranatidae (del Hoyo et al. 1992). Most treatments propose that helping behaviour evolved as alloparental care within family groups formed through delayed dispersal (Brown 1987; Ligon & Stacey 1991; Ligon & Burt 2004). In this scenario, non-reproductive delayed dispersers might be stimulated to provide care for non-descendant offspring by exposure to the stimulus of begging. This idea is supported by occasional observations of typically non-cooperative bird species feeding conspecific offspring belonging to another pair, or even feeding the offspring of another species (Shy 1982;

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Avian cooperative breeding Skutch 1987). If the feeding of conspecific offspring confers some form of fitness benefit, either directly or indirectly via kin selection (Hamilton 1964), then adaptive helping behaviour within more or less stable family groups would evolve. This model proposes that helping and independent breeding will generally be sequential; delayed dispersal and a period of helping followed by acquisition of reproductive status (either by dispersal or ascendancy to dominant status within the natal group) and then independent reproduction. An alternative evolutionary route to cooperation is more opportunistic and has been described as cooperative breeding within kin neighbourhoods rather than within well-defined family groups (Dickinson & Hatchwell 2004; Ligon & Burt 2004). The existence of kin neighbourhoods provides opportunities for helping behaviour beyond the confines of a particular group and also permits greater flexibility in the ordering of helping and independent reproduction. For example, in long-tailed tits Aegithalos caudatus, all members of a population breed independently, but failed breeders may become helpers at the nest of close kin towards the end of a temporally constrained breeding season when the prospect of successful independent reproduction is low (MacColl & Hatchwell 2002; Hatchwell & Sharp 2006). Similar behaviour is seen among family members in western bluebirds Sialia mexicana (Dickinson et al. 1996), and within ‘clans’ of the colonial white-fronted bee-eater Merops bullockoides, where helpers may even be recruited by disruption of relatives’ breeding attempts (Emlen & Wrege 1992). More extensive social networks with complex investment patterns occur in the ‘coteries’ of bell miners Manorina melanophrys (Clarke & Fitz-Gerald 1994). This kind of social organization has been neglected because of the focus on the more traditional concept of cooperation within stable nuclear family groups (Ligon & Burt 2004), despite the very substantial fitness consequences that this form of helping may have (e.g. Emlen & Wrege 1991; MacColl & Hatchwell 2004). Following the initial evolution of helping behaviour via one or other of these routes, variation among species in evolutionary history, ecology and life history would have resulted in the diverse social systems among extant birds. However, despite that adaptive radiation in social organization and complexity, it is clear that the imagined ancestral pattern of cooperative behaviour evolving predominantly among members of family groups still holds among extant cooperative breeders. Among the 9 per cent of bird species that Cockburn (2006) described as cooperative, only a small minority have been described in sufficient detail to characterize their kin structure precisely. The social organization of many species remains completely unstudied, and in some cases only rudimentary information is available on what are likely to be entire families of cooperative species, such as the Galbulidae (del Hoyo et al. 2002). However, if social structure is inferred from those species whose kin associations are known to other members of their respective families, then 55/84 (65%) of families with Phil. Trans. R. Soc. B (2009)

B. J. Hatchwell

3219

species that exhibit regular cooperative breeding can be broadly characterized as having cooperative groups composed of kin or not. Of these 55 families, 44 (80%) can be provisionally described as being cooperative within kin groups. If a family’s characterization is extrapolated to all the species within that family, then 612/820 (75%, excluding species of uncertain affinity) cooperative species can be characterized, and of these 556/612 (91%) can be provisionally described as being cooperative predominantly within kin groups (appendix A). The remaining taxa (20% of families, 9% of species), in which cooperation occurs mainly among unrelated individuals, are dominated by cooperative polygamists where all individuals within groups are ‘hopeful reproductives’. As explained above, some definitions of cooperative breeding have omitted such systems, regarding them as different in kind from those in which helpers feed broods in which they have no direct reproductive stake (e.g. Ligon & Burt 2004). Instead, it could be argued that they are best considered within conventional mating systems theory (Emlen & Oring 1977), arising from conflict between the sexes over their preferred mating system (e.g. Davies 1992). Therefore, it is important to acknowledge the likelihood that some cooperative polygamous systems have evolved via different routes to the more conventional cooperative breeding systems that are the main focus of this review. It is also important to note that the dichotomous classification of families as having either kin-based cooperative systems or not, may be perfectly valid in some cases, but less so in others. For example, in the Neosittidae, Corcoracidae, Sturnidae, Sittidae and Mimidae, the breeding systems of many or all of their cooperative species are fairly well known (del Hoyo et al. 2005, 2006, 2007, 2008; Woxvold et al. 2006; Rubenstein & Lovette 2007; Beck et al. 2008), whereas among families such as the Bucconidae, Lybiidae and Dacelonidae, the inference is more speculative (del Hoyo et al. 2001, 2002). Furthermore, in a few families, such as the Psittacidae, in which some species are well described, the social structures are sufficiently diverse to defy generalization (del Hoyo et al. 1997). Among those taxa with kin-based cooperative systems, the importance of helping behaviour within kin neighbourhoods has probably been under-estimated (Dickinson & Hatchwell 2004). Using Cockburn’s (2006) compilation, I characterized 44 families as having kin-based cooperation (see above), and helping of this sort occurs in at least 18 (41%) of those families (appendix A). Unfortunately, the scant information available prevents the assessment of its significance at the level of species, but it may have been the main route to helping in certain families, such as the Meropidae (del Hoyo et al. 2002) and Aegithalidae (del Hoyo et al. 2008). An interesting feature of kin neighbourhoods is that the permissive conditions for kin-directed cooperation to evolve may be more frequent than in the more extreme form of family structure that results from delayed dispersal. On the other hand, if the benefits of cooperation are dependent on help being directed towards kin, then for

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3220

B. J. Hatchwell

Review. Avian cooperative breeding

fitness gains to be maximized some mechanism of kin recognition may be required (Komdeur & Hatchwell 1999; Komdeur et al. 2008). Why should kin association be so important in setting the scene for the evolution of avian societies and cooperation? The obvious answer to this question is that close association of kin creates the opportunity for kin selection to operate (Hamilton 1964). Although the weight of evidence in favour of kin-selected cooperative breeding is debated (e.g. Clutton-Brock 2002; Cockburn 1998), the evidence for kin-selected fitness benefits of cooperative breeding is very strong for many birds (Dickinson & Hatchwell 2004). This is not to say that kin selection is always important: (i) there are many examples of cooperation among non-kin; (ii) there may be various sources of direct fitness benefits for both related and unrelated individuals within cooperative groups, that may have been under-estimated in the past; (iii) the role of indirect fitness benefits may have been over-estimated in some cases by a failure to test whether help in family groups is kin-selected and to take account of confounding effects (for reviews, see Cockburn 1998; Clutton-Brock 2002; Dickinson & Hatchwell 2004). Furthermore, costs of competing with kin are often neglected (Griffin & West 2002). Therefore, although studies have identified various fitness benefits from cooperative breeding, the relative importance of kin selection in the evolution of avian societies is still not fully resolved. Kinship may also be important in stabilizing and reducing conflict within cooperative groups through inbreeding avoidance, at least within nuclear families. There is good evidence of this in several cooperative breeders, although in others incest is commonplace (Koenig & Haydock 2004). Close kinship between breeders and helpers who are potential breeders may reduce conflict over reproduction, and the scale of this stabilizing effect is illustrated by the intense power struggles that may develop among opposite sex kin when a reproductive vacancy arises through death of a parent in acorn woodpeckers Melanerpes formicivorus (Koenig et al. 1998). However, the impact of incest avoidance on social birds remains poorly understood (Koenig & Haydock 2004). In summary, this review of potential routes to cooperative breeding has provided quantitative support for the contention that cooperation typically occurs among relatives. This is not to say that social groups are invariably composed of kin, nor that kin selection has always been a major selective force in the evolution of avian cooperative breeding. Nevertheless, despite these caveats, it is reasonable to conclude that the key to understanding the evolution of cooperative breeding in birds lies in understanding how kin associations develop. In other words, how do we explain the development of kin-structured populations?

4. ECOLOGICAL CONSTRAINTS AND DISPERSAL Hamilton (1964) proposed that in viscous populations, where dispersal is either delayed or limited, the opportunities to interact with kin increase. This idea has provided the context for all adaptive Phil. Trans. R. Soc. B (2009)

hypotheses for the evolution of cooperative breeding. It is not my intention to review the history and development of explanations for the evolution of avian societies in any depth here, because there have been several recent reviews (Cockburn 1998; Hatchwell & Komdeur 2000; Dickinson & Hatchwell 2004), but it is worth briefly summarizing their key features and similarity. Selander (1964) set the ball rolling with the habitat saturation hypothesis, proposing that the opportunities for dispersal and independent breeding are limited in saturated habitats so that offspring remain on their natal territory and wait for suitable reproductive vacancies to appear. Developments of this idea incorporated the merits of delayed dispersal relative to floating (Brown 1969, 1974; Verbeek 1973), the benefits of prolonged parental care (Ekman et al. 2001) and the importance of gradients in habitat quality for dispersal decisions (Koenig & Pitelka 1981; Stacey & Ligon 1987, 1991; Zack 1990). These various proposals can be accommodated within the generalized ecological constraints hypothesis of Emlen (1982) and the delayed dispersal threshold model of Koenig et al. (1992). These two landmark papers make the common point that the various hypotheses presented above are essentially variants on the same theme: that individuals help when the balance of costs and benefits are weighed against floating, dispersing or attempting to breed independently and in favour of delayed dispersal, deferred reproduction and cooperation. The various hypotheses differ in the emphasis that they place on different components of that cost– benefit equation and the context in which this analysis is made, but they share the same fundamental principles (Emlen 1994). More recently, Covas & Griesser (2007) have proposed the adaptive delayed dispersal hypothesis that treats delayed dispersal as a life-history decision that weighs the relative costs and benefits of dispersal in the long term (i.e. over an individual’s lifetime) rather than in the short term (i.e. the chance of filling a breeding vacancy immediately). This hypothesis is important in emphasizing the long-term consequences of decision-making and its recognition of the interplay between parental and offspring decision-making. However, it can be argued that it does not differ in its essentials from previous explanations, simply in the time-span over which costs and benefits of dispersal decisions are weighed. How strong is the evidence that ecological constraints driving family formation? Again, this issue has been extensively reviewed (Cockburn 1998; Hatchwell & Komdeur 2000; Dickinson & Hatchwell 2004; Covas & Griesser 2007; Hatchwell 2007), so I will present only a brief summary of the evidence here. First, a number of intraspecific studies have investigated the relationship between specific constraints and the prevalence of cooperative breeding either by observation (e.g. Emlen 1984; Russell 2001) or experiment (Pruett-Jones & Lewis 1990; Komdeur 1992; Walters et al. 1992; Covas et al. 2004), and have provided consistently strong evidence that specific ecological and/or demographic constraints limit dispersal and promote cooperation. By contrast, interspecific comparisons that have sought common ecological factors that drive

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Avian cooperative breeding family formation and cooperative breeding have proved equivocal (e.g. Ford et al. 1988; DuPlessis et al. 1995; Cockburn 1996; Arnold & Owens 1999; Rubenstein & Lovette 2007). Therefore, no consensus has emerged about whether cooperatively breeding species share key ecological or demographic traits, and despite its intuitive sense, the notion that constraints drive family formation is less compelling than was once thought because we still lack a predictive framework to explain cooperative breeding (Cockburn 1998; Hatchwell & Komdeur 2000). In the following section I consider in greater detail the processes that lead to kin-structured populations, with the aim of generating insights into the traits that should be examined in such comparisons. 5. WHAT FACTORS GENERATE KIN-STRUCTURED POPULATIONS? Few studies have explored the fine-scale genetic structure of bird populations, and certainly not enough to attempt any systematic comparison of cooperative and non-cooperative species. Among cooperative species, kin structure has been demonstrated in superb fairy wrens Malurus cyaneus (Double et al. 2005), white-breasted thrashers Ramphocinclus brachyurus (Temple et al. 2006), apostlebirds Struthidea cinerea (Woxvold et al. 2006) and whitewinged chough (Beck et al. 2008), but all these species have retained offspring, so such structure is hardly surprising. Among species that exhibit helping within kin neighbourhoods, population genetic structure has been measured genetically only for the bell miner Manorina melanophrys (Painter et al. 2000), sociable weaver Philetairus socius (Covas et al. 2006) and long-tailed tit (S. P. Sharp & B. J. Hatchwell 2009, unpublished data), again revealing significant kin structure, especially among the predominant helping sex. Among the non-cooperative species whose population structure has been measured, it is notable that many of them also exhibit significant fine-scale kin structure, e.g. Brunnich’s guillemots Uria lomvia (Friesen et al. 1996), manakins Manacus manacus (Shorey et al. 2000), black grouse Tetrao tetrix (Hoglund et al. 1999), red grouse Lagopus lagopus (Piertney et al. 2008) and blue tits Cyanistes caeruleus (Foerster et al. 2006). Therefore, even if this is a biased sample of non-cooperative species, it is clear that genetically structured populations are widespread in non-cooperative species as well as cooperative ones. In addition to direct genetic evidence, indirect methods may also be used. I first consider the evidence that population viscosity (i.e. patterns of natal dispersal) differs in the predicted manner and ask whether dispersal always acts to disrupt kinship ties. Finally, I describe a broader perspective on the processes contributing to the kin structure of populations. (a) Population viscosity Hamilton (1964) and most subsequent workers have identified population viscosity as being the most important process generating the kin structure required for kin-selected cooperation to evolve, leading to the clear prediction that dispersal will be lower in cooperative species than in non-cooperative species. It is patently Phil. Trans. R. Soc. B (2009)

B. J. Hatchwell

3221

true that for those species in which helping occurs within nuclear families formed through philopatry, that dispersal is extremely limited at least during the period of helping. In such species, helping typically occurs prior to natal dispersal from the home territory, and dispersal distance following this period of helping may have no impact on the cooperative system because there is little post-dispersal interaction with kin remaining on the natal territory (Stacey & Koenig 1990). However, cooperative species with nuclear family structure and non-cooperative species are not completely differentiated in this respect because family-living is much more widespread among birds than cooperative breeding is (Ekman et al. 2004; Covas & Griesser 2007), although the full extent of family-living without cooperative breeding has not been assessed systematically. Furthermore, among those species that have evolved cooperative breeding within kin neighbourhoods, often with redirected helping following reproductive failure, there must be some natal dispersal prior to breeding (e.g. Dickinson et al. 1996; Painter et al. 2000; Sharp et al. 2008a,b). Dispersal at this stage is likely to generate further overlap in dispersal strategies between cooperative and noncooperative species, although species in which cooperation occurs within kin neighbourhoods would still be expected to exhibit less dispersal on average than non-cooperative species. Unfortunately, despite its significance for ecology and evolution, variation among individuals or species in dispersal strategy remains poorly understood (Clobert et al. 2001), and there has been no systematic comparison of dispersal distances of cooperative and non-cooperative species beyond broad classifications of species as sedentary, nomadic or migratory (DuPlessis et al. 1995; Arnold & Owens 1999). Of those species exhibiting help within kin neighbourhoods, natal dispersal has been determined for long-tailed tits, showing that most males (the more philopatric and predominant helping sex) disperse less than 400 m (Sharp et al. 2008a). However, such dispersal distances are not atypical of non-cooperative temperate passerine birds (Paradis et al. 1998; figure 1) and detailed studies of many noncooperative species show very similar dispersal distributions, e.g. great tit Parus major (Szulkin & Sheldon 2008), magpie Pica pica (Eden 1987) and song sparrow Melospiza melodia (Arcese 1989). The measurement of dispersal is fraught with problems (Koenig et al. 1996; Nathan 2001), so any comparison across species or populations must be qualified by the recognition of biases in estimating dispersal distances. Russell (1999) conducted a more systematic comparison of dispersal in four non-cooperative and one cooperative species (long-tailed tit) occupying the same habitats, using the recapture rates at the same site of very large samples of ringed juveniles as a measure of philopatry. Recapture rates did not differ, and hence there was no indication that long-tailed tits had unusually limited dispersal. Therefore, despite its intuitive plausibility, at present there is no strong evidence that sedentary species exhibiting cooperation within kin neighbourhoods have an unusual pattern of dispersal relative to non-cooperators. A fundamental assumption of the argument that population viscosity increases the opportunity for the

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3222

B. J. Hatchwell

Review. Avian cooperative breeding

18

frequency

16 14 12 10 8 6 4 2 0 1 2 3 4 5 10 20 30 geometric mean natal dispersal distance (km) Figure 1. Geometric mean natal dispersal distances for 47 UK passerine species. Black and grey bars represent resident and migratory species, respectively; the only UK species exhibiting kin-directed cooperative breeding, the longtailed tit, is represented by the white bar. Data from Paradis et al. (1998).

evolution of kin-selected cooperation is that dispersal is a largely random process with respect to kinship (Hamilton 1964; Perrin & Goudet 2001; Gardner & West 2006). However, kin association during natal dispersal has been recorded in both social (Heinsohn et al. 2000; Koenig et al. 2000; Williams & Rabenold 2005; Sharp et al. 2008b) and non-social birds (e.g. Shutler & Clark 2003; Matthysen et al. 2005). Kin association during dispersive movements may also occur at a much larger scale, serving to maintain kin structure in populations despite the occurrence of longdistance migration. The observation that cooperative breeding is not expected to occur in migratory species because of the disruptive effect of large-scale movements on kinship has been made frequently (Brown 1987; Russell 1989; Cockburn 1996, 1998; Kokko & Lundberg 2001). However, kin-directed cooperative breeding has evolved in migratory bee-eaters (Lessells et al. 1994; Boland 2004), dusky woodswallows Artamus cyanopterus (Sims 2007) and long-tailed tits (B. K. Woodward 2008, personal communication). Indeed, figure 1 illustrates that the natal dispersal distances of migrants overlap considerably with those of resident species. To summarize, the difference between the population viscosity of cooperative and non-cooperative species appears less clear-cut than is generally assumed. In particular, the limited evidence available suggests that there is much overlap in dispersal strategies of non-social species and those social species where helping occurs within kin neighbourhoods. Furthermore, even when dispersal does occur it does not preclude the evolution of kin-directed cooperation. It is also clear that our understanding of the role of dispersal in generating the permissive conditions for the evolution of cooperative breeding is generally poor and would benefit greatly from more systematic study. (b) Life history and demography Life-history traits have been formally included as a potential influence on the evolution of society in the life-history hypothesis (Brown 1987; Arnold & Phil. Trans. R. Soc. B (2009)

Owens 1998). Life-history traits are highly conserved in avian evolution (Owens & Bennett 1995), so the strong phylogenetic signal in cooperative behaviour fits well with this hypothesis. However, the results of comparative analyses are again inconsistent (Yom-Tov et al. 1992; Poiani & Jermiin 1994; Arnold & Owens 1998), although the most extensive of them concluded that low adult mortality was the key factor predisposing certain avian lineages to cooperate (Arnold & Owens 1998). In these comparative studies, consideration of life-history traits as factors influencing the evolution of cooperative breeding has been in the context of population viscosity, and their influence on the rate at which breeding vacancies arise and to which helpers can disperse. Therefore, Hatchwell & Komdeur (2000) argued that the life-history hypothesis is complementary to the ecological constraints hypothesis rather than an alternative, because ecological factors and life-history traits will act in concert to influence dispersal decisions. However, life-history traits and demographic processes might affect the opportunity for cooperation to evolve in ways that have been neglected hitherto. A recent theoretical study indicates that rather than focusing solely on population viscosity, a broader perspective on factors influencing the kin structure of populations would be worthwhile. Beckerman et al. (submitted) used a demographic model to explore the consequences of variation in population size, adult longevity and recruitment, as well as dispersal, on the emergent kin structure of a population. In addition, the model demonstrates that the pattern of offspring mortality plays a critical role in determining the probability of a kin neighbourhood developing among adults. The model is based on the redirected helping system of long-tailed tits and similar species, and formalizes the verbal arguments of Riehm (1970) and Russell (1999). Mortality occurs either at the nestling phase, removing whole families from the pool of potential recruits, or at the post-fledging stage, when individuals rather than whole families will be lost. This simple difference in the timing of offspring mortality has a substantial impact on the size and relatedness of the pool of juveniles from which recruits must be drawn, and hence has a profound effect on the genetic structure of the population in the following year, even when all other variables are held constant. Thus, the kin structure of two populations may be strikingly different even though dispersal does not differ between them. The model can be generalized to predict the combinations of life history and demographic traits that generate kin structure in the absence of variation in dispersal, and the outcome has particular relevance for those cooperative systems where helping occurs within kin neighbourhoods (Beckerman et al. submitted).

6. CONCLUSION In summary, despite several decades of research into cooperatively breeding birds, including some of the most detailed ecological and behavioural studies of any vertebrate species, we are still some way from understanding the evolution of avian societies. In this

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Avian cooperative breeding review, my first aim has been to build on the important compilation of Cockburn (2006) to emphasize the importance of the development of kin associations for the subsequent evolution of cooperation. These associations are not necessarily stable nuclear families, but in a surprisingly large number of taxa are better described as kin neighbourhoods (Dickinson & Hatchwell 2004), often characterized by a more flexible or opportunistic system of helping. Second, I have sought to highlight the deficiencies in our understanding of the key demographic process thought to be responsible for the development of families, i.e. dispersal. Measurement of dispersal is a challenge in both social and non-social systems but it is clear that there is considerable overlap in dispersal strategy between the two, with family-living more common than cooperative breeding, and helping frequently occurring following natal dispersal. Finally, I suggest that consideration of the factors influencing the kin structure of populations, and hence generating the permissive conditions for the evolution of kin-directed cooperation have been too narrowly focused on population viscosity, and that a broader perspective that encompasses life history and demographic processes may provide fresh insights into the circumstances in which avian societies have evolved. My thanks to many colleagues with whom I have had stimulating discussions about cooperative birds and who have influenced my thoughts (although not necessarily in the way they might have wished). In particular, I thank Stuart Sharp, Andrew Beckerman, Andy Russell, Andrew MacColl, Jess Meade, Andrew Cockburn, Rob Magrath, Michael Griesser, Rita Covas and Claire Doutrelant. My research on cooperatively breeding birds has been supported mainly by the Natural Environment Research Council and I was supported by a Leverhulme Research Fellowship during the preparation of this article; I am most grateful to both organizations for their support.

B. J. Hatchwell

Table 1. (Continued.) familya

CB kinb

n

KNc reference

Bucconidae

33

5

1

0

Lybiidae

41 26

1

0

Ramphastidae

48 11

?

?

214 18

1

0

51 20

1

0

Picidae Bucerotidae Bucorvidae

2

2

1

0

Upupidae

2

2

0

0

Phoeniculidae

5

5

1

0

Coraciidae

12

1

?

?

Meropidae

25 20

1

1

1

1

0

59 14

1

0

Cerylidae Dacelonidae

9

Todidae

5

5

?

?

Coliidae

6

6

1

0

140

4

0

0

1

1

1

0

Psittacidae

347 19

?

?

Apodidae

91 12

?

?

Musophagidae

23

5

?

?

3

3

0

0

132 18

1

1

Cuculidae Opisthocomidae

Psophiidae

APPENDIX A Rallidae

Occurrence of kin-based groups and kin neighbourhoods among avian families that contain cooperative species (table 1). Table 1. Avian taxa (family level) containing cooperative species (from Cockburn 2006), showing the number of species in the taxon (n), the number of cooperative species (CB), whether cooperative groups in most of those cooperative species are composed of kin (kin) and whether cooperative species within that taxon includes systems where cooperation occurs within kin neighbourhoods (KN) (Dickinson & Hatchwell 2004). familya

CB kinb

n

KNc reference

Rheidae

2

1

0

0

Apterygidae

5

1

?

?

Anseranatidae

1

1

0

0

18 18

?

?

Galbulidae

del Hoyo et (1992) del Hoyo et (1992) del Hoyo et (1992) del Hoyo et (2002)

Phil. Trans. R. Soc. B (2009)

Rhynchocetidae

1

1

1

0

Mesitornithidae

3

2

1

0

Stercorariidae

8

1

0

0

Charadriidae

65

1

?

?

Haematopodidae

10

1

0

0

Accipitridae

235 14

0

0

Falconidae

62 15

0

0

al.

Scopidae

1

1

?

?

al.

Acanthisittidae

2

1

1

1

al.

Eurylamiidae

15

3

?

?

al.

Thamnophilidae 188

2

?

?

(Continued.)

3223

del Hoyo et al. (2002) del Hoyo et al. (2002) del Hoyo et al. (2002) del Hoyo et al. (2002) del Hoyo et al. (2001) del Hoyo et al. (2001) del Hoyo et al. (2001) del Hoyo et al. 2001 del Hoyo et al. (2001) del Hoyo et al. (2001) del Hoyo et al. (2001) del Hoyo et al. (2001) del Hoyo et al. (2001) del Hoyo et al. (2001) del Hoyo et al. (1997) del Hoyo et al. (1996) del Hoyo et al. (1997) del Hoyo et al. (1999) del Hoyo et al. (1997) del Hoyo et al. (1996) del Hoyo et al. (1996) del Hoyo et al. (1996) del Hoyo et al. (1996) del Hoyo et al. (1996) del Hoyo et al. (1996) del Hoyo et al. (1996) Kimball et al. (2003) Kimball et al. (2003) del Hoyo et al. (1992) del Hoyo et al. (2004) del Hoyo et al. (2003) del Hoyo et al. (2003) (Continued.)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3224

B. J. Hatchwell

Review. Avian cooperative breeding Table 1. (Continued.)

Table 1. (Continued.) familya

n

KNc reference

familya

Furnariidae

213

7

1

0

Cettidae

27

3

?

?

Cotingidae

67

1

?

?

10

4

?

?

337

6

?

?

72 20

—

—

7

5

1

1

Malagasy warblers Passerida incertae sedis Troglodytidae

Tyrannidae

74 16

1

0

28 28

1

0

Sittidae

25

2

1

0

Meliphagidae

174 22

1

1

112 18

1

1

Pardalotidae

67 29

1

1

6

1

1

Muscicapidae

291 23

1

0

Turdidae

143

4

1

1

Promeropidae

4

1

?

?

Nectariniidae

123

3

?

?

13 13

0

0

268 19

1

1

Climacteridae Maluridae

CB kinb

Pomatostomidae

5

5

1

1

Neosittidae

2

2

1

1

53 80

1 5

? 1

? 0

2

2

1

0

28

2

?

?

24 17 101 23

1 1

1 0

Vireonidae Campephagidae Falcunculidae Oriolodae Artamidae Malaconotidae Dicruridae Corcoracidae

23

1

?

?

2

2

1

1

Monarchidae

90

1

1

0

Laniidae

30

6

1

0

116 47

1

1

Corvoidea incertae sedis Picathartidae

24 12

—

—

1

1

0

Petroicidae

43 12

?

?

Paridae

62 20

1

0

Stenostiridae

10

2

1

0

Alaudidae

86

2

?

?

Aegithalidae

10

4

1

1

Pycnonotidae

121 20

?

?

Cisticolidae

116 12

?

?

Timaliidae

385 84

1

1

1

0

Corvidae

Acrocephalidae

3

42

4

del Hoyo et al. (2003) del Hoyo et al. (2004) del Hoyo et al. (2004) del Hoyo et al. (2007) del Hoyo et al. (2007) del Hoyo et al. (2008) del Hoyo et al. (2008) del Hoyo et al. (2007) del Hoyo et al. (2007) Cockburn (2006) del Hoyo et al. (2005) del Hoyo et al. (2007) del Hoyo et al. (2008) Sims (2007) Urban et al. (1997) Thangamani et al. (1981) Heinsohn (2000); A. F. Russell (2009), unpublished data del Hoyo et al. (2006) del Hoyo et al. (2008) Madge & Burn (1994) —d del Hoyo et al. (2007) del Hoyo et al. (2007) del Hoyo et al. (2007) Urban et al. (1997) del Hoyo et al. (2004) del Hoyo et al. (2008) del Hoyo et al. (2005) del Hoyo et al. (2006) del Hoyo et al. (2007) del Hoyo et al. (2006) (Continued.)

Phil. Trans. R. Soc. B (2009)

Sturnidae Mimidae

Prunellidae Ploceidae Passeridae

CB kinb

n

34

KNc reference

36

2

?

?

Fringillidae Passeroidea: Calcarius Emberizidae

159 6

5 1

? 0

? 0

603 53

?

?

Parulidae Icteridae

115 1 96 12

? 1

? 1

del Hoyo et al. (2006) del Hoyo et al. (2006) —d del Hoyo et al. (2005) del Hoyo et al. (2008) Rubenstein & Lovette (2007) del Hoyo et al. (2005) del Hoyo et al. (2005) del Hoyo et al. (2005) del Hoyo et al. (2008) del Hoyo et al. (2008) del Hoyo et al. (2005) Fry & Keith (2004) Fry & Keith (2004) Pratt (2005) Briskie et al. (1998) Alves (1990); Skutch (1987) King et al. (2000) Fraga (1991)

a

Phylogeny and categorization of species as cooperative or non-cooperative followed Cockburn (2006). b Taxa were categorized as having groups composed predominantly of kin (1), non-kin (0) or unknown (?). In most families, species have similar social structures, but where they do not (e.g. Acciptridae and Falconidae), they were assigned to the category most prevalent within the taxon. One taxon, Psittacidae, has several well-described species, but no prevalent classification was possible due to the diversity of social organization. c Taxa with kin-directed cooperation were categorized as having helpers operating within kin neighbourhoods (1) if helpers in at least one species redirected their care to a relative’s brood following failure of their own breeding attempt, or if helping occurred at multiple nests within clans, coteries, etc. If taxa were composed of species in which cooperative groups were not kin-based or helping occurred only within stable nuclear family groups, they were categorized as not having kin neighbourhoods (0). d Taxa of uncertain affinity were not assigned family-level characteristics.

REFERENCES Alves, M. A. S. 1990 Social system and helping behaviour of the white-banded tanager (Neothraupis fasciata). Condor 92, 470–474. (doi:10.2307/1368243) Arcese, P. 1989 Intrasexual competition, mating system, and natal dispersal in song sparrows. Anim. Behav. 38, 958 –979. (doi:10.1016/S0003-3472(89)80137-X) Arnold, K. E. & Owens, I. P. F. 1998 Cooperative breeding in birds: a comparative test of the life history hypothesis. Proc. R. Soc. Lond. B 265, 739 –945. (doi:10.1098/rspb. 1998.0355)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Avian cooperative breeding Arnold, K. E. & Owens, I. P. F. 1999 Cooperative breeding in birds: the role of ecology. Behav. Ecol. 10, 465–471. (doi:10.1093/beheco/10.5.465) Beck, N. R., Peakall, R. & Heinsohn, R. 2008 Social constraint and an absence of sex-biased dispersal drive fine-scale genetic structure in white-winged choughs. Mol. Ecol. 17, 4346–4358. (doi:10.1111/j.1365-294X.2008.03906.x) Beckerman, A. P., Sharp, S. P. & Hatchwell, B. J. Submitted. Demography, life history and the emergence of kin-structured populations. Boland, C. R. J. 2004 Breeding biology of rainbow bee-eaters (Merops ornatus): a migratory, colonial, cooperative bird. Auk 121, 811 –823. (doi:10.1642/ 0004-8038(2004)121[0811:BBORBM]2.0.CO;2) Brown, J. L. 1969 Territorial behavior and population regulation in birds. Wilson Bull. 81, 293 –329. Brown, J. L. 1974 Alternate routes to sociality in jays with a theory for the evolution of altruism and communal breeding. Am. Zool. 14, 63–80. Brown, J. L. 1987 Helping and communal breeding in birds. Princeton, NJ: Princeton University Press. Briskie, J. V., Montgomerie, R., Poldmaa, T. & Boag, P. T. 1998 Paternity and paternal care in the polygynandrous Smith’s longspur. Behav. Ecol. Sociobiol. 43, 181 –190. Clarke, M. F. & Fitz-Gerald, G. F. 1994 Spatial organisation of the cooperatively breeding bell miner Manorina melanophrys. Emu 94, 96– 105. Clobert, J., Danchin, E., Dhondt, A. A. & Nichols, J. D. 2001 Dispersal. Oxford, UK: Oxford University Press. Clutton-Brock, T. H. 2002 Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69– 72. (doi:10.1126/science.296.5565.69) Cockburn, A. 1996 Why do so many Australian birds cooperate: social evolution in the Corvida? In Frontiers of population ecology (eds R. B. Floyd, A. W. Shepherd & P. J. D. Barro), pp. 451–472. Melbourne, Australia: CSIRO Publishing. Cockburn, A. 1998 Evolution of helping behavior in cooperatively breeding birds. Annu. Rev. Ecol. Syst. 29, 141 –177. (doi:10.1146/annurev.ecolsys.29.1.141) Cockburn, A. 2004 Mating systems and sexual conflict. In Cooperative breeding in birds (eds W. D. Koenig & J. L. Dickinson), pp. 81–101. Cambridge, UK: Cambridge University Press. Cockburn, A. 2006 Prevalence of different modes of parental care in birds. Proc. R. Soc. B 273, 1375–1383. (doi:10. 1098/rspb.2005.3458) Covas, R. & Griesser, M. 2007 Life history and the evolution of family living in birds. Proc. R. Soc. B 274, 1349–1357. (doi:10.1098/rspb.2007.0117) Covas, R., Doutrelant, C. & DuPlessis, M. A. 2004 Experimental evidence of a link between breeding conditions and the decision to breed or to help in a colonial cooperative breeder. Proc. R. Soc. Lond. B 271, 827 –831. (doi:10.1098/rspb.2003.2652) Covas, R., Dalecky, A., Caizergues, A. & Doutrelant, C. 2006 Kin associations and direct vs indirect fitness benefits in colonial cooperatively breeding sociable weavers Philetairus socius. Behav. Ecol. Sociobiol. 60, 323 –331. (doi:10.1007/s00265-006-0168-2) Darwin, C. 1859 On the origin of species. London, UK: John Murray. Davies, N. B. 1992 Dunnock behaviour and social evolution. Oxford, UK: Oxford University Press. del Hoyo, J., Elliott, A. & Sargatal, J. 1992 Handbook of the birds of the world, vol. 1. Barcelona, Spain: Lynx Edicions. del Hoyo, J., Elliott, A. & Sargatal, J. 1996 Handbook of the birds of the world, vol. 3. Barcelona, Spain: Lynx Edicions. del Hoyo, J., Elliott, A. & Sargatal, J. 1997 Handbook of the birds of the world vol. 4 Barcelona, Spain: Lynx Edicions. del Hoyo, J., Elliott, A. & Sargatal, J. 1999 Handbook of the birds of the world vol. 5 Barcelona, Spain: Lynx Edicions. Phil. Trans. R. Soc. B (2009)

B. J. Hatchwell

3225

del Hoyo, J., Elliott, A. & Sargatal, J. 2001 Handbook of the birds of the world, vol. 6. Barcelona, Spain: Lynx Edicions. del Hoyo, J., Elliott, A. & Sargatal, J. 2002 Handbook of the birds of the world, vol. 7. Barcelona, Spain: Lynx Edicions. del Hoyo, J., Elliott, A. & Sargatal, J. 2003 Handbook of the birds of the world, vol. 8 Barcelona, Spain: Lynx Edicions. del Hoyo, J., Elliott, A. & Sargatal, J. 2004 Handbook of the birds of the world, vol. 9 Barcelona, Spain: Lynx Edicions. del Hoyo, J., Elliott, A. & Christie, D. A. 2005 Handbook of the birds of the world, vol. 10 Barcelona, Spain: Lynx Edicions. del Hoyo, J., Elliott, A. & Sargatal, J. 2006 Handbook of the birds of the world, vol. 11. Barcelona, Spain: Lynx Edicions. del Hoyo, J., Elliott, A. & Christie, D. A. 2007 Handbook of the birds of the world, vol. 12. Barcelona, Spain: Lynx Edicions. del Hoyo, J., Elliott, A. & Christie, D. A. 2008 Handbook of the birds of the world, vol. 13. Barcelona, Spain: Lynx Edicions. Dickinson, J. L. & Hatchwell, B. J. 2004 The fitness consequences of helping. In Cooperative breeding in birds (eds W. D. Koenig & J. L. Dickinson), pp. 48–66. Cambridge, UK: Cambridge University Press. Dickinson, J. L., Koenig, W. D. & Pitelka, F. A. 1996 The fitness consequences of helping behavior in the western bluebird. Behav. Ecol. 7, 168 –177. (doi:10.1093/ beheco/7.2.168) Double, M. C., Peakall, R., Beck, N. R. & Cockburn, A. 2005 Dispersal, philopatry and infidelity: dissecting local genetic structure in superb fairy-wrens Malurus cyaneus. Evolution 59, 625 –635. DuPlessis, M. A., Siegfried, W. R. & Armstrong, A. J. 1995 Ecological and life history correlates of cooperative breeding in South African birds. Oecologia 102, 180 –188. Eden, S. F. 1987 Natal philopatry of the magpie Pica pica. Ibis 129, 477 –490. Edwards, S. V. & Naeem, S. 1993 The phylogenetic component of cooperative breeding in perching birds. Am. Nat. 141, 754–789. (doi:10.1086/285504) Ekman, J., Baglione, V., Eggers, S. & Griesser, M. 2001 Delayed dispersal: living under the reign of nepotistic parents. Auk 118, 1–10. (doi:10.1642/00048038(2001)118[0001:DDLUTR]2.0.CO;2) Ekman, J., Dickinson, J. L., Hatchwell, B. J. & Griesser, M. 2004 Delayed dispersal. In Cooperative breeding in birds (eds W. D. Koenig & J. L. Dickinson), pp. 35–47. Cambridge, UK: Cambridge University Press. Emlen, S. T. 1982 The evolution of helping. I. An ecological constraints model. Am. Nat. 119, 29–39. (doi:10.1086/ 283888) Emlen, S. T. 1984 Cooperative breeding in birds and mammals. In Behavioural ecology: an evolutionary approach (eds J. R. Krebs & N. B. Davies), pp. 305– 339. Sunderland, MA: Sinauer. Emlen, S. T. 1994 Benefits, constraints and the evolution of the family. Trends Ecol. Evol. 9, 282 –285. (doi:10.1016/ 0169-5347(94)90030-2) Emlen, S. T. & Oring, L. W. 1977 Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223. (doi:10.1126/science.327542) Emlen, S. T. & Wrege, P. H. 1991 Breeding biology of whitefronted bee-eaters at Nakuru: the influence of helpers on breeder fitness. J. Anim. Ecol. 60, 309 –326. Emlen, S. T. & Wrege, P. H. 1992 Parent –offspring conflict and the recruitment of helpers among bee-eaters. Nature 356, 331–333. (doi:10.1038/356331a0) Foerster, K., Valcu, M., Johnsen, A. & Kempenaers, B. 2006 A spatial genetic structure and effects of relatedness on mate choice in a wild bird population. Mol. Ecol. 15, 4555–4567. (doi:10.1111/j.1365-294X.2006. 03091.x)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3226

B. J. Hatchwell

Review. Avian cooperative breeding

Ford, H. A., Bell, H., Nias, R. & Noske, R. 1988 The relationship between ecology and the incidence of cooperative breeding in Australian birds. Behav. Ecol. Sociobiol. 22, 239 –249. (doi:10.1007/BF00299838) Fraga, R. M. 1991 The social system of a communal breeder, the bay-winged cowbird Molothrus badius. Ethology 89, 195 –210. Friesen, V. L., Montevecchi, W. A., Gaston, A. J., Barrett, R. T. & Davidson, W. S. 1996 Molecular evidence for kin groups in the absence of large scale genetic differentiation in a migratory bird. Evolution 50, 924 –930. (doi:10.2307/2410865) Fry, C. H. & Keith, S. 2004 The birds of Africa, vol. VII. London, UK: Christopher Helm. Gardner, A. & West, S. A. 2006 Demography, altruism and the benefits of budding. J. Evol. Biol. 19, 1707–1716. (doi:10.1111/j.1420-9101.2006.01104.x) Griffin, A. S. & West, S. A. 2002 Kin selection: fact and fiction. Trends Ecol. Evol. 17, 15–21. (doi:10.1016/ S0169-5347(01)02355-2) Hackett, S. J. et al. 2008 A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768. (doi:10.1126/science.1157704) Hamilton, W. D. 1964 The genetical evolution of social behavior I & II. J. Theor. Biol. 7, 1–52. (doi:10.1016/ 0022-5193(64)90038-4) Hartley, I. R. & Davies, N. B. 1994 Limits to cooperative polyandry in birds. Proc. R. Soc. Lond. B 257, 67– 73. (doi:10.1098/rspb.1994.0095) Hatchwell, B. J. 2007 Avian reproduction: role of ecology in the evolution of cooperative breeding. Curr. Biol. 17, R845 –R847. (doi:10.1016/j.cub.2007.08.004) Hatchwell, B. J. & Komdeur, J. 2000 Ecological constraints, life history traits and the evolution of cooperative breeding. Anim. Behav. 59, 1079–1086. (doi:10.1006/anbe.2000.1394) Hatchwell, B. J. & Sharp, S. P. 2006 Kin selection, constraints and the evolution of cooperative breeding in long-tailed tits. Adv. Stud. Behav. 36, 355 –395. (doi:10. 1016/S0065-3454(06)36008-1) Heinsohn, R. G. 1992 Cooperative enhancement of reproductive success in white-winged chough. Evol. Ecol. 6, 97–114. (doi:10.1007/BF02270705) Heinsohn, R. G., Dunn, P., Legge, S. & Double, M. C. 2000 Coalitions of relatives and reproductive skew in cooperatively breeding white-winged chough. Proc. R. Soc. Lond. B 267, 243 –249. Hoglund, J., Alatalo, R. V., Lundberg, A., Rintakmaki, P. T. & Lindell, J. 1999 Microsatellite markers reveal the potential kin selection on black grouse leks. Proc. R. Soc. Lond. B 266, 813–816. Kimball, R. T., Parker, P. G. & Bednarz, J. C. 2003 Occurrence and evolution of cooperative breeding among the diurnal raptors (Accipitridae and Falconidae). Auk 120, 712 –729. King, D. I., Champlin, T. B. & Champlin, P. J. 2000 An observation of cooperative breeding in the ovenbird. Wilson Bull. 112, 382 –384. Koenig, W. D. & Haydock, J. 2004 Incest and incest avoidance. In Cooperative breeding in birds (eds W. D. Koenig & J. L. Dickinson), pp. 142–156. Cambridge, UK: Cambridge University Press. Koenig, W. D. & Pitelka, F. A. 1981 Ecological factors and kin selection in the evolution of cooperative breeding in birds. In Natural selection and social behaviour (eds R. D. Alexander & D. W. Tinkle), pp. 261–280. New York, USA: Chiron Press. Koenig, W. D., Pitelka, F. A., Carmen, W. J., Mumme, R. L. & Stanback, M. T. 1992 The evolution of delayed dispersal in cooperative breeders. Q. Rev. Biol. 67, 111 –150. (doi:10.1086/417552) Phil. Trans. R. Soc. B (2009)

Koenig, W. D., VanVuren, D. & Hooge, P. N. 1996 Detectability, philopatry and the distribution of dispersal distances in vertebrates. Trends Ecol. Evol. 11, 514–517. (doi:10.1016/S0169-5347(96)20074-6) Koenig, W. D., Haydock, J. & Stanback, M. T. 1998 Reproductive roles in the cooperatively breeding acorn woodpecker: incest avoidance versus reproductive competition. Am. Nat. 151, 243– 255. (doi:10.1086/286115) Koenig, W. D., Hooge, P. N., Stanback, M. T. & Haydock, J. 2000 Natal dispersal in the cooperatively breeding acorn woodpecker. Condor 102, 492 –502. (doi:10.1650/00105422(2000)102[0492:NDITCB]2.0.CO;2) Kokko, H. & Lundberg, P. 2001 Dispersal, migration and offspring retention in saturated habitats. Am. Nat. 157, 188 –202. (doi:10.1086/318632) Komdeur, J. 1992 Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358, 493 –495. (doi:10.1038/ 358493a0) Komdeur, J. & Hatchwell, B. J. 1999 Kin recognition: function and mechanism in avian societies. Trends Ecol. Evol. 14, 237–241. (doi:10.1016/S0169-5347(98)01573-0) Komdeur, J., Richardson, D. S. & Hatchwell, B. J. 2008 Kin recognition mechanisms in cooperative breeding systems: ecological causes and behavioural consequences of variation. In Ecology of social evolution (eds J. Korb & J. Heinze), pp. 175– 193. Berlin, Germany: SpringerVerlag. Lessells, C. M., Avery, M. I. & Krebs, J. R. 1994 Nonrandom dispersal of kin: why do European bee-eater (Merops apiaster) brothers nest close together? Behav. Ecol. 5, 105– 113. (doi:10.1093/beheco/5.1.105) Ligon, J. D. & Burt, D. B. 2004 Evolutionary origins. In Cooperative breeding in birds (eds W. D. Koenig & J. L. Dickinson), pp. 5–34. Cambridge, UK: Cambridge University Press. Ligon, J. D. & Stacey, P. B. 1991 The origin and maintenance of helping in birds. Am. Nat. 138, 254 –258. (doi:10.1086/285215) MacColl, A. D. C. & Hatchwell, B. J. 2002 Temporal variation in fitness payoffs promotes cooperative breeding in long-tailed tits Aegithalos caudatus. Am. Nat. 160, 186 –194. (doi:10.1086/341013) MacColl, A. D. C. & Hatchwell, B. J. 2004 Determinants of lifetime fitness in a cooperative breeder, the long-tailed tit Aegithalos caudatus. J. Anim. Ecol. 73, 1137 –1148. (doi:10.1111/j.0021-8790.2004.00887.x) Madge, S. & Burn, H. 1994 Crows and jays: a guide to crows, jays and magpies of the world. London, UK: Christopher Helm. Matthysen, E., Van de Casteele, T. & Adriaensen, F. 2005 Do sibling tits (Parus major, P. caeruleus) disperse over similar distances ad in similar directions? Oecologia 143, 301 –307. (doi:10.1007/s00442-004-1760-7) Nathan, R. 2001 The challenges of studying dispersal. Trends Ecol. Evol. 16, 481 –483. (doi:10.1016/S01695347(01)02272-8) Owens, I. P. F. & Bennett, P. M. 1995 Ancient ecological diversification explains life-history variation among living birds. Proc. R. Soc. Lond. B 261, 227–232. (doi:10.1098/rspb.1995.0141) Painter, J. N., Crozier, R. H., Poiani, A., Robertson, R. J. & Clarke, M. F. 2000 Complex social organization reflects genetic structure and relatedness in the cooperatively breeding bell miner Manorina melanophrys. Mol. Ecol. 9, 1339–1347. (doi:10.1046/j.1365-294x.2000. 01012.x) Paradis, E., Baillie, S. R., Sutherland, W. J. & Gregory, R. D. 1998 Patterns of natal and breeding dispersal in birds. J. Anim. Ecol. 67, 518–536. (doi:10.1046/j.1365-2656. 1998.00215.x)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Avian cooperative breeding Perrin, N. & Goudet, J. 2001 Inbreeding, kinship, and the evolution of natal dispersal. In Dispersal (eds J. Clobert, E. Danchin, A. A. Dhondt & J. D. Nichols), pp. 123–142. Oxford, UK: Oxford University Press. Peterson, A. T. & Burt, D. B. 1992 Phylogenetic history of social evolution and habitat use in Apehlocoma jays. Anim. Behav. 32, 861–870. Piertney, S. B. et al. 2008 Temporal changes in kin structure through a population cycle in a territorial bird, the red grouse Lagopus lagopus scoticus. Mol. Ecol. 17, 2544– 2551. (doi:10.1111/j.1365-294X.2008.03778.x) Poiani, A. & Jermiin, L. S. 1994 A comparative analysis of some life-history traits between cooperatively and noncooperatively breeding Australian passerines. Evol. Ecol. 8, 471 –488. (doi:10.1007/BF01238252) Pratt, H. D. 2005 The Hawaiian honeycreepers: Drepanidinae. Oxford, UK: Oxford University Press. Pruett-Jones, S. G. & Lewis, M. J. 1990 Sex ratio and habitat limitation promote delayed dispersal in superb fairy-wrens. Nature 348, 541 –542. (doi:10.1038/ 348541a0) Ricklefs, R. E. & Starck, J. M. 1998 The evolution of development mode in birds. In Avian growth and development: evolution within the altricial-precocial spectrum (eds J. M. Starck & R. E. Ricklefs), pp. 366 –380. Oxford, UK: Oxford University Press. ¨ kologie und Verhalten der Schwanzmeise Riehm, H. 1970 O (Aegithalos caudatus). Zool. Jahr. Syst. 97, 338 –400. Rubenstein, D. R. & Lovette, I. J. 2007 Temporal environmental variability drives the evolution of cooperative breeding in birds. Curr. Biol. 17, 1414 –1419. (doi:10. 1016/j.cub.2007.07.032) Russell, E. M. 1989 Co-operative breeding: a Gondwanan perspective. Emu 89, 61–62. Russell, A. F. 1999 Ecological constraints and the cooperative breeding system of the long-tailed tit Aegithalos caudatus. PhD thesis, University of Sheffield, UK. Russell, A. F. 2001 Dispersal costs set the scene for helping in an atypical avian cooperative breeder. Proc. R. Soc. Lond. B 268, 95– 99. (doi:10.1098/rspb. 2000.1335) Selander, R. K. 1964 Speciation in wrens of the genus Campylorhynchus. Univ. Calif. Publ. Zool. 74, 1 –224. Sharp, S. P., Hadfield, J., Baker, M. B., Simeoni, M. & Hatchwell, B. J. 2008 Natal dispersal and recruitment in a social bird. Oikos 117, 1371– 1379. (doi:10.1111/j. 0030-1299.2008.16392.x) Sharp, S. P., Simeoni, M. & Hatchwell, B. J. 2008 Dispersal of sibling coalitions promotes helping among immigrants in a cooperatively breeding bird. Proc. R. Soc. B 275, 2125– 2130. (doi:10.1098/rspb.2008.0398) Shorey, L., Piertney, S., Stone, J. & Hoglund, J. 2000 Fine scale genetic structuring on Manacus manacus leks. Nature 408, 352–353. (doi:10.1038/35042562) Shutler, D. & Clark, R. G. 2003 Causes and consequences of tree swallow (Tachycineta bicolor) dispersal in

Phil. Trans. R. Soc. B (2009)

B. J. Hatchwell

3227

Saskatchewan. Auk 120, 619 –631. (doi:10.1642/00048038(2003)120[0619:CACOTS]2.0.CO;2) Shy, M. M. 1982 Interspecific feeding among birds: a review. J. Field Ornithol. 53, 370–393. Sims, R. A. 2007 Ecology of cooperative breeding in the colonial nesting and migratory dusky woodswallow. PhD thesis, Australian National University, Canberra. Skutch, A. F. 1987 Helpers a birds’ nests. Iowa City, IA: University of Iowa Press. Stacey, P. B. & Koenig, W. D. 1990 Cooperative breeding in birds: long-term studies of ecology and behaviour. Cambridge, UK: Cambridge University Press. Stacey, P. B. & Ligon, J. D. 1987 Territory quality and dispersal options in the acorn woodpecker, and a challenge to the habitat saturation model of cooperative breeding. Am. Nat. 130, 654–676. (doi:10.1086/284737) Stacey, P. B. & Ligon, J. D. 1991 The benefits of philopatry hypothesis for the evolution of cooperative breeding: variance in territory quality and group size effects. Am. Nat. 137, 831–846. (doi:10.1086/285196) Szulkin, M. & Sheldon, B. C. 2008 Dispersal as a means of inbreeding avoidance in a wild bird population. Proc. R. Soc. B 275, 703 –711. (doi:10.1098/rspb.2007. 0989) Temple, H. J., Hoffman, J. I. & Amos, W. 2006 Dispersal, philopatry and intergroup relatedness: fine-scale genetic structure in the white-breasted thrasher Ramphocinclus rachyurus. Mol. Ecol. 15, 3449–3458. (doi:10.1111/j. 1365-294X.2006.03006.x) Thangamani, A., Paramanandham, K. & Johnsingh, A. J. T. 1981 ‘Helpers’ among the black drongo (Dicrurus adsimilis). J. Bombay Nat. Hist. Soc. 78, 602 –603. Urban, E. K., Fry, C. H. & Keith, S. 1997 The birds of Africa, vol. V. London, UK: Academic Press. Verbeek, N. A. M. 1973 The exploitation system of the yellow-billed magpie. Univ. Calif. Publ. Zool. 99, 1– 58. Walters, J. R., Copeyon, C. K. & Carter, J. H. 1992 Test of the ecological basis of cooperative breeding in redcockaded woodpeckers. Auk 109, 90– 97. West, S. A., Griffin, A. S. & Gardner, A. 2007 Evolutionary explanations for cooperation. Curr. Biol. 17, R661 –R672. (doi:10.1016/j.cub.2007.06.004) Williams, D. A. & Rabenold, K. N. 2005 Male-biased dispersal, female philopatry and routes to fitness in a social corvid. J. Anim. Ecol. 74, 150– 159. (doi:10.1111/j. 1365-2656.2004.00907.x) Woxvold, I. A., Adcock, G. J. & Mulder, R. A. 2006 Fine-scale genetic structure and dispersal in cooperatively breeding apostlebirds. Mol. Ecol. 15, 3139–3146. (doi:10. 1111/j.1365-294X.2006.03009.x) Yom-Tov, Y., McCleery, R. & Purchase, D. 1992 The survival rate of Australian passerines. Ibis 134, 374 –379. (doi:10.1111/j.1474-919X.1992.tb08017.x) Zack, S. 1990 Coupling delayed breeding with short distance dispersal in cooperatively breeding birds. Ethology 86, 265–286.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3229–3242 doi:10.1098/rstb.2009.0120

Review

Structure and function in mammalian societies Tim Clutton-Brock* Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK Traditional interpretations of the evolution of animal societies have suggested that their structure is a consequence of attempts by individuals to maximize their inclusive fitness within constraints imposed by their social and physical environments. In contrast, some recent re-interpretations have argued that many aspects of social organization should be interpreted as group-level adaptations maintained by selection operating between groups or populations. Here, I review our current understanding of the evolution of mammalian societies, focusing, in particular, on the evolution of reproductive strategies in societies where one dominant female monopolizes reproduction in each group and her offspring are reared by other group members. Recent studies of the life histories of females in these species show that dispersing females often have little chance of establishing new breeding groups and so are likely to maximize their inclusive fitness by helping related dominants to rear their offspring. As in eusocial insects, increasing group size can lead to a progressive divergence in the selection pressures operating on breeders and helpers and to increasing specialization in their behaviour and life histories. As yet, there is little need to invoke group-level adaptations in order to account for the behaviour of individuals or the structure of mammalian groups. Keywords: societies; evolution; mammals; cooperation; reproductive strategies; life-histories

1. INTRODUCTION Early attempts to explain the evolution of animal and human societies argued that their structure has important functions for the lives of individuals (Kropotkin 1908; Richards 1939; Radcliffe Brown 1952; Wynne-Edwards 1962; Gartlan 1968). In contrast, most modern interpretations of the evolution of animal societies have focused on the evolution of reproductive strategies in individuals and have interpreted variation in the structure of societies (including contrasts in the size and structure of groups, in patterns of interaction between group members and in the form of mating systems) as byproducts of the evolution of individual strategies (Crook et al. 1976; Clutton-Brock 1989c; Krebs & Davies 1993; Kitchen & Packer 1999). Over the last 50 years, this approach has led to dramatic developments in our understanding of the evolution of parental investment (Trivers 1972), fighting strategies (Parker 1974), mate choice (Andersson 1994), nepotism (Hamilton 1964; Emlen 1991) and cooperation (Dugatkin 1997; Nowak 2006), which, in turn, have provided a framework for explaining species differences in the size, age, sex and kinship structure of groups, in the contribution of females and males to parental care and in the structuring of interactions between individuals

*[email protected] One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

(Jarman 1974; Bradbury & Vehrencamp 1976, 1977; Clutton-Brock & Harvey 1977; Wrangham 1980; Rood 1986; Clutton-Brock 1989c). In this paper, I briefly review our understanding of the evolution of mammalian societies. As polygynous breeding systems are common among mammals while cooperative societies are rare, I initially review our understanding of polygynous societies, which are often characterized by intense competition between males. Subsequently, I focus on societies where young are raised primarily by non-breeding group members and reproductive competition between females is intense. Though these societies occur in a small proportion of social mammals, the evolution of non-breeding helpers provides an important challenge to our understanding of social evolution and mammals include the most specialized cooperative breeding systems found among vertebrates (Alexander et al. 1991; Sherman et al. 1991; Clutton-Brock 2006). A review of the evolution of cooperative societies is timely since recent re-evaluations of the role of group selection have suggested that many cooperative activities and aspects of group structure in social mammals represent group-level adaptations rather than by-products of the adaptive strategies of individuals (Wilson & Wilson 2007). In the final discussion, I briefly compare the cooperative breeding systems of mammals with those of birds and social insects and reassess arguments that cooperative societies should be interpreted as group-level adaptations.

3229

This journal is # 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

T. Clutton-Brock

Review. Mammalian societies

2. THE EVOLUTION OF MAMMALIAN POLYGYNY In many mammals, females either form unstable groups or herds consisting primarily of unrelated individuals or live in stable groups consisting primarily of matrilineal relatives (Clutton-Brock 1989c). In addition, in a small number of species, females normally disperse from their natal group at adolescence and (as in many group-living birds) stable groups consist of several unrelated females defended by one or more males (Clutton-Brock 1989b). Where females live in stable groups with matrilineal relatives, group members often cooperate to defend feeding or breeding territories, though non-territorial groups of related females are also common, especially in large, wideranging species. The benefits of aggregation to females vary between species, but include improved detection of and defence against predators, benefits associated with social foraging or hunting and advantages in competition with neighbouring groups (Bertram 1978; Clutton-Brock & Harvey 1978; Wrangham 1980; Van Schaik 1983). In addition, in a small number of species where females form stable groups with matrilineal relatives, they cooperate to rear young (see below). The fundamental structure of female groups and the distribution of cooperative behaviour in mammals consequently show many parallels with the structure of groups in social insects (Boomsma 2007, 2009; Helantera¨ & Bargum 2007). In contrast, in most birds, breeding females form breeding pairs with a single male, often defending nest sites or feeding territories against other females (Lack 1968). While colonies are common in species where food supplies cannot be economically defended, they are typically open aggregations of unstable membership, consisting of multiple socially monogamous pairs (Lack 1968). In bird species where females form stable groups and share access to a group range or territory, one female usually monopolizes reproduction, her female offspring typically disperse at adolescence (so that female group members are seldom close relatives), and cooperation between females is seldom highly developed (Greenwood 1980; Koenig & Haydock 2004). The likely reason why female mammals more commonly form stable groups that include multiple breeding females than birds is that many mammals are able to feed largely or exclusively on vegetable matter whose relative abundance frees females from dependence on male assistance in rearing young and permits local population densities and biomass to reach higher levels than in birds (figure 1). As might be expected, monogamous breeding systems and dispersal of adolescent females are both relatively common in carnivorous mammals (Kleiman 1977; Gittleman 1989) while their population density is relatively low (McNab 1980). The frequent aggregation of female mammals in stable groups combined with their capacity to rear young independently allows individual males to guard multiple mating partners, leading to the evolution of pre-copulatory mate guarding and polygynous mating systems. Variation in the size, stability and ranging patterns of female groups affect the defensibility of females by males and the degree of polygyny and consequently affect variance in male reproductive success, the Phil. Trans. R. Soc. B (2009)

3.5 3.0 log average population density (n per square kilometre)

3230

2.5 2.0 1.5 1.0 0.5 0 –0.5 0

1

2 3 4 5 6 log average body mass (g)

7

8

Figure 1. Variation in population density of North American birds (open circles) and mammals (filled squares) of different body mass (adapted from Silva et al. 1997).

strength of selection pressures favouring characteristics influencing competitive success in males (such as body size or weapon development) and the evolution of sex differences in behaviour, physiology and anatomy (Bradbury & Vehrencamp 1977; Wade & Arnold 1980; Clutton-Brock 1983, 1989c; Clutton-Brock et al. 1993). In many mammals, intense competition combined with the limited ability of females to evade persistent males has favoured the evolution of coercive strategies and male infanticide (Hrdy 1977; Smuts & Smuts 1993; Clutton-Brock & Parker 1995; Ebensperger 1998a; Van Schaik 2000) with important consequences both for female mating preferences (Ebensperger 1998b; Clutton-Brock & McAuliffe 2009) and for associated selection pressures on the reproductive anatomy of males (Harcourt et al. 1981). Intense competition between males in polygynous mammals and associated adaptations, such as increased male body mass, generate energetic costs and increase the risk of injury: in highly polygynous species, adult males are commonly more susceptible to starvation than females, have higher annual rates of mortality than females, age more quickly and die at younger ages (Trivers 1972; Clutton-Brock et al. 1982b, 1985; Clutton-Brock & Isvaran 2007; Donald 2007). One important consequence of the relatively short breeding lifespans of males in polygynous species is that, in many societies, relatively few females reach breeding age in groups where their father still monopolizes access to receptive females, so that females can remain and breed in their natal group without risking inbreeding, allowing the development of kin-based female groups (Clutton-Brock 1989a). In contrast, in vertebrates where males have breeding lifespans that are typically longer than the age of females at first breeding (including a few social mammals and many groupliving birds), females frequently reach maturity while their father is still reproductively active and typically disperse at adolescence (Clutton-Brock 1989c), so that

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Mammalian societies adult female group members are usually unrelated to each other (Greenwood 1980; Clarke et al. 1997). 3. REPRODUCTIVE COMPETITION BETWEEN FEMALES Since Darwin’s time, the intensity of male competition and the evolution of striking secondary sexual characters in males initially focused the attention of biologists on the evolution of male strategies and traits (Darwin 1871/1958; Andersson 1994). Only more recently has it come to be appreciated that life in stable social groups also generates intense reproductive competition and large individual differences in female breeding success which can have far-reaching consequences for selection pressures operating on both sexes, for the evolution of life histories and reproductive strategies and for the structure of societies (Hauber & Lacey 2005; Clutton-Brock et al. 2006; Clutton-Brock 2007, 2009). As local populations approach the carrying capacity, female group members compete for resources, and frequent interactions between the same individuals commonly generate dominance hierarchies where the status of individuals is associated with consistent differences in resource access, fecundity and rearing success (Clutton-Brock et al. 1982a, 1984; Walters & Seyfarth 1986; Holekamp & Swale 2000). However, females do not show obvious hierarchies in all social species: for example, there is little evidence of consistent differences in social status among African lions (Panthera leo) and individual differences in reproductive success are small (Packer et al. 2001). Where female groups are sufficiently large that they include females belonging to more than one matriline, female relatives commonly support each other and are intolerant of offspring born to subordinate matrilines, who often show relatively low survival (Silk et al. 1981; Holekamp et al. 1996). In some macaques, dominant females even focus their aggression on female juveniles born to subordinate mothers who, unlike males, will remain in the group and so represent potential competitors for their own offspring (Dittus 1979; Silk et al. 1981). In a substantial number of mammalian societies, females direct regular aggression against other breeding females and commonly attempt to interfere directly with their breeding attempts, killing their young when opportunity arises (Ebensperger 1998a; Digby 2000) and (Ebensperger 1998a; Digby 2000; CluttonBrock 2009). As groups typically consist of matrilineal relatives, competitors are usually kin but proximity of kinship appears to have little effect on the probability of infanticidal behaviour, which is typically directed at likely competitors, however closely they are related (Hoogland 1995). In extreme cases, competition between females can lead to situations where only one female per group breeds regularly and, as in most eusocial insects, many females never breed successfully at any stage of their lifespan (Creel & Waser 1997; Faulkes & Abbott 1997; Creel & Creel 2001; Hauber & Lacey 2005; Clutton-Brock et al. 2006). 4. REPRODUCTIVE SUPPRESSION While occasional cooperation occurs in many social mammals, cooperative breeding systems (where young Phil. Trans. R. Soc. B (2009)

T. Clutton-Brock

3231

born to one or more breeding females in each group are reared by non-breeding helpers) are rare and are most highly developed in four groups: the marmosets and tamarins (Callitrichidae) (Goldizen 1987a,b; Digby et al. 2007); the dogs (Canidae) (Moehlman 1986; Creel & Creel 2001); diurnal mongooses (Herpestidae) (Rood 1986; Creel & Waser 1997; Clutton-Brock 2006) and African mole-rats (Bathyergidae) (Bennett & Faulkes 2000; Faulkes & Bennett 2007). Cooperative systems in these four groups range from species living in monogamous pairs, occasionally assisted by one or two young from the previous breeding season where parents are responsible for a high proportion of parental care, as in silver-backed jackals (Canis mesomelas; Moehlman 1986) to naked mole-rats (Heterocephalus glaber), where groups can consist of more than 100 individuals. These groups include a single breeding male and a single breeding female, who are unable to rear young successfully without helpers (Sherman et al. 1991), and breeding females share a number of traits with queens in social insects, including enhanced body size, dominance over all other colony members and unusually long lifespans (Braude 1991; Brett 1991; Sherman et al. 1991; Sherman & Jarvis 2002; Faulkes & Bennett 2007). The kinship structure of breeding groups varies widely. In some species, breeding females and helpers of both sexes have usually been born in the group while breeding males are immigrants (meerkats, Suricata suricatta, Damaraland mole-rats, Cryptomys damarensis); in others, breeding females are typically immigrants while breeding males have often been born in the group (African wild dogs, Lycaon pictus, some marmosets); in some, breeders of either sex may either be immigrants or natals (marmosets and tamarins, banded mongooses, Mungos mungo) and in a few, breeders of both sexes are usually natals (naked mole-rats). As in birds (Bennett & Owens 2002; Blumstein & Møller 2008), there are no simple associations in mammals between cooperative breeding and diet or habitat; in mammals, cooperative breeders include herbivores (the mole-rats), frugivores and gumivores (the callitrichid primates), insectivores (the mongooses) and carnivores (the canids) (Clutton-Brock 2006). The likely benefits of sociality and cooperation vary between groups, ranging from the maintenance of extensive tunnel systems in mole-rats, improved hunting success in the larger canids, transport of dependent offspring in the callitrichids and cooperative detection of predators and defence in the diurnal mongooses (Clutton-Brock 2006). In many cooperative mammals, dominant females routinely evict subordinate females, though the age at which dominants evict subordinates varies with important consequences for the age structure and size of groups. In the callitrichid primates and the smaller canids, resident breeding females are usually intolerant of other adult females, who are either evicted or disperse voluntarily. As a result, groups commonly contain a single fully adult female and a variable number of males, which may include a mixture of natals and immigrants (Moehlman & Hofer 1997; Creel & Creel 2001; Goldizen 2003; Digby et al. 2007). In meerkats, which live in larger groups,

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

T. Clutton-Brock

probability of being evicted

(a)

Review. Mammalian societies (b)

0.9

probability of being evicted

3232

0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0

<12

13–24

>24

subordinate female age (months)

0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0

<10

15

20

25

30

30+

group size

probability of conceiving

(c) 1.0

0.8

0.6

0.4

0.2

0 1

2 3 4 age (years) Figure 2. Eviction of subordinate females in meerkats: (a) the probability that subordinate females will be evicted by dominant females in their first, second and third year of life; (b) the probability that subordinate females will be evicted from groups of different size; (c) the probability that subordinates (shaded bars) and dominants (open bars) conceive during a three-month period at different ages (adapted from Clutton-Brock et al. 2008).

dominant females tolerate adult subordinate females for 1 or 2 years after they are sexually mature, directing increasingly frequent aggression at older or heavier subordinates and eventually evicting all females before they are 5 years old (Clutton-Brock et al. 1998b, 2001a; Young & Clutton-Brock 2006; Young et al. 2006; Clutton-Brock et al. 2008) (figure 2a). Though groups of evictees are sometimes able to establish new breeding groups, the new dominant soon evicts them again, so that virtually all females are either dominant or dead by the time they are 4 years old, while males disperse to breed in other groups at around the same age. In naked mole-rats, subordinate females rarely disperse and may remain in their natal group throughout their lives, so that colonies contain subordinates of a wide range of ages (Brett 1991; Sherman & Jarvis 2002). When dominant females die and a new dominant female has established herself, she kills or evicts her competitors within the next year (Reeve & Sherman 1991) (P. Sherman 2006, personal communication). In naked mole-rats, males, too, usually remain in the colony, though a proportion adopt a divergent growth trajectory and disperse when conditions are favourable (O’Riain et al. 1996). How commonly dominant breeding males in natural groups are immigrants versus natals is not yet known. Phil. Trans. R. Soc. B (2009)

Dominant females also suppress the fecundity of subordinate females, and frequently kill any offspring they produce, though the extent to which the reproductive function of subordinates is suppressed varies widely. In many societies, subordinate females show lower levels of luteinizing hormone (LH) or oestrogen than dominant females either throughout the breeding season or over the period of oestrous (Abbott 1984; French 1997; O’Riain et al. 2000a; Creel & Creel 2001). In some species (including meerkats), differences in LH levels disappear when subordinates are challenged with gonadotropin-releasing hormone (GnRH), indicating that suppression can be quickly reversed. In others (including marmosets and naked mole-rats), differences in LH levels between dominants and subordinates persist, indicating that reproductive function is more deeply suppressed (Abbott 1993; Faulkes & Abbott 1997; French 1997). However, even here, the removal of dominant females or the provision of access to unrelated males leads to relatively rapid increases in levels of sex hormones and reproductive competition in subordinates (Faulkes et al. 1997; Cooney & Bennett 2000). In naked mole-rats (but not, as yet, in other species), dominant females also suppress the development of subordinate males (Faulkes & Abbott 1997)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Mammalian societies (M. J. O’Riain 2006, personal communication), possibly because subordinate females will mate with close relatives so that natal males are prospective breeding partners. Because breeding females are frequently the mothers or sisters of subordinate females, suppressing the development of subordinates, killing their pups or evicting them from the group are likely to have substantial costs to the inclusive fitness of dominants. So why do dominants suppress subordinate reproduction in most cooperative breeders? The likely answer is that female group members have the capacity to produce more young than the group is able to raise and that simultaneous litters dilute the investment of helpers and reduce the growth and survival of offspring born to the dominant females (Hodge 2009). Experimental increases in the size of meerkat litters reduce the food intake and growth of pups, which are closely related to their survival (Clutton-Brock et al. 2001b). In addition, where helpers raise litters born to dominants at the same time as litters born to subordinate mothers, the growth of the dominant female’s pups is reduced if older pups are present (Hodge 2009). As would be expected, the extent to which dominants tolerate subordinates appears to vary in relation to the risk of reproductive competition. In meerkats, dominant females are more likely to evict subordinates and to kill their pups if they themselves are pregnant than if they are not (Clutton-Brock et al. 1998b). The age at which they evict subordinates coincides with increases in the probability that subordinates will attempt to breed if they remain in the group (figure 2b) (Clutton-Brock et al. 2008) and they are also more likely to evict individuals if they have attempted to breed or which are relatively distant relatives (Young et al. 2006; Clutton-Brock et al. 2008). Dominant females do not attempt to prevent subordinates from breeding in all cooperative species and, in some, including African lions and banded mongooses, multiple females breed regularly (Lewis & Pusey 1997; Russell 2004; Clutton-Brock 2006). Evidence of the benefits of suppressing subordinate reproduction to dominants (Hodge 2009) prompts the related question why breeding females do not always suppress subordinates. One possible explanation is that subordinate breeding does not reduce the breeding success of dominants in all cooperative breeders. For example, in banded mongooses, where multiple females commonly breed in synchrony, the pups of dominant females show higher survival rates if one or more subordinate females breed at the same time as the dominant than if they do not, though why this is the case is not yet fully clear (Hodge 2003, 2009). An alternative or additional possibility is that, in some societies, the costs of suppression to dominant females may be very high. For example, the possession of lethal weaponry by lionesses may effectively preclude both established dominance relations and any form of reproductive suppression (see Packer et al. 2001).

5. SUBORDINATE STRATEGIES By their persistent attempts to prevent subordinate females from breeding, dominant females restrict the Phil. Trans. R. Soc. B (2009)

T. Clutton-Brock

3233

reproductive options of subordinates in high skew societies to three main alternatives: disperse in an attempt to form a new breeding group elsewhere and establish themselves as the dominant female in it; challenge the existing dominant for her position; or remain in the natal group, with the possibility either of breeding as a subordinate when the dominant’s ability to control subordinate reproduction is reduced or of inheriting the breeding position on her death. In many high-skew societies where females live in stable groups, none of these three options offers a substantial chance of successful reproduction to the majority of subordinates. In species that live in territorial, matrilineal groups, such as meerkats or mole-rats, female immigration is usually resisted by all group members whether local density is saturated or not and successful immigration by females into established groups is very rare. Without other individuals to assist them, solitary females seldom survive for long and, even if several dispersing females manage to establish a new group, only one will acquire the dominant position and the others will rapidly be evicted to face an uncertain future again (Clutton-Brock et al. 1998b, 2006; Young & Clutton-Brock 2006). In addition, the chances that a newly established dominant female will breed successfully are low, because group size and helper number are likely to be low (CluttonBrock 1998; Clutton-Brock et al. 2001a; Courchamp et al. 2003). As a result, it is unsurprising that, in many cooperative mammals, including meerkats and naked mole-rats, subordinate females only leave their natal group if they are evicted by force and make extensive efforts to induce the dominant female to allow them to remain (Clutton-Brock et al. 1998b; Kutsukake & Clutton-Brock 2006). Challenging the established dominant is also rarely successful. In some species, including naked molerats, and, to a lesser extent, in meerkats, individuals that acquire dominant status increase in size and body mass and show increased levels of testosterone so that subordinate females are unlikely to win contests with established dominants (Faulkes & Abbott 1997; O’Riain et al. 2000b; Russell et al. 2004) (figure 3a). In addition, dominant females may evict subordinates before they reach full adult size (figure 2). Moreover, replacing an established breeder may reduce the challenger’s inclusive fitness if the breeding female is a close relative for, in many cooperative breeders, the annual breeding success of new breeders is low (Woolfenden & Fitzpatrick 1984; Waser et al. 1995; Creel & Creel 2001; Sherman & Jarvis 2002; Hodge et al. 2008). As a result, it may seldom benefit mature daughters to attempt to replace dominant mothers where their father is still the resident breeding male, so that subsequent offspring produced by their mother will be full sibs (see Bourke 2007). As in eusocial insects (see Keller & Nonacs 1993; Beekman & Ratnieks 2003; Beekman et al. 2003; Hart & Ratnieks 2005; Keller 2009; Ratnieks & Helantera¨ 2009), there has been a longstanding debate as to whether reproductive suppression in subordinate mammals is best interpreted as a consequence of constraints imposed by dominants or is better interpreted as the outcome of reproductive

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

T. Clutton-Brock (a)

Review. Mammalian societies

750 mean weight (g)

1.0

(b)

800

probability of retaining dominance

3234

700

650

600 female

(d )

0.4 0.2

20

40 60 80 tenure (months)

100

120

30

60

25 median breeding success

breeding success

0.6

0

male

70

(c)

0.8

50 40 30 20

20 15 10 5

10

0 0

50 100 tenure (months)

150

male

female

Figure 3. (a) Mean mass of females and males that acquired dominant status three months before becoming dominant and six months after becoming dominant (unfilled bar, subordinate; filled bar, dominant); (b) probability (Kaplan–Meier estimates) of dominant female (thick line) and male (thin line) meerkats in a naturally regulated population retaining their status for different periods of time; (c) cumulative reproductive success of female (filled diamonds) and male (open squares) meerkats with increasing tenure and (d) mean breeding success of females and males that acquire dominant status in their group (adapted from Clutton-Brock et al. 2006).

restraint by subordinates (Creel & Creel 2001; Young et al. 2006). Aspects of their phenotype (including their condition, foraging ability and reproductive experience) as well as their social and ecological circumstances and the likely response of the dominant female to any breeding attempts will affect the pay-offs of breeding attempts to subordinates (Ratnieks & Wenseleers 2008; Ratnieks & Helantera¨ 2009). In theory, examples of ‘pure’ restraint could evolve in cooperative societies if the presence and behaviour of dominants had no effect on the pay-offs of breeding attempts to subordinates but, as in social insects, the presence and behaviour of dominant females usually appears to play an important role in determining the pay-offs of breeding attempts (see Ratnieks & Helantera¨ 2009). As the characteristics of subordinates will also affect the outcome of breeding attempts, and interactions are likely to be common, attempts to distinguish between adaptive constraint and reproductive restraint are a rather theoretical exercise. Where the chances that individual subordinates will acquire the breeding position are low and subordinates Phil. Trans. R. Soc. B (2009)

are unlikely to breed successfully, the relative benefits of increasing the indirect component of their inclusive fitness by assisting in rearing young born to related dominants (who commonly are either their mother or their sister) are likely to be relatively large (West-Eberhard 1975, 1981; Sherman et al. 1995; Shellman-Reeve 1997; Bourke 1999; Ratnieks & Helantera¨ 2009). In meerkats and wild dogs, as well as in several cooperative birds, assistance has substantial effects on the growth of the dominant female’s offspring, the frequency with which she breeds and the survival of her offspring (Clutton-Brock et al. 2001b; Creel & Creel 2001; Russell et al. 2003a). Moreover, the contributions of individual helpers to cooperative rearing are usually conditional on their weight, age and reproductive condition, so that the costs of helping to their own growth and fitness are likely to be low (Wright et al. 2000; Clutton-Brock et al. 2002; Russell et al. 2003b). However, opportunistic attempts to breed as a subordinate when the dominant female’s control is relaxed may often provide subordinates with the best chance of direct reproduction and are

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Mammalian societies common in some species (Clutton-Brock et al. 2001a; Creel & Creel 2001; Clutton-Brock et al. 2008). Where breeding increases the risk that the subordinate will attract aggression from the dominant female and be evicted (see Young et al. 2006), subordinates would be expected either to attempt to disguise their reproductive status or to placate dominants, and there is some evidence of strategies of this kind. In meerkats, for example, older and heavier female subordinates that are likely to be evicted by dominant females commonly attempt to groom dominants and readily submit to minor threats (Kutsukake & Clutton-Brock 2006). Subordinates might also be expected to adjust their relative investment in cooperative behaviour in relation to their chances of breeding successfully. Recent studies of mole-rats provide convincing evidence of strategies of this kind. In Damaraland mole-rats, subordinates can be divided into frequent and infrequent helpers (Scantlebury et al. 2006). Infrequent workers increase their daily energy expenditure after rainfall and may be more likely to disperse, while frequent workers do not. Similarly, in naked mole-rats, some males show increased growth and fat deposits, reduced levels of cooperative behaviour and an increased probability of dispersing (O’Riain et al. 1996).

6. ADAPTATIONS OF BREEDING FEMALES IN HIGH-SKEW SOCIETIES In the more specialized cooperative vertebrates where reproductive skew is pronounced, dominant females often show unusual adaptations that resemble the characteristics of queens in eusocial insects (Alexander et al. 1991). Both in meerkats and naked mole-rats, levels of circulating testosterone rise in females that acquire the breeding position and, although they are already fully adult, dominant females increase in size and body mass (Faulkes & Abbott 1997; O’Riain et al. 2000b; Russell et al. 2004; Clutton-Brock et al. 2006) (see figure 3a). Studies of meerkats show that increases in the number of helpers reduce the costs of breeding to the dominant female and the interval between successive litters, leading to increases in her rate of reproduction (Clutton-Brock et al. 1998a; Russell et al. 2003a) and, both in meerkats and in social mole-rats, dominant females show unusually high levels of fecundity, conceiving again shortly after giving birth and producing multiple litters per year (Jarvis 1991a; Clutton-Brock et al. 2001a; Russell et al. 2003a). Cooperative breeding is also associated with relatively long lifespans in breeding females (Arnold & Owens 1998; Carey 2001; Sherman & Jarvis 2002). In meerkats, where breeding females forage independently and so are exposed to a regular extrinsic risk of mortality, dominant females can continue to breed for 8 – 10 years (figure 3b) and in several of the social mole-rats, breeding females can also live for 10 years or more (Dammann & Burda 2006) (N. Bennett 2009, personal communication). In naked mole-rats, breeding females have even longer lifespans and can breed for more than 20 years (Sherman & Jarvis 2002). Though no studies of wild populations Phil. Trans. R. Soc. B (2009)

T. Clutton-Brock

3235

have yet documented ageing rates and studies of captive colonies have produced variable results (Sherman & Jarvis 2002; Ross-Gillespie et al. 2007) (M. J. O’Riain 2006, personal communication), it seems likely that the social mole-rats, like some eusocial insects (Carey 2001), have evolved mechanisms that defer senescence in breeding females. Comparisons between naked mole-rats and mice show that protein structural stability, oxidation and degradation show relatively little change with increasing age in naked mole-rats (Perez et al. 2009). In addition, broader comparisons between small mammals with relatively long lifespans and species with relatively short ones show that long-lived species maintain tightly regulated basal levels of vitamin D, insulin, glucocorticoid and thyroid endocrine systems (Buffenstein & Pinto 2009). As a result of high levels of reproductive skew, rapid rates of reproduction and relatively long lifespans, individual differences in breeding success among females are often unusually large in cooperative breeders (Hauber & Lacey 2005; Clutton-Brock et al. 2006). For example, in meerkats, successful breeding females can rear up to a hundred surviving offspring during their lives (figure 3c) while, in naked molerats, this may rise to over 1000 (Sherman & Jarvis 2002). Because the majority of females fail to breed altogether (Clutton-Brock et al. 2006), selection pressures on females favouring traits associated with the acquisition and maintenance of the dominant position, like relative weight can be extremely strong. In meerkats, heavier females are more likely to acquire and maintain dominant status (figure 4a,b) and their daughters are also more likely to do so in their turn (figure 4c). The intensity of selection on traits associated with competitive success in females probably explains why they show more pronounced changes in hormonal status and growth than males after they acquire alpha status (Faulkes & Abbott 1997; Russell et al. 2004; Clutton-Brock et al. 2006).

7. ADAPTATIONS OF MALES IN HIGH-SKEW SOCIETIES High reproductive skew in females also has important consequences for males. The restriction of effective female reproduction to one relatively long-lived breeding female per group typically limits the opportunity for polygyny in males and favours close mate guarding and monogamous breeding (Clutton-Brock 2006). In many of the specialized cooperative breeders, a single male guards reproductive access to the breeding female and extra-pair paternity appears to be rare. For example, in meerkat groups, one dominant male monopolizes breeding access to the dominant female and sires over 90 per cent of her young (Griffin et al. 2003; Spong et al. 2008). In naked mole-rats too, a single male monopolizes access to the breeding female ( Jarvis 1991a; Bennett & Faulkes 2000) while, in African wild dogs and callitrichids, groups commonly include several breeding males and multiple males may mate but subordinates apparently sire few offspring (Girman et al. 1997; Creel & Creel 2001; Goldizen 2003; Heyman 2003). In this respect,

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3236

T. Clutton-Brock (a)

Review. Mammalian societies (b)

800

100 tenure (months)

mean weight (g)

760

120

720 680

80 60 40

640 20 600 0 –200

560 female

male

probability of becoming dominant

(c)

–100

0

100

200

weight difference (g)

0.5

0.4

0.3

0.2

0.1

0 dominant

subordinate

Figure 4. The acquisition and maintenance of dominant status in meerkats: (a) mean body mass in the three months before a dominance change of female and male meerkats that successfully (unfilled bar) acquired dominant status compared with a same-aged or older unsuccessful (filled bar) competitor; (b) tenure of the dominant position in female (filled diamonds) and male (open squares) helpers in relation to the difference in body weight between them and the oldest same sex subordinate in their group and (c) probability that daughters and sons born to dominant and subordinate mothers will acquire dominant status (unfilled bar, female; filled bar, male) (Clutton-Brock et al. 2006).

Damaraland mole-rats Cryptomys damarensis appear to be an exception and extra-group mating and multiple paternity within litters appear to be common (Burland et al. 2004). Where dominant males monopolize access to a single breeding female, they usually do so for several seasons, generating large differences in breeding success between males as well as between females (figure 3c) and relatively high coefficients of relatedness between young born in successive litters. However, in meerkats and, possibly, in naked molerats, the reproductive tenure of dominant males is shorter than that of dominant females (figure 3b), so that reproductive skew and individual differences in breeding success are not as large as in females (figure 3d ) and a higher proportion of males breed as dominants at some stage in their lifespans (Clutton-Brock et al. 2006) (M. J. O’Riain 2006, personal communication). Two separate mechanisms Phil. Trans. R. Soc. B (2009)

may be responsible for the shorter tenure of males. First, breeding males whose partners die are often the father of all females in the group, including the new dominant female. ‘Widowers’ rarely guard or mate with related dominant females, play an enlarged role in guarding litters and leave their group to search for breeding opportunities in other groups while ‘widows’ invariably remain in their breeding group and so avoid the risks of dispersal (T. H. CluttonBrock 2009, unpublished data). Second, breeding males, unlike breeding females, commonly face competition for their position from any related males that immigrated with them, as well as from unrelated immigrants from other groups. In contrast to breeding females, whose principal competitors are younger animals born in the same group, males have no opportunity to restrict the development of potential competitors or to evict them from the group before they become a serious threat to their position. This

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Mammalian societies argument also suggests a possible reason for the contrast in relative longevity between breeding females in cooperative and eusocial societies and males in polygynous species, where high reproductive skew is associated with a reduction in longevity (CluttonBrock & Isvaran 2007). While dominant females in most cooperative and eusocial societies are usually able to minimize the risk of competition or challenge by suppressing the development of potential competitors or evicting them from the group, in most polygynous species males are not, with the result that high levels of reproductive skew are associated with frequent challenges for the breeding position and frequent, costly fights (Clutton-Brock et al. 1979).

8. DISCUSSION As yet, the number of studies of cooperative mammals providing detailed information on the life histories and reproductive success of breeders and helpers in natural populations is small and generalizations are necessarily tenuous. However, it is clear that, across animal societies, cooperative breeding is closely associated with high levels of reproductive skew. In some societies (and possibly in most), simultaneous reproduction by other breeding females reduces the survival of offspring born to dominant females, favouring the suppression of breeding by other females and leading to high levels of reproductive skew in both sexes. Suppression of reproduction by subordinate females restricts their reproductive options and favours the evolution of nepotistic cooperation. Assistance in rearing young is associated with reductions in the fitness costs of breeding to dominant females and positive correlations between age and breeding success, strengthening selection pressures for longevity in breeders. Where helpers also provision breeding females, as in naked mole-rats, this can further reduce their extrinsic risk of mortality, leading to the evolution of unusually long lifespans in breeding females, which augment variance in breeding success among females and the degree of reproductive skew. Variation in the life histories of breeders have profound consequences for the structure of vertebrate societies. In species where the mortality of breeding females is relatively high (as in many cooperative birds), subordinates have a substantial chance of acquiring breeding status outside their natal group. As a result, selection on subordinates is likely to favour dispersal, helpers are unlikely to remain for more than one or two seasons in their natal group, group size is relatively small and breeders are forced to contribute to rearing their own young. In these societies, selection pressures operating on helpers and breeders are relatively similar and differences in behaviour, physiology and anatomy between them are usually relatively small. At the other extreme are animal societies where mortality of breeders is relatively low, subordinates have little chance of acquiring breeding status outside their natal group, selection on subordinates favours philopatry and (if dominant females allow subordinates to remain) groups can be large. Under these conditions, selection on subordinates is likely to favour strategies adapted to raising Phil. Trans. R. Soc. B (2009)

T. Clutton-Brock

3237

indirect components of their fitness by assisting related breeders and specializations for helping are likely to evolve, including adaptations in behaviour, reproductive physiology and growth. Increases in the number and specialization of helpers raise the potential reproductive rate of breeders, generating selection pressures on breeders to increase their fecundity, to improve their control of the behaviour and development of other group members and to extend their lifespans, which, in turn, reinforce selection pressures favouring indirect reproduction in subordinates. This explanation of cooperative societies suggests that contrasts in colony or group size (and associated differences in the degree of reproductive skew) may help to account for contrasts in complexity. Specialized, eusocial societies are probably more widespread in insects than in vertebrates because the number of individuals per colony is so large that the per capita chances that an individual will occupy the breeding role are extremely low (Alexander et al. 1991; Bourke 1999). Obligate sterility and specialized, eusocial societies may be absent in cooperative vertebrates because the larger body size and greater energetic requirements of individuals restricts the potential size of groups, limiting the extent of divergence in the selection pressures operating on helpers and breeders (see Boomsma 2009). As would be expected, the most specialized cooperative societies found among vertebrates occur in herbivorous rodents of relatively small body size where the distribution of their food supply and the energetic requirements of individuals permit the formation of relatively large groups (Alexander et al. 1991; Bennett & Faulkes 2000; Faulkes & Bennett 2007). Similarly, among the carnivores, the most specialized cooperative societies occur in diurnal insectivores of relatively small body size, where heavy predation pressure favours the formation of large groups. In contrast, group size is comparatively small in most cooperative birds, which may explain why no species show a degree of specialization in cooperative breeding comparable to that of naked mole-rats (Russell 2004; Clutton-Brock 2006). There are probably several reasons for the evolution of extended lifespans in breeding females in cooperative and eusocial species. In many of these species (including naked mole-rats), breeding females are routinely provisioned by other group members and this is likely to reduce extrinsic mortality associated with independent foraging (Alexander et al. 1991; Sherman & Jarvis 2002). Cooperative rearing may also reduce the survival costs of breeding to dominant females (Creel & Creel 2001; Clutton-Brock et al. 2006). Finally, increases in the annual reproductive success of breeding females throughout much of their period of tenure are common in cooperative species (Woolfenden & Fitzpatrick 1984; Creel & Creel 2001; Hodge et al. 2008) and are likely to favour the evolution of long breeding lifespans (Sherman & Jarvis 2002). A similar association between unusually long lifespans in breeding females and age-related increases in body size, fecundity and survival (‘negative senescence’) has been documented in a number of fish showing indeterminate growth (Vaupel et al. 2004). This brief review of the evolution of cooperative behaviour provides a basis for assessing suggestions

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3238

T. Clutton-Brock

Review. Mammalian societies

that cooperation is best interpreted as a group-level adaptation maintained by group selection (Wilson & Wilson 2007). There is no question that the actions of individuals commonly affect the fitness of other group members and can generate variation in breeding success or survival between groups. For example, in polygynous societies, the eviction of other males by one dominant male may (conceivably) enhance the resources available for females, generating increases in the fitness of members of one-male groups. Similarly, it is possible that the monopolization of reproduction by a single dominant female in cooperative breeders reduces interference between females and increases recruitment in groups where subordinate females are suppressed. However, in both these cases, the behaviour of dominant individuals is likely to increase their own reproductive success and effects on the fitness of other group members may be unselected by-products of the adaptive strategies of individuals. While it is more tempting to view cooperative behaviour and its consequences (group territoriality, the construction of nests or burrows and the cooperative rearing of young) as group-level adaptations, here, too, there is no need to interpret them in this way. In many cooperative societies, the selfish strategies of individuals constrain opportunities for direct reproduction among subordinates to such an extent that maximizing the indirect component of their inclusive fitness represents an individual’s optimal strategy (see Ratnieks & Helantera¨ 2009). Although it is possible to argue that activities that increase the fitness of multiple relatives represent a form of group selection, where groups consist of related individuals, the distinction between group selection and kin selection is semantic (West et al. 2007a,b,c; Gardner & Grafen 2009). In the relatively small number of cases where stable groups consist of unrelated individuals, cooperation is seldom strongly developed and, where it does occur, is either coerced by dominant group members or increases the fitness of cooperators. The ultimate test of evolutionary explanations of social behaviour is whether they extend our understanding of variation in the behaviour of individuals and the structure of groups, either within or between species. In a previous review of mammalian societies, Kitchen & Packer (1999) tried to envisage a scenario where mammalian societies had evolved through evolutionary processes dominated by group selection and the activities of group members were adapted to maximizing benefits to the group. Competition between individuals should be minimal, reproductive interference and enforced evictions should be rare, cooperation between unrelated individuals should be common and birth sex ratios should be strongly biased towards females. This is a deeply unfamiliar picture to anyone acquainted with non-human mammals: in most social mammals, competition between group members is intense, reproductive interference is common, the more costly forms of cooperation are confined to relatives, average primary sex ratios are close to parity and the structure of societies appears to be a consequence of the attempts of individuals to maximize their inclusive fitness (Russell 2004; Clutton-Brock 2006). While this argument does not exclude the possibility that group Phil. Trans. R. Soc. B (2009)

selection plays some role in maintaining cooperative behaviour, it suggests that, as in polygynous societies, the reproductive strategies of individuals in cooperative animals are best interpreted as attempts to maximize their inclusive fitness (see Grafen 2009). In this respect, the societies of non-human mammals differ from human societies, where accepted group norms commonly constrain the capacity of individuals to maximize their fitness at a cost to other group members, unrelated individuals often cooperate with each other, teamwork is frequently highly developed and extreme self-sacrifice is not uncommon (Bowles & Gintis 2003; Richerson et al. 2003; Boyd & Richerson 2009). I am grateful to Nigel Bennett, Matt Bell, Jon Blount, Andrew Bourke, Mike Cant, Heikki Helantera¨, Sarah Hodge, Rufus Johnstone, Dieter Lukas, Justin O’Riain, Francis Ratnieks, Andy Russell, Colin Selman, Stuart Sharp and Stuart West for comments, discussion or access to unpublished data and to Penny Roth for preparing the manuscript. I am grateful to M Silvas and the Journal of Animal Ecology for permission to reprint figure 1, to the Association for the Study of Animal Behaviour for permission to reprint figure 2 and to the Editor of Nature for permission to reprint figures 3 and 4.

REFERENCES Abbott, D. H. 1984 Behavioral and physiological suppression of fertility in subordinate marmoset monkeys. Am. J. Primatol. 6, 169–186. (doi:10.1002/ajp.1350060305) Abbott, D. H. 1993 Social conflict and reproductive suppression in marmosets and tamarin monkeys. In Primate social conflict (eds W. A. Mason & S. P. Mendoza), pp. 331–372. Albany, NY: State University of New York Press. Alexander, R. D., Nonan, K. M. & Crespi, B. J. 1991 The evolution of eusociality. In The biology of the naked mole-rat (eds P. W. Sherman, J. U. M. Jarvis & R. D. Alexander), pp. 3– 44. Princeton, NJ: Princeton University Press. Andersson, M. 1994 Sexual selection. Princeton, NJ: Princeton University Press. Arnold, K. E. & Owens, I. P. F. 1998 Cooperative breeding in birds: a comparative test of the life history hypothesis. Proc. R. Soc. Lond. B 265, 739 –745. (doi:10.1098/rspb. 1998.0355) Beekman, M. & Ratnieks, F. L. W. 2003 Power and reproduction in insect societies. Phil. Trans. R. Soc. Lond. B 258, 1741– 1753. (doi:10.1098/rstb.2002.1262) Beekman, M., Komdeur, J. & Ratnieks, F. L. W. 2003 Reproductive conflicts in social animals—who has power? Trends Ecol. Evol. 18, 277–282. (doi:10.1016/ S0169-5347(03)00068-5) Bennett, N. C. & Faulkes, C. G. 2000 African mole-rats: ecology and eusociality. Cambridge, UK: Cambridge University Press. Bennett, P. M. & Owens, I. P. F. 2002 Evolutionary ecology of birds. Oxford, UK: Oxford University Press. Bertram, B. C. R. 1978 Living in groups: predators and prey. In Behavioural ecology: an evolutionary approach (eds J. R. Krebs & N. B. Davies), pp. 64–96. Oxford, UK: Blackwell. Blumstein, D. T. & Møller, A. P. 2008 Is sociality associated with high longevity in North American birds? Biol. Lett. 4, 146 –148. (doi:10.1098/rsbl.2007.0606) Boomsma, J. J. 2007 Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17, R673–R683. (doi:10.1016/j.cub.2007.06.033)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Mammalian societies Boomsma, J. J. 2009 Lifetime monogamy and the evolution of eusociality. Phil. Trans. R. Soc. B 364, 3191–3207. (doi:10.1098/rstb.2009.0101) Bourke, A. F. G. 1999 Colony size, social complexity and reproductive conflict in social insects. J. Evol. Biol. 12, 245 –257. (doi:10.1046/j.1420-9101.1999.00028.x) Bourke, A. F. G. 2007 Kin selection and the evolutionary theory of aging. Annu. Rev. Ecol. Syst. 38, 103–128. (doi:10.1146/annurev.ecolsys.38.091206.095528) Bowles, S. & Gintis, H. 2003 Origins of human cooperation. In Genetic and cultural evolution of cooperation (ed. P. Hammerstein), pp. 420 –443. Berlin, Germany: Dahlem University Press. Boyd, R. & Richerson, P. J. 2009 Culture and the evolution of human cooperation. Phil. Trans. R. Soc. B 364, 3281– 3288. (doi:10.1098/rstb.2009.0134) Bradbury, J. W. & Vehrencamp, S. L. 1976 Social organization and foraging in emballonurid bats. I Field studies. Behav. Ecol. Sociobiol. 1, 337 –381. (doi:10.1007/ BF00299399) Bradbury, J. W. & Vehrencamp, S. L. 1977 Social organization and foraging in emballonurid bats. III Mating systems. Behav. Ecol. Sociobiol. 2, 1 –17. (doi:10.1007/ BF00299284) Braude, S. T. 1991 The behaviour and demographics of the naked mole-rat Heterocephalus glaber. PhD thesis, University of Michigan, Ann Arbor, MI, USA. Brett, R. A. 1991 The population structure of naked mole-rat colonies. In The biology of the naked mole-rat (eds P. W. Sherman, J. U. M. Jarvis & R. D. Alexander), pp. 97– 136. Princeton, NJ: Princeton University Press. Buffenstein, R. & Pinto, M. 2009 Endocrine function in naturally long-living small mammals. Mol. Cell. Endocrinol. 299, 101–111. (doi:10.1016/j.mce.2008.04.021) Burland, T. M., Bennett, N. C., Jarvis, J. U. M. & Faulkes, C. G. 2004 Colony structure and parentage in wild colonies of cooperatively breeding Damaraland mole-rats suggest incest avoidance alone may not maintain reproductive skew. Mol. Ecol. 13, 2371–2379. (doi:10.1111/ j.1365-294X.2004.02233.x) Carey, J. R. 2001 Demographic mechanisms for the evolution of long life in social insects. Exp. Gerontol. 36, 713 –722. (doi:10.1016/S0531-5565(00)00237-0) Clarke, A. L., Saether, B. E. & Roskaft, E. 1997 Sex biases in avian dispersal: a reappraisal. Oikos 79, 429 –438. (doi:10. 2307/3546885) Clutton-Brock, T. H. 1983 Selection in relation to sex. In Evolution from molecules to men (ed. B. J. Bendall), pp. 457 –481. Cambridge, UK: Cambridge University Press. Clutton-Brock, T. H. 1989a Female transfer and inbreeding avoidance in social mammals. Nature 337, 70–71. (doi:10.1038/337070a0) Clutton-Brock, T. H. 1989b Female transfer, male tenure and inbreeding avoidance in social mammals. Nature 337, 70– 72. (doi:10.1038/337070a0) Clutton-Brock, T. H. 1989c Mammalian mating systems. Proc. R. Soc. Lond. B 236, 339 –372. (doi:10.1098/rspb. 1989.0027) Clutton-Brock, T. H. 1998 Reproductive skew: disentangling concessions from control. A reply to Emlen and Reeve. Trends Ecol. Evol. 13, 459. (doi:10.1016/S01695347(98)01470-0) Clutton-Brock, T. H. 2006 Cooperative breeding in mammals. In Cooperation in primates and humans (eds P. M. Kappeler & C. P. Van Schaik), pp. 173 –190. Berlin, Germany: Springer Verlag. Clutton-Brock, T. H. 2007 Sexual selection in males and females. Science 318, 1882– 1885. (doi:10.1126/science. 1133311) Phil. Trans. R. Soc. B (2009)

T. Clutton-Brock

3239

Clutton-Brock, T. H. 2009 Sexual selection in females. Anim. Behav. 77, 3–11. (doi:10.1016/j.anbehav.2008.08.026) Clutton-Brock, T. H. & Harvey, P. H. 1977 Primate ecology and social organization. J. Zool. 183, 1 –39. Clutton-Brock, T. H. & Harvey, P. H. 1978 Mammals, resources and reproductive strategies. Nature 273, 191–195. (doi:10.1038/273191a0) Clutton-Brock, T. & Isvaran, K. 2007 Sex differences in ageing in natural populations of vertebrates. Proc. R. Soc. B 274, 3097 –3104. (doi:10.1098/rspb.2007.1138) Clutton-Brock, T. H. & Mcauliffe, K. 2009 Female mate choice in mammals. Q. Rev. Biol. 84, 3–27. (doi:10. 1086/596461) Clutton-Brock, T. H. & Parker, G. A. 1995 Sexual coercion in animal societies. Anim. Behav. 49, 1345–1365. (doi:10.1006/anbe.1995.0166) Clutton-Brock, T. H., Albon, S. D., Gibson, R. M. & Guinness, F. E. 1979 The logical stag: adaptive aspects of fighting in red deer (Cervus elaphus L.). Anim. Behav. 27, 211 –225. (doi:10.1016/0003-3472(79)90141-6) Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E. 1982a Competition between female relatives in a matrilocal mammal. Nature 300, 178 –180. (doi:10.1038/300178a0) Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. 1982b Red Deer: the behaviour and ecology of two sexes. Edinburgh, UK: University Press. Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E. 1984 Maternal dominance, breeding success and birth sex ratios in red deer. Nature 308, 358 –360. (doi:10.1038/ 308358a0) Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E. 1985 Parental investment and sex differences in juvenile mortality in birds and mammals. Nature 313, 131– 133. (doi:10.1038/313131a0) Clutton-Brock, T. H., Deutsch, J. C. & Nefdt, R. J. C. 1993 The evolution of ungulate leks. Anim. Behav. 46, 1121–1138. (doi:10.1006/anbe.1993.1302) Clutton-Brock, T. H. et al. 1998a Costs of cooperative behaviour in suricates Suricata suricatta. Proc. R. Soc. Lond. B 265, 185– 190. (doi:10.1098/rspb.1998.0281) Clutton-Brock, T. H., Brotherton, P. N. M., Smith, R., Mcilrath, G., Kansky, R., Gaynor, D., O’Riain, M. J. & Skinner, J. D. 1998b Infanticide and expulsion of females in a cooperative mammal. Proc. R. Soc. Lond. B 265, 2291–2295. (doi:10.1098/rspb.1998.0573) Clutton-Brock, T. H. et al. 2001a Cooperation, conflict and concession in meerkat groups. Science 291, 478– 481. (doi:10.1126/science.291.5503.478) Clutton-Brock, T. H., Russell, A. F., Sharpe, L., Brotherton, P. N. M., Mcilrath, G. M., White, S. & Cameron, E. Z. 2001b Effects of helpers on juvenile development and survival in meerkats. Science 293, 2446–2449. (doi:10.1126/ science.1061274) Clutton-Brock, T. H., Russell, A. F., Sharpe, L. L., Young, A. J., Balmforth, Z. & Mcilrath, G. M. 2002 Evolution and development of sex differences in cooperative behavior in meerkats. Science 297, 253 –256. (doi:10.1126/ science.1071412) Clutton-Brock, T. H., Hodge, S. J., Spong, G., Russell, A. F., Jordan, N. R., Bennett, N. C. & Manser, M. B. 2006 Intrasexual competition and sexual selection in cooperative meerkats. Nature 444, 1065– 1068. (doi:10. 1038/nature05386) Clutton-Brock, T. H., Hodge, S. J. & Flower, T. P. 2008 Group size and the suppression of subordinate reproduction in Kalahari meerkats. Anim. Behav. 76, 689– 700. (doi:10.1016/j.anbehav.2008.03.015). Cooney, R. & Bennett, N. C. 2000 Incest avoidance and reproductive skew in a cooperative mammal. Proc. R. Soc. Lond. B 267, 801–806. (doi:10.1098/rspb.2000.1074)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3240

T. Clutton-Brock

Review. Mammalian societies

Courchamp, F., Woodroffe, R. & Roemer, G. W. 2003 Removing protected populations to save endangered species. Science 302, 1532–1532. (doi:10.1126/science. 1089492) Creel, S. & Creel, N. M. 2001 The African wild dog: behavior, ecology and conservation. Princeton, NJ: Princeton University Press. Creel, S. R. & Waser, P. M. 1997 Variation in reproductive suppression among dwarf mongooses: interplay between mechanisms and evolution. In Cooperative breeding in mammals (eds N. G. Solomon & J. A. French), pp. 150 –170. Cambridge, UK: Cambridge University Press. Crook, J. H., Ellis, J. E. & Goss-Custard, J. D. 1976 Mammalian social systems: structure and function. Anim. Behav. 24, 261–274. (doi:10.1016/S0003-3472(76)80035-8) Dammann, P. & Burda, H. 2006 Sexual activity and reproduction delay ageing in a mammal. Curr. Biol. 16, R117 –R118. (doi:10.1016/j.cub.2006.02.012) Darwin, C. 1871/1958 The descent of man and selection in relation to sex. New York, NY: The Modern Library. Digby, L. 2000 Infanticide by female mammals: implication for the evolution of social systems. In Infanticide by males (eds C. P. V. Schaik & C. H. Jansen), pp. 423 –446. Cambridge, UK: Cambridge University Press. Digby, L. J., Ferrari, S. F. & Saltzman, W. 2007 Callitrichines: the role of competition in cooperatively breeding species. In Primates in perspective (eds C. J. Campbell & E. Al), pp. 85–106. Oxford, UK: Oxford University Press. Dittus, W. J. P. 1979 The evolution of behavior regulating density and age-specific sex ratios in a primate population. Behaviour 69, 265 –301. (doi:10.1163/ 156853979X00511) Donald, P. F. 2007 Adult sex ratios in wild bird populations. Ibis 149, 671 –692. (doi:10.1111/j.1474-919X.2007. 00724.x) Dugatkin, L. A. 1997 Cooperation among animals: an evolutionary perspective. Oxford, UK: Oxford University Press. Ebensperger, L. A. 1998a Strategies and counter-strategies to infanticide in mammals. Biological Review 73, 321 –346. (doi:10.1017/S0006323198005209) Ebensperger, L. A. 1998b Do female rodents use promiscuity to prevent male infanticide? Ethol. Ecol. Evol. 10, 129 –141. Emlen, S. T. 1991 Evolution of cooperative breeding in birds and mammals. In Behavioural ecology: an evolutionary approach (eds J. R. Krebs & N. B. Davies), pp. 301–337, 3rd edn. Oxford, UK: Blackwell Scientific Publications. Faulkes, C. G. & Abbott, D. H. 1997 The physiology of a reproductive dictatorship: regulation of male and female reproduction by a single breeding female in colonies of naked mole-rats. In Cooperative breeding in mammals (eds N. G. Solomon & J. A. French), pp. 302 –334. Cambridge, UK: Cambridge University Press. Faulkes, C. G. & Bennett, N. C. 2007 African mole-rats social and ecological diversity. In Rodent societies (eds J. O. Wolff & P. W. Sherman). Chicago, IL: Chicago University Press. Faulkes, C. G., Bennett, N. C., Bruford, M. W., O’Brien, H. P., Aguilar, G. H. & Jarvis, J. U. M. 1997 Ecological constraints drive social evolution in the African mole-rat. Proc. R. Soc. Lond. B 264, 1619–1627. (doi:10.1098/rspb.1997.0226) French, J. A. 1997 Proximate regulation of singular breeding in callitrichid primates. In Cooperative breeding in mammals (eds N. G. Solomon & J. A. French), pp. 34– 75. Cambridge, UK: Cambridge University Press. Gardner, A. & Grafen, A. 2009 Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659 –671. (doi:10.1111/j.1420-9101.2008.01681.x) Phil. Trans. R. Soc. B (2009)

Gartlan, J. S. 1968 Sturcture and function in primate society. Folia Primatol. 8, 89–120. (doi:10.1159/000155138) Girman, D. J., Mills, M. G. L., Geffen, E. & Wayne, R. K. 1997 A molecular genetic analysis of social structure, dispersal, and interpack relationships of the African wild dog (Lycaon pictus). Behav. Ecol. Sociobiol. 40, 187–198. (doi:10.1007/s002650050332) Gittleman, J. L. 1989 Carnivore group living: comparative trends. In Carnivore behaviour, ecology and evolution (ed. J. L. Gittleman), pp. 183–207. Ithaca, NY: Cornell University Press. Goldizen, A. W. 1987a Facultative polyandry and the role of infant carrying in wild saddle-back tamarins (Saguinus fusicollis). Behav. Ecol. Sociobiol. 20, 99–109. (doi:10.1007/BF00572631) Goldizen, A. W. 1987b Tamarins and marmosets: communal care of offspring. In Primate societies (eds B. B. Smutz & E. Al), pp. 34 – 43, Chicago, IL: Chicago University Press. Goldizen, A. W. 2003 Social monogamy and its variations in callitrichids: do these relate to the costs of infant care? In Monogamy. (ed. C. Boesch), pp. 232–247. Cambridge, UK: Cambridge University Press. Greenwood, P. J. 1980 Mating systems, philopatry and dispersal in birds and mammals. Anim. Behav. 28, 1140– 1162. (doi:10.1016/S0003-3472(80)80103-5) Griffin, A. S., Pemberton, J. M., Brotherton, P. N. M., Gaynor, D. & Clutton-Brock, T. H. 2003 A genetic analysis of breeding success in the cooperative meerkat (Suricata suricatta). Behav. Ecol. 14, 472–480. (doi:10. 1093/beheco/arg040) Grafen, A. 2009 Formalizing Darwinism and inclusive fitness theory. Phil. Trans. R. Soc. B 364, 3135– 3141. (doi:10.1098/rstb.2009.0056) Hamilton, W. D. 1964 The genetical evolution of social behaviour. I. II. J. Theor. Biol. 7, 1–52. (doi:10.1016/ 0022-5193(64)90038-4) Harcourt, A. H., Harvey, P. H., Larson, S. G. & Short, R. V. 1981 Testis weight, body weight and breeding system in primates. Nature 293, 55–57. (doi:10.1038/293055a0) Hart, A. G. & Ratnieks, F. L. W. 2005 Crossing the taxonomic divide: conflict and its resolution in societies of reproductively totipotent individuals. J. Evol. Biol. 13, 383 –395. (doi:10.1111/j.1420-9101.2004.00832.x) Hauber, M. E. & Lacey, E. A. 2005 Bateman’s principle in cooperatively breeding vertebrates: the effects of nonbreeding alloparents on variability in female and male reproductive success. Integr. Comp. Biol. 45, 903–914. (doi:10.1093/icb/45.5.903) Helantera¨, H. & Bargum, K. 2007 Pedigree relatedness, not greenbeard genes, explains eusociality. Oikos 116, 217 –220. (doi:10.1111/j.0030-1299.2007.15411.x) Heyman, E. W. 2003 Monogamy in New World primates: what can patterns of olfactory communication tell us? In Monogamy (ed. C. Boesch), pp. 248–261. Cambridge, UK: Cambridge University Press. Hodge, S. J. 2003 Evolution of helping in a communal breeder: the banded mongoose. Cambridge, UK: University of Cambridge. Hodge, S. J. 2009 Understanding variation in reproductive skew: directions for future empirical research. In Reproductive skew in vertebrates: proximate and ultimate causes (eds R. Hager & C. B. Jones), pp. 439– 466. Cambridge, UK: Cambridge University Press. Hodge, S. J., Manica, A., Flower, T. P. & Clutton-Brock, T. H. 2008 Determinants of reproductive success in dominant female meerkats. J. Anim. Ecol. 77, 92–102. (doi:10.1111/j.1365-2656.2007.01318.x) Holekamp, K. E. & Swale, L. 2000 Feisty females and meek males: reproductive strategies in the spotted hyena.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Mammalian societies In Reproduction in context (eds K. Wallen & J. Schneider), pp. 257 –285. Cambridge, MA: MIT Press. Holekamp, K. E., Smale, L. & Szykman, M. 1996 Rank and reproduction in the female spotted hyena. J. Reprod. Fertil. 108, 229 –237. Hoogland, J. L. 1995 In The black-tailed prairie dog: social life of a burrowing mammal. Chicago, IL: University of Chicago Press. Hrdy, S. B. 1977 The Langurs of Abu: female and male strategies of reproduction. Harvard, MA: University Press. Jarman, P. J. 1974 The social organisation of antelope in relation to their ecology. Behaviour 48, 215–267. (doi:10.1163/156853974X00345) Jarvis, J. U. M. 1991a Reproduction in naked mole-rats. In The biology of the naked mole-rat. (eds P. W. Sherman, J. U. M. Jarvis & R. D. Alexander), pp. 384–425. Princeton, NJ: Princeton University Press. Keller, L. 2009 Adaptation and the genetics of social behaviour. Phil. Trans. R. Soc. B 364, 3209 –3216. (doi:10.1098/rstb.2009.0108) Keller, L. & Nonacs, P. 1993 The role of queen pheromones in social insects: queen control or queen signal? Anim. Behav. 45, 787 –794. (doi:10.1006/anbe.1993.1092) Kitchen, D. M. & Packer, C. R. 1999 Complexity in vertebrate societies. In Levels of selection in evolution (ed. L. Keller), pp. 176– 196. Princeton, NJ: Princeton University Press. Kleiman, D. G. 1977 Monogamy in mammals. Q. Rev. Biol. 52, 39–69. Koenig, W. & Haydock, J. 2004 Incest and incest avoidance. In Ecology and evolution of cooperative breeding in birds (eds W. Koenig & J. L. Dickinson), pp. 142 –156. Cambridge, UK: Cambridge University Press. Krebs, J. R. & Davies, N. B. 1993 An introduction to behavioural ecology, 3rd edn. Oxford, UK: Blackwell Scientific. Kropotkin, P. 1908 Mutual aid. London, UK: William Heinneman. Kutsukake, N. & Clutton-Brock, T. H. 2006 Aggression and submission reflect reproductive conflict between females in cooperatively breeding meerkats Suricata suricatta. Behav. Ecol. Sociobiol. 59, 541– 548. (doi:10.1007/ s00265-005-0079-7) Lack, D. 1968 Ecological adaptation for breeding in birds. London, UK: Methuen. Lewis, S. E. & Pusey, A. E. 1997 Factors influencing the occurrence of communal care in plural breeding mammals. In Cooperative breeding in mammals (eds N. G. Solomon & J. A. French), pp. 335–363. Cambridge, UK: Cambridge University Press. Mcnab, B. K. 1980 Food habits, energetics and the population biology of mammals. Am. Nat. 116, 106–124. (doi:10.1086/283614) Moehlman, P. D. 1986 Ecology of cooperation in canids. In Ecological aspects of social evolution in birds and mammals (eds D. I. Rubenstein & R. W. Wrangham), pp. 282– 302. Princeton, NJ: Princeton University Press. Moehlman, P. D. & Hofer, H. 1997 Cooperative breeding, reproductive suppression and body mass in canids. In Cooperative breeding in mammals (eds N. G. Solomon & J. A. French), pp. 76–128. Cambridge, UK: Cambridge University Press. Nowak, M. A. 2006 Five rules for the evolution of cooperation. Science 314, 1560– 1565. (doi:10.1126/ science.1133755) O’Riain, M. J., Jarvis, J. U. M. & Faulkes, C. G. 1996 A dispersive morph in the naked mole-rat. Nature 380, 619 –621. (doi:10.1038/380619a0) O’Riain, M. J., Bennett, N. C., Brotherton, P. N. M., Mcilrath, G. & Clutton-Brock, T. H. 2000a Reproductive suppression and inbreeding avoidance in wild populations Phil. Trans. R. Soc. B (2009)

T. Clutton-Brock

3241

of cooperatively breeding meerkats (Suricata suricatta). Behav. Ecol. Sociobiol. 48, 471 –477. (doi:10.1007/ s002650000249) O’Riain, M. J., Jarvis, J. U. M., Alexander, R., Buffenstein, R. & Peeters, C. 2000b Morphological castes in a vertebrate. Proc. Natl Acad. Sci. USA 97, 13194– 13197. (doi:10.1073/pnas.97.24.13194) Packer, C. R., Pusey, A. E. & Eberly, L. E. 2001 Egalitarianism in female African lions. Science 293, 690 –693. (doi:10.1126/science.1062320) Parker, G. A. 1974 Assessment strategy and the evolution of fighting behaviour. J. Theor. Biol. 47, 223 –243. (doi:10. 1016/0022-5193(74)90111-8) Perez, V. I. et al. 2009 Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat. Proc. Natl Acad. Sci. 106, 3059–3064. (doi:10.1073/pnas.0809620106) Radcliffe Brown, A. R. 1952 Structure and friction in primitive society. London, UK: Cohen and West. Ratnieks, F. L. W. & Helantera¨, H. 2009 The evolution of extreme altruism and inequality in insect societies. Phil. Trans. R. Soc. B 364, 3169–3179. (doi:10.1098/rstb. 2009.0129) Ratnieks, F. L. W. & Wenseleers, T. 2008 Altruism in insect societies and beyond: voluntary or enforced? Trends in Ecol. Evol. 23, 45–52. (doi:10.1016/j.tree.2007.09.013) Reeve, H. K. & Sherman, P. W. 1991 Intracolonial aggression and nepotism by the breeding female naked mole-rat. In The ecology of the naked mole-rat (eds P. W. Sherman, J. U. M. Jarvis & R. D. Alexander), pp. 337 –357. Princeton, NJ: Princeton University Press. Richards, A. 1939 Land, labour and diet in Northern Rhodesia: an economic study of the Bemba tribe. Oxford, UK: Oxford University Press. Richerson, P. J., Boyd, R. T. & Henrich, J. 2003 Cultural evolution of human cooperation. In Genetic and cultural evolution of cooperation (ed. P. Hammerstein), pp. 357–388. Berlin, Germany: Dahlem. Rood, J. P. 1986 Ecology and social evolution in the mongooses. In Ecological aspects of social evolution (eds D. I. Rubenstein & R. W. Wrangham), pp. 131– 152. Princeton, NJ: Princeton University Press. Ross-Gillespie, A., O’Riain, M. J. & Keller, L. F. 2007 Viral epizootic reveal inbreeding depression in a habitually inbreeding mammal. Evolution 61, 2268–2273. (doi:10. 1111/j.1558-5646.2007.00177.x) Russell, A. F. 2004 Mammals: comparisons and contrasts. In Ecology and evolution of cooperative breeding in birds (eds W. Koenig & J. Dickinson), pp. 210– 227. Cambridge, UK: Cambridge University Press. Russell, A. F., Brotherton, P. N. M., Mcilrath, G. M., Sharpe, L. L. & Clutton-Brock, T. H. 2003a Breeding success in cooperative meerkats: effects of helper number and maternal state. Behav. Ecol. 14, 486– 492. (doi:10.1093/beheco/arg022) Russell, A. F., Sharpe, L. L., Brotherton, P. N. M. & Clutton-Brock, T. H. 2003b Cost minimization by helpers in cooperative vertebrates. Proc. Natl Acad. Sci. USA 100, 3333–3338. (doi:10.1073/pnas.0636503100) Russell, A. F., Carlson, A. A., Mcilrath, G. M., Jordan, N. R. & Clutton-Brock, T. H. 2004 Adapative size modification by dominant female meerkats. Evolution 58, 1600–1607. Scantlebury, M., Speakman, J. R., Oosthuizen, M. K. & Bennett, N. C. 2006 Energetics reveals physiologically distinct castes in a eusocial mammal. Nature 440, 795–797. (doi:10.1038/nature04578) Shellman-Reeve, J. S. 1997 The spectrum of eusociality in termites. In The evolution of social behaviour in insects and arachnids (eds J. C. Choe & B. J. Crespi), pp. 52–93. Cambridge, UK: Cambridge University Press.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3242

T. Clutton-Brock

Review. Mammalian societies

Sherman, P. W. & Jarvis, J. U. M. 2002 Extraordinary life spans of naked mole-rats (Heterocephalus glaber). J. Zool. 258, 307– 311. (doi:10.1017/S0952836902 001437) Sherman, P. W., Jarvis, J. U. M. & Alexander, R. D. (eds) 1991 The biology of the naked mole-rat. Princeton, NJ: Princeton University Press. Sherman, P. W., Lacey, E. A., Reeve, H. W. & Keller, L. 1995 The eusociality continuum. Behav. Ecol. 6, 102 – 108. (doi:10.1093/beheco/6.1.102) Silk, J. B., Clark-Wheatley, C. B., Rodman, P. S. & Samuels, A. 1981 Differential reproductive success and facultative adjustment of sex ratios among captive female bonnet macaques (Macaca radiata). Anim. Behav. 29, 1106–1120. (doi:10.1016/S0003-3472(81)80063-2) Silva, M., Brown, J. H. & Downing, J. A. 1997 Differences in population density and energy use between birds and mammals: a macroecological perspective. J. Anim. Ecol. 66, 327 –340. (doi:10.2307/5979) Smuts, B. B. & Smuts, R. W. 1993 Male aggression and sexual coercion of females in non-human primates and other mammals: evidence and theoretical implications. Adv. Study Anim. Behav. 22, 1 –63. (doi:10.1016/ S0065-3454(08)60404-0) Spong, G. F., Hodge, S. J., Young, A. J. & Clutton-Brock, T. H. 2008 Factors affecting reproductive success of dominant male meerkats. Mol. Ecol. 17, 2287–2299. (doi:10.1111/j.1365-294X.2008.03734.x) Trivers, R. L. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man, 1871– 1971 (ed. B. Campbell), pp. 136 –179. Chicago, IL: AldineAtherton. Van Schaik, C. P. 1983 Why are diurnal primates living in groups? Behaviour 87, 120 –144. (doi:10.1163/ 156853983X00147) Van Schaik, C. P. 2000 Infanticide by male primates: the sexual selection hypothesis revisited. In Infanticide by males and its implications (eds C. P. V. Schaik & C. H. Jansen), pp. 27–60. Cambridge, UK: Cambridge University Press. Vaupel, J. W., Baudisch, A., Dolling, M., Roach, D. A. & Gampe, J. 2004 The case for negative senescence. Theor. Popul. Biol. 65, 339 –351. Wade, M. J. & Arnold, S. J. 1980 The intensity of sexual selection in relation to male behaviour, female choice and sperm precedence. Anim. Behav. 28, 446 –461. (doi:10.1016/S0003-3472(80)80052-2) Walters, J. R. & Seyfarth, R. M. 1986 Conflict and cooperation. In Primate societies. (eds B. B. Smuts,

Phil. Trans. R. Soc. B (2009)

D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker), pp. 306 –317. Chicago, IL: Chicago University Press. Waser, P. M., Elliott, L. F., Creel, N. M. & Creel, S. R. 1995 Habitat variation and mongoose demography. In Serengeti II: dynamics, management and conservation of an ecosystem (eds A. R. E. Sinclair & P. Arcese), pp. 421 –447. Chicago, IL: Chicago University Press. West, S. A., Griffin, A. S. & Gardner, A. 2007a Evolutionary explanations for cooperation. Curr. Biol. 17, R661–R672. West, S. A., Griffin, A. S. & Gardiner, A. 2007b Social semantics: how useful has group selection been? J. Evol. Biol. 21, 374– 385. West, S. A., Griffin, A. S. & Gardiner, A. 2007c Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415–432. (doi:10.1111/j.1420-9101.2006.01258.x) West-Eberhard, M. J. 1975 The evolution of social behaviour by kin selection. Q. Rev. Biol. 50, 1 –35. (doi:10.1086/ 408298) West-Eberhard, M. J. 1981 Intra-group selection and the evolution of insect societies. In Natural selection and social behavior (eds R. A. Alexander & D. W. Tinkle), pp. 3 –17. New York, NY: Chiron Press. Wilson, D. S. & Wilson, E. O. 2007 Rethinking the theoretical foundation of sociobiology. Q. Rev. Biol. 82, 327–348. (doi:10.1086/522809) Woolfenden, G. E. & Fitzpatrick, J. W. 1984 The Florida scrub jay: demography of a cooperative-breeding bird. Princeton, NJ: Princeton University Press. Wrangham, R. W. 1980 An ecological model of femalebonded primate groups. Behaviour 75, 262–300. (doi:10.1163/156853980X00447) Wright, J., Malkakov, A. A. & Khazin, V. 2000 Statedependent sentinels: an experimental study in the Arabian babbler. Proc. R. Soc. Lond. B 268, 821–826. (doi:10.1098/rspb.2000.1574) Wynne-Edwards, V. C. 1962 In Animal dispersion in relation to social behaviour. Edinburgh, UK: Oliver and Boyd. Young, A. J. & Clutton-Brock, T. H. 2006 Infanticide by subordinates influences reproductive sharing in cooperatively breeding meerkats. Biol. Lett. 2, 385 –387. (doi:10.1098/rsbl.2006.0463) Young, A. J., Carlson, A. A., Monfort, S. L., Russell, A. F., Bennett, N. C. & Clutton-Brock, T. 2006 Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc. Natl Acad. Sci. USA 103, 12 005– 12 010. (doi:10.1073/pnas.0510038103)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3243–3254 doi:10.1098/rstb.2009.0118

Review

Nepotistic cooperation in non-human primate groups Joan B. Silk* Department of Anthropology, University of California, Los Angeles, CA, USA Darwin was struck by the many similarities between humans and other primates and believed that these similarities were the product of common ancestry. He would be even more impressed by the similarities if he had known what we have learned about primates over the last 50 years. Genetic kinship has emerged as the primary organizing force in the evolution of primate social organization and the patterning of social behaviour in non-human primate groups. There are pronounced nepotistic biases across the primate order, from tiny grey mouse lemurs (Microcebus murinus) that forage alone at night but cluster with relatives to sleep during the day, to cooperatively breeding marmosets that rely on closely related helpers to rear their young, rhesus macaque (Macaca mulatta) females who acquire their mother’s rank and form strict matrilineal dominance hierarchies, male howler monkeys that help their sons maintain access to groups of females and male chimpanzees (Pan troglodytes) that form lasting relationships with their brothers. As more evidence of nepotism has accumulated, important questions about the evolutionary processes underlying these kin biases have been raised. Although kin selection predicts that altruism will be biased in favour of relatives, it is difficult to assess whether primates actually conform to predictions derived from Hamilton’s rule: br . c. In addition, other mechanisms, including contingent reciprocity and mutualism, could contribute to the nepotistic biases observed in non-human primate groups. There are good reasons to suspect that these processes may complement the effects of kin selection and amplify the extent of nepotistic biases in behaviour. Keywords: kin selection; cooperation; kin recognition; primate; altruism

1. INTRODUCTION In 1838, Charles Darwin made the acquaintance of Jenny, the first orangutan exhibited in England. His visits with Jenny at the Regents Park Zoo in London made a deep impression on him: ‘Let man visit Ouranoutang in domestication, hear its expressive whine, see its intelligence when spoken [to]; as if it understands every word said—see its affection. —to those it knew. —see its passion & rage, sulkiness, & very actions of despair; . . . and then let him boast of his proud preeminence. . . Man in his arrogance thinks himself a great work, worthy the interposition of a deity. More humble and I believe true to consider him created from animals’. Others were also struck by the similarities between humans and apes. When Queen Victoria contemplated Jenny’s replacement and namesake in May 1842, she found her ‘. . . frightful, and painfully and disagreeably human’. Darwin believed that the similarity between apes and humans was the consequence of shared ancestry, but so little was known about the origin and behaviour of apes and other primates that he did not appreciate the full extent of the connections between humans and other primates. Today, 170 years after Darwin

*[email protected] One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

first met Jenny, we have a firm understanding of the phylogenetic relationships between ourselves and other primates, and we have accumulated a large body of information about the social behaviour of the diverse members of the primate order. Biological kinship has emerged as a primary organizing force in the evolution of primate social organization and the patterning of social behaviour within primate groups. Had Darwin known that other primates distinguish kin from non-kin, form enduring relationships with their offspring, selectively groom, support and reconcile conflicts with their relatives and are aware of the kinship relationships between other group members, he would have been even more certain of the deep evolutionary links between humans and other animals. The first clue about the role of biological kinship in primate groups emerged from studies of indigenous populations of Japanese macaques (Macaca fuscata). Imanishi and his co-workers were the first to systematically monitor the behaviour of known (and named) individuals and to conduct continuous, long-term observations of social groups (Matsuzawa & McGrew 2008). These observations allowed them to construct dominance hierarchies for both sexes and to construct matrilineal geneologies. This led to the discovery that females acquire their mothers’ dominance ranks (Kawai 1958; Kawamura 1958). These findings were complemented by pioneering observations of the behaviour of rhesus macaques (Macaca mulatta) on

3243

This journal is # 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3244

J. B. Silk

Review. Primate nepotism

Cayo Santiago Island, which documented strong and enduring maternal kin biases in association, tolerance, grooming and play in rhesus macaques (Rawlins & Kessler 1986). But it was not until the publication of Wilson’s (1975) Sociobiology: the new synthesis that primatologists linked these empirical findings about nepotistic biases in social behaviour to kin selection theory (Kurland 1977). Then, primatologists began to focus on the role of kin selection in the distribution of altruistic behaviours, such as grooming and support, in primate groups (Chapais & Berman 2004), and the logic of kin selection was integrated into socioecological models of the evolution of primate social organization (Wrangham 1980; van Schaik 1983; Sterck et al. 1997; Isbell & Young 2002). In this paper, I review what we have learned about the mechanisms underlying kin recognition and the nature and extent of kin biases in behaviour in primates. I use primate social organization as the organizing framework for the review of nepotistic biases in behaviour because the size and composition of social groups influence the availability of kin and the potential for kin biases in behaviour to develop. We know much more about the effects of maternal relatedness on the distribution of altruistic behaviour than we do about the effects of paternal relatedness because of uncertainties about the paternity of infants born in multi-male groups. In addition, research effort has not been evenly distributed across the primate order so we know much more about the behavioural strategies of some Old World monkeys and apes than we do about most New World primates or prosimians. 2. KIN RECOGNITION MECHANISMS In order for kin selection (Hamilton 1964) to favour the evolution of altruistic behaviour, animals must direct altruism selectively to relatives. Hamilton (1987) predicted that the ability to identify kin would be most fully developed in species that live in social groups; when there are opportunities for costly behaviours, such as egg dumping or infanticide; and when passive, context-dependent mechanisms for distinguishing kin from non-kin are not likely to be effective. Primates clearly fit these three conditions. Most primates live in large and relatively stable social groups (Smuts et al. 1987). Even the most solitary primates such as orangutans and galagos have regular interactions with familiar conspecifics (Galdikas 1988; Nash 2004). Primates engage in a variety of fitness-reducing behaviours, including severe intragroup aggression and infanticide (van Schaik & Janson 2000). Finally, most primates live for extended periods of time in groups that include both relatives and non-relatives, so context-driven mechanisms for distinguishing kin are likely to be of limited use.

Mothers nurse, nuzzle and inspect their newborns and are thought to learn to recognize their smell, voice or appearance during the first few weeks of life. Similarly, infants may learn to recognize their mothers during this period. The importance of early familiarity is supported by the evidence that captive ‘foster’ mothers routinely accept strange infants, even when they are not the same sex, exact ages or species as their own infants (Deets & Harlow 1974; Bernstein 1991; Owren & Dieter 1989). Lasting associations between mothers and offspring may also provide opportunities for identifying other categories of maternal kin. Juveniles may see their mothers nursing younger offspring, providing cues about their relationship to siblings. Mothers may observe their adult daughters nursing their grandoffspring, and females may observe their sisters nursing nephews or nieces. Other behavioural cues such as high rates of association or grooming may enable young monkeys to identify their older siblings, aunts and grandmothers. In some cases, group membership may provide reliable cues of kinship. In cooperatively breeding and pair-bonded species, most infants born in the group will be half or full siblings. However, extrapair copulations may reduce relatedness among offspring to the level of half siblings. Group membership and early association provide less information about paternal kinship than maternal kinship. In most primate species, females do not form extended associations with their mates, limiting infants’ abilities to deduce their fathers’ identity through associations with their mothers. Baboons may constitute an exception to this rule, as close associations between mothers of newborn infants and their former mating partners may provide reliable predictors of paternity (Buchan et al. 2003; Moscovice et al. 2009). Paternal kin recognition may also be based on consistent correlates of relatedness within primate groups. As Altmann (1979) originally pointed out, when a single male monopolizes mating opportunities within a group, age mates are likely to be paternal half siblings. Therefore, primates might use age similarity as a proxy for paternal relatedness. Genetic evidence indicates that there is considerable reproductive skew in many primate species, including species that normally live in multi-male groups (reviewed by Widdig 2007). Within the genus Macaca, the extent of male reproductive skew is associated with the nature of female – female relationships within groups. In species with the most reproductive skew, and presumably the highest levels of paternal relatedness, females have the most tolerant social relationships (Schu¨lke & Ostner 2008). Thus, contextual cues such as age similarity may be reliably associated with paternal relatedness in a broad range of primate species.

(a) Familiarity Close association early in life is generally thought to be the primary basis for kin recognition in mammalian groups (Holmes & Sherman 1983), including primates (Bernstein 1991; Rendall 2004). In most species of monkeys and apes, infants remain in constant contact with their mothers during the first few weeks of life.

(b) Phenotypic cues Phenotypic cues such as odour, vocal qualities or physical appearance could all play a role in primate kin recognition systems (reviewed by Rendall 2004; Widdig 2007). Animals may detect phenotypic similarities between themselves and others or acquire a

Phil. Trans. R. Soc. B (2009)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Primate nepotism template based on the phenotype of familiar relatives and use this template to identify other relatives (Holmes & Sherman 1983; Tang-Martinez 2001; Holmes & Mateo 2007). Odour, which is linked to variation in major histocompatability complex (MHC) alleles, plays an important role in kin recognition systems in some mammalian species. However, over the course of primate evolution, there has been a reduction of emphasis on olfaction and a concomitant increase in emphasis in vision. In macaques and chimpanzees (Pan troglodytes), approximately one-third of the olfactory receptor genes carry one or more coding gene disruptions and have become pseudogenes (Widdig 2007). In humans, over half of the analogous genes have become pseudogenes. Nonetheless, human mothers can recognize the odour of their own offspring, and humans can distinguish the odours of kin, friends and strangers (Weisfeld et al. 2003). In addition, women are attracted to the odour of men with human leucocyte antigen genes (equivalent to MHC) that are similar, but not identical, to their own ( Jacob et al. 2002). This suggests that while monkeys and apes may have lost much of their olfactory acuity, olfactory cues could still play some role in their kin recognition systems. Efforts to determine the role of phenotypic cues in primate kin recognition systems have generated mixed results. The first attempt to examine this question was conducted by Wu et al. (1980). They showed that young pig-tailed macaques (Macaca nemestrina), who were reared apart from all relatives, showed consistent preferences for unfamiliar half siblings over unfamiliar non-kin (matched for age and sex) on their first encounter. In these experiments, preferences were measured using differential rates of approaches and visual inspections of the unfamiliar monkeys. Later, Fredrickson & Sackett (1984) and Sackett & Frederickson (1987) designed an experiment to assess the relative importance of familiarity and kinship in young peer-housed pig-tailed macaques’ social preferences. They created four categories of test stimuli (familiar kin, unfamiliar kin, familiar non-kin and unfamiliar non-kin) and presented pairs of test stimuli to their subjects. Subjects showed strong preferences for familiar kin over unfamiliar kin and for familiar non-kin over unfamiliar non-kin, but the effects of kinship on their social preferences were more equivocal. When subjects were presented with unfamiliar kin and unfamiliar non-kin, they tended to prefer kin. On the other hand, the monkeys did not distinguish between familiar kin and familiar non-kin. Based on these two studies, Frederickson & Sackett concluded that ‘. . . familiarity alone is responsible for preference in these laboratory choice tests’. They suggested that the findings reported by Wu et al. were the product of a type I statistical error. Two additional laboratory studies, which attempted to disentangle familiarity and genetic kinship, failed to demonstrate paternal kin recognition (Welker et al. 1987; Erhart et al. 1997), whereas a third study provided some evidence of preferences for unfamiliar paternal kin (MacKenzie et al. 1985). These findings led most researchers to conclude that phenotypic Phil. Trans. R. Soc. B (2009)

J. B. Silk

3245

cues do not play an important role in primate kin recognition systems (e.g. Rendall 2004). Holmes (2004), one of the authors of the original paper, has questioned Frederickson & Sackett’s rationale for discounting the original results. He points out that the two studies generated quite similar patterns for the one comparison that was common to both studies: unfamiliar kin versus unfamiliar non-kin. In both cases, monkeys showed a preference for unfamiliar kin over unfamiliar non-kin, although the authors reached different conclusions about the statistical significance of the results. However, if monkeys can reliably discriminate between unfamiliar kin and non-kin, then why did not they differentiate between familiar kin and familiar non-kin in Frederickson & Sackett’s study? It is possible that close, continuous association very early in life is a cue used to discriminate maternal kin from others. If so, infants who are reared from birth in small peer groups may (falsely) label all members of their groups as maternal kin. But when confronted with unfamiliar monkeys, they may make use of a different set of cues, such as similarity to themselves. The debate about the importance of phenotypic cues in primate kin recognition systems was rekindled when Parr & de Waal (1999) reported that chimpanzee females were able to match digitized photographs of unfamiliar females with their sons (but not with their daughters). Because the chimpanzees were unfamiliar with the individuals in the photographs and had no physical, auditory or olfactory contact with them, their ability to identify mother– son pairs suggested that chimpanzees use visual cues to assess similarity. However, a detailed analysis of features of the images revealed that there were subtle differences in the ways that the photographic images were framed, and this is probably what enabled subjects to match mothers with sons, but not with daughters (Vokey et al. 2004). Several studies indicated that primates can discriminate between paternal kin and others in more naturalistic settings (reviewed by Widdig 2007; discussed subsequently). Although the mechanisms underlying paternal kin recognition in these cases have not been established, some evidence suggests that monkeys do not rely entirely on contextual cues, such as age similarity or maternal associations, to identify paternal kin (Alberts 1999; Widdig et al. 2001). For example, Widdig and her co-workers found that rhesus macaques distinguished peers who were paternal half siblings and peers who were unrelated to themselves, suggesting that age proximity is not the only cue that the monkeys used to identify paternal kin.

3. EPOTISTIC BIASES IN PRIMATE SOCIETIES (a) Non-gregarious primates In a number of prosimian primates, adults spend much of their time alone or in the company of their dependent offspring. In some of these species, maternal kinship structures the neighbourhoods in which females live. Dwarf lemurs (Mirza coquereli ) in Madagascar forage alone during the night, and rest

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3246

J. B. Silk

Review. Primate nepotism

alone during the day. However, females tend to establish territories near their mothers, creating a multi-generational matrilineal community of females (Kappeler et al. 2002). Similar patterns may characterize some galago species (Nash 2004) as well as orangutans (Pongo pygmaeus), the only solitary ape (Delgado & van Schaik 2000). Grey mouse lemurs, Microcebus murinus, elaborate on this pattern. The home ranges of matrilineal female kin are clustered in space, and females forage alone at night. However, females often gather together to sleep during the day and sometimes nurse one another’s young (Eberle & Kappeler 2006). These sleeping groups are primarily composed of matrilineal female kin (Radespiel et al. 2001; Wimmer et al. 2002; Eberle & Kappeler 2006). (b) Cooperatively breeding species Marmosets and tamarins, members of the subfamily Callitrichinae, live in small territorial groups that are composed of a single breeding pair, several nonbreeding adults, who are generally same-sexed siblings of the breeding pair or mature offspring from previous litters of the breeding pair, and dependent offspring (French 1997; Tardiff 1997; Dietz 2004). Breeding females typically give birth to fraternal twins and can produce two litters per year. The cost of reproduction in callitrichids, measured in terms of litter weight and standardized for allometry, is considerably higher than in solitary, pair-bonded or plural breeding primate species (Harvey et al. 1986). After females give birth, all mature group members provide extensive help carrying and provisioning infants. Pairs with helpers sustain higher rates of fertility than pairs without helpers. Genetic chimerism may have facilitated the evolution of cooperative breeding within this lineage. Callitrichid twins typically share a common placenta and chorion (the membrane that surrounds the growing embryo in the uterus). Stem cells are passed from one twin to the other (Haig 1999). This process extends to somatic tissues and gametes (Ross et al. 2007). This means that individuals sometimes pass along their twin’s genes, not their own. Chimerism effectively raises the degree of relatedness among twins and may increase the inclusive fitness benefits derived from helping to rear nephews and nieces (Haig 1999). (c) Species with female philopatry There are pronounced matrilineal biases in behaviour in a number of primate taxa that are characterized by female philopatry and male dispersal, particularly cercopithecine primates, including all species of macaques (Macaca spp.), savannah baboons (Papio cynocephalus spp.) and vervet monkeys (Clorocebus aethiops). In these species, affiliative and cooperative behaviours are biased in favour of kin. For example, female baboons spend much of their time in close proximity to related females, and they groom kin at considerably higher rates than they groom unrelated individuals. Similarly, females reconcile conflicts with kin at higher rates than they reconcile conflicts with Phil. Trans. R. Soc. B (2009)

non-kin. Females in these species also intervene on behalf of close kin when they are involved in aggressive interactions more often than they intervene on behalf of more distantly related relatives or non-relatives. The most risky forms of intervention tend to be limited to close relatives. For detailed reviews of the kin biases in cercopithecine primate groups, see Berman (2004), Chapais (2001), Kapsalis (2004) and Silk (2001, 2005). Preferential treatment generally extends to mothers, offspring, siblings, grandmothers, grandoffspring and sometimes to aunts and nieces, but not to more distant kin (Kapsalis & Berman 1996). Thus, the threshold for nepotism seems to be somewhere between 0.25 and 0.125. It is not clear if this threshold represents the boundaries of kin recognition or reflects the fact that it is progressively more difficult to satisfy Hamilton’s rule as relatedness declines. Sherman (1980, 1981) suggested that kin selection will not favour the ability to recognize categories of relatives that are not encountered on a regular basis. In the provisioned groups of macaques that were first studied in Japan and on Cayo Santiago, predators are rare, food is plentiful, female fertility is high and infant mortality is low. This produces very large matrilineal units and considerable generational overlap. In more naturalistic settings, matrilines are considerably smaller, and certain categories of kin are surprisingly uncommon. For example, adult female baboons virtually never live in groups with adult granddaughters and have very few cousins (Silk et al. 2006a). Maternal kin biases contribute to the formation of matrilineal dominance hierarchies in macaques, baboons and vervets. Mothers sometimes support their juvenile offspring when they are involved in disputes with group members that the mother outranks. As they mature, young females typically acquire rank positions immediately below their mothers (reviewed by Chapais 2002). Mothers typically support younger daughters over older daughters and maturing females normally rise in rank over their older sisters. Several lines of evidence suggest that nepotistic support plays a critical role in rank acquisition. First, if females are orphaned when they are young, they may not achieve their mothers’ original rank (Walters 1980; Johnson 1987). Second, small juveniles from high-ranking matrilines can defeat larger juveniles from lower ranking matrilines when their mothers are nearby, but not when their mothers are some distance away (Datta 1983a,b,c; Horrocks & Hunte 1983). Third, Chapais designed a series of experiments to assess the importance of nepotistic support in the formation of matrilineal dominance hierarchies in macaque groups (Chapais 1988a,b; Chapais et al. 1997). The basic protocol involved removing pairs or trios of monkeys from their social group and housing them in temporary subgroups. Chapais (1988a) found that when juveniles were paired with a higher ranking juvenile of their own size and age, they did not challenge them. But when the same juveniles were joined in these subgroups by their mothers (r ¼ 0.5), older sisters (r ¼ 0.25) or grandmothers (r ¼ 0.25), they challenged higher ranking peers,

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Primate nepotism were frequently supported by their older relatives and successfully reversed their ranks. Matrilineal dominance hierarchies are remarkably stable over time (Kapsalis 2004), and this was originally attributed to coalitionary alliances among maternal kin (e.g. Chapais 1988a,b; Silk 2001). However, there is now some uncertainty about the role of nepotistic support in the maintenance of dominance relationships within groups. In an experimental study, Chapais & St-Pierre (1997) showed that alliances among unrelated females against lower ranking females may contribute to the stability of dominance relationships within macaque groups. Moreover, in a series of papers (Henzi & Barett 1999; Barrett & Henzi 2002, 2005), it has been pointed out that the rates of intervention in baboon groups with very stable dominance hierarchies are often quite low and, in some cases, are not seen at all. In some groups, females maintain high ranks for many years, even though they have no adult relatives in the group. Thus, high levels of active coalitionary support from kin may not be needed for females to maintain their ranks. However, it is possible that the frequency of coalitionary support is not an accurate measure of its importance. The presence of potential allies may deter challenges from subordinate females (Cords 2002). Moreover, less-active forms of coalitionary support may play an important role in mediating disputes among females. Most studies of coalitionary support focus on active forms of intervention, such as chasing or threatening a common opponent. Wittig et al. (2007) showed that females sometimes give aggressive vocalizations when they observe conflicts involving others. These ‘vocal alliances’ occur 1.4 times as often as more active forms of support, and both vocal alliances and active support are biased in favour of close kin (mothers, daughters and sisters). Playback experiments showed that aggressive vocalizations by close relatives of their former opponents altered aggressors’ behaviour: they were more likely to behave submissively and less likely to approach their former opponents. Kin biases in behaviour are linked to female reproductive success in two different ways. First, high-ranking cercopithecine females tend to mature at earlier ages, grow faster, produce healthier infants, have shorter interbirth intervals and achieve higher lifetime fitness than low-ranking females (reviewed by Harcourt 1987; Silk 1993; Altmann & Alberts 2003; Cheney et al. 2004). The magnitude of the effects of dominance rank varies over time and across populations. However, any reproductive advantages that high-ranking females accrue will be magnified over time because dominance hierarchies remain stable over time. Second, female baboons, who are more fully integrated into their social groups (Silk et al. 2003) and have stronger social bonds with adult females (Silk et al. 2009), have high survivorship among their offspring than other females within their groups. These effects are independent of differences in female dominance rank and variation in the quality of the environment in which females live. We know much more about the behaviour of macaques, baboons and vervets than we do about Phil. Trans. R. Soc. B (2009)

J. B. Silk

3247

the behaviour of other primates with female philopatry, such as South American capuchin monkeys (Cebus spp.) and ring-tailed lemurs (Lemur catta). The most complete analyses of maternal kin biases among capuchins come from a 10-year study of one group of white-faced capuchins, Cebus capucinus, in Costa Rica (Perry et al. 2008). In this group, females selectively groomed and associated with their mothers, daughters and maternal sisters (both full and half sisters). Maternal kin biases were more pronounced when the group was relatively large and average degrees of relatedness among females were relatively low than when the group was smaller and average degrees of relatedness among females were relatively high. Although females showed kin biases in support, they did not form matrilineal dominance hierarchies and the dominance hierarchy was not as stable as those in cercopithecine species. Ring-tailed lemur groups are composed of several matrilines. Like white-faced capuchins, female ringtailed lemurs show nepotistic biases in affiliative behaviour, but do not form matrilineal dominance hierarchies (Nakamichi 1997; Nakamichi & Koyama 1997; Jolly & Pride 1999; Sauther et al. 1999). Although coalitionary aggression is rare (Nakamichi & Koyama 1997; Sauther et al. 1999), nepotistic alliances may play an important role in some circumstances. For example, Nakamichi (1997) describes one case in which a female was able to regain her high-ranking position with the support of her adult daughter. Moreover, when groups become too large, members of one matriline may collectively target members of another matriline for eviction (Sauther et al. 1999). Although single females never move from one group to another, mothers and daughters are sometimes able to do so together (Sauther et al. 1999). Several recent studies have demonstrated patrilineal kin biases in species with female philopatry. In baboon and rhesus macaque groups, females are more likely to associate with and groom paternal half sisters than unrelated females (Widdig et al. 2001, 2002; Smith et al. 2003; Silk et al. 2006a). Female rhesus macaques do not selectively support their paternal half sisters in agonistic encounters, but they do avoid intervening against them (Widdig et al. 2006). Juvenile mandrills show preferences for adult paternal half siblings over unrelated adults, but not for juvenile paternal half siblings over unrelated juveniles (Charpentier et al. 2007). Females baboons and macaques generally form substantially stronger bonds with maternal half sisters than with paternal half sisters (Widdig et al. 2001, 2002; Silk et al. 2006a), but female baboons form stronger bonds with their paternal half sisters when close maternal kin are not available (Silk et al. 2006a). In contrast to the patterns observed in baboon and macaque groups, white-faced capuchins do not show preferences for paternal half sisters over unrelated individuals (Perry et al. 2008), even though male reproductive skew is as high in these groups as it is in baboon and macaque groups (Muniz et al. 2005). There are not yet enough studies of paternal kin discrimination to identify ecological, demographic or phylogenetic factors that might facilitate paternal

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3248

J. B. Silk

Review. Primate nepotism

kin discrimination or favour paternal kin biases in behaviour in some species, but not others. (d) Species with male philopatry Male philopatry characterizes a small number of primate species, including chimpanzees, bonobos (Pan paniscus), spider monkeys, muriquis and woolly spider monkeys (Pusey & Packer 1987). Social relationships among male chimpanzees have been studied almost as extensively as social relationships among cercopithecine primate females. Chimpanzee males spend a considerable amount of time in parties with other males, and males groom, hunt, share meat, aid and patrol the borders of their territories with one another (Muller & Mitani 2005; Gilby & Wrangham 2008). The structure of males’ social bonds is strikingly similar to that of social bonds among female baboons, although the extent of nepotism is considerably less pronounced (Mitani 2009). In chimpanzee communities, males tend to form close relationships with their maternal brothers when they are available (Nishida 1979; Goodall 1986; Langergraber et al. 2007; Mitani 2009), but many males do not have brothers in their groups and kinship does not seem to be a necessary ingredient of close relationships among male chimpanzees (Langergraber et al. 2007; Gilby & Wrangham 2008). Male chimpanzees do not seem to discriminate between paternal half brothers and unrelated males (Langergraber et al. 2007). For male chimpanzees, contingent reciprocity may play a more important role than kinship in shaping social relationships. Although chimpanzee males spend much of their time in the company of other males, they do spend some time travelling and foraging alone. When males are alone, they range in the core areas of their mothers, even if their mothers are no longer alive (Murray et al. 2008). High-ranking females occupy higher quality core areas than low-ranking females, so their sons may gain advantages from inheriting their core areas. There are a number of parallels between male chimpanzees, spider monkeys and male muriquis, although our knowledge of the social dynamics in these New World monkeys is much less complete. Like chimpanzees, male spider monkeys and muriquis associate and affiliate at high rates (Strier et al. 2002; Slater et al. 2009). Spider monkeys launch joint raids into neighbouring territories (Aureli et al. 2006), and male muriquis cooperate in hostile intergroup encounters (Strier 1994). Muriqui males maintain egalitarian social relationships and share access to receptive females (Strier et al. 2002). Limited evidence suggests that maternal kinship is not a necessary ingredient of social bonds among male muriquis (Strier et al. 2002), but we do not yet know whether there are kin biases among spider monkeys. (e) Kin biases in the dispersing sex Maternal kin biases can also be detected in some species in which females emigrate from their natal groups. For example, most female mountain gorillas (Gorilla gorilla berengei) leave their natal groups, but dispersing females sometimes join groups that contain Phil. Trans. R. Soc. B (2009)

females from their natal group. In some cases, females, who are likely to be sisters, emigrate together (Harcourt & Stewart 1987). Thus, even though females are not philopatric, nearly 70 per cent of the females spend at least some of their reproductive years in the company of female kin (Watts 1996). When females live with related females, they tend to show strong nepotistic preferences. Adult female mountain gorillas spend more time resting and feeding near their relatives than non-relatives, rarely fight with kin and are more likely to groom and support kin than non-kin (Harcourt & Stewart 2007). Similarly, some chimpanzee females remain in their natal groups throughout their lives. When they do, they often develop enduring social relationships with their mothers (Williams et al. 2002; Gilby & Wrangham 2008). In red howler (Alouatta seniculus) groups, opportunities for maternal kin biases vary over the course of time. New groups are formed when solitary migrating females meet, form ties, attract males, establish territories and begin to reproduce (Pope 2000). As time passes, the natal females are recruited and the average degree of relatedness among females rises. Eventually, the average degree of relatedness approaches 0.5 (Pope 1998, 2000). This has adaptive consequences for females because their reproductive success is correlated with the degree of relatedness within their groups (Pope 2000).

(f) Paternal care Until recently, true paternal care was assumed to be limited to pair-bonded species with high paternity certainty. However, a growing body of evidence suggests that paternal care is more widespread. In some multi-male baboon groups, males selectively support their own offspring in agonistic encounters (Buchan et al. 2003) but in others paternal biases are not detected (Moscovice et al. 2009). The presence of fathers also accelerates the maturation of their offspring (Charpentier et al. 2008). Male chimpanzees play more with their own offspring than with unrelated infants (Lehmann et al. 2006), and juvenile mandrills associate at higher rates with their fathers than with unrelated males (Charpentier et al. 2007). Males in a number of species protect their own offspring from harassment by potentially infanticidal males (Palombit 2000). Alliances among fathers and sons may develop in some primate species. When local habitats are saturated and red howler groups are large, single males have difficulty defending groups of females. In these situations, red howler males sometimes form coalitions. Although the dominant male within the coalition monopolizes conceptions, males collectively defend females against incursions by foreign males and jointly challenge residents for access to groups of females. Some coalitions are composed of related males, often fathers and sons (Sekulic 1983). Father– son coalitions stay together considerably longer and have more stable dominance relationships than coalitions of unrelated males (Pope 1990). Kinship may enhance the stability of coalitions

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Primate nepotism because the lower-ranking male gains inclusive fitness benefits by assisting his father or son to reproduce. Similarly, mountain gorillas generally form onemale groups, but multi-male groups can be formed when silverbacks are joined by younger natal males (Harcourt & Stewart 1997; Watts 2000). Male residents cooperate in aggression against outside males. The males who form these coalitions may be fathers and sons (Watts 2000). When lowland gorilla (Gorilla gorilla gorilla) males leave their natal groups, they sometimes establish territories within the same area. The resident males in neighbouring lowland gorilla groups are closely related (Bradley et al. 2004), and their relatedness may explain why male silverbacks from neighbouring territories have relatively peaceful relationships. Patrilineal associations are also suspected to occur in hamadryas baboons (Papio hamadryas), which form multi-level societies (Stammbach 1987). The resident males in one-male units are sometimes replaced by males who are thought to be their sons (Sigg et al. 1982). Although one-male units spend much of their time near one another, leaders of one-male units rarely attempt to take females from other males in their clans and are quite tolerant of the males in their clans. Based on phenotypic similarities, males in the same band are thought to be related (Stammbach 1987).

4. DO PRIMATES CONFORM TO HAMILTON’S RULE? There is abundant evidence of nepotistic biases in primate groups. Altruistic behaviours, including grooming, coalitionary support and food sharing, are selectively directed towards genetic relatives. Moreover, these behaviours are preferentially directed towards closer kin over more distant kin. Both these patterns are consistent with qualitative predictions derived from kin selection theory and are commonly interpreted as the product of kin selection. It is much more difficult to determine whether the distribution of altruistic behaviour fits quantitative predictions derived from Hamilton’s rule, br . c. This is because we are unable to measure the fitness benefits of altruistic acts for recipients and the costs of altruistic acts for donors. There is not even complete agreement about whether particular forms of behaviour are altruistic (Chapais 2001; Chapais & Be´lisle 2004). For example, Dunbar (1988) and Dunbar & Sharman (1984) concluded that grooming must not be costly to perform because females do not reduce the amount of time that they devote to social grooming when they are under time budget constraints and do reduce the amount of time that they devote to other energetically expensive activities. But the same data could be interpreted to mean that grooming is costly, but serves essential social functions, and is too important to be neglected even in difficult times. Similarly, there is debate about the costs and benefits of coalitionary aggression, sharing access to food, giving alarm calls, forming friendships with new mothers and so on. Phil. Trans. R. Soc. B (2009)

J. B. Silk

3249

Quantitative predictions about the distribution of altruism are difficult to formulate because they depend on assumptions about the shape of the curve of benefits across time. For example, if the benefits of being groomed are constant across time, then all grooming should be directed towards the closest kin available (Altmann 1979). But if there are declining returns from grooming across time, then groomers should eventually switch to less closely related partners. Constraints on time and energy, variation in the availability of preferred categories of partners, the opportunity costs of choosing more closely related partners over more competent partners, the possible benefits derived from reciprocity and a number of other factors further complicate predictions about the deployment of altruism in primate groups (Chapais & Be´lisle 2004). As a result, ‘the optimal allocation of altruism is unknown’ (Altmann 1979), and Hamilton’s rule cannot be tested with any degree of precision. Chapais has suggested that this ambiguity may have encouraged us to overestimate the role of kin selection and underestimate the importance of other forces in the distribution of altruistic behaviour (Chapais 2001, 2006; Chapais & Be´lisle 2004). There are at least two processes besides kin selection that could generate high rates of interaction among kin: (i) kin biases could reflect an attraction to animals of similar rank or (ii) kin biases could be a by-product of extended associations between mothers and their offspring. In species with matrilineal dominance hierarchies, nepotistic biases may reflect an attraction to animals of similar rank, not an attraction to kin per se. This argument was first proposed by Seyfarth (1977), who suggested that females might exchange grooming for support in agonistic conflicts. Because high-ranking females make the most powerful allies, he predicted that all females would direct their grooming efforts towards the highest ranking females in their groups. However, time budgets constrain the amount of time available for being groomed (Dunbar 1991), so females would have to compete for access to the highest ranking females. High-ranking females would be able to monopolize access to other high-ranking females, forcing lower ranking females to settle for grooming partners closer to their own rank and to trade grooming in kind. Related females occupy adjacent ranks, so this process would incidentally generate high rates of grooming among kin. Thus, kin biases emerge from competition over access to high-ranking allies. Several of the primary predictions of Seyfarth’s model are well supported. Correlations between grooming and support are consistently observed, and monkeys interact at high rates with those of similar rank (Schino 2001; Schino & Aureli 2007). However, there are several reasons to suspect that kin biases in behaviour are not simply an artefact of an attraction to females of similar rank. First, in baboons and macaques, females’ preferences for maternal kin are stronger than their preference for unrelated females of adjacent rank (Silk 1982; De Waal 1991; Kapsalis & Berman 1996; Silk et al. 1999). Second, dominance rank and maternal kinship

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3250

J. B. Silk

Review. Primate nepotism

are disassociated in some species, but nepotistic biases persist (hanuman langurs, Borries et al. 1992; mountain gorillas, Watts & Pusey 1993; capuchins, Perry et al. 2008; ring-tailed lemurs, Sauther et al. 1999). Third, female baboons and macaques show preferences for paternal kin, who do not hold adjacent ranks (references above). In species with female philopatry, matrilineal biases in behaviour may be the by-product of mother – infant association patterns, not the products of kin selection (Chapais 2001, 2006). Mothers form close and enduring ties with their offspring. This means that as mothers wean one infant and produce another, they continue to associate with their older offspring. Maternal siblings are drawn together by their joint association with their mother. As daughters mature and produce offspring of their own, grandmothers and their grandoffspring will be brought together often. Aunts are similarly connected to their sister’s daughters, their own nieces. If females interacted at random with their associates, high rates of interaction among kin would emerge without any deliberate preference for interacting with relatives. This sort of process may influence the interactions of females in some situations. Young macaques interact at higher rates with the offspring of females that their mothers associate with at higher rates, and the degree of infants’ kin biases is linked to the degree of their mothers’ kin biases (Berman 2004). In the Amboseli baboon groups, females groom and associate with their adult sisters and their sisters’ daughters (nieces) at higher rates than they associate with unrelated females. Rates of interactions between aunts and nieces decline when the female who connects them dies (the aunt’s sister and the niece’s mother; Silk et al. 2006a). But there are several reasons to believe that this is not the whole story. In the Amboseli baboon population, rates of interaction among maternal and paternal sisters rise after their mothers’ deaths. This suggests that relationships among sisters are the product of a positive attraction towards preferred categories of partners. Moreover, if high rates of affiliation among close kin are simply a by-product of high rates of association, then we would also expect to observe elevated rates of aggression among them (Perry et al. 2008). But rates of aggression among capuchins do not track rates of affiliation or the degree of relatedness among females, suggesting that ‘kin-biased distribution of grooming and coalitionary support is a product of selection for specifically benign dispositions towards females recognized as close kin’ (Perry et al. 2008). Chapais also points out that cooperative interactions among related females may be regulated by contingent reciprocity and mutualism, rather than kin selection. In fact, there is good reason to believe that these processes will reinforce each other. Kinship can enhance the stability of contingent reciprocity by making defections less costly and would also increase the benefits derived from mutualistic partnerships. There is some evidence that kinship enhances contingent reciprocity in baboon groups as females form more well-balanced grooming relationships with close female kin than with more distantly related kin and Phil. Trans. R. Soc. B (2009)

unrelated partners (Silk et al. 2006a,b; see also Janus 1989). Similarly, high-ranking matrilines show the most pronounced nepotistic biases (Berman 1980; Silk et al. 1999), perhaps because kin selection enhances the individual benefits derived from developing alliances with powerful partners. At the same time, reciprocity and mutualism do not provide plausible explanations for some forms of unilateral costly kin-biased behaviour described earlier. These include rank reversals among aged female baboons and their daughters, support for immature macaques involved in disputes with individuals from higher ranking families, fathers’ protection of offspring from infanticidal attacks and female macaques’ tolerance of subordinate relatives at feeding sites.

5. SUMMARY AND CONCLUSIONS More than 100 years after Darwin met Jenny in the London zoo, the first detailed descriptions of the social organization and behaviour in primate groups were published. Over the last 50 years, these accounts have been amplified and extended, as primatologists have documented the frequency, distribution and function of social interactions in a diverse range of primate species. Across the primate order, kinship plays an important role in structuring the evolution of primate social systems and the development of social relationships in primate groups. There are pronounced nepotistic biases in the distribution of altruistic behaviours such as grooming, coalitionary support and food sharing, and these biases emerge whenever relatives live together for extended periods of time. The distribution of cooperative behaviours conforms to qualitative predictions derived from Hamilton’s rule, but uncertainties about costs and benefits of behavioural acts make it impossible to test predictions derived from Hamilton’s rule with precision. It seems likely that other processes, including contingent reciprocity and mutualism, may complement the effects of kin selection and amplify the extent of nepotistic biases in behaviour. There are important gaps in our knowledge of nepotism in primate groups. First, we still know much more about kin biases in behaviour in cercopithecine primate species and chimpanzees than we do about kin biases in prosimians, New World monkeys, colobines or the other great apes. This makes it difficult to draw inferences about the forces that have shaped the evolution of sociality within the primate order. Second, most behavioural analyses focus on the pattern of interactions among maternal kin, but it is becoming clear that nepotism may extend to paternal kin in some species. Species with high reproductive skew and well-defined birth cohorts are likely candidates for patrilineal biases in behaviour. Third, it may be fruitful to explore the mechanisms underlying kin recognition in primates. Reassessment of experimental findings and new data from field studies suggest that familiarity, age similarity, mating history and phenotypic features may all contribute to kin recognition. Fourth, mutualism and reciprocity often complement the effects of kin selection. Carefully

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Primate nepotism controlled experimental studies can be used to tease apart these processes in the laboratory but in nature they may often be confounded, making it difficult to weigh their contributions to the evolution of cooperation in primate groups.

REFERENCES Alberts, S. 1999 Paternal kin discrimination in wild baboons. Proc. R. Soc. Lond. B 266, 1501 –1506. (doi:10.1098/ rspb.1999.0807) Altmann, J. 1979 Age cohorts as paternal sibships. Behav. Ecol. Sociobiol. 6, 161–169. (doi:10.1007/BF00292563) Altmann, J. & Alberts, S. C. 2003 Intraspecific variability in fertility and offspring survival in a nonhuman primate: behavioral control of ecological and social sources. In Offspring: the biodemography of fertility and family behavior (eds K. W. Wachter & R. A. Bulatao), pp. 140–169. Washington, DC: National Academy Press. Aureli, F., Schaffner, C. M., Verpooten, J., Slater, K. & Ramos-Fernandez, G. 2006 Raiding parties of male spider monkeys: insights into human warfare? Am. J. Phys. Anthropol. 131, 486 –497. (doi:10.1002/ajpa.20451) Barrett, L. & Henzi, S. P. 2002 Constraints on relationship formation among female primates. Behaviour 139, 263 –289. (doi:10.1163/156853902760102672) Barrett, L. & Henzi, P. 2005 The social nature of primate cognition. Proc. R. Soc. B 272, 1865–1875. (doi:10. 1098/rspb.2005.3200) Berman, C. M. 1980 Early agonistic experience and peer rank acquisition among free-ranging infant rhesus monkeys. Int. J. Primatol. 1, 153– 170. (doi:10.1007/ BF02735595) Berman, C. M. 2004 Developmental aspects of kin bias in behavior. In Kinship and behavior in primates (eds C. M. Berman & B. Chapais), pp. 317 –346. Oxford, UK: University Press. Bernstein, I. S. 1991 The correlation between kinship and behaviour in non-human primates. In Kin recognition (ed. P. G. Hepper), pp. 7–29. Cambridge, UK: Cambridge University Press. Borries, C. 1992 Grooming site preferences in female langurs (Presbytis entellus). Int. J. Primatol. 13, 19–32. (doi:10.1007/BF02547725) Bradley, B. J., Doran-Sheehy, D. M., Boesch, C. & Vigilant, L. 2004 Dispersed male networks in western gorillas. Curr. Biol. 14, 510–513. (doi:10.1016/j.cub.2004.02.062) Buchan, J. C., Alberts, S. C., Silk, J. B. & Altmann, J. 2003 True paternal care in a multi-male primate society. Nature 425, 179 –181. (doi:10.1038/nature01866) Chapais, B. 1988a Experimental matrilineal inheritance of rank in female Japanese macaques. Anim. Behav. 36, 1025– 1037. (doi:10.1016/S0003-3472(88)80062-9) Chapais, B. 1988b Rank maintenance in female Japanese macaques: experimental evidence for social dependency. Behaviour 104, 41–59. (doi:10.1163/156853988X00593) Chapais, B. 2001 Primate nepotism: what is the explanatory value of kin selection? Int. J. Primatol. 22, 203–229. (doi:10.1023/A:1005619430744) Chapais, B. 2002 The role of alliances in social inheritance of rank among female primates. In Coalitions and alliances in humans and other animals (eds A. H. Harcourt & F. B. M. de Waal), pp. 29–59. Oxford, UK: Oxford Science Publications. Chapais, B. 2006 Kinship, competence and cooperation in primates. In Cooperation in primates and humans (eds P. M. Kappeler & C. P. van Schaik), pp. 43–60. Berlin, Germany: Springer. Phil. Trans. R. Soc. B (2009)

J. B. Silk

3251

Chapais, B. & Be´lisle, P. 2004 Constraints on kin selection in primate groups. In Kinship and behavior in primates (eds B. Chapais & C. M. Berman), pp. 365 –386. Oxford, UK: Oxford University Press. Chapais, B. & Berman, C. M. 2004 Kinship and behavior in primates. Oxford, UK: Oxford University Press. Chapais, B. & St-Pierre, E. G. 1997 Kinship bonds are not necessary for maintaining matrilineal rank in captive Japanese macaques. Int. J. Primatol. 18, 375– 385. (doi:10.1023/A:1026334400201) Chapais, B., Gauthier, C., Proud’homme, J. & Vasey, P. 1997 Relatedness threshold for nepotism in Japanese macaques. Anim. Behav. 53, 1089– 1101. (doi:10.1006/ anbe.1996.0365) Charpentier, M. J. E., Peignot, P., Hossaert-Mckey, M. & Wickings, E. J. 2007 Kin discrimination in juvenile mandrills, Mandrillus sphinx. Anim. Behav. 73, 37–45. (doi:10.1016/j.anbehav.2006.02.026) Charpentier, M. J. E., van Horn, R. C., Altmann, J. & Alberts, S. C. 2008 Paternal effects on offspring fitness in a multimale primate society. Proc. Natl Acad. Sci. USA 105, 1988– 1992. (doi:10.1073/pnas.0711219105) Cheney, D. L., Seyfarth, R. M., Fischer, J., Beehner, J., Bergman, T., Johnson, S. E., Kitchen, D. M., Palombit, R. A. & Silk, J. B. 2004 Factors affecting reproduction and mortality among baboons in the Okavango Delta, Botswana. Int. J. Primatol. 25, 401 –428. (doi:10.1023/ B:IJOP.0000019159.75573.13) Cords, M. 2002 Friendship among adult female blue monkeys (Cercopithecus mitis). Behaviour 139, 291 –314. (doi:10.1163/156853902760102681) Datta, S. B. 1983a Relative power and the acquisition of rank. In Primate social relationships: an integrated approach (ed. R. A. Hinde), pp. 93–103. Sunderland, MA: Sinauer Associates. Datta, S. B. 1983b Relative power and the maintenance of dominance. In Primate social relationships: an integrated approach (ed. R. A. Hinde), pp. 103–112. Sunderland, MA: Sinauer Associates. Datta, S. B. 1983c Patterns of agonistic interference. In Primate social relationships: an integrated approach (ed. R. A. Hinde), pp. 289–297. Sunderland, MA: Sinauer Associates. Deets, A. C. & Harlow, H. F. 1974 Adoption of single and multiple infants by rhesus monkey mothers. Primates 15, 193–203. Delgado, R. & van Schaik, C. P. 2000 The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): a tale of two islands. Evol. Anthropol. 9, 201– 218. (doi: 10.1002/1520-6505(2000)9:5,201::AID-EVAN2.3.0. CO;2-Y) De Waal, F. B. M. 1991 Rank distance as a central feature of rhesus monkey social organization: a sociometric analysis. Anim. Behav. 41, 383– 395. Dietz, J. M. 2004 Kinship structure and reproductive skew in cooperatively breeding primates. In Kinship and behavior in primates (eds B. Chapais & C. M. Berman), pp. 223–241. Oxford, UK: Oxford University Press. Dunbar, R. I. M. 1988 Primate social systems. Ithaca, NY: Cornell University Press. Dunbar, R. I. M. 1991 Functional significance of social grooming in primates. Folia Primatol. 57, 121– 131. (doi:10.1159/000156574) Dunbar, R. I. M. & Sharman, M. 1984 Is social grooming altruistic? Zeit. Tierpsychol. 64, 163 –173. Eberle, M. & Kappeler, P. M. 2006 Family insurance: kin selection and cooperative breeding in a solitary primates (Microcebus murinus). Behav. Ecol. Sociobiol. 60, 582–588. (doi:10.1007/s00265-006-0203-3) Erhart, E. M., Coelho Jr, A. M. & Bramblett, C. A. 1997 Kin recognition by paternal half-siblings in captive Papio

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3252

J. B. Silk

Review. Primate nepotism

cynocephalus. Am. J. Primatol. 43, 147 –157. (doi:10.1002/ (SICI)1098-2345(1997)43:2,147::AID-AJP4.3.0.CO; 2-X) Fredrickson, W. T. & Sackett, G. P. 1984 Kin preferences in primates (Macaca nemestrina): relatedness or familiarity? J. Comp. Pyschol. 98, 29–34. (doi:10.1037/0735-7036. 98.1.29) French, J. A. 1997 Proximate regulation of singular breeding in callitrichid primates. In Cooperative breeding in mammals (eds N. G. Solomon & J. A. French), pp. 34– 75. Cambridge, UK: Cambridge University Press. Galdikas, B. M. F. 1988 Orangutan diet, range, and activity at Tanjung Putting, Central Borneo. Int. J. Primatol. 9, 1– 35. (doi:10.1007/BF02740195) Gilby, I. C. & Wrangham, R. W. 2008 Association patterns among wild chimpanzees (Pan troglodytes schweinfurthii) reflect sex differences in cooperation. Behav. Ecol. Sociobiol. 62, 1831–1842. (doi:10.1007/s00265-008-0612-6) Goodall, J. 1986 The chimpanzees of Gombe: patterns of behavior. Cambridge, MA: Harvard University Press. Haig, D. 1999 What is a marmoset? Am. J. Primatol. 49, 285 –296. (doi:10.1002/(SICI)1098-2345(199912)49: 4,285::AID-AJP1.3.0.CO;2-X) Hamilton, W. D. 1964 The genetical evolution of social behavior. I and II. J. Theor. Biol. 7, 1 –52. (doi:10.1016/ 0022-5193(64)90038-4) Hamilton, W. D. 1987 Discriminating nepotism: expectable, common, overlooked. In Kin recognition in animals (eds D. J. C. Fletcher & C. D. Michener), pp. 417 –437. New York, NY: Wiley. Harcourt, A. H. 1987 Dominance and fertility among female primates. J. Zool. Lond. 213, 471–487. (doi:10.1111/ j.1469-7998.1987.tb03721.x) Harcourt, A. H. & Stewart, K. J. 2007 Gorilla societies. Chicago, IL: University of Chicago Press. Harvey, P. H. & Clutton-Brock, T. H. 1987 Life histories in comparative perspective. In Primate societies (eds B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker), pp. 181–196. Chicago, IL: University of Chicago Press. Henzi, S. P. & Barett, L. 1999 The value of grooming to female primates. Primates 40, 57–59. Holmes, W. G. 2004 The early history of Hamiltonian-based research on kin recognition. Ann. Zool. Fennici 41, 691 –711. Holmes, W. G. & Mateo, J. M. 2007 Kin recognition in rodents: issues and evidence. In Rodent societies (eds J. O. Wolff & P. W. Sherman), pp. 216 –228. Chicago, IL: University of Chicago Press. Holmes, W. G. & Sherman, P. W. 1983 Kin recognition in animals. Sci. Am. 71, 46– 55. Horrocks, J. & Hunte, W. 1983 Maternal rank and offspring rank in vervet monkeys: an appraisal of the mechanisms of rank acquisition. Anim. Behav. 31, 772 –782. (doi:10. 1016/S0003-3472(83)80234-6) Isbell, L. A. & Young, T. P. 2002 Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behaviour 139, 177 –2002. (doi:10.1163/156853902760102645) Jacob, S., McClintock, M. K., Zelano, B. & Ober, C. 2002 Paternally inherited HLA alleles are associated with women’s choice of male odor. Nat. Genet. 30, 175 –179. (doi:10.1038/ng830) Janus, M. 1989 Reciprocity in play, grooming, and proximity in sibling and non-sibling young rhesus monkeys. Int. J. Primatol. 10, 243 –261. (doi:10.1007/BF02735203) Johnson, J. A. 1987 Dominance rank in olive baboons, Papio anubis: the influence of gender, size, maternal rank and orphaning. Anim. Behav. 35, 1694– 1708. (doi:10.1016/ S0003-3472(87)80062-3) Phil. Trans. R. Soc. B (2009)

Jolly, A. & Pride, E. 1999 Troop histories and range inertia of Lemur catta at Berenty, Madagascar: a 33-year perspective. Int. J. Primatol. 20, 359–373. (doi:10.1023/ A:1020548620372) Kappeler, P. M., Wimmer, B., Zinner, D. & Tautz, D. 2002 Hidden matrilineal group structure of a solitary lemur: implications for primate social evolution. Proc. R. Soc. Lond. B 269, 1755 –1763. (doi:10.1098/rspb. 2002.2066) Kapsalis, E. 2004 Matrilineal kinship and primate behavior. In Kinship and behavior in primates (eds B. Chapais & C. M. Berman), pp. 153– 176. Oxford, UK: Oxford University Press. Kapsalis, E. & Berman, C. M. 1996 Models of affiliative relationships among free-ranging macaque monkeys (Macaca mulatat) I. Criteria for kinship. Behaviour 133, 1209– 1234. Kawai, M. 1958 On the system of social ranks in a natural troop of Japanese monkeys. 1. Basic rank and dependent rank. Primates 1, 111 –130. (doi:10.1007/BF01813699) Kawamura, S. 1958 The matriarchal social order in the Minoo-B group. Primates 1, 149 –156. (doi:10.1007/ BF01813701) Kurland, J. A. 1977 Kin selection in the Japanese monkey. Basel, Switzerland: Karger. Langergraber, K. E., Mitani, J. C. & Vigilant, L. 2007 The limited impact of kinship on cooperation in wild chimpanzees. Proc. Natl Acad. Sci. USA 104, 7787–7790. Lehmann, J., Fickenscher, G. & Boesch, C. 2006 Kin biased investment in wild chimpanzees. Behaviour 143, 931–955. (doi:10.1163/156853906778623635) MacKenzie, M. M., McGrew, W. C. & Chamove, A. S. 1985 Social preferences in stumptailed macaques (Macaca arcoides): effects of companionship, kinship, and rearing. Dev. Psychobiol. 18, 115 –123. (doi:10.1002/dev. 420180204) Matsuzawa, T. & McGrew, W. C. 2008 Kinji Imanishi and 60 years of Japanese primatology. Curr. Biol. 18, R587 –R591. (doi:10.1016/j.cub.2008.05.040) Mitani, J. C. 2009 Male chimpanzees form enduring and equitable social bonds. Anim. Behav. 77, 633–640. (doi:10.1016/j.anbehav.2008.11.021) Moscovice, L., Di Fiore, A., Seyfarth, R. M. & Cheney, D. L. 2009 Paternity alone does not predict long-term investment in juveniles by male baboons. Behav. Ecol. Sociobiol. 63, 1471–1482. (doi:10.1007/s00265-0090781-y) Muller, M. N. & Mitani, J. C. 2005 Conflict and cooperation in wild chimpanzees. Adv. Study Behav. 35, 275–331. (doi:10.1016/S0065-3454(05)35007-8) Muniz, L., Perry, S., Manson, J. H., Gilkenson, H., GrosLouis, J. & Vigilant, L. 2005 Father –daughter inbreeding avoidance in a wild primate population. Curr. Biol. 16, R156 –R157. (doi:10.1016/j.cub.2006.02.055) Murray, C., Gilby, I. C., Mane, S. V. & Puse, A. E. 2008 Adult male chimpanzees inherit maternal ranging patterns. Curr. Biol. 18, 20–24. (doi:10.1016/j.cub. 2007.11.044) Nakamichi, M. 1997 Effects of spatial proximity and alliances on dominance relations among female ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. Primates 38, 331 –340. (doi:10.1007/BF02381620) Nakamichi, M. & Koyama, N. 1997 Social relationships among ring-tailed lemurs (Lemur catta) in two freeranging troops at Berenty Reserve, Madagascar. Int. J. Primatol. 18, 73–93. (doi:10.1023/A:1026393223883) Nash, L. 2004 Kinship and behavior among nongregarious nocturnal prosimians. In Kinship and behavior in primates (eds B. Chapais & C. M. Berman), pp. 200 –222. Oxford, UK: Oxford University Press.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Primate nepotism Nishida, T. 1979 The social structure of chimpanzees of the Mahale Mountains. In The great apes (eds D. Hamburg & E. McCown), pp. 72–121. Menlo Park, CA: Benjamin Cummings. Owren, M. J. & Dieter, J. A. 1989 Infant cross-fostering between Japanese (Macaca fuscata) and rhesus macaques (M. mulatta). Am. J. Primatol. 18, 245 –250. (doi:10. 1002/ajp.1350180308) Palombit, R. A. 2000 Infanticide and the evolution of male– female bonds in animals. In Infanticide by males and its implications (eds C. P. van Schaik & C. H. Janson), pp. 239 –268. Cambridge, UK: Cambridge University Press. Parr, L. & de Waal, F. B. M. 1999 Visual kin recognition in chimpanzees. Nature 399, 647– 648. (doi:10.1038/ 21345) Perry, S., Manson, J. H., Muniz, L., Gros-Louis, J. & Vigilant, L. 2008 Kin-biased social behaviour in wild adult female white-faced capuchins, Cebus capucinus. Anim. Behav. 76, 187 –199. (doi:10.1016/j.anbehav. 2008.01.020) Pope, T. R. 1990 The reproductive consequences of male cooperation in the red howler monkey: paternity exclusion in multi-male and single-male troops using genetic markers. Behav. Ecol. Sociobiol. 27, 439– 446. (doi:10. 1007/BF00164071) Pope, T. R. 1998 Effects of demographic change on group kin structure and gene dynamics of populations of red howling monkeys. J. Mamm. 79, 692–712. (doi:10. 2307/1383081) Pope, T. R. 2000 Reproductive success increases with degree of kinship in cooperative coalitions of female red howler monkeys (Alouatta seniculus). Behav. Ecol. Sociobiol. 48, 253 –267. (doi:10.1007/s002650000236) Pusey, A. E. & Packer, C. 1987 Dispersal and philopatry. In Primate societies (eds B. B. Smuts, D. L. Cheney, R. M. Seyfarth, , R. W. Wrangham & T. T. Struhsaker), pp. 250 –266. Chicago, IL: University of Chicago Press. Radespiel, U., Sarikaya, Z., Zimmerman, E. & Bruford, M. I. 2001 Sociogenetic structure in a free-living nocturnal primate population: sex-specific differences in the grey mouse lemur (Microcebus murinus). Behav. Ecol. Sociobiol. 50, 493–502. (doi:10.1007/s002650100402) Rawlins, R. G. & Kessler, M. J. (eds) 1986 The Cayo Santiago macaques: history, biology, and behavior. Albany, NY: SUNY Press. Rendall, D. 2004 ‘Recognizing’ kin: mechanisms, media, minds, modules, and muddles. In Kinship and behavior in primates (eds B. Chapais & C. M. Berman), pp. 295 –316. Oxford, UK: Oxford University Press. Ross, C. N., French, J. A. & Orti, G. 2007 Germ-line chimerism and paternal care in marmosets (Callithrix kuhlii). Proc. Natl Acad. Sci. USA 104, 6278–6282. (doi:10.1073/pnas.0607426104) Sackett, G. P. & Fredrickson, W. T. 1987 Social preferences by pigtail macaques: familiarity versus degree and type of kinship. Anim. Behav. 35, 603 –607. (doi:10.1016/S00033472(87)80290-7) Sauther, M. L., Sussman, R. W. & Gould, L. 1999 The socioecology of the ringtailed lemur: thirty-five years of research. Curr. Anthropol. 8, 120 –132. Schino, G. 2001 Grooming, competition and social rank among female primates: a meta-analysis. Anim. Behav. 62, 265– 271. (doi:10.1006/anbe.2001.1750) Schino, G. & Aureli, F. 2007 Grooming reciprocation among female primates: a meta-analysis. Biol. Lett. 4, 9 –11. (doi:10.1098/rsbl.2007.0506) Schu¨lke, O. & Ostner, J. 2008 Male reproductive skew, paternal relatedness, and female social relationships. Am. J. Primatol. 70, 695–698. (doi:10.1002/ajp.20546) Phil. Trans. R. Soc. B (2009)

J. B. Silk

3253

Sekulic, R. 1983 Male relationships and infant deaths in red howler monkeys (Alouatta seniculus). Z. Tierpsychol. 61, 185–202. Seyfarth, R. M. 1977 A model of social grooming among adult female monkeys. J. Theor. Biol. 65, 671 –698. (doi:10.1016/0022-5193(77)90015-7) Sherman, P. W. 1980 The limits of ground squirrel nepotism. In Sociobiology: beyond nature/nurture? (eds G. W. Barlow & J. Silverberg), pp. 504–544. Boulder, CO: Westview Press. Sherman, P. W. 1981 Kinship, demography, and Belding’s ground squirrel nepotism. Behav. Ecol. Sociobiol. 8, 251–260. (doi:10.1007/BF00299523) Sigg, H., Stolba, A., Abeglen, J. J. & Dasser, V. 1982 Life history of hamadryas baboons: physical development, infant mortality, reproductive parameters and family relationships. Primates 23, 473–487. (doi:10.1007/ BF02373959) Silk, J. B. 1982 Altruism among female Macaca radiata: explanations and analysis of patterns of grooming and coalition formation. Behaviour 79, 162 –168. (doi:10. 1163/156853982X00238) Silk, J. B. 1993 The evolution of social conflict among primate females. In Primate social conflict (eds W. A. Mason & S. Mendoza), pp. 49–83. Albany, NY: SUNY Press. Silk, J. B. 2001 Ties that bond: the role of kinship in primate societies. In New directions in anthropological kinship (ed. L. Stone), pp. 71–92. Boulder, CO: Rowman and Littlefield. Silk, J. B. 2005 Practicing Hamilton’s rule: kin selection in primate groups. In Cooperation in primates and humans (eds P. M. Kappeler & C. P. van Schaik), pp. 21–42. Berlin, Germany: Springer. Silk, J. B., Cheney, D. L. & Seyfarth, R. M. 1999 The structure of social relationships among female savannah baboons in Moremi Reserve, Botswana. Behaviour 136, 679–703. (doi:10.1163/156853999501522) Silk, J. B., Alberts, S. C. & Altmann, J. 2003 Social bonds of female baboons enhance infant survival. Science 302, 1331–1334. Silk, J. B., Alberts, S. C. & Altmann, J. 2006a Social relationships among adult female baboons (Papio cynocephalus) II. Variation in the quality and stability of social bonds. Behav. Ecol. Sociobiol. 61, 197 –204. (doi:10. 1007/s00265-006-0250-9) Silk, J. B., Altmann, J. & Alberts, S. C. 2006b Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behav. Ecol. Sociobiol. 61, 183–195. (doi:10.1007/s00265-006-0249-2) Silk, J. B., Beehner, J. C., Berman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., Wittig, R. M., Seyfarth, R. M. & Cheney, D. L. 2009 The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc. R. Soc. B 276, 3099–3104. (doi:10.1098/rspb.2009.0681) Slater, K., Schaffner, C. & Aureli, F. 2009 Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatenensis). Am. J. Primatol. 71, 21–29. (doi:10.1002/ ajp.20618) Smith, K. L., Alberts, S. C. & Altmann, J. 2003 Wild female baboons bias their social behaviour towards paternal halfsisters. Proc. R. Soc. Lond. B. 270, 503 –510. (doi:10. 1098/rspb.2002.2277) Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W. & Struhsaker, T. T. (eds) 1987 Primate societies. Chicago, IL: University of Chicago Press. Stammbach, E. 1987 Desert, forest and montane baboons: multilevel societies. In Primate societies (eds B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker), pp. 112– 120. Chicago, IL: University of Chicago Press.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3254

J. B. Silk

Review. Primate nepotism

Sterck, E. H. M., Watts, D. P. & van Schaik, C. P. 1997 The evolution of female social relationships in non human primates. Behav. Ecol. Sociobiol. 46, 1 –13. Strier, K. B. 1994 Brotherhoods among atelins. Behaviour 130, 151 –167. (doi:10.1163/156853994X00505) Strier, K. B., Dib, L. T. & Figueira, J. E. C. 2002 Social dynamics of male muriquis (Brachyteles arachnoids hypoxanthus). Behaviour 139, 315 –342. (doi:10.1163/ 156853902760102690) Tang-Martinez, Z. 2001 The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation. Behav. Process. 53, 21–40. (doi:10.1016/S0376-6357(00)00148-0) Tardiff, S. D. 1997 The bioenergetics of parental behavior and the evolution of alloparental care in marmosets and tamarins. In Cooperative breeding in mammals (eds N. G. Solomon & J. A. French), pp. 11–33. Cambridge, UK: Cambridge University Press. van Schaik, C. P. 1983 Why are diurnal primates living in groups? Behaviour 87, 120 –144. (doi:10.1163/ 156853983X00147) van Schaik, C. P. & Janson, C. H. (eds) 2000 Infanticide by males and its implications. Cambridge, MA: Cambridge University Press. Vokey, J. R., Rendall, D., Tangen, J. M., Parr, L. A. & de Waal, F. B. M. 2004 Visual kin recognition and family resemblance in chimpanzees (Pan troglodytes). J. Comp. Psychol. 118, 194–199. (doi:10.1037/07357036.118.2.194) Walters, J. R. 1980 Interventions and the development of dominance relationships in female baboons. Folia Primatol. 34, 61–89. (doi:10.1159/000155948) Watts, D. P. 1996 Comparative socioecology of gorillas. In Great ape societies (eds W. C. McGrew, L. F. Marchant & T. Nishida), pp. 16–28. Cambridge, UK: Cambridge University Press. Watts, D. P. 2000 Causes and consequences of variation in male mountain gorilla life histories and group membership. In Primate males: causes and consequences of variation in group membership (ed. P. M. Kappeler), pp. 169 –179. Cambridge, UK: Cambridge University Press. Watts, D. P. & Pusey, A. E. 1993 Behavior of juvenile and adolescent great apes. In Juvenile primates: life history, development and behavior (eds M. E. Pereira & L. F. Fairbanks), pp. 148 –167. New York, NY: Oxford University Press. Weisfeld, G. E., Czilli, T., Phillips, K. A., Gall, J. A. & Lichtman, C. M. 2003 Possible olfaction-based

Phil. Trans. R. Soc. B (2009)

mechanisms in human kin recognition and inbreeding avoidance. J. Exp. Child Psychol. 85, 279 –295. (doi:10. 1016/S0022-0965(03)00061-4) Welker, C., Schwibbe, M. H., Scha¨ffer-Witt, C. & Visalberghi, E. 1987 Failure of kin recognition in Macaca fasicularis. Folia Primatol. 49, 216–221. (doi:10. 1159/000156327) Widdig, A. 2007 Paternal kin discrimination: the evidence and likely mechanisms. Biol. Rev. 82, 319– 334. (doi:10. 1111/j.1469-185X.2007.00011.x) Widdig, A., Nu¨rnberg, P., Krawczak, M., Streich, W. J. & Bercovitch, F. 2001 Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. Proc. Natl Acad. Sci. USA 98, 13 769 –13 773. (doi:10.1073/pnas.241210198) Widdig, A., Nu¨rnberg, P., Krawczak, M., Streich, W. J. & Bercovitch, F. 2002 Affiliation and aggression among adult female rhesus macaques: a genetic analysis of paternal cohorts. Behaviour 139, 371 –391. (doi:10. 1163/156853902760102717) Widdig, A., Streich, W. J., Nu¨rnberg, P., Croucher, P. J. P., Bercovitch, F. & Krawczak, M. 2006 Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta). Behav. Ecol. Sociobiol. 61, 205 –214. (doi:10.1007/s00265-006-0251-8) Williams, J. M., Liu, H. & Pusey, A. E. 2002 Costs and benefits of grouping for female chimpanzees at Gombe. In Behavioural diversity in chimpanzees and bonobos (eds C. Boesch & G. Hohmann & L. Marchant), pp. 192 –203. Cambridge, UK: Cambridge University Press. Wilson, E. O. 1975 Sociobiology: the new synthesis. Cambridge, MA: Harvard University Press. Wimmer, B., Tautz, D. & Kappeler, P. M. 2002 The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behav. Ecol. Sociobiol. 52, 166 –175. (doi:10.1007/s00265-0020497-8) Wittig, R. M., Crockford, C., Seyfarth, R. M. & Cheney, D. L. 2007 Vocal alliances in chacma baboons (Papio hamadryas ursinus). Behav. Ecol. Sociobiol. 61, 899 –909. (doi:10.1007/s00265-006-0319-5) Wrangham, R. W. 1980 An ecological model of the evolution of female-bonded groups of primates. Behaviour 75, 262 –300. (doi:10.1163/156853980X00447) Wu, H. M., Holmes, W. G., Medina, S. R. & Sackett, G. P. 1980 Kin preferences in infant Macaca nemestrina. Nature 285, 225 –227. (doi:10.1038/285225a0)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3255–3266 doi:10.1098/rstb.2009.0116

Evolving the ingredients for reciprocity and spite Marc Hauser1,2, *, Katherine McAuliffe2 and Peter R. Blake3 1

Department of Psychology, 2Department of Human Evolutionary Biology, and 3Graduate School of Education, Harvard University, Cambridge, MA, USA

Darwin never provided a satisfactory account of altruism, but posed the problem beautifully in light of the logic of natural selection. Hamilton and Williams delivered the necessary satisfaction by appealing to kinship, and Trivers showed that kinship was not necessary as long as the originally altruistic act was conditionally reciprocated. From the late 1970s to the present, the kinship theories in particular have been supported by considerable empirical data and elaborated to explore a number of other social interactions such as cooperation, selfishness and punishment, giving us what is now a rich description of the nature of social relationships among organisms. There are, however, two forms of theoretically possible social interactions—reciprocity and spite—that appear absent or nearly so in non-human vertebrates, despite considerable research efforts on a wide diversity of species. We suggest that the rather weak comparative evidence for these interactions is predicted once we consider the requisite socioecological pressures and psychological mechanisms. That is, a consideration of ultimate demands and proximate prerequisites leads to the prediction that reciprocity and spite should be rare in non-human animals, and common in humans. In particular, reciprocity and spite evolved in humans because of adaptive demands on cooperation among unrelated individuals living in large groups, and the integrative capacities of inequity detection, future-oriented decision-making and inhibitory control. Keywords: reciprocal altruism; spite; ultimate pressures; proximal constraints

1. INTRODUCTION In The descent of man, Darwin (1871) pondered the evolutionary origins of altruism and self-sacrifice among humans. The puzzle, as Darwin realized, was that such behaviours pose significant costs to the individual: ‘he who was ready to sacrifice his life, as many a savage has been, rather than betray his comrades, would often leave no offspring to inherit his noble nature’ (p.163). To solve this problem, Darwin assumed that self-sacrifice might payoff in the currency of group benefits. He thus stated, if ‘a tribe including many members who . . . were always ready to give aid to each other and sacrifice themselves for the common good, would be victorious over most other tribes; and this would be natural selection’ (p.166). In other words, the costs to the individual of selfsacrifice and other altruistic behaviour could evolve if the individual’s group benefited relative to other groups lacking such behaviours. As this history has been recounted many times, here we simply reiterate the key ideas and findings in telegraphic form so as to set up the essential problems discussed in this essay. In brief, sociobiologists raised what Dawkins (1976) famously described as the problem of subversion from within, that is, in a group of self-sacrificial altruists, defectors immediately win as they reap the benefits without paying the costs.

* Author for correspondence ([email protected]). One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

Thus, group selection was attacked as, at best, a weak account of the evolution of altruistic behaviour. As an alternative, Hamilton (1964) and Williams (1966) proposed and developed a gene’s eye view of altruism, arguing that self-sacrifice would evolve if the costs to the individual were offset by benefits to the individual’s close kin. What drives the evolution of altruism, therefore, is a consideration of the distribution of winning genes, rather than winning individuals or groups. But what about altruistic behaviour among genetically unrelated individuals? The solution, provided by Trivers (1971), was reciprocal altruism: self-sacrifice is offset because the initial act of altruism is conditioned upon a reciprocated act of altruism in the future. These brilliant ideas can be placed in the context of a social matrix that considers the gains (benefits) and losses (costs) of an act from the perspective of a donor and putative recipient or recipients (figure 1). Moving clockwise from the top left, altruism arises when the donor incurs a loss but delivers a gain to the recipient. Spite occurs when both the donor and the recipient incur losses, but typically, the cost to the recipient outweighs the cost to the donor. Cooperation arises when both donor and recipient accrue gains. Finally, selfishness arises when the donor gains, but the recipient loses. Needless to say, there are several important distinctions within each of these cells, but critically for our purposes, are the differences within the cooperation cell. In particular, some forms of cooperation entail joint action and mutual, simultaneous benefit, whereas others (i.e. reciprocity) entail delays.

3255

This journal is q 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3256

M. Hauser et al.

Evolving reciprocity and spite receiver

gains

losses

losses donor

altruistic

spiteful

cooperative

selfish

gains

Figure 1. A social matrix of interactions based on gains (plus) and losses (minus) to the donor and recipient.

Based on the clarity of these ideas, a torrent of empirical research soon emerged, confirming the logic of the gene’s eye view of sociality. There were, however, two noticeable puzzles: though studies of insects, fishes, amphibians, birds and mammals explored the issues of reciprocity and spite, there is, at best, only a few studies that provide the necessary evidence, and many authors have concluded that there is no evidence at all (Foster et al. 2001; Hammerstein 2003; Hauser 2006; Jensen et al. 2006; Noe 2006); these authors, and the reviews that they have written, generally distinguish within- from between-species interactions, and consequently, do not address the much more significant evidence for reciprocity among, for example, cleaner fish and their hosts (Bshary & Grutter 2005, 2006). To explain this apparent phylogenetic gap, especially why we may be one of the only species to engage in reciprocity and spite with members of our own species and we turn first to a re-analysis of the logic of reciprocity and spite, focusing on both ultimate pressures and proximate requirements. We argue that accounts of the evolution of reciprocity and spite that neglect the requisite mechanisms for these social behaviours will fail. Similarly, studies that attempt to describe the underlying mechanisms without considering why such mechanisms evolved will fail as well. To understand the evolution of reciprocal altruism and spite, both proximate and ultimate factors must be considered. Based on a review of some recent work on human and non-human animals, we show that only our own species evolved under conditions that favoured reciprocal altruism and spiteful interactions, and importantly, evolved the brains to carry out such behaviours, even early in life. 2. RECIPROCAL ALTRUISM Trivers developed his adaptationist’s analysis of reciprocity (primarily direct as opposed to indirect) by laying out the structure of the interaction, targeting its economic, temporal and conditional properties. Specifically, reciprocity will evolve if: (i) the cost associated with helping is small relative to the benefit obtained by the recipient; Phil. Trans. R. Soc. B (2009)

(ii) the initial act of helping is contingent upon receiving help in the future; (iii) there is a time lag between the initial act of helping and the reciprocated act. The first conditional is, fundamentally, the biological definition of altruism. The second conditional links the two altruistic acts, setting up the original altruistic act as an if-and-only-if contingency; this move establishes direct reciprocity as a selfish behaviour. The third conditional places a waiting period between the originally altruistic act and the reciprocated act. From a conceptual and modelling perspective, the three core conditions for the evolution of reciprocal altruism are clear enough. From an empirical perspective, however, they are less clear, at least in terms of the kind of evidence that would constitute a sufficient test. For example, a considerable amount of research aimed at uncovering evidence of reciprocity in animals has focused on grooming (Seyfarth & Cheney 1984; Hart & Hart 1989; Hemelrijk & Luteijn 1998; Barrett et al. 1999; Schino et al. 2007; Gumert & Ho 2008; Schino & Aureli 2008). In some studies, analyses focus on the exchange of grooming for grooming, whereas others explore the exchange of grooming for other commodities, such as support in coalitions or opportunities for co-feeding. Several studies show that animals tend to groom most of those who groom them. That is, there is a positive correlation between the time that any given animal grooms another and the amount of time that they are groomed. Such analyses are problematic because correlations establish only an association, not the contingent nature of reciprocity. Further, while reciprocal altruism could be the mechanism in play, more parsimonious explanations should be employed until contingency can be demonstrated. The difficultly of demonstrating contingency has come to light in a recent debate focused on mobbing behaviour in pied flycatchers (Ficedula hypoleuca). Pied flycatchers attempt to drive predators away by mobbing them and will assist neighbouring groups that initiate a mobbing response. In a series of elegant experiments, Krams et al. (2008) showed that pied flycatchers are more likely to assist neighbours who have assisted them in the recent past than those who have refused to assist them. The authors interpret their results as evidence of reciprocity (Krams et al. 2008; Wheatcroft & Price 2008). In response to this interpretation, Russell & Wright (2008) argued that although this behaviour is consistent with what would be expected in a reciprocally altruistic relationship, their experiments failed to demonstrate that the reciprocators’ behaviour was contingent on an initially altruistic act. Instead, one can interpret these results as evidence for by-product mutualism (see Wheatcroft & Krams 2008 for response). This debate illustrates that simple and more common forms of cooperation should be evoked to account for seemingly reciprocal behaviour until all three components of reciprocal altruism are satisfied. In addition to the three core conditions for the evolution of reciprocal altruism, Trivers also noted that reciprocity was most likely to evolve in highly social

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Evolving reciprocity and spite species that are long-lived and have the opportunity to engage in repeated interactions with the same individuals. These added conditions were necessary because if the odds of a future encounter are low, then the contingency conditional is stripped away, allowing for the possibility that one’s partner will fail to reciprocate; such failures could arise due to natural circumstances (e.g. frequent emigrations, low survival rate), making the recipient unable to reciprocate, or to more strategic and planned situations as when the recipient decides to renege because of more profitable opportunities. Building on these ideas, Nowak (2006) recently unified several models for the evolution of cooperation, arguing that direct reciprocity evolves when the probability that another interaction between altruist and recipient exceeds the cost – benefit ratio of the altruistic act. Thus, a common assumption or consideration in virtually all models of reciprocity is that individuals have the opportunity to interact with others, frequently, and with fairly dependable outcomes with respect to exchanging resources. A wide variety of mammals and birds satisfy these life history and demographic conditions. That is, in a number of species, individuals live for many years, in relatively stable social groups and with numerous opportunities to interact. That said, a fundamental question, and one for which we have little understanding, is whether animals living in such groups are sufficiently dependent upon reciprocal interactions among genetically unrelated individuals to favour the evolution of reciprocity. Animals may have multiple opportunities to help non-kin, and to be helped by them, but selection on such relationships may be weak because most of the time animals can rely upon aid from close kin. For example, in Wilkinson’s (1984) classic study of reciprocity among vampire bats (Desmodus rotundus), the vast majority (over 90%) of blood regurgitations arise between either mother and daughter (r ¼ 0.5) or grandparent and grandchild (r ¼ 0.25). The remaining cases among individuals with lower degrees of relatedness contribute little, at least in terms of the number of observations, and as in other studies of reciprocity, it is possible that these are instances of mistaken kin recognition (Coyne & Sohn 1978; Hammerstein 2003; Hauser 2006). Critically, therefore, it appears that reciprocity may be only weakly selected because in most animal societies, individuals can rely on kin-based helping to survive. An additional evolutionary (ultimate) consideration is the type of resource exchanged, and the relative benefits of receiving it. Whatever the currency or resource type, interactants must be able to quantify it, including the relative costs of giving it up and the relative benefits of receiving it. As Whitlock et al. (2007) have noted, for resource sharing by means of reciprocity to evolve, the fitness value of the resource must differ between reciprocating partners, and this differential must reverse at some point in the interaction. That is, at time T, resource R is worth more to player 1 than it is to player to 2, but at time T þ 1, R is worth more to player 2 than it is to player 1. Based on a series of models, Whitlock and co-workers (p. 1774) show ‘that the conditions for Phil. Trans. R. Soc. B (2009)

M. Hauser et al.

3257

the evolution of resource sharing by reciprocity will become extremely difficult to satisfy. In all but a few cases, resource sharing is unlikely to evolve by reciprocity, but sharing may evolve readily via kin selection.’ In sum, several recent theoretical analyses and modelling efforts suggest that on ultimate grounds, reciprocity is unlikely to evolve and be selected for in most, if not all animal societies. Most animals societies are small, consist of a significant number of kin, and the differential in resource value among non-kin is insufficient to put pressure on reciprocal relationships. The opposite seems to be the case for most human societies, including those that appeared in our early origins. Thus far, we have focused on ultimate considerations. The proximate prerequisites for reciprocity are no less significant and, we suggest, impose substantial constraints on its evolution and stability over time. Had these been mapped out in detail at the start, theorists may have predicted that reciprocal altruism would not evolve in animals! Trivers was, of course, sensitive to many of the mechanistic requirements for reciprocity, pointing to the importance of individual recognition, memory for prior interactions, and quantification of costs and benefits. Other mechanisms are also important, but were not considered in early writings, including the ability to delay gratification and read intentions, processes we discuss in greater detail below. There is no question that these cognitive abilities are firmly in place in adult humans. And although some of these capacities are also in play in some animals, we suggest that they are weakly integrated with each other, thus limiting the ability to both initiate and maintain stable reciprocal exchanges. We first provide a brief, but critical description of three experiments on reciprocal altruism in animals; each provides some support for reciprocity, but also reveals the limits of this work and of the evidence to date. We then turn to a discussion of the mechanisms required to support reciprocity, showing that although the pieces are largely in place, they fail to combine in the context of initiating and maintaining a reciprocal relationship. In a clever experiment with captive jays (Cyanocitta cristata), Clements & Stephens (1995) set up an operant experiment in which individuals were either playing the role of cooperator or defector. Individuals paired-off and started with a payoff matrix that simulated either mutualism or a Prisoner’s Dilemma. Mutual cooperation yielded the highest payoff for each in the mutualism game, whereas defection – cooperation yielded the highest payoff for the defector in the Prisoner’s Dilemma game (figure 2). Subjects played several rounds of one game before switching to the other. The results were striking and clear: subjects rapidly gravitated to cooperate – cooperate in the mutualism game, but precipitously turned to defect – defect in the Prisoner’s Dilemma game. Thus, subjects were able to maximize individual payoffs in the mutualism game, but suffered relatively large costs in the Prisoner’s Dilemma. Critically, in a follow-up experiment by Stephens et al. (2002) in

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3258

M. Hauser et al.

Evolving reciprocity and spite experiment 1

D

1

C

2

C D

mean nice OR

experiment 2

player 2

player 2

coop defect

coop defect

coop

coop

player 1

player 1

defect

defect

Prisoner’s Dilemma

mutualism

Figure 2. Cooperative games among captive jays (Clements & Stephens 1995). Each jay had access to a cooperate (C) and defect (D) button, each associated with a different payoff. Pairs of jays played several rounds of either the Prisoner’s Dilemma game or the mutualism game, each associated with a different payoff matrix. In the matrices above, the size of the circle represents the relative payoffs from the perspective of player 1. Thus, in the Prisoner’s Dilemma, the highest payoff to player 1 arises with defect –cooperate. For mutualism, the highest payoff to player 1 arises with cooperate– cooperate.

which individual payoffs were delayed, jays were able to solve the Prisoner’s Dilemma and stabilize on cooperate – cooperate. That is, by taking away the temptation to immediately obtain the potentially largest payoff—defect (against cooperate)—the jays were able to settle on the long term, but more profitable strategy of cooperate – cooperate. As Stephens and colleagues noted, however, this capacity to solve the Prisoner’s Dilemma must be placed in the context of a highly unnatural testing environment, one that would never arise in the wild. In other words, though jays have the cognitive ability to solve the Prisoner’s Dilemma, they required thousands of opportunities to interact over a short period of time, as well as enforced delays for all reward payouts. Such a situation would never arise under natural conditions, perhaps for any animal. In a study of cotton-top tamarins (Sanguinus oedipus), Hauser et al. (2003) attempted to test three properties of a reciprocal relationship: altruistic contingency, reputation tracking and distinguishing intentional from accidental outcomes. Genetically unrelated tamarins played in four different games, each requiring an actor to decide whether to pull a tool that would deliver food to either self, the other or both (figure 3). In each game, there were 24 trials per session, with each subject playing 12 alternating trials. In game 1, individual subjects played against one of the two trained stooges, one nice cooperative tamarin trained to pull the tool 100 per cent of the time, and one mean uncooperative tamarin trained to never pull the tool. In this game pulling the tool resulted in one piece of food for the recipient and no food for the actor, and thus, was considered an Phil. Trans. R. Soc. B (2009)

sessions 1, 2, 3 and 5

session 4

experiment 3

player-1

player-2

experiment 4

active

passive

Figure 3. Four different games played by genetically unrelated cotton-top tamarins. In experiment 1, each subject played alternating sessions (24 trials, 12 trials each) with either a nice stooge (trained to pull the tool 100% of the time) or a mean stooge (trained to pull the tool 0% of the time). In experiment 2, subjects played a reciprocating altruism game (i.e. no food for actor but one piece for recipient) for the first three sessions, the fourth session as byproduct mutualism game (i.e. a piece of food for the actor and the recipient), and the final fifth session as a reciprocating altruism game. In experiment 3, one subject was assigned to the player-1 position (pulling provided one piece to the actor and three pieces to the recipient) and one to the player-2 position (pulling provided no food for the actor and two pieces to the recipient). In experiment 4, the active tamarin could pull as an altruistic act (no food for self, one for the recipient), while the passive tamarin had no opportunity to pull; instead, when the tool switched to the passive tamarin’s side, the experimenter pushed the tool on 100 per cent of the trials, thus mimicking the payoff structure for the nice stooge in experiment 1.

altruistic act targeting a genetically unrelated individual. Results showed that subjects pulled significantly more often when paired in games with the nice stooge than the mean stooge. This suggests that tamarins can distinguish recipients based on their cooperative tendencies, and respond contingently. However, two criticisms immediately arise. First, identifying cooperators requires an ability to recognize the partner’s

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Evolving reciprocity and spite motivations—do they incur a cost in order to cooperate (altruism) or do they only cooperate when they also benefit (mutualism). Experiments 2 and 3 explored this possibility. Second, subjects may pull more when they themselves receive food, and this situation arises most when playing against the nice stooge who always delivers food. In other words, the higher rates of pulling when paired with the nice stooge is simply a reflection of the higher rates of reinforcement, a situation that could just as easily be achieved by a machine delivering food. Experiment 4 attempted to test this alternative account. In experiment 2, two genetically unrelated tamarins played five sessions, with sessions 1, 2, 3 and 5 associated with altruistic actions (the actor’s pull results in no food for self but one piece of food for the recipient) and session 4 associated with food delivery as a byproduct (the actor’s pull results in one piece of food for self and one for the recipient). Here, we expected the rate of pulling to decline from sessions 1 – 3, then rise to 100 per cent in session 4 (i.e. the actor selfishly gains regardless of food delivered to recipient). If subjects perceive session 4 as altruistic—that is, each pull consists of an attempt by the actor to give (at some cost) food to the recipient—then actors should pull at higher rates in session 5 than in session 3; in other words, session 4 should kick start cooperation in session 5. In contrast, if subjects perceive session 4 as a case of byproduct mutualism, where food is obtained as an accidental byproduct of otherwise selfish behaviour, then pulling rates should decline or remain the same in session 5. Results showed that pulling rates in session 5 were not significantly different from session 3, supporting the byproduct mutualism hypothesis, and rejecting the more general interpretation of experiment 1 in terms of reinforcement history. To push on the interpretation of experiment 2, experiment 3 set up different payoffs for each of the two players; although each tamarin played in both the player-1 and -2 roles across different games (i.e. different partners), each player kept their role within a game. In the player-1 position, pulling the tool brought one piece of food to the actor and three pieces to the recipient. In the player-2 position, pulling the tool brought no food to the actor and two pieces to the recipient. Thus, if both players pulled, each would obtain three pieces of food after a round of two trials. The interpretation of the results of this game hinge on player-2’s analysis of player-1’s pulls. If player-2 perceives player-1’s pulls as selfish (and we assumed player-1 would pull on virtually 100% of the trials as the act delivers one piece of food to self), then player-2 should never pull as the receipt of three pieces of food from player-1 is an accidental byproduct. In contrast, if player-2 perceives player-1’s act of pulling as intentional in some sense, driven by the goal of giving player-2 three pieces of food, then player-2 should pull as a reciprocated altruistic gesture. Results showed that player-2 virtually never pulled, supporting the first interpretation, and suggesting that tamarins make economically relevant decisions on the basis of subjects’ underlying motivations as opposed to the outcomes alone. This Phil. Trans. R. Soc. B (2009)

M. Hauser et al.

3259

conclusion is supported by other studies of non-human primates in both economic decisionmaking contexts as well as other situations (de Waal 2000; Call et al. 2004; Rochat et al. 2007; Warneken et al. 2007; Buttelmann et al. 2008; Lakshminaryanan et al. 2008; Wood et al. 2008). In the final study, tamarins were placed in a set up that was virtually identical to experiment 1, except that instead of the nice tamarin stooge, a human experimenter pushed the tool towards the tamarin, providing a reward structure that was identical to the nice stooge. That is, after every trial in which the active tamarin had an opportunity to altruistically give food to a passive tamarin recipient, the tool then changed sides and now, the experimenter pushed the tool towards the active tamarin, giving him or her a piece of food. Once again, if tamarins only attend to the reinforcement structure of games (i.e. only outcomes as opposed to the means by which they are attained), then the active tamarin should pull at a high rate, comparable to the rates observed in experiment 1 with the nice stooge. In contrast, if tamarins pay attention to the means, and recognize that the passive tamarin played no role at all in the delivery of food, then the active tamarin should rarely pull. Results showed that tamarins rarely pulled in this condition, with rates approximating to those observed in experiment 1 for the mean stooge. Together, these studies suggest that tamarins are sensitive to some of the important proximal ingredients that enter into reciprocity, including altruistic contingency, reputation tracking and distinguishing the means by which outcomes are obtained. That said, when one explores the longer term pattern of cooperation observed in these experiments, it is clear that tamarins are incapable of sustaining reciprocity as even a rather brief period of defection causes the cooperative relationship to unravel. In particular, based on a game theoretic analysis of the tamarin results from the non-stooge games, it is clear that after two consecutive rounds of defection, tamarins stop pulling in the altruistic condition, and never recover the reciprocally cooperative relationship (Chen & Hauser 2005). Thus, although tamarins may have some of the cognitive prerequisites for reciprocity, these capacities appear insufficient to sustain reciprocity. Moreover, and paralleling the study on jays, the reciprocity observed among tamarins only emerges under fairly artificial conditions, including the presentation of discrete packages of food, highly predictable periods of interaction, and with individuals trained to be pure cooperators or defectors. The final study of reciprocity concerns a set of experiments on captive chimpanzees (Pan troglodytes). In thinking about the cognitive building blocks of reciprocity, as well as the evolutionary pressures that would select for this kind of cooperation, chimpanzees would seem to be the most promising of animal species (Stevens & Hauser 2004; Melis et al. 2008). For example, under natural conditions, chimpanzees show significant levels of cooperation in the context of coalitions during aggressive competition (both within- and between-groups) as well as during hunting. Although chimpanzees do not live in large

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Evolving reciprocity and spite

Phil. Trans. R. Soc. B (2009)

nice stooge

OR

mean stooge

room 3

food

room 1

room 2

room 3

peg

OR

room 1

peg

ch ai n

peg

ch ai n

groups, the fission – fusion nature of their social organization means that they cannot always rely on particular individuals for help. Perhaps as a result, recent molecular and behavioural research shows that chimpanzee cooperation occurs between kin and non-kin (Langergraber et al. 2007). Added on to these ultimate considerations are experiments and observations targeting proximate mechanisms. In particular, chimpanzees have the capacity for numerical quantification (Boysen & Berntson 1995; Boysen et al. 1996; Kawai & Matsuzawa 2000; Beran et al. 2008), show significant levels of delayed gratification (Evans & Beran 2007; Rosati et al. 2007), inequity detection (Brosnan et al. 2005; Brauer et al. 2006), prosocial helping in non-food contexts (Warneken & Tomasello 2006; Warneken et al. 2007), vengeance (Jensen et al. 2007b), discrimination of intentional and accidental actions (Call et al. 2004), selectively choosing previous collaborators over non-collaborators in joint cooperation tasks (Melis et al. 2006), and recognizing individuals by face and voice (Parr 2003). Taking advantage of these capacities, Melis et al. (2008) designed an elegant series of experiments with captive chimpanzees, asking whether subjects would preferentially choose to reciprocate an altruistic action towards a previously nice and cooperative stooge over a previously mean and uncooperative stooge. Underlying these experiments was prior evidence that chimpanzees could recruit collaborators in a joint action task (i.e. a task in which two subjects must work together to attain a reward, and where defection by one leads to an overall failure such that no one attains any reward), and preferentially select the most collaborative collaborator (Melis et al. 2006). In experiment 1, subjects first learn that the nice stooge always provides them with access to a rope, that if jointly pulled, brings food, whereas the mean stooge never gives them access. Following this exposure phase, subjects are then presented with an opportunity to allow either the nice or mean stooge to join them at the pulling tray. In the first block of trials, one out of eight subjects picked the nice stooge, two were indifferent, and five actually picked the mean stooge. In the second block of trials, three subjects picked the nice stooge (only one with a strong preference), two were indifferent and three picked the mean stooge. Although there was a slight increase in the preference for the nice stooge over the baseline period, this effect was only just significant at the p , 0.05 level and with a one-tailed test. Thus, based on analyses of individual preferences, there was, at best, only weak evidence of reciprocity. In a second series of experiments (figure 4), the nice stooge altruistically opened the door for the subject to get food, whereas the mean stooge opened the door to selfishly get food for himself. As in experiment 1, the question here was whether subjects would give the nice stooge more frequent access to the pulling tray when compared with the mean stooge. Pooling across individuals, there was no evidence that subjects opened the door more often for the nice than the mean stooge. On an individual level, only one subject out of eight showed a significant difference between stooges in the predicted direction, opening the door on every trial for the nice

target door

M. Hauser et al.

target door

3260

food room 2

Figure 4. Experiments on reciprocity in captive chimpanzees by Melis et al. (2008). The top panel shows the initial set up used to establish the reputation of the nice (green dot) and mean (red dot) stooges. When the subject removed the peg for the nice stooge, this individual entered and collaborated in pulling in the tray with food. When the subject removed the peg for the mean stooge, this individual entered and consumed the food alone. The bottom panel reveals the set up for the critical test phase in which the subject has the opportunity to open the door, on separate trials, either the nice or mean stooge.

stooge and never for the mean stooge. In summary, as the authors note, this study provides only weak evidence of reciprocity in chimpanzees. What, therefore, is missing in the toolkit of animal cognition that appears in human cognition? Why, in most studies, are animals apparently incapable of engaging in reciprocal altruism, and in those cases where there is some evidence, why are the effects weak and dependent upon quite extreme experimental setups that rarely, if ever, arise under natural conditions (de Waal 2000; Stephens et al. 2002; Hauser et al. 2003; Melis et al. 2008)? The research on chimpanzees reveals the fundamental contrast with humans. Here is a species with the capacity to delay gratification, quantify potential payoffs, detect inequities and punish individuals for norm violations, but these ingredients do not combine to create a system for reciprocity. By contrast, human children understand norms of reciprocity by early elementary school (De Cooke 1992) and use these norms to establish friendships (for review see Eisenberg et al. 2006). The ability to delay gratification (Mischel et al. 1989) and integrate intentions and outcomes may take longer to develop (Sutter 2007), but children appear fully capable of reciprocal altruism by about

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Evolving reciprocity and spite 9 years of age. Our proposal is that animals generally lack the capacity to integrate cognitive functions required for reciprocal altruism, while for humans that integration occurs as a normal part of development (see §4). What ultimate pressures might encourage a cognitive system that enables reciprocal altruism to evolve? One possibility is that over the course of human evolution, the gradual expansion of small kin groups into large stable groups of unrelated individuals led to the evolution of reciprocity, and subsequently, strong demands on the capacity to detect and punish cheaters. As Boyd and his colleagues (Boyd & Richerson 1992; Boyd et al. 2003) have noted, stable cooperation requires not only punishment of cheaters but punishment of those who do not punish cheaters. And because punishment plays such a critical role in human social interaction, it appears to spill over into other forms of social behaviour, including spiteful actions (see §3) that are often accompanied by feeling good about another’s misfortunes, an emotion that only the German language has assigned to a single word: Schadenfreude. Thus, when we punish others for what we see as a wrongdoing, including cases where we incur a personal cost for imposing such punitive measures, our actions are personally rewarding as evidenced by the fact that the reward areas of the brain are significantly activated (de Quervain et al. 2004). Thus far, there is little evidence that chimpanzees, or any other species, directly punish (i.e. as opposed to indirect punishment in the form of ostracism, which may be present in animals) individuals who fail to cooperate, and in fact, explicit experimental and observational evidence that they do not (Heinsohn & Packer 1995; Wilson et al. 2001; Jensen et al. 2007b). Thus, for example, although chimpanzees will move out in groups during border patrols and when confronted by territorial intruders, there is no cost to individuals that lag behind (Wilson et al. 2001). What makes the absence of punitive action in these cooperative contexts of interest is that punitive behaviour arises in other, non-cooperative situations ( Jensen et al. 2007b). For example, chimpanzees will take food away from another chimpanzee who has taken food from them in the recent past. This shows that chimpanzees can engage in a form of ‘vengeful punishment’ when a norm violation has arisen (e.g. theft of property), but do not tap this capacity in the context of cooperation.

3. SPITE As Gardner & West (2004) noted in the most recent review of the literature, spite is the ‘relatively neglected ugly sister of altruism’ (p.1195). Although there has certainly been less research on spite than on other forms of social interaction (see figure 1 and the matrix of social interactions), we suggest that the lack of research has perhaps less to do with neglect than with the ultimate and proximate considerations required for spite to evolve, and the confusions in the literature concerning the criterion for demonstrating spite (Foster et al. 2001; West et al. 2007). Part of Phil. Trans. R. Soc. B (2009)

M. Hauser et al.

3261

this problem stems from the fact that different disciplines have approached spite from different angles. Evolutionarily oriented researchers have focused on the ultimate conditions for the evolution of spite, targeting the significance of genetic relatedness and fitness consequences. By contrast, much of the more psychologically oriented research has been done by behavioural economists targeting the proximate processes that underlie fairness and the detection of inequities (Kirchsteiger 1994; Fehr & Fischbacher 2005). Thus, to distinguish these two approaches to spite, we call the evolutionary view genetic spite and the proximate approach psychological spite. Following on the heels of his conceptual analysis of the evolution of altruism by means of kinship, Hamilton (1970, 1971) argued that genetic spite—an action that imposes a significant cost on another with either no fitness costs or a relatively small cost to the actor—can evolve as long as actors and agents are negatively related. Negative relatedness arises when r , 0, meaning that the odds that actor and agent share genes in common is less likely than with a randomly selected individual from the population. Selection can therefore favour genetic spite among negatively related individuals because it reduces the frequency of competitive genes in the population. Wilson (1975) considered an alternative route to the evolution of genetic spite by considering the potential role of a third-party, non-interacting observer. As defined, if observer O is related to actor A, and if the benefit to O from A’s spiteful action outweighs the costs to A and the recipient R of such spite, then genetic spite can evolve. Interestingly, though both Hamilton and Wilson considered the evolution of genetic spite as possible, both argued that it was unlikely to represent a significant form of social interaction in animals. For Hamilton in particular, the prediction that genetic spite would be relatively rare was based on the supposition that socially living animals (i) should infrequently find themselves in a situation of negative relatedness; (ii) most likely lack the requisite fine-grained kin recognition mechanisms; and (iii) typically engage in actions with significant costs as opposed to no or little cost, as the theory demanded. During the first 30 years or so of empirical exploration post-Hamilton’s analysis, several examples of genetic spite were put forward in the animal literature. Most, if not all, however, could be better explained as cases of selfishness or as a form of punishment where the actor’s personal fitness ultimately benefits from the spiteful interaction (Clutton-Brock & Parker 1995). That is, though the actor’s behaviour indeed imposed a cost on the recipient, the actor typically gained from this action, either immediately or after some delay. For example, in several species of birds and primates, adults aggressively harass and even attack juveniles, or copulating couples. Though such attacks are clearly associated with a cost in terms of energy loss to the attacker, and presumably even greater costs to the juveniles and mating couples, the attacker reaps competitive gains (Foster et al. 2001; Gardner & West 2004). In behavioural economic circles, the problem of psychological spite has focused more on the relevant

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3262

M. Hauser et al.

Evolving reciprocity and spite

proximate ingredients, and in particular, on notions of fairness with respect to payoffs. Thus, as Fehr & Fischbacher (2005) note, ‘A spiteful or envious person always values the economic payoff of relevant reference agents negatively. The person is, therefore, willing to decrease the economic payoff of a reference agent at a personal cost to himself . . . irrespective of the payoff distribution and irrespective of the reference agent’s fair or unfair behaviour.’ On this view, there is, contrary to the evolutionary approach, no burden to show negative relatedness among the players. However, there is a need to provide evidence that an agent imposes a cost on another by incurring a personal cost, and with such evidence, explain the individual utility of spiteful actions, starting with assessing the cognitive factors involved. Two recent studies by Jensen et al. (2007a,b) set out to provide a test of psychological spite in chimpanzees. In the first study, they set up a task that was designed to mimic important details of the payoff structure of an ultimatum game. In particular, in each of the four conditions, the donor had the opportunity to choose between two payoff distributions and the recipient had the option of accepting or rejecting the offer; acceptance led to the donor and recipient gaining access to the associated reward, whereas rejection led to no food for either donor or recipient. The four option pairings were always anchored against eight for the donor and two for the recipient: (1) 5 versus 5; (2) 2 versus 8; (3) 8 versus 2; and (4) 10 versus 0. Thus, condition-1 provided a fair option, condition-2 a hyper-fair option, condition-3 no option, and condition-4 a hyper-selfish option. There were two central results. Donors typically proposed the option that provided them with the highest returns, and critically, recipients accepted all non-zero offers. That is, and in contrast with human subjects similarly tested, chimpanzees did not act spitefully, rejecting unfair offers at a personal cost, and an even greater cost to the donors. However, the chimpanzee responders did draw the line at offers of zero in condition 4, refusing to endorse the division when they had nothing to gain. In the second task, briefly described above in the reciprocity section, Jensen and colleagues set up a collapsible table between an actor and either an empty room or another chimpanzee. In each condition, the actor had access to a rope that allowed him or her to collapse the table, dumping any item on top of the table onto the floor. In the two critical conditions, the actor either faced another chimpanzee on the other side of the table with food or an empty room. If chimpanzees are psychologically spiteful, then they should actively dump the table (i.e. pull the rope) when the other individual has access to food and they don’t; they should pull the rope more often in this social condition than when there is inaccessible food on the table, but the adjacent room is empty. In contrast, if chimpanzees are simply frustrated by their own inability to access the food, then they should pull the rope equally frequently in the social and non-social conditions. Results strongly confirmed the latter hypothesis: chimpanzees pulled equally frequently in the social and non-social conditions, Phil. Trans. R. Soc. B (2009)

revealing that frustration, but not psychological spite, drives their behaviour. Thus, and as noted in the previous section, chimpanzees are capable of vengeance, but not psychological spite. For psychological spite to evolve, subjects must be willing to incur a direct cost in order to decrease the welfare of another and even in cases where there is no cost to the self, subjects must accept the possibility that the recipient will retaliate. Recipients will not take an attack sitting down so to speak. Thus, psychological spite is a risky behaviour that requires the computation of current and future costs and benefits, capacities that seem to be in play at some level, in both apes and corvids (Mulcahy & Call 2006; Raby et al. 2007). Additionally, psychological spite requires some degree of inhibitory control. Using the example of chimpanzees above, actors would have to inhibit their frustration when food is out of reach and only collapse the tray when a peer enjoys the advantage of access to the food. Similarly, in the ultimate game, chimpanzees would have to resist the temptation of a small reward in order to reject a disadvantageous outcome. Though these inhibitory and computational capacities are, to some extent, present in chimpanzees, they once again seem weakly integrated into a single system. In contrast to other species, humans clearly engage in spiteful actions, and certainly engage in behaviour that is costly to self and even more costly to others (Trivers 1971; Fehr & Gachter 2002; Fehr & Henrich 2003; Henrich et al. 2006). Again, experiments in behavioural economics provide important details. As noted above, in the ultimatum game chimpanzees do not reject inequity—as long as responders receive some reward, they endorse unequal allocations of food. However, human versions of this game became an important test case for economic theory precisely because responders are willing to reject non-zero offers. Review of the many variations of ultimatum games leads to the conclusion that responders reject offers of 20 per cent or less of the stake about half of the time (Camerer 2003). The high rejection rates in the game constitute a form of punishment (as opposed to psychological spite which is not reactive to a norm transgression)—proposers have intentionally violated some norm of fairness which responders are willing to punish at a cost to themselves. However, responders continue to reject low offers even when intentions have been removed. When unequal offers are generated by a computer (Blount 1995) or by a roll of dice (Falk et al. 2008), over 60 per cent of participants still reject offers that favour the other player. Notably, responses to inequity appear to be shaped by culture. Henrich et al. (2005) found wide variation in levels of rejection in ultimatum games across smallscale societies. Their study showed that while individuals in all societies demonstrate a sensitivity to fairness, the perception of what constitutes a fair offer is shaped by cultural norms. For example, in two societies in particular—the Au and Gnau of Papua New Guinea—responders even rejected very generous offers. While the authors explain this phenomenon in terms of cultural practices such as competitive giftgiving, what remains to be seen is what aspects of

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Evolving reciprocity and spite human cognition underlie the willingness to reject any non-zero offer, prior to the influence of culture. Research on children’s development provides an opportunity to assess the emergence of different cognitive capacities in relation to behavioural outcomes. Economic experiments with children have shown that 9-year-olds are willing to reject unequal rewards in ultimatum games even when the proposer has no choice in the allocation. Notably, children of this age reject inequity both when they receive less than a peer and, to a lesser extent, when they receive more (Sutter 2007). This latter result differs markedly from adults of the same Western culture who were quite willing to accept generous offers (only 3% rejected). To assess the developmental origins of children’s aversion to inequity, we designed a series of competitive games for young children between the ages of 4 and 8 (Blake et al. submitted). In these experiments, one individual always played the role of donor, and the other the role of receiver. Subjects were unfamiliar and genetically unrelated. For a given game, two children sat across from each other with the test apparatus placed in between them. The donor had access to two levers that controlled the action of two plates, one proximally associated with the donor, the other with the receiver. If the donor pulled the green lever, the plates tipped up and caused rewards (candy) to roll, respectively, towards the donor and recipient. If the donor pulled the red lever, the plates tipped down and caused the rewards to roll into a bowl and disappear. Thus, pulling the green lever was associated with accepting the distribution of rewards, whereas pulling the red lever was associated with rejecting the rewards. Each pair of children played a total of 12 trials. Within a session, there were always six trials with an equitable distribution of one candy for the donor and one for the recipient. The other six trials were either set up as an advantageous inequity game (pulling the green lever brought four candies to the donor and only one candy to the recipient) or a disadvantageous inequity game (pulling the green lever brought one candy to the donor and four pieces to the recipient). In both the equity and inequity games, pulling the red lever caused all of the candies to roll out of reach, thus creating a round of no rewards for either child. Rejecting the rewards in the advantageous condition represents an example of self-sacrifice, whereas rejecting the rewards in the disadvantageous condition represents a case of psychological spite. Pilot data collected thus far, and restricted to the equity and disadvantageous inequity conditions, indicate that children of all ages accepted the majority of the equity trials, thus demonstrating that one piece of candy was sufficiently motivating to continue distributing an equal reward to a peer. In the disadvantageous inequity condition, even the youngest children demonstrated a willingness to reject one piece of candy in order to prevent their peer from getting four pieces. Though preliminary, these results are surprising given that sacrificing any candy requires inhibitory control which develops slowly with age (Davidson et al. 2006) making sacrificial rejections much more likely for older children. Placing these results in the context of the animal work discussed above, some striking patterns appear. Phil. Trans. R. Soc. B (2009)

M. Hauser et al.

3263

First, although young children tend towards selfinterest they soon demonstrate a willingness to inhibit their desire for candy in order to prevent a peer from getting more than them—a form of psychological spite (see also Fehr et al. 2008). Notably, rejections in the disadvantageous condition were in reaction to the relative outcomes alone as opposed to being in response to actions of the peer. Thus, by the functional definitions in the payoff matrix (figure 1), even 4-yearolds engage in psychological spite. Paralleling our comments in the section on reciprocity, it appears that psychological spite evolved in humans both because the requisite cognitive capacities were in place and because there was significant selection on punishing norm violators, even at personal cost; whether genetic spite also exists is unclear, and as in animal studies, may be difficult to demonstrate due to the challenges of proving negative relatedness and of demonstrating spite in isolation of a larger punishment interaction. But given the evidence for psychological spite, humans clearly evolved the ability to detect inequities, control immediate desires, foresee the virtues of norm following, and gain the personal, emotional rewards that come from seeing another punished. Though some animals have some of these capacities, only humans evolved a brain that integrates them into one system, and enables spiteful behaviour. On an ultimate level, we speculate that psychologically spiteful behaviour evolved in humans as a byproduct of selection on punishment. In particular, and as previously noted, punishment was favoured in human evolution because of the increasing significance of social norms, the increase in group size, and in particular, the relative increase in cooperation between genetically unrelated and unfamiliar others. These factors placed intense selective pressure on the capacity to detect and discourage defection. Though some animals punish others in certain restrictive contexts, punishment neither emerges as a means to enforce cooperation, nor does it appear necessary. Thus, the lack of punishment in a cooperative context, and the lack of psychological spite makes sense, if our account of the evolution of human spite as a byproduct of punishment is correct.

4. CONCLUSIONS Darwin knew that altruism, and morality more generally, represent genuine puzzles in light of his theory of natural selection. Adopting the gene’s eye view, these altruistic actions no longer represent a challenge to Darwin’s logic. The costs of altruism are either neutralized by kinship or by the prospects of a reciprocally altruistic relationship. As well as this theoretical perspective works, it largely fails to account for the virtual absence among social vertebrates of reciprocal altruism and spite. In this essay, we have argued that consideration of proximate and ultimate factors leads to the prediction that reciprocity and spite (both genetic and psychological) should be rare or absent in non-human animal populations. In particular, we have suggested that non-human animals do not live in the kinds of societies that would create

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3264

M. Hauser et al.

Evolving reciprocity and spite

strong pressure on individuals to require reciprocity to obtain help given that the density of kin is high, and thus, the probability of interacting with them is high as well; in other words, individuals can rely on their kin in times of need. Similar, ultimate level arguments apply to spite. That is, in most cases where an individual does something to impose costs on another, the underlying motivation for such behaviour is selfish. Given that there are many other ways other than spite to increase one’s relative fitness, the costs of spite will very rarely be favoured. Even if selection favoured reciprocity and spite, the mechanisms required to support these social interactions are, we have argued, largely absent in non-human animals. More specifically, even in cases where some of the relevant psychological components are in place, what is missing are the interfaces between these components. Thus, to support reciprocity, animals must be able to quantify the costs and benefits, time the returns, delay gratification, assess reputation, compute the contingencies and punish cheaters. Though many animals have the requisite skills of quantification, as well as the capacity to wait for beneficial returns and punish those who violate social norms, these capacities are not integrated into one functional system that can subserve reciprocal interactions. Similarly, though animals can sometimes behave in a purely prosocial manner (helping another at a cost and without expecting reciprocal returns; e.g. Warneken & Tomasello 2006; Warneken et al. 2007), and even though they can inhibit some actions with the goal of waiting for a more preferable outcome (Evans & Beran 2007; Rosati et al. 2007), they are not able to integrate these abilities in the service of not only detecting inequities, but acting upon them in such a way as to deliver a severe cost to another, while incurring a personal cost—psychological spite. It is this capacity—the ability to create interfaces between different psychological processes—that is perhaps the hallmark of our uniquely human cognition (Hauser 2009). Though human thought, like animal thought, is built from modular processes, we have the distinctive capacity to integrate the outputs from these processes to create novel representations, or more generally, novel solutions to old and new problems. Thus, we have the capacity to quantify how much money we borrowed (number system), tag the cardinality with a linguistic symbol (language system), take the money and exchange it for some food (economic system), realize that we could have bought it for half the price at a nearby store (number, economics and language) and then experience outrage (emotional system) because the store owner ripped us off (moral system). In sum, what enabled humans to engage in reciprocity and spite was not only a particular set of socioecological conditions that favoured such interactions, but also, a critical set of psychological mechanisms that made them possible in the first place. Thus, proximate and ultimate factors partnered up at some point in human evolution, paving the way to a species that could follow the golden rule and just as easily spite their neighbour. Phil. Trans. R. Soc. B (2009)

REFERENCES Barrett, L., Henzi, S., Weingrill, T., Lycett, J. & HIll, R. 1999 Market forces predict grooming reciprocity in female baboons. Proc. R. Soc. Lond. B 266, 665– 670. Beran, M., Evans, T. & Harris, E. 2008 When in doubt, chimpanzees rely on estimates of past reward amounts. Proc. R. Soc. B 276, 309–314. (doi:10.1098/rspb. 2008.1027) Blake, P. R., McAuliffe, K. & Hauser, M. D. Submitted. The development of inequity aversion and self-sacrifice in children. Blount, S. 1995 When social outcomes aren’t fair: the effect of causal attributions on preferences. Organ. Behav. Human Decision Process. 63, 131– 144. (doi:10.1006/ obhd.1995.1068) Boyd, R. & Richerson, P. J. 1992 Punishment allows the evolution of cooperation (or anything else) in sizeable groups. Ethol. Sociobiol. 113, 171–195. Boyd, R., Gintis, H., Bowles, S. & Richerson, P. J. 2003 The evolution of altruistic punishment. Proc. Natl Acad. Sci. USA 100, 3531–3535. (doi:10.1073/pnas.0630443100) Boysen, S. T. & Berntson, G. G. 1995 Responses to quantity: Perceptual versus cognitive mechanisms in chimpanzees (Pan troglodytes). J. Comp. Psychol. 21, 82–86. Boysen, S. T., Berntson, G. G., Hannan, M. B. & Cacioppo, J. T. 1996 Quantity-based inference and symbolic representations in chimpanzees (Pan troglodytes). J. Exp. Psychol.: Anim. Behav. Process. 22, 76– 86. (doi:10.1037/ 0097-7403.22.1.76) Brauer, J., Call, J. & Tomasello, M. 2006 Are apes really inequity averse? Proc. R. Soc. B 273, 3123– 3128. (doi:10.1098/rspb.2006.3693) Brosnan, S., Schiff, H. C. & de Waal, F. B. 2005 Tolerance for inequity may increase with social closeness in chimpanzees. Proc. R. Soc. B 272, 253 –258. (doi:10. 1098/rspb.2004.2947) Bshary, R. & Grutter, A. 2005 Punishment and partner switching cause cooperatve behaviour in a cleaning mutualism. Biol. Lett. 1, 396–399. (doi:10.1098/rsbl.2005.0344) Bshary, R. & Grutter, A. 2006 Image scoring and cooperation in a cleaner fish mutualism. Nature 441, 975 –978. (doi:10.1038/nature04755) Buttelmann, D., Carpenter, M., Call, J. & Tomasello, M. 2008 Rational tool use and tool choice in human infants and great apes. Child Dev. 79, 609 –626. (doi:10.1111/ j.1467-8624.2008.01146.x) Call, J., Hare, B., Carpenter, M. & Tomasello, M. 2004 ‘Unwilling’ versus ‘unable’: chimpanzees’ understanding of human intentional action. Dev. Sci. 7, 488 –498. (doi:10.1111/j.1467-7687.2004.00368.x) Camerer, C. F. 2003 Behavioral game theory: experiments in strategic interactions. Princeton, NJ: Princeton University Press. Chen, M. K. & Hauser, M. 2005 Modeling reciprocation and cooperation in primates: evidence for a punishing strategy. J. Theoret. Biol. 235, 5–12. (doi:10.1016/j.jtbi. 2004.12.015) Clements, K. C. & Stephens, D. W. 1995 Testing models of non-kin cooperation: mutualism and the Prisoner’s Dilemma. Anim. Behav. 50, 527 –535. (doi:10.1006/ anbe.1995.0267) Clutton-Brock, T. H. & Parker, G. A. 1995 Punishment in animal societies. Nature 373, 209–216. (doi:10.1038/ 373209a0) Coyne, J. A. & Sohn, J. J. 1978 Interspecific brood care in fishes: reciprocal altruism or mistaken identity? Am. Nat. 112, 447– 450. (doi:10.1086/283287) Darwin, C. 1871 The descent of man and selection in relation to sex. London, UK: John Murray.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Evolving reciprocity and spite Davidson, M. C., Amso, D., Anderson, L. C. & Diamond, A. 2006 Development of cognitive control executive functions from 4 to 13 years: evidence from manipulations of memory, inhibition, and task switching. Neuropsychologia 44, 2037–2078. (doi:10.1016/j.neuropsychologia.2006. 02.006) Dawkins, R. 1976 The selfish gene. Oxford, UK: Oxford University Press. De Cooke, P. A. 1992 Children’s understanding of indebtedness as a feature of reciprocal help exchanges between peers. Dev. Psychol. 28, 948– 954. (doi:10.1037/00121649.28.5.948) de Quervain, D. J.-F., Fischbacher, U., Treyer, V., Schelhammer, M., Schnyder, U., Buck, A. & Fehr, E. 2004 The neural basis of altruistic punishment. Science 305, 1254– 1258. (doi:10.1126/science.1100735) de Waal, F. B. M. 2000 Attitudinal reciprocity in food sharing among brown capuchin monkeys. Anim. Behav. 60, 253 –261. (doi:10.1006/anbe.2000.1471) Eisenberg, N., Fabes, R. A. & Spinrad, T. L. 2006 Prosocial development. In Handbook of child psychology, vol. 3 (ed. N. Eisenberg), pp. 646–718. New York, USA: Wiley. Evans, T. A. & Beran, M. J. 2007 Chimpanzees use selfdistraction to cope with impulsivity. Biol. Lett. 3, 599 –602. (doi:10.1098/rsbl.2007.0399) Falk, A., Fehr, E. & Fischbacher, U. 2008 Testing theories of fairness—intentions matter. Games Econ. Behav. 62, 287 –303. (doi:10.1016/j.geb.2007.06.001) Fehr, E. & Fischbacher, U. 2005 The economics of strong reciprocity. In Moral sentiments and material interests (eds H. Gintis, S. Bowles, R. T. Boyd & E. Fehr), pp. 151 –192. Cambridge, USA: MIT Press. Fehr, E. & Gachter, S. 2002 Altruistic punishment in humans. Nature 415, 137 –140. (doi:10.1038/415137a) Fehr, E. & Henrich, J. 2003 Is strong reciprocity a maladaptation? On the evolutionary foundations of human altruism. In The genetic and cultural evolution of cooperation (ed. P. Hammerstein), pp. 55–82. Cambridge, USA: MIT Press. Fehr, E., Bernhard, H. & Rockenbach, B. 2008 Egalitarianism in young children. Nature 454, 1079–1083. (doi:10. 1038/nature07155) Foster, K. R., Wenseleers, T. & Ratnieks, F. L. 2001 Spite: Hamilton’s unproven theory. Ann. Zool. Fennici 38, 229 –238. Gardner, A. & West, S. A. 2004 Spite and the scale of competition. J. Evol. Biol. 17, 1195– 1203. (doi:10. 1111/j.1420-9101.2004.00775.x) Gumert, M. D. & Ho, M. R. 2008 The trade balance of grooming and its coordination of reciprocation and tolerance in Indonesian long-tailed macaques (Macaca fascicularis). Primates 49, 176–185. (doi:10.1007/ s10329-008-0089-y) Hamilton, W. D. 1964 The genetical evolution of social behavior. J. Theoret. Biol. 7, 1 –52. (doi:10.1016/00225193(64)90038-4) Hamilton, W. D. 1970 Selfish and spiteful behaviour in an evolutionary model. Nature 228, 1218– 1220. (doi:10. 1038/2281218a0) Hamilton, W. D. 1971 Selection of selfish and altruistic behaviour in some extreme models. In Man and beast: comparative social behavior (eds J. F. Eisenberg & W. S. Dillon), pp. 57–91. Washington, USA: Smithsonian Press. Hammerstein, P. 2003 Why is reciprocity so rare in social animals? A protestant appeal. In Genetic and cultural evolution of cooperation (ed. P. Hammerstein), pp. 83–94. Cambridge, USA: MIT Press. Hart, B. L. & Hart, L. A. 1989 Reciprocal allogrooming in impala, Aepyceros melampus. Anim. Behav. 44, 1073– 1084. (doi:10.1016/S0003-3472(05)80319-7) Phil. Trans. R. Soc. B (2009)

M. Hauser et al.

3265

Hauser, M. D. 2006 Moral minds: how nature designed our sense of right and wrong. New York, USA: Ecco/Harper Collins. Hauser, M. D. 2009 The possibility of impossible cultures. Nature 460, 190– 196. (doi:10.1038/460190a) Hauser, M. D., Chen, M. K., Chen, F. & Chuang, E. 2003 Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back. Proc. R. Soc. Lond. B 270, 2363–2370. (doi:10.1098/rspb.2003.2509) Heinsohn, R. & Packer, C. 1995 Complex cooperative strategies in group-territorial African lions. Science 269, 1260–1262. (doi:10.1126/science.7652573) Hemelrijk, C. K. & Luteijn, M. 1998 Philopatry, male presence and grooming reciprocation among female primates: a comparative perspective. Behav. Ecol. Sociobiol. 42, 207–215. (doi:10.1007/s002650050432) Henrich, J. et al. 2005 ‘Economic man’ in cross-cultural perspective: behavioral experiments in 15 small-scale societies. Behav. Brain Sci. 28, 795 –855. Henrich, J. et al. 2006 Costly punishment across human societies. Science 312, 1767–1770. (doi:10.1126/science. 1127333) Jensen, K., Hare, B., Call, J. & Tomasello, M. 2006 What’s in it for me? Self-regard precludes altruism and spite in chimpanzees. Proc. R. Soc. B 273, 1013–1021. (doi:10. 1098/rspb.2005.3417) Jensen, K., Call, J. & Tomasello, M. 2007a Chimpanzees are rational maximizers in an ultimatum game. Science 318, 107–109. (doi:10.1126/science.1145850) Jensen, K., Call, J. & Tomasello, M. 2007b Chimpanzees are vengeful but not spiteful. Proc. Natl Acad. Sci. 104, 13046– 13050. (doi:10.1073/pnas.0705555104) Kawai, N. & Matsuzawa, T. 2000 Numerical memory span in a chimpanzee. Nature 403, 39 –40. (doi:10.1038/ 47405) Kirchsteiger, G. 1994 The role of envy in ultimatum games. J. Econ. Behav. Org. 25, 373 –389. (doi:10.1016/01672681(94)90106-6) Krams, I., Krama, T., Igaune, K. & Mand, R. 2008 Experimental evidence of reciprocal altruism in the pied flycatcher. Behav. Ecol. Sociobiol. 62, 599 –605. (doi:10. 1007/s00265-007-0484-1) Lakshminaryanan, V., Chen, M. & Santos, L. 2008 Endowment effect in capuchin monkeys. Phil. Trans. R. Soc. B 363, 3837–3844. (doi:10.1098/rstb.2008.0149) Langergraber, K. E., Mitani, J. C. & Vigilant, L. 2007 The limited impact of kinship on cooperation in wild chimpanzees. Proc. Natl Acad. Sci. USA 104, 7786–7790. (doi:10.1073/pnas.0611449104) Melis, A., Hare, B. & Tomasello, M. 2006 Chimpanzees recruit the best collaborators. Science 311, 1297–1300. (doi:10.1126/science.1123007) Melis, A. P., Hare, B. & Tomasello, M. 2008 Do chimpanzees reciprocate received favours? Anim. Behav. 76, 951–962. (doi:10.1016/j.anbehav.2008.05.014) Mischel, W., Shoda, Y. & Rodriguez, M. L. 1989 Delay of gratification in children. Science 244, 933–938. (doi:10. 1126/science.2658056) Mulcahy, N. & Call, J. 2006 Apes save tools for future use. Science 312, 1038–1040. (doi:10.1126/science.1125456) Noe, R. 2006 Cooperation experiments: coordination through communication versus acting apart together. Anim. Behav. 71, 1–18. (doi:10.1016/j.anbehav.2005.03.037) Nowak, M. 2006 Five rules for the evolution of cooperation. Science 314, 1560–1563. (doi:10.1126/science.1133755) Parr, L. A. 2003 The discrimination of faces and their emotional content by chimpanzees (Pan troglodytes). Ann. NY Acad. Sci. 1000, 56– 78. (doi:10.1196/annals. 1280.005)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3266

M. Hauser et al.

Evolving reciprocity and spite

Raby, C. R., Alexis, D. M., Dickinson, A. & Clayton, N. S. 2007 Planning for the future by western scrub-jays. Nature 445, 919 –921. (doi:10.1038/nature05575) Rochat, M., Serra, E., Fadiga, L. & Gallese, V. 2007 The evolution of social cognition: goal familiarity shapes monkeys’ action understanding. Curr. Biol. 18, 227 –232. (doi:10.1016/j.cub.2007.12.021) Rosati, A. G., Stevens, J. R., Hare, B. & Hauser, M. 2007 The evolutionary origins of human patience, temporal preferences in chimpanzees, bonobos and human adults. Curr. Biol. 17, 1663–1668. (doi:10.1016/j.cub.2007. 08.033) Russell, A. F. & Wright, J. 2008 Avian mobbing: byproduce mutualism not reciprocal altrusim. Trends Ecol. Evol. 24, 3– 5. (doi:10.1016/j.tree.2008.09.003) Schino, G. & Aureli, F. 2008 Grooming reciprocation among female primates: a meta-analysis. Biol. Lett. 4, 9–11. (doi:10.1098/rsbl.2007.0506) Schino, G., di Sorrentino, E. P. & Tiddi, B. 2007 Grooming and coalitions in Japanese macaques (Macaca fuscata): partner choice and the time frame reciprocation. J. Comp. Psychol. 121, 181–188. (doi:10.1037/07357036.121.2.181) Seyfarth, R. M. & Cheney, D. L. 1984 Grooming alliances and reciprocal altruism in vervet monkeys. Nature 308, 541 –543. (doi:10.1038/308541a0) Stephens, D. W., McLinn, C. M. & Stevens, J. R. 2002 Discounting and reciprocity in an iterated Prisoner’s Dilemma. Science 298, 2216– 2218. (doi:10.1126/ science.1078498) Stevens, J. R. & Hauser, M. D. 2004 Why be nice? Psychological constraints on the evolution of cooperation. Trends Cogn. Sci. 8, 60–65. (doi:10.1016/j.tics.2003. 12.003) Sutter, M. 2007 Outcomes versus intentions: on the nature of fair behavior and its development with age. J. Econ. Psychol. 28, 69– 78. (doi:10.1016/j.joep.2006.09.001)

Phil. Trans. R. Soc. B (2009)

Trivers, R. L. 1971 The evolution of reciprocal altruism. Quart. Rev. Biol. 46, 35–57. Warneken, F. & Tomasello, M. 2006 Altruistic helping in human infants and young chimpanzees. Science 311, 1301– 1303. (doi:10.1126/science.1121448) Warneken, F., Hare, B., Melis, A., Hanus, D. & Tomasello, M. 2007 Spontaneous altruism by chimpanzees and young children. PLoS Biol. 5, 5–10. West, S., Griffin, A. & Gardner, A. 2007 Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415 –432. (doi:10. 1111/j.1420-9101.2006.01258.x) Wheatcroft, D. J. & Krams, I. 2008 Response to Russell and Wright: avian mobbing. Trends Ecol. Evol. 24, 5–6. (doi:10.1016/j.tree.2008.09.002) Wheatcroft, D. J. & Price, T. D. 2008 Reciprocal cooperation in avian mobbing: playing nice pays. Trends Ecol. Evol. 23, 416 –419. (doi:10.1016/j.tree.2008.04.011) Whitlock, M., Davis, B. & Yeaman, S. 2007 The costs and benefits of resource sharing: reciprocity requires resource heterogeneity. J. Evol. Biol. 20, 1772–1782. (doi:10. 1111/j.1420-9101.2007.01387.x) Wilkinson, G. S. 1984 Reciprocal food sharing in the vampire bat. Nature 308, 181– 184. (doi:10.1038/ 308181a0) Williams, G. C. 1966 Adaptation and natural selection. Princeton, NJ: Princeton University Press. Wilson, E. O. 1975 Sociobiology: a new synthesis. Cambridge, MA: Harvard University Press. Wilson, M. L., Hauser, M. D. & Wrangham, R. W. 2001 Does participation in cooperative intergroup conflict depend on numerical assessment, range location, or rank for wild chimpanzees? Anim. Behav. 61, 1203–1216. (doi:10.1006/anbe.2000.1706) Wood, J. N., Glynn, D. & Hauser, M. D. 2008 Rhesus monkeys’ understanding of actions and goals. Social Neurosci. 3, 60–68. (doi:10.1080/17470910701563442)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3267–3279 doi:10.1098/rstb.2009.0136

The ecology of social transitions in human evolution Robert Foley1,* and Clive Gamble2 1

Leverhulme Centre for Human Evolutionary Studies, University of Cambridge, Fitzwilliam Street, Cambridge, Cambridgeshire CB2 1QH, UK 2 Department of Geography, Royal Holloway, Egham, Surrey, UK

We know that there are fundamental differences between humans and living apes, and also between living humans and their extinct relatives. It is also probably the case that the most significant and divergent of these differences relate to our social behaviour and its underlying cognition, as much as to fundamental differences in physiology, biochemistry or anatomy. In this paper, we first attempt to demarcate what are the principal differences between human and other societies in terms of social structure, organization and relationships, so that we can identify what derived features require explanation. We then consider the evidence of the archaeological and fossil record, to determine the most probable context in time and taxonomy, of these evolutionary trends. Finally, we attempt to link five major transitional points in hominin evolution to the selective context in which they occurred, and to use the principles of behavioural ecology to understand their ecological basis. Critical changes in human social organization relate to the development of a larger scale of fission and fusion; the development of a greater degree of nested substructures within the human community; and the development of intercommunity networks. The underlying model that we develop is that the evolution of ‘human society’ is underpinned by ecological factors, but these are influenced as much by technological and behavioural innovations as external environmental change. Keywords: human evolution; social structure; social evolution; hominin behaviour; technological evolution

1. INTRODUCTION The evolutionary, or Darwinian, study of society has a long and often controversial history, encompassing as it does the early days of social Darwinism and the sociobiological debate of the 1970s (Wilson 1975; Allen 1976). A number of things have perhaps made this a less contentious topic than it was. Of these, the most important is the fact that the phrase ‘The Evolution of Society’ is no longer synonymous with the evolution of human society. A century of research in animal behaviour has extended the social world well beyond humans (Wilson 1975; Trivers 1985; Runciman et al. 1996). Social animals can be found across all the major groups (Vos & Velicer 2006). In the first part of this paper, we will consider what some of these key general social traits might be, as a basis for considering their evolutionary history and role. In other words, ‘what distinguishes human society, from that of other animals, particularly, given the recency of the last common ancestor, from chimpanzees (Pan troglodytes) and bonobos (Pan paniscus)?’. Additionally, advances have come in understanding the principles underlying variation in social behaviour (Crook 1970; Krebs & Davies 1984). Such principles range from the costs and benefits of cooperation (Clutton-Brock 1991), parental certainty (Davies

* Author for correspondence ([email protected]). One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

1991) to life history (Charnov & Berigan 1993) to the threat of predation (Van Schaik & Ho¨rstermann 1994) to the costs of territorial defence (Lowen & Dunbar 1994). Key to all of these, however, is the general consensus that social structure is shaped by resources. The principles of socioecology provide a powerful framework for studying social evolution, and provide the basis for the main thrust of this paper—‘that the major patterns of human social evolution have been shaped by changes in the environment or changes in the ecological relationships between humans and their resources, which can be tracked through time’. As we shall argue, over the course of human evolution, changes in male foraging behaviour have led to them having increased control over resources, and influencing the distribution and behaviour of females. This shift represents not just a change in socioecology, but also in the underlying model of behavioural ecology, and may be one way in which we can understand the unique nature of human society (figure 1).

2. BASAL HOMININ SOCIALITY At the most basic level, the parameters describing human society are the same as those for any other vertebrate group. The most obvious of these is the tendency to be social itself, namely to live in groups made up of known individuals (Hinde 1983). Other basic parameters that appear to be common across

3267

This journal is q 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3268

R. Foley & C. Gamble

Social transitions in human evolution

distribution of resources

controls distribution of females and their reproductive potential

classic socioecological cascade model based on asymmetry of reproductive costs for males and females

determines distribution of males in terms of access to females human ecological uniqueness: closure of the classic socioecological cascade males control distribution of resources Figure 1. The classical model of socioecology, in which owing to the different costs of male and female reproduction, females are more strongly influenced by resources, and males by the distribution of females (Wrangham 1980). During the course of human social evolution, the increased ability of males to control resources has led to a closure of the cascade model, with males exerting control over female distribution through the control over resources.

humans and non-humans are more prolonged parental relationships, which might be either sex or both, kinbased relationships among resident adults, sex-based patterns of dispersal, more or less prolonged relationships between adult males and females, with one or more partners, some degree of tolerance of the presence of other members of the ‘society’, a lack of equivalent tolerance for members of another group (or at least a different pattern of behaviour) and some degree of structured or repeated style of relationship between individuals (e.g. dominance, submission, friendliness, aggression, etc.). At this level, these basic parameters may be considered either as plesiomorphic traits that have evolved deep in vertebrate history or as forms of homoplasy common to all social animals. By looking more specifically at apes, especially the chimpanzee/bonobo as a sister clade, we can identify a number of basal traits which it is reasonable to assume were present in the earliest hominins. Although it has been criticized (Sayers & Lovejoy 2008), the genus Pan serves as the most parsimonious basis for determining basal hominin social traits (table 1, column A). The assumption here is that the earliest hominins lived in multi-male, multi-female ‘communities’, and this is the fundamental unit of human social organization (Ghiglieri 1987; Wrangham 1987; Foley 1989). This is important, as much theorizing in anthropology has tended to place primacy on the family unit, but we see this as a trait that emerges during the course of our evolution. On the basis of comparison with the apes more widely, it is also probable that male residence and female transfer was the primary organizational principle for reproduction. What follows from this is an emphasis on relationships between males being mediated by kinship and between females by non-kin-based affiliation. A further inference, based on chimpanzee analogy, would be hostile relationships between communities. Finally, a key element of the community-based Phil. Trans. R. Soc. B (2009)

socioecology of chimpanzees, and presumed here for the earliest hominins, would be the occurrence of a level of daily fission and fusion in foraging activities, with smaller parties forming the activity groups. Daily fusion would occur in the context of sleeping trees/shelter.

3. DERIVED HUMAN SOCIAL PATTERNS Derived human traits can be divided into three categories—those that show little structural change and essential continuity from the basal hominin/last common ancestor, even if they have been elaborated (column B); those that are similar in form to the ancestral condition, but have changed significantly in quantitative terms (column C); and those that appear to be derived features that are more or less novel (column D). It is clear that a number of key traits develop during the course of human evolution, which alter the fundamental structure of society. In practice, these are underpinned by unique mechanisms associated with human cultural capacities, but, at a socioecological level, these are properties found elsewhere in the animal kingdom, and therefore can be considered to have evolved as behavioural traits in response to resource-based conditions—the massive extension of a fission–fusion system (elephants, Loxodonta africana) (Couzin 2006); much greater substructuring within multi-male, multi-female communities (hamadryas baboons, Papio hamadryas) (Kummer 1968); strong and persistent male–female relationships (many birds, for example) (Mock & Fujioka 1990); higher levels of paternal investment (primates, many birds) (Charpentier et al. 2008); and larger group sizes (Janson & Goldsmith 1995).

4. KEY TRANSITIONS IN HUMAN EVOLUTION The increasingly complex pattern of hominin evolution (figure 2) contradicts previous models of a

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Social transitions in human evolution 0

Ma

floresiensis cepranensis

1

erectus

habilis

R. Foley & C. Gamble

heidelbergensis

sapiens

helmei rhodesiensis antecessor

neanderthalensis

3269

boisei ergaster georgicus

robustus

2 3 afarensis

aethiopicus garhi africanus platyops bahrelghazali

rudolfensis

4 ramidus

anamensis

5 kadabba tugenensis

6 7

tchadensis

8

Figure 2. The pattern of hominin evolution. First and last appearance ages of recognized hominin taxa provide chronological ranges. The colour coding indicates major groupings that represent adaptive shifts discussed in the text. Red bars, earliest hominins; blue bars, australopithecines and allies; orange bars, smaller-brained Homo; green bars, larger-brained Homo.

Table 1. The development of key traits during the course of human evolution. The structure of the derived traits is underpinned by unique mechanisms associated with human cultural capacities, but at a socioecological level, these are properties found elsewhere in the animal kingdom, and therefore can be considered to have evolved as behavioural traits in response to resource-based conditions. A (plesiomorphic traits)

B (derived hominin social traits)

C (derived hominin social traits)

D (derived features)

social characteristics of the basal hominins based on comparison with Pan as model of last common ancestor

strongly continuous with basal hominins/last common ancestor

quantitative extensions of basal hominin/last common ancestor traits

human novelties

multi-male, multi-female community structure male resident, female dispersal on maturity weak male –female bonding intercommunity hostility male hierarchy female hierarchy

compulsive sociality community structure at root of social organization multi-male, multi-female communities male-kin bonding female transfer predominant intergroup hostility

larger community sizes exploded or extended fission – fusion extension of kinship structures through generations and formations of lineages organized (female) mate transfer

strong male–female bonding and persistence of relationships higher paternal investment development of affinal kin relationships strong substructure within communities sex-based roles age-related dominance extensive parental investment and heritability of social status context-dependent intercommunity relationships male control of resources

continuous and gradual change towards the human condition. Rather, a summary of the archaeological and anatomical evidence (table 2 and figure 3) identifies a patchy pattern of change, especially when the different elements of the record are considered Phil. Trans. R. Soc. B (2009)

independently. We argue that, within this patchiness, clusters of significant events lead us to determine five key transitions (figure 4). (i) African ape to terrestrial bipedal ape (approx. 4 Ma). The date of this transition is uncertain,

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3270

R. Foley & C. Gamble

Social transitions in human evolution

Table 2. Summary of selected evidence for transitions in human evolution using five broad categories. The categories reflect the major ecological, life-history and behaviour aspects of hominin evolution and are by no means exhaustive. The evidence is drawn from the fossil and archaeological record. Dates are approximate estimates. Data relating to sexual dimorphism and brain size are shown in figure 3 and the overall distribution of hominin taxa in figure 1. The sum of these lines of evidence is used to propose five key transitions (given in italics in date column) (see also figure 4 and text). date

lithic technology

locomotion

life history

foraging

10 ka

domestication of plants and animals associated with increased sedentism

15 ka

earliest domestication of plants

20 ka

seed grinding technology/cereal exploitation

60 ka

80 ka

post last glacial maximum dispersals

first evidence of H. sapiens outside Africa and adjacent zones intensive specialized hunting

modes 4 and 5 (enhanced prepared core technology with blade and microlith production; emphasis on lightweight composite tools)

120 ka

exploitation of aquatic resources

150 ka

earliest H. sapiens dispersal

modern human life-history parameters

250 ka

400 ka

dispersal

mode 3 (Neanderthal lineage) dispersals systematic mediumsized ungulate hunting

mode 3 (prepared core technology; emphasis on projectiles and earliest hafting)

700 ka

larger brained Homo dispersals into Eurasia (H. heidelbergensis, H. antecessor)

800 ka

mode 2B (Acheulean biface technology with enhanced symmetry)

1.6 Ma

mode 2A (large flakes and Acheulean biface technology)

1.8 Ma

first evidence for fire (and cooking?)

human body shape shifts towards modern human condition

first shift in life history towards modern condition

increased evidence for regular meat-eating

first dispersals beyond Africa (Eurasian H. erectus dispersals) (Continued.)

Phil. Trans. R. Soc. B (2009)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Social transitions in human evolution

R. Foley & C. Gamble

3271

Table 2. (Continued.) date

lithic technology

2.6 Ma

mode 1 (flakes, pebble tools and the origins of percussive technology)

locomotion

life history

foraging

dispersal

shift to carnivory

3 Ma

australopithecine dispersals within Africa

4 Ma

unambiguous evidence for bipedalism

6 Ma

first evidence for bipedalism? (a)

(b) Ma 0

H. sapiens H. neanderthalensis Atapuerca H. heidelbergensis

1 Dmanisi H. georgicus (erectus) 2 3

A. afarensis

4 5 6 7

900

8 1500 110

cm3

120 130 male as % of female

140

Figure 3. (a) Pattern of evolution in brain size and (b) sexual dimorphism as indicated by the fossil record. Points shown are approximate, and ranges and potential errors can be considerable, especially for sexual dimorphism.

depending upon whether the proposal that Sahelanthropus and Ororrin are bipeds is sustained (Brunet et al. 2002). The date of around 4.0 Ma is used here and broadly coincides with the emergence and radiation of the australopithecines (Leakey et al. 1998), the group that responded to the opportunities posed by bipedalism, and dispersed widely across Africa. However, the context in which bipedalism arose is more likely to be the early part of the Pliocene. There is little other relevant evidence, but there are many grounds for seeing the major shift in locomotion as a critical adaptive and ecological change. (ii) Terrestrial bipedal ape (australopithecine) to ‘early Homo’ (approx. 2.0 Ma). Between 2.5 and 1.8 Ma, there is an enormous amount of change in the hominin Phil. Trans. R. Soc. B (2009)

lineage and its associated behaviour. In the early part of this period, the genus Homo evolves, and there is the first evidence for meat-eating and lithic technology (modes 1 and 2a) (Prat et al. 2005). From shortly after 2.0 Ma, the hominin body plan is reorganized from the ‘bipedal ape’ posture of the australopithecines to something very similar to modern humans (Walker & Leakey 1993); brain size increases substantially, and patterns of dental development indicate a delayed process of maturation (i.e. a shift in the life-history strategy) (Smith 1994). Perhaps most significantly, the impact of these changes can be seen in the rapid dispersal of hominins across Africa, and, for the first time, beyond. (iii) Early Homo to Homo heidelbergensis (1.0– 0.8 Ma). Between 1.0 and 0.8 Ma, another major

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3272

R. Foley & C. Gamble (a)

Ma

evolution

0

Social transitions in human evolution

locomotion

life history

brain size

sexual technology foraging dispersals dimorphism

T4 Homo heidelbergensis larger-brained Homo T3 terrestrial early hominins early Homo

1

T2 early Homo Homo heidelbergensis

2

3

4

T1 African apes terrestrial early hominins

5

6

7

8

(b) 0

Ka

evolution

locomotion

life history

brain size

sexual technology foraging dispersals dimorphism

50

large-brained hominins modern humans post-Pleistocene humans 100

150

200

Figure 4. The timing of the five key transitions discussed in the text, based on archaeological and palaeontological evidence (table 2). (a) The first four transitions occurring on a time scale of millions of years; (b) the fifth transition on a time scale of thousands of years.

change occurs. Although the fossil record is particularly poor, this is when H. heidelbergensis (derived from Homo erectus/ergaster depending upon terminology) evolves. However, more significantly, it is when the true ‘Acheulean’ stone technology develops (mode 2B), and spreads across much of Eurasia, providing the first significant colonization of more northerly environments (Gamble 1993). A number of shifts, perhaps including the extensive use of fire and even cooking (Wrangham et al. 1999), may provide the basis for a major change in hominin socioecology at this time, albeit at a regional scale. (iv) Homo heidelbergensis to larger brained Homo ( from 500 ka). From around half a million years ago, Phil. Trans. R. Soc. B (2009)

there is an increase in the rate of evolution of the brain. This can be seen in two lineages (Homo sapiens and Homo neanderthalensis), and may be a single evolutionary event, followed by later divergence (Foley & Lahr 1997) or convergence (Stringer & Hublin 1999). Among the changes that can be seen in this period are shifts in life history, the development of mode 3 technology and changes in subsistence behaviour (Stiner et al. 2000). (v) Larger-brained Homo to H. sapiens (200 – 0 ka). The final transition is the evolution of modern humans (Stringer 2002). This has often been considered a speciation event, as part of the ‘Out of

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Social transitions in human evolution Africa’ model, with morphological and behavioural change. However, the fossil, genetic and archaeological evidence suggest that these were cumulative changes spread over a period of more than 200 000 years (figure 3b), and continue through to the development of agriculture. The finer resolution of the archaeological and palaeontological records points to the multiple character of transitions (Foley & Lahr 1997; Foley 2005), a feature that is obscured in earlier examples (figure 3a). Evidence exists for the exploitation of aquatic resources, more specialized hunting behaviour, greater use of complex technology, the appearance of symbolic material culture as well as massive demographic growth (d’Errico et al. 2003; Marean et al. 2007; Atkinson et al. 2008).

5. TOWARDS AN ECOLOGICAL MODEL FOR THE EVOLUTION OF HUMAN SOCIETY: EXPLAINING KEY TRANSITIONS Having briefly described the evidence available, and inferred some key points in hominin evolutionary history, we can now turn to their explanation in terms of the relationship between ecological conditions and behavioural or social outcomes.

6. TRANSITION 1: BIPEDALISM AND RANGE SIZE The significant factor that is key to understanding the emergence of the early bipedal hominins is the change in climate and environment that occurs at the end of the Miocene and into the Early Pliocene. At this time, there was pronounced global cooling. The effect of this varied regionally, but there is general consensus that in Africa there was increasing aridity, a decline in closed forest habitats and a spread of more wooded, bushed and grassy environments, often with pronounced seasonality. There is a general trend towards terrestriality among the catarrhines during this period (Fleagle 1999), and the hominins in one sense represent the hominoid extreme in this context. Although there is debate about the environment in which bipedalism evolved, there is none concerning the extent to which it provides the basis for adaptation to terrestrial environments. In terms of behavioural ecology, there is a change towards more dispersed and patchy plant resources, many of which would have been of relatively poor quality. The key shift, and one likely to have played a major part in the selection for bipedalism, is towards longer day ranges. Furthermore, the more patchy environments are likely to have promoted a greater degree of fissioning behaviour in feeding parties, and this may also have become more extensive if sleeping sites were both more dispersed and less suitable for larger communities. One of the bases for later human social behaviour, extensive fissioning and fusing may have had its roots in this change. A further implication might also have been, through the fissioning, a greater tendency for the formation of substructuring within the larger communities. Derived from general models, a further expectation would be that there was a decrease in Phil. Trans. R. Soc. B (2009)

R. Foley & C. Gamble

3273

community size (counter to later trends in human evolution) (Foley 2001). One of the interesting but uncertain implications of this concerns the nature of intergroup relationships under these circumstances. Smaller communities would have been vulnerable to attack, and also more reluctant to patrol borders. The costs of hostility may have been high, and it is possible that, compared with chimpanzees, these communities may have had more variable intergroup encounters. However, although there are shifts in the socioecology of these early australopithecines, the basic changes that are likely to have occurred would be well within the normal expectations for ape social behaviour and organization, and there is little evidence for any marked shifts in the direction of human sociality. Bipedalism, though, with its implications for both ranging and carrying (Foley & Elton 1998), is one of the building blocks for later adaptive changes.

7. TRANSITION 2: TOOLS AND MEAT The transition occurring around 2.0 Ma involves many traits changing, although the evidence is insufficient to determine a particular sequence or coevolutionary relationship. Many of these features are correlated in that they are all strongly associated with both later Homo and modern humans—larger brains, delayed and elongated life-history parameters and the use of technology as a part of behavioural adaptation. This more ‘human’ package is to some extent confirmed by the more modern body proportions, including a reduced gut (Aiello & Wheeler 1995). These are not fully modern humans—the brain size is around two-thirds of modern humans, the rate of maturation is more rapid and there is evidence that they were incapable of speech production. The period prior to 2.0 Ma is characterized by a continuation of the trend towards cooler and drier environments, and there is some suggestion that at this time there was an expansion of grasslands and grazing faunas (Bobe & Behrensmeyer 2004). It is a period of extensive evolutionary change across a range of mammals, with high levels of lineage diversity. However, while environmental change is important, it can also be argued that there was a more direct impact on hominin evolution driven by its own adaptive change. The two critical events are the development of more extensive meat-eating (as indicated by cut marks on bones and faunal assemblages in association with artefacts) and the use of tools. It is probable that, while earlier hominins made use of some level of technology, the use of a percussive technology, which produces strong cutting edges, provided a major advantage in terms of access to animal carcasses. Within a behavioural ecological model, the implications of this change would be a more reliable access to high-quality resources, especially during dry seasons, and a smoothing out of seasonal variation This change led to a greater availability of energy for mothers, and a relaxation of the constraints on the energetic costs of larger brains, especially when tied to a delayed life-history strategy (Foley & Lee 1991). It has also been argued that this may have involved

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3274

R. Foley & C. Gamble

Social transitions in human evolution

greater bonding between males and females, greater male investment in offspring as well as a divergence in male and female economic roles (Hill & Kaplan 1993). In sum, around two million years ago, Homo lived in communities in which the relationships between males and females and the reproductive tactics of each in terms of a more expensive offspring were changing. This change, we would argue, is directly related to greater access through technology to meat. That it was a significant change is suggested by the massive expansion of geographical range of hominins shortly after this time.

8. TRANSITION 3: FIRE, FAMILIES AND FOCUS The geographical range of Homo now ranged from the tropics to 558N, but across such ecological diversity, stone technology stayed remarkably constant and formed two major provinces. In China and southeast Asia, technology remained as mode 1 (Moore & Brumm 2007). By contrast, in India, southwest Asia, Europe and Africa, mode 2 bifaces came to dominate, although mode 1 was still common. These bifaces now displayed greater symmetry and precision in knapping skills than the earlier examples. This is the classic Acheulean that continues in Europe to at least 300 ka. It is in this second province that we can track this transition, while in the former, stasis and conservatism occur. Hominins followed familiar environmental conditions to achieve a northern distribution. At the eastern English site of Pakefield (Parfitt et al. 2005), dating to 750 ka, soil carbonates indicate a Mediterranean environment. Major glaciations had not yet occurred, but even so the population ebbed and flowed into the northernmost parts of its range according to local ecological conditions. This suggests a constrained pattern of fission and fusion that was as yet unable to adapt to the seasonal shortages of higher latitudes by more fluid social arrangements. One possibility is that cooking, rather than stone technology, may have been the critical adaptive change at this point, especially as there may have been a link between the control of fire and the ability to survive in colder environments. It also radically changed hominin socioecology. Wrangham (Wrangham et al. 1999; Wrangham & Conklin-Brittain 2003; Boback et al. 2007; Wobber et al. 2008) has argued that cooking is essential as a means of making meat in larger quantities energetically viable within a time budget and that it also massively increases the digestibility of plant foods. The control of fire, evidence for which becomes stronger at the period, is essential for this, and would have had a major impact on interdependence of individuals, the spatial structure of social interactions and the roles of males and females in subsistence. The Jordan Valley site of Gesher-Benot-Ya’Aqov (Goren-Inbar et al. 2002, 2004; Madsen & Goren-Inbar 2004), dated to 780 ka, has evidence for small hearths in which nuts and seeds were processed as well as an advanced mode 2B stone technology. The critical question is how a change in ecological energetics through fire and cooking shaped Phil. Trans. R. Soc. B (2009)

social evolution. One possibility is that it placed a greater emphasis on bonding between individual males and females, which strengthened smaller family units within the larger community structure. Cooking, spatial patterns shaped by hearth structures and specialized roles by sex were factors that both changed male– female relationships and produced the nested social structures that characterize humans (i.e. family units embedded within larger kin-based communities). Indirect evidence for this type of change may be provided by the very marked increase in the symmetry and quality of mode 2B Acheulean bifaces. The knapping skills indicate not only novel cognitive skills (Wynn 1988) when compared with mode 1 or mode 2A (and now demonstrated by neuroimaging; Stout & Chaminade 2007), but also the human skill of focused attention. The ability to focus attention so single-mindedly on the making of an object, and its constant repetition across three continents and many millennia, is testament to a high level of attention in practical operations. However, it may also allow us to infer the coevolutionary development of close male – female bonding at this time supported by a similar focused attention, most commonly expressed psychologically as our propensity for infatuation, the love-struck gaze. But this Acheulean gaze was not the only derived human trait that appeared at this time. Using the correlation between brain and community size, Dunbar (2003) has proposed that hominins in this period possessed a theory of mind and accompanying orders of intentionality. Gamble (2009) has argued for the importance of behaviours that amplified the strength and persistence of social bonds in such an advanced hominin cognition. These would include social laughter and crying as well as other mood enhancers such as collective dance and music.

9. TRANSITION 4: SOCIAL BRAINS AND TECHNOLOGIES At around 300 ka, there is a further change in technology, the abandonment of the hand-axe, which was a consistent part of Afro – Eurasian populations for a considerable period of time, and the elaboration of a lithic technology based on prepared core technology (mode 3). There are a number of significant aspects of this technology; first, it can be argued that it involves a considerable level of planning in its production, suggesting greater cognitive competence. Second, it is a means of mass production of flakes and blades of a predictable shape. And third, it is the basis for a projectile technology. Its appearance is poorly understood, and some argue that it arose several times and was prefigured in the Acheulean giant core/flake technology (McNabb et al. 2004). However, it broadly correlates with the evolution of two large-brained hominin lineages (Neanderthals and modern humans) and an acceleration in the rate of encephalization. It is during this period that hominin brain size becomes equivalent to that found in living humans, and on occasion exceeds it.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Social transitions in human evolution There is little doubt that both Neanderthals and modern humans are significantly different from other hominins. Indeed, despite the many arguments about how they differ from each other, what they share is far more striking when compared with any other hominin. Both for tens of thousands of years had a basic mode 3 Middle Stone Age/Palaeolithic technology, with the emergence of distinctive regional traits. They had similar but not identical life-history schedules; both probably had speech and language (MacLarnon & Hewitt 1999), and the capacity for considerable cultural variation. The ecological basis for this proposed transition is that effective and relatively replicable projectiles provided access to medium-sized ungulates, at a time when other more easily obtainable prey were declining (possibly in response to human pressure; Stiner et al. 2000). Well-fashioned wooden spears were used to hunt herds of horses at the German site of Scho¨ningen, dating to 400 ka (Thieme 2005). These are associated with several lakeside hearths. It is possible that during this period, prior to the evolution of modern humans in Africa, these archaic hominins were undergoing major changes in two aspects of their social life. The first is that there was a greater degree of demographic packing, with populations now competing more severely for space and resources. The greater regionality of the archaeological record may suggest this is taking place, with material culture at least one line of evidence for stronger signals of community affiliation. In other words, this period sees a much greater emphasis on groups as units. This may have been the critical pre-condition for the evolution of cultural capacities that would enforce social norms more effectively, and which set the basis for modern humans with their broader cultural repertoire. It may also be the case that at this point, with an emphasis on group affiliation, the importance of strong clan/lineage-based kinship systems became a major adaptive facet of their social life. Furthermore, such strong affiliation might also indicate the existence of hostile relationships between groups. Some support for this local group model of later Middle Pleistocene hominins comes from the evidence for small effective population sizes (based on palaeogenetics and modern genetics) for both Neanderthals and modern humans—in other words, a highly structured population. The second impact is the explosion of the scale of fission – fusion in response to these ecological changes. It is generally accepted (table 1) that fission –fusion is an important element of chimpanzee social organization and that it may have been enhanced among the earlier hominins (transition 1). However, among modern humans, fission – fusion occurs at a different order of magnitude. Individuals, families, bands, etc. can split up for very long periods of time, and disperse over large distances, while still maintaining a common social network. The ecology and demographic structure at the time of this transition may have been the spur to this exploded form of fission – fusion. Projectiles and the exploitation of mid-sized ungulates, for example, imply more seasonally variable foraging patterns and might correlate with greater Phil. Trans. R. Soc. B (2009)

R. Foley & C. Gamble

3275

fission – fusion. A further indication of a significant change in ranging patterns comes from the evidence that lithic raw materials were extracted and transported over greater distances than before. It is during this period that almost 30 per cent of hominin encephalization occurred (figure 2a). This has been related to an increase in community size, but it may also have been selected for by the greater cognitive demand of maintaining social relationships over distance and time.

10. TRANSITION 5: ECOLOGICAL INTENSIFICATION Three features stand out in this transition. First, there is the appearance of our current anatomical and genetic characteristics in Africa (Stringer & Andrews 1988; Noonan et al. 2006). Second, there is the global dispersal of these characteristics allied, in many cases with a novel technology, to the previously uninhabited 75 per cent of the globe. This occurs late, beginning with the sea crossing to Australia some 60 ka ago. It concludes with the settlement of remote Polynesia within the last millennium. Third, there is the rapid increase in population numbers following the retreat of the last glaciation that began some 16 ka ago (Lowe et al. 2008). In transition 3 nested complexity arose within groups and in transition 4 the spatial and temporal extension of that pattern was associated with greater fission – fusion. Now further change resulted from the emergence of intergroup complexity based initially on a more energy-rich ecology. This involved the use of aquatic and smaller animal resources, the exploitation of which was made possible by specialized technologies (modes 4 and 5) and domestic units of production. During the course of this transition (after 30 ka), it also becomes clear that human populations were able to exist at much higher densities and to intensify their foraging strategies of seedharvesting, cereal agriculture and animal domestication. The evidence for complexity in intergroup relationships takes several forms. A rise in the quantity and diversity of cultural forms, including composite tools, art and architecture, is matched by widespread distributions of distinctive cultural markers that signal group affiliation at a large geographical scale. Mobility ceases to be the key foraging tactic as more long-lived settlements occur in response to greater demographic packing. Territorial markers appear in the form of cemeteries and defended settlements, while extensive networks of exchange are now found through which items such as shell, obsidian, amber and other localized resources are channelled. At this point, a fundamental shift that goes beyond the normal range of the socioecological model occurred. Technological dependence, spatially restricted and controlled staples such as domesticates, defended flocks, fields and stores, opened the possibility for greater male control over access to resources at local, regional and inter-regional scales. If we take it as axiomatic to the model that female reproduction is dependent upon access to resources, and males by access to females,

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3276

R. Foley & C. Gamble

Social transitions in human evolution

Table 3. Summary of the ecological basis for, and social consequence of, the five transitions in hominin evolution discussed in the text. key structural shifts in human social evolution

hominin taxon with derived social behaviour

transition

time

ecological change

social implications

T1 (bipedalism, range size and fission fusion)

6–4 Ma

terrestriality and longer ranging distances

more dispersed social communities and greater fission and fusion

fission –fusion

australopithecines

T2 (tools and meat)

2.6–1.6 Ma

greater access to animal resources (technology); more reliable food supply; smoothing of seasonal variation

more prolonged male –female bonding

male– female relationships

early Homo

T3 (fire, families and focus)

800– 700 ka

more energy-richfood sources through cooking and technology

more stable male – female bonds; establishment of nested units within community structure (family units)

nested hierarchical community structures

H. heidelbergensis

T4 (social brains and technologies (projectiles))

400 –300 ka

more reliable food resources across greater range of environments (projectiles); greater demographic packing

greater fission – fusion and development of stable social life at a distance greater regional differentiation of communities and beginnings of structures beyond the level of the community

exploded fission – fusion and supracommunity structures

Homo helmei, H. neanderthalensis, H. sapiens

T5 (ecological intensification)

200– 10 ka

energy-rich ecology through aquatic resources, cereal harvesting, hunting and domestication of animals.

intergroup and regional social structures and networks male control of resources and thus of female distribution

regional social systems and networks social structure dominated by resource ownership, defence and control

H. sapiens

then the open-ended model becomes closed when males themselves control the resources. Complex social structures that interweave marriage patterns and resources, which characterize all human societies, represent an entirely novel socioecology that is uniquely human. Transition 5 is classically the origins of H. sapiens and modern human behaviour. Recent contributions to this topic have tended to focus on such a transition being relatively chronologically constrained. In contrast, we would argue here that it is a prolonged and cumulative transition, stretching from the biological changes over 150 ka to the emergence of a fully sedentary, agricultural and ethnically complex world in the last 15 ka (table 3 and figure 5). Phil. Trans. R. Soc. B (2009)

11. EVOLUTION OF HUMAN SOCIETY: TRENDS AND PRINCIPLES All too often, the reconstruction in both popular and scientific accounts of how human social behaviour evolved is mere speculation. This unsatisfying situation arises when the archaeological and fossil data that exist to test competing hypotheses are ignored and mishandled. Our strategy in this paper has been to maximize the points at which reconstruction articulates with archaeological and paleobiological data, thereby ensuring consistency with general principles drawn from neo-behavioural ecology. There is much to learn still, but some general points can be made. One such point is that if the ‘community’,

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Social transitions in human evolution

R. Foley & C. Gamble

3277

supracommunity structures – regional social networks – regulated intercommunity interactions the ‘community as the fundamental unit of basal hominin social organization (cf. chimpanzee community, with multi-male/multi-female structure, male kin-bonded, and limited fission–fusion)

T4/T5

T1

the hominin community – larger ranges – more extensive fission–fusion T2/T3 infragroup structures – nested units – male–female bonding – families – lineages, clans and – exploded fission–fusion

Figure 5. The community is the fundamental hominin and African hominoid social unit, and during the course of hominin evolution, it has been elaborated by increased fissioning and fusion (transition 1 and later transitions), greater infracommunity structure (transitions 2 and 3) and greater supracommunity networks and associations (transitions 4 and 5). See text for discussion.

in the sense used to describe both chimpanzee groups and human social units (Foley & Lahr 2001), was present from the last common ancestor to the emergence of modern humans, the key development is the addition of social structures both below—families and descent groups—and above—shared political systems, segmentary lineage systems and trade networks. The community, however, remains the core and the basis for elaboration. A second point is that across the course of human evolution, one of the strongest trends is that human ‘society’ has evolved to cope with more and more ‘fissioning’. If the community is one of the most basic building blocks of human society—a group with shared dialects, kin bonds and political organization—then it is clear that humans have the capacity to maintain these in the absence of close social proximity, and with long periods where there is no contact. The social and cognitive apparatus that has evolved provides the mechanisms for this. However, from a socioecological perspective, the fissioning potential (which may become permanent as groups do diverge and form new ones) provides ecological flexibility to human communities and to individuals pursuing their reproductive and other goals. Human society is essentially a chimpanzee community with exploded fission – fusion; a society that has achieved release from the constraints of proximity (Rodseth et al. 1991) that dominate the negotiation and often daily affirmation of social bonds and hierarchies among primates. Social extension in time and space was not achieved by all hominins. It appeared late in human evolution, as indicated by overwater dispersal to Australia and then throughout Polynesia as well as Phil. Trans. R. Soc. B (2009)

coping in the extreme continental environments of boreal Siberia with longer periods of fission, and very low population densities owing to highly seasonal resources. A third important implication is that kinship runs like a thread through the course of human evolution, from the beginnings of the last common ancestor through to the present day. The maintenance of kinship through several generations (descent groups) is both a truly unique development and also fundamental to the way in which communities both hold together and ultimately divide. This may be as recent as the global dispersal 60 ka ago (Gamble 2008). The complexities of other kinship systems are probably superimposed on top of this, but lineage systems have the power to enhance the deployment of larger groups of individuals for both economic and military advantage. This provides expandability to human society, and is likely to have been essential to the process of global colonization. The fourth general point relates to the role of the environment. Most of the major changes of human behavioural evolution coincide with climatic and environmental changes (although there are other phases of climatic change with no such evolutionary response). However, some of the changes that occurred also involved the consequences of more endogenous elements of the hominins themselves— including technology, fire and cultural mechanisms for maintaining larger groups. In this sense, there is a strong feedback element in the links between ecological and social factors in hominin evolution, which helps to account for the rapid acceleration in social change in the last 60 ka.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3278

R. Foley & C. Gamble

Social transitions in human evolution

Finally, the specific aspects of human social evolution may change the principles of socioecology, and thus in turn help produce a different type of evolution. It is generally accepted that female reproductive success is more closely tied to access to resources, and in that sense, female distribution in relation to resources plays the fundamental role in shaping social systems and strategies. Males, more constrained by access to females, adapt to the distribution of those females. However, over the course of human evolution, it is probably the case that male behaviour has meant that males have had increasing control over resources and have defended such resources extensively. This is particularly the case with animal domesticates, and lies at the heart of most pastoralist societies, for example. This means that females have increasingly had to adapt to a distribution of resources that is itself controlled by males—closing the socioecological loop. The consequences of this for human society, social behaviour and cultural practice, have probably been very marked.

REFERENCES Aiello, L. C. & Wheeler, P. 1995 The expensive tissue hypothesis. Curr. Anthropol. 36, 199–222. (doi:10.1086/204350) Allen, E. E. 1976 Against sociobiology. New York Review of Books, 182. Atkinson, Q. D., Gray, R. D. & Drummond, A. J. 2008 mtDNA variation predicts population size in humans and reveals a major southern Asian chapter in human prehistory. Mol. Biol. Evol. 25, 468–474. (doi:10.1093/molbev/msm277) Boback, S. M., Cox, C. L., Ott, B. D., Carmody, R., Wrangham, R. W. & Secor, S. M. 2007 Cooking and grinding reduces the cost of meat digestion. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 148, 651–656. (doi:10. 1016/j.cbpa.2007.08.014) Bobe, R. & Behrensmeyer, A. K. 2004 The expansion of grassland ecosystems in Africa in relation to mammalian evolution and the origin of the genus Homo. Palaeogeogr. Palaeoclimatol. Palaeoecol. 207, 399 –420. (doi:10.1016/ S0031-0182(04)00049-5) Brunet, M. et al. 2002 A new hominid from the Upper Miocene of Chad, central Africa. Nature 418, 145 –151. (doi:10.1038/nature00879) Charnov, E. & Berigan, D. 1993 Why do female primates have such long lifespans and so few babies? or life in the slow lane. Evol. Anthropol. 1, 191 –194. (doi:10.1002/ evan.1360010604) Charpentier, M. J. E., Van Horn, R. C., Altmann, J. & Alberts, S. C. 2008 Paternal effects on offspring fitness in a multimale primate society. Proc. Natl Acad. Sci. USA 105, 1988–1992. (doi:10.1073/pnas.0711219105) Clutton-Brock, T. H. 1991 The evolution of parental care. Princeton: Princeton University Press. Couzin, I. D. 2006 Behavioral ecology: Social organization in fission – fusion societies. Curr. Biol. 16, R633 –R635. (doi:10.1016/j.cub.2006.02.042) Crook, J. H. 1970 The socio-ecology of primates. In Social behaviour in birds and mammals (ed. J. H. Crook). London, UK: Academic Press. Davies, N. B. 1991 Mating systems. Behavioural ecology. An evolutionary approach (ed. J. R. Krebs & N. B. Davies), 3rd edn, pp. 263–294. London, UK: Blackwell Scientific Publications. d’errico, F. et al. 2003 Archaeological evidence for the emergence of language, symbolism, and music—an alternative Phil. Trans. R. Soc. B (2009)

multidisciplinary perspective. J. World Prehist. 17, 1 –70. (doi:10.1023/A:1023980201043) Dunbar, R. I. M. 2003 The social brain: mind, language, and society in evolutionary perspective. Annu. Rev. Anthropol. 32, 163–181. (doi:10.1146/annurev.anthro. 32.061002.093158) Fleagle, J. 1999 Primate adaptations and evolution. London, UK: Academic Press. Foley, R. A. 1989 The evolution of hominid social behaviour. In Comparative socioecology: the behavioural ecology of humans and other mammals (eds V. Standen & R. A. Foley), pp. 474 –493. Oxford, UK: Blackwells Scientific Publications. Foley, R. A. 2001 Evolutionary perspectives on the origins of human social institutions. Proc. Br. Acad. 110, 171–195. Foley, R. A. 2005 The emergence of culture in the context of hominin evolutionary patterns. In Evolution and culture (eds S. Levinson & P. Jaisson), pp. 53–78. Boston, MA: MIT Press. Foley, R. & Elton, S. 1998 Time and energy: the ecological context for the evolution of bipedalism. In Primate locomotion: recent advances (eds E. Strasser, J. Fleagle, A. Rosenberger & H. Mchenry), pp. 419–434. New York, NY: Plenum Press. Foley, R. A. & Lahr, M. M. 1997 Mode 3 technologies and the evolution of modern humans. Camb. Archaeol. J. 7, 3 –36. (doi:10.1017/S0959774300001451) Foley, R. A. & Lahr, M. M. 2001 The anthropological, demographic and ecological context of human evolutionary genetics. In Genes, fossils and behaviour: an integrated approach to modern human origins. (eds P. Donnelly & R. A. Foley), pp. 223–245. Omaha, NE: IOS Press. Foley, R. A. & Lee, P. C. 1991 Ecology and energetics of encephalization in hominid evolution. Phil. Trans. R. Soc. Lond. B 334, 223 –232. (doi:10.1098/rstb. 1991.0111) Gamble, C. 1993 Timewalkers. London, UK: Allen Lane. Gamble, C. S. 2008 Kinship and material culture: archaeological implications of the human global diaspora. In Kinship and evolution (eds N. J. Allen, H. Callan, R. Dunbar & W. James), pp. 27– 40. Oxford, UK: Blackwell. Gamble, C. 2009 Technologies of separation and the evolution of social extension. In Social brain and distributed mind (eds R. Dunbar, C. Gamble & J. A. J. Gowlett), pp. 17–42. Oxford, UK: Proceedings of the British Academy 158. Ghiglieri, M. P. 1987 Sociobiology of the great apes and the hominid ancestor. J. Hum. Evol. 16, 319–357. (doi:10. 1016/0047-2484(87)90065-0) Goren-Inbar, N., Sharon, G., Melamed, Y. & Kislev, M. E. 2002 Nuts, nut cracking, and pitted stones at Gesher Benot Ya’aqov, Israel. Proc. Natl Acad. Sci. USA 99, 2455– 2460. (doi:10.1073/pnas.032570499) Goren-Inbar, N., Alperson, N., Kislev, M. E., Simchoni, O., Melamed, Y., Ben-Nun, A. & Werker, E. 2004 Evidence of hominin control of fire at Gesher Benot Ya’aqov, Israel. Science 304, 725 –727. (doi:10.1126/science. 1095443) Hill, K. & Kaplan, H. 1993 On why male foragers hunt and share food. Curr. Anthropol. 34, 701–710. Hinde, R. A. 1983 In Primate social relationships: an integrated approach. Oxford: Blackwell Scientific Publications. Janson, C. H. & Goldsmith, M. L. 1995 Predicting group size in primates: foraging costs and predation risks. Behav. Ecol. 6, 326 –336. (doi:10.1093/beheco/6.3.326) Krebs, J. & Davies, N. B. 1984 Behavioural ecology. Oxford, UK: Blackwell. Kummer, H. 1968 Social organization of the hamadryas baboon. Chicago, IL: University of Chicago Press.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Social transitions in human evolution Leakey, M. G., Feibel, C. S., Mcdougall, I., Ward, C. & Walker, A. 1998 New specimens and confirmation of an early ape for Australopithecus anamensis. Nature 393, 62– 66. (doi:10.1038/29972) Lowe, J. J., Rasmussen, S. O., Bjo¨rck, S., Hoek, W. Z., Steffensen, J. P., Walker, M. J. C. & Yu, Z. C. 2008 Synchronisation of palaeoenvironmental events in the North Atlantic region during the Last Termination: a revised protocol recommended by the intimate group. Q. Sci. Rev. 27, 6 –17. (doi:10.1016/j.quascirev.2007.09.016) Lowen, C. & Dunbar, R. I. M. 1994 Territory size and defendability in primates. Behav. Ecol. Sociobiol. 35, 347 –354. (doi:10.1007/BF00184423) Maclarnon, A. M. & Hewitt, G. P. 1999 The evolution of human speech: the role of enhanced breathing control. Am. J. Phys. Anthropol. 109, 341– 363. (doi:10.1002/ (SICI)1096-8644(199907)109:3,341::AID-AJPA5.3.0. CO;2-2) Madsen, B. & Goren-Inbar, N. 2004 Acheulian giant core technology and beyond: an archaeological and experimental case study. Eurasian Prehist. 2, 3– 52. Marean, C. W. et al. 2007 Early human use of marine resources and pigment in South Africa during the Middle Pleistocene. Nature 449, 905 –908. (doi:10. 1038/nature06204) Mcnabb, J., Binyon, F. & Hazelwood, L. 2004 The large cutting tools from the South African Acheulean and the question of social traditions. Curr. Anthropol. 45, 653 –677. (doi:10.1086/423973) Mock, D. W. & Fujioka, M. 1990 Monogamy and long-term bonding in vertebrates. Trends Ecol. Evol. 5, 39–43. (doi:10.1016/0169-5347(90)90045-F) Moore, M. W. & Brumm, A. 2007 Stone artifacts and hominins in island southeast Asia: new insights from Flores, Eastern Indonesia. J. Hum. Evol. 52, 85– 102. (doi:10. 1016/j.jhevol.2006.08.002) Noonan, J. P. et al. 2006 Sequencing and analysis of Neanderthal genomic DNA. Science 314, 1113–1118. (doi:10.1126/science.1131412) Parfitt, S. et al. 2005 The earliest record of human activity in northern Europe. Nature 438, 1008–1012. (doi:10.1038/ nature04227) Prat, S. et al. 2005 First occurrence of early Homo in the Nachukui formation (West Turkana, Kenya) at 2.3 –2.4 Myr. J. Hum. Evol. 49, 230 –240. (doi:10.1016/ j.jhevol.2005.03.009) Rodseth, L., Wrangham, R. W., Harrigan, A. & Smuts, B. B. 1991 The human community as a primate society. Curr. Anthropol. 32, 221–254. (doi:10.1086/203952) Runciman, W. G., Maynard Smith, J. & Dunbar, R. I. M. (eds) 1996 Evolution of social behaviour patterns in primates and man. London, UK: British Academy. Sayers, K. & Lovejoy, C. O. 2008 The chimpanzee has no clothes: a critical examination of Pan troglodytes in models of human evolution. Curr. Anthropol. 49, 87–99. (doi:10.1086/523675) Smith, B. H. 1994 Patterns of dental development in Homo, Australopithecus, Pan, and Gorilla. Am. J. Phys. Anthropol. 94, 307–325. (doi:10.1002/ajpa.1330940303)

Phil. Trans. R. Soc. B (2009)

R. Foley & C. Gamble

3279

Stiner, M. C., Munro, N. D., Surovell, T. A., Tchernov, E. & Bar-Yosef, O. 2000 Paleolithic population growth pulses evidenced by small animal exploitation. Science 283, 190–194. Stout, D. & Chaminade, T. 2007 The evolutionary neuroscience of tool making. Neuropsychologia 45, 1091–1100. (doi:10.1016/j.neuropsychologia.2006.09.014) Stringer, C. 2002 Modern human origins: progress and prospects. Phil. Trans. R. Soc. Lond. B 357, 563– 579. (doi:10.1098/rstb.2001.1057) Stringer, C. & Andrews, P. 1988 Genetic and fossil evidence for the origin of modern humans. Science 239, 1263–1268. (doi:10.1126/science.3125610) Stringer, C. B. & Hublin, J. J. 1999 New age estimates for the Swanscombe hominid, and their significance for human evolution. J. Hum. Evol. 37, 873– 877. (doi:10. 1006/jhev.1999.0367) Thieme, H. 2005 The Lower Palaeolithic art of hunting: the case of Scho¨ningen 13 II-4, Lower Saxony, Germany. In The individual hominid in context: archaeological investigations of Lower and Middle Palaeolithic landscapes, locales and artefacts (eds C. Gamble & M. Porr), pp. 115 –132. London, UK: Routledge. Trivers, R. 1985 Social evolution. Menlo Park, CA: The Benjamin/Cummings Publishing Company, Inc. Van Schaik, C. P. & Ho¨rstermann, M. 1994 Predation risk and the number of adult males in a primate group: a comparative test. Behav. Ecol. Sociobiol. 35, 261– 272. (doi:10.1007/BF00170707) Vos, M. & Velicer, G. J. 2006 Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale. Appl. Environ. Microbiol. 72, 3615–3625. (doi:10. 1128/AEM.72.5.3615-3625.2006) Walker, A. C. & Leakey, R. E. (eds) 1993 The Nariokotome skeleton. Cambridge, UK: Harvard University Press. Wilson, E. O. 1975 Sociobiology: the new synthesis. Cambridge, MA: Harvard University Press. Wobber, V., Hare, B. & Wrangham, R. 2008 Great apes prefer cooked food. J. Hum. Evol. 55, 340– 348. (doi:10.1016/j.jhevol.2008.03.003) Wrangham, R. W. 1980 An ecological model of female bonded primate groups. Behaviour 75, 262– 300. (doi:10.1163/156853980X00447) Wrangham, R. W. 1987 The significance of African apes for reconstructing human social evolution. In The evolution of human behaviour: primate models (ed. W. G. Kinzey), pp. 51–71. Albany, NY: University of New York Press. Wrangham, R. & Conklin-Brittain, N. 2003 Cooking as a biological trait. Comp. Biochem. Physiol. A Molec. Integr. Physiol. 136, 35–46. (doi:10.1016/S1095-6433(03) 00020-5) Wrangham, R. W., Jones, J. H., Laden, G., Pilbeam, D. & Conklin-Brittain, N. 1999 The raw and the stolen— cooking and the ecology of human origins. Curr. Anthropol. 40, 567– 594. (doi:10.1086/300083) Wynn, T. 1988 Tools and the evolution of human intelligence. In Machiavellian intelligence (eds R. Byrne & A. Whiten), pp. 271–284. Oxford, UK: Clarendon Press.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3281–3288 doi:10.1098/rstb.2009.0134

Review

Culture and the evolution of human cooperation Robert Boyd1,* and Peter J. Richerson2 1

Department of Anthropology, University of California, Los Angeles, CA 90095, USA School of Environmental Science and Policy, University of California, Davis, CA 95616, USA

2

The scale of human cooperation is an evolutionary puzzle. All of the available evidence suggests that the societies of our Pliocene ancestors were like those of other social primates, and this means that human psychology has changed in ways that support larger, more cooperative societies that characterize modern humans. In this paper, we argue that cultural adaptation is a key factor in these changes. Over the last million years or so, people evolved the ability to learn from each other, creating the possibility of cumulative, cultural evolution. Rapid cultural adaptation also leads to persistent differences between local social groups, and then competition between groups leads to the spread of behaviours that enhance their competitive ability. Then, in such culturally evolved cooperative social environments, natural selection within groups favoured genes that gave rise to new, more pro-social motives. Moral systems enforced by systems of sanctions and rewards increased the reproductive success of individuals who functioned well in such environments, and this in turn led to the evolution of other regarding motives like empathy and social emotions like shame. Keywords: cooperation; culture; coevolution

1. INTRODUCTION Humans cooperate on a larger scale than most other mammals. Among social mammals, cooperation is mainly limited to relatives. There is little division of labour, no trade and no large scale conflict. Communication is limited to a small repertoire of self-verifying signals. The sick and disabled must fend for themselves. The strong take from the weak without fear of sanctions by third parties. Amend Hobbes to account for nepotism, and his picture of society is not so far off for most other species. In stark contrast, even in foraging societies people regularly cooperate with many unrelated individuals. Division of labour, trade and large scale conflict are prominent features of most known human societies. Human language allows low-cost, generally honest communication of virtually unlimited complexity. The sick and disabled are often cared for, and social life is regulated by shared moral systems that specify the rights and duties of individuals enforced, albeit imperfectly, by third party sanctions. The scale of human cooperation is an evolutionary puzzle. All of the available evidence suggests that the societies of our Pliocene ancestors were like those of other social primates (Foley & Gamble 2009). Sometime during the last two million years, important changes occurred in human psychology that support larger, more cooperative societies. Given the magnitude and complexity of the changes, the most

plausible hypothesis is that they were the product of natural selection. However, the limited cooperation seen in other mammals fits more comfortably within the received theory of evolution than does human large-scale cooperation among non-kin. Something makes our species different, and in this paper we argue that something is cultural adaptation. This hypothesis rests on three claims:

* Author for correspondence ([email protected]). One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

3281

(i) Over the last million years or so, people evolved the ability to learn from each other, creating the possibility of cumulative, non-genetic evolution. These capacities were favoured by ordinary natural selection in the rapidly varying climates of the Middle and Upper Pleistocene, because cumulative cultural evolution allows humans to culturally evolve highly refined adaptations to local environments relatively quickly compared with genetic evolution. (ii) Rapid cultural adaptation also vastly increased heritable variation between groups. Systems of reciprocity and reputation can stabilize a vast range of behaviours ranging from ruthless spite to prosocial cooperation. Rapid cultural adaptation can then lead to persistent differences between local social groups, and then competition between groups leads to the spread of behaviours that enhance the competitive ability of groups. (iii) Then, in such culturally evolved cooperative social environments, social selection within groups favoured genes that gave rise to new, more pro-social motives. Moral systems enforced by systems of sanctions and rewards This journal is # 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3282

R. Boyd & P. J. Richerson

Review. Culture and human cooperation

increased the reproductive success of individuals who functioned well in such environments, and this in turn led to the evolution of other regarding motives like empathy and social emotions like shame. In the remainder of this paper, we explain the logic behind each of these claims, and sketch the empirical evidence that supports them. 2. CULTURE ALLOWS RAPID LOCAL ADAPTATION ‘Now, if some one man in a tribe, more sagacious than the others, invented a new snare or weapon, or other means of attack or defense, the plainest self-interest, without the assistance of much reasoning power, would prompt the other members to imitate him; and all would thus profit.’ (Charles Darwin, The Descent of Man 1871, p. 155)

The human species occupies a wider range of habitats, uses a much greater range of resources, and lives in more diverse social systems than any other animal species. We constitute a veritable adaptive radiation, albeit one without any true speciation. For better or worse, our ability to convert matter and energy into people in almost every terrestrial habitat has made us the Earth’s dominant species. Most accounts of human evolution explain our ecological success as the result of superior cognitive abilities (e.g. Tooby & DeVore 1987). While it is probable that individual humans are smarter than other animals, we do not think this is the most important cause of our success. Think about what people have to know to survive and prosper in just one habitat where human foragers have flourished, the North American Arctic. They have to know how to make dozens of essential tools—kayaks, warm clothing, toggle harpoons, oil lamps, shelters built of skin and snow, goggles to prevent snow blindness, dog sleds and the tools to make these tools. They also have to know how to use all of this stuff, where and when to hunt and gather, what to seek, how to process it if you succeed, and so on and on. Then they have to decide how to organize their society: how to regulate exchange of resources, how to organize marriage, resolve conflicts and so on and on. If individual intelligence were the key, individuals could create all of this knowledge on their own. While we are rather clever animals, we cannot do this because we are not close to clever enough. A kayak is a highly complex object with many different attributes. Designing a good one means finding one of the extremely rare combination of attributes that produces a useful boat. The number of combinations of attributes grows geometrically as the number of dimensions increases, rapidly exploding into an immense number. The problem would be much easier if we had a kayak module that constrained the problem, so we would have fewer choices to evaluate (Tooby & Cosmides 1992, pp. 104 – 108). However, environments are changing far too quickly and are far too variable spatially for selection to shape the psychologies of Arctic populations in this way. The same Phil. Trans. R. Soc. B (2009)

learning psychology has to do for all the other knowledge, institutions and technologies necessary to survive in the Arctic. It also has to do for birch bark canoes, reed rafts, dugout canoes, rabbit drives, blow-guns, hxaro exchange and the myriad marvellous, specialized, environment-specific technology, knowledge and social institutions that human foragers have culturally evolved. Our learning and inference mechanisms simply are not up to the task. Arctic foragers could make and do all the other things that they needed because they could make use of a vast pool of useful information available in the behaviour and teachings of other people in their population. The information contained in this pool is adaptive because combining even limited, imperfect learning mechanisms with cultural transmission can lead to relatively rapid, cumulative adaptation. Even if most individuals imitate most of the time, some people will attempt to improve on what they learned. Relatively small improvements are easier than large ones, so most successful innovations will lead to small changes. These modest attempts at improvement give behaviours a nudge in an adaptive direction, on average. Cultural transmission preserves the nudges, and exposes the modified traditions to another round of nudging. Very rapidly by the standards of evolution by natural selection, many small nudges generate new adaptations. Much theoretical work suggests that this qualitative picture of cumulative cultural adaptation is cogent (Boyd & Richerson 1996, see Richerson & Boyd 2005 for a review)—coupling learning and social transmission allows populations of humans to rapidly varying environments. Culture leverages individual creativity in just the way Darwin imagined. Scraps of individual insight and luck are spread widely to others, recombined with other scraps, and form the basis for additional innovations, all rather quickly. We have hypothesized (Richerson & Boyd 2005; Richerson et al. 2005) that the psychological capacities that allow humans to learn from others evolved during the Middle Pleistocene in response to increased rapid, high amplitude climate variation. Since the midMiocene Earth’s mean temperature has dropped several degrees and the amplitude of temperature fluctuations have greatly increased (Lamb 1977; Partridge et al. 1995; Bradley 1999; Cronin 1999). Higher resolution data indicate that the period of these fluctuations has decreased over the last 400 000 years or so, and that during the last two glacial periods substantial changes in world temperature have occurred over periods of a few decades. It seems plausible that the capacities that allow cultural adaptation would be strongly favoured in such a chaotic, rapidly changing world. 3. RAPID CULTURAL ADAPTATION POTENTIATES GROUP SELECTION ‘It must not be forgotten that although a high standard of morality gives but a slight or no advantage to each individual man and his children over the other men of the same tribe, yet that an increase in the number of well-endowed men and an advancement in the standard of morality will certainly give an immense

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Culture and human cooperation advantage to one tribe over another . . . At all times throughout the world tribes have supplanted other tribes; and as morality is one important element in their success, the standard of morality and the number of well-endowed men will thus everywhere tend to rise and increase.’ (Charles Darwin, The Descent of Man 1871, p. 159)

In this paper we use the word cooperation to mean costly behaviour performed by one individual that increases the payoff of others. Opportunities for cooperation are omnipresent in social life. Exchange and division of labour increase the efficiency of productive processes for all the reasons given by Adam Smith in The wealth of nations. However, in all but the simplest transactions, individuals experience a cost now in return for a benefit later and thus are vulnerable to defectors who take the benefit but do not produce the return. Imperfect monitoring or effort and quality also give rise to opportunities for free riding. The potential for conflict over land, food and other resources is everywhere. In such conflicts larger more cooperative groups defeat smaller less cooperative groups. However, each warrior’s sacrifice benefits everyone in the group whether or not they too went to war and thus defectors can reap the fruits of victory without risking their skins. Honest, low-cost communication provides many benefits—coordination is greatly facilitated, resources can be used more efficiently, hazards avoided; the list is long. However, once individuals come to rely on the signals of others, the door is open for liars, flim-flam artists and all the rest. Capital facilities like roads, fortifications and irrigation systems can provide huge benefits. However, the benefits often flow to everyone, whether or not they contributed to the construction. However, aside from humans, only a few other taxa, most notably social insects, make cooperation a cornerstone of their adaptation. Those that do are spectacular evolutionary successes. It has been estimated, for example, that termites account for half of the animal biomass in the tropics, and that human biomass exceeds that of all other terrestrial vertebrates combined. Nonetheless, cooperative behaviour does not usually evolve because it is vulnerable to exploitation. Even if everyone benefits by behaving cooperatively, selection usually favours individuals who take the benefits without paying the cost, and, as a result, the immense benefit that can be generated for everyone through cooperation remains untapped. (a) Reciprocity and reputation can explain the stability but not the evolution of larger scale cooperation While there is some controversy, the evolution of large scale cooperation in other species (Foster et al. 2005) seems to require kinship, perhaps supplemented by policing (Ratinieks & Wenseleers 2005). This explanation obviously does not work for large scale human cooperation among unrelated individuals. Instead, evolutionary thinkers typically explain human cooperation as the resulting from the ‘three Rs’: reputation, reciprocation and retribution (e.g. Trivers 1971; Alexander 1987; Haley & Fessler 2005; Phil. Trans. R. Soc. B (2009)

R. Boyd & P. J. Richerson

3283

Nowak & Sigmund 2005). If cheaters are despised by others in their group, and, as a consequence, suffer social costs—lose status, mating opportunities, the benefits of mutual aid when ill or injured—then they may be motivated to cooperate, even though prosocial motivations are entirely absent from their psychology. Of course, punishment may be costly, so we also need to explain why punishers are not replaced by second-order free riders who cooperate, but do not punish. However, there are by now several plausible solutions to this second order free rider problem (Henrich & Boyd 2001; Boyd et al. 2003; Panchanathan & Boyd 2004) and so it seems probable that the three Rs can explain why cooperation is evolutionarily stable. The problem is that the three Rs can stabilize any behaviour. If everybody agrees that individuals must do X, and punish those who do not do X, then X will be evolutionarily stable as long as the costs of being punished exceed the costs of doing X. It is irrelevant whether X benefits the group or is socially destructive. It will pay to do X. Thus, the three Rs can explain how cooperative behaviours like participating in group defense can be favoured by evolution, but they can also explain anything else. Since cooperative behaviours are a tiny subset of all possible behaviours, the three Rs do not explain why large-scale cooperation is so widely observed. In other words, the three Rs may sustain large-scale cooperation, but are not sufficient to explain why it evolves in the first place. As was first pointed out by Axelrod & Hamilton (1981), cooperation in very small groups can readily be explained by the combination of the three Rs and the weak kin selection created by low levels of background relatedness typically observed in social groups (e.g. Bowles 2006). However, all of the analysis done so far suggests that the same is not true of larger groups (Boyd & Richerson 1988, 1992; Gardner & West 2004; Panchanathan & Boyd 2004). Something has to be added to the model.

(b) Multiple equilibria plus rapid adaptation5stable variation among groups So what explains the evolution of large scale human cooperation? We believe that the most probable explanation is that rapid cultural adaptation greatly increased the amount of behavioural variation between groups. We have seen that repeated interactions can stabilize a vast range of alternative behaviours in different groups. A variety of other mechanisms also can lead to multiple stable equilibria (discussed in Boyd & Richerson in press). When this is the case, different groups may evolve to different equilibria—one set of practices gets higher reputational benefits in one group, a different set in another group, a third set in a third group and so on. Thus, the social environment varies from group to group, and as a result different behaviours will be favoured by selection or analogous cultural adaptive processes in different groups. Such disruptive selection increases behavioural variation among groups. This tendency will be opposed by the flow of genes or cultural variants between groups due to migration and other kinds of social contact. If local adaptation is rapid compared with mixing,

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3284

R. Boyd & P. J. Richerson

Review. Culture and human cooperation

the variation among groups will persist; if mixing is stronger, all groups will converge to a single genetic or cultural variant. The following simple model illustrates this idea. There are three independent evolving traits, each with two variants labelled 0 and 1. Each variant is evolutionarily stable when common, and thus there are eight stable equilibria (0,0,0),(1,0,0), . . . ,(1,1,1). The selection coefficient for each trait is s. The population is subdivided into 256 subpopulations dispersed in a two-dimensional space. Each subpopulation exchanges a fraction m of its members with its four nearest neighbours. Initial frequencies are assigned at random. In figure 1, the frequencies of the three variants in each subpopulation are represented by the RGB colours, so for example a population with the vector of frequencies (1,0,0) is 100 per cent red, 0 per cent green and blue. When mixing is stronger than local adaptation (m . s), evolution proceeds as if there were no groups and evolves toward which ever combination of variants is initially more common. When local adaptation is stronger, mixing and local adaptation balance leading to persistent variation among groups. Stronger local adaptation leads to variation on smaller spatial scales. Cultural adaptation is much more rapid than genetic adaptation. Indeed, if we are correct, this is the reason why we have culture—to allow different groups to accumulate different adaptations to a wide range of environments. Thus a shift from genetic adaptation to cultural adaptation should greatly increase the heritable behavioural variation among groups. In other primate species, there is little heritable variation among groups because natural selection is weak compared with migration. Although the strength of selection varies among traits, most selection is relatively weak, and selection coefficients are of the order of 1 per cent. Since one sex leaves at maturity in most primate species, and there are roughly two generations present in a group, migration rates are of the order of 25 per cent per generation. This is why group selection at the level of whole primate groups is not an important evolutionary force. In contrast, there is a great deal of behavioural variation among human groups. And this behavioural variation exists on a wide range of spatial scales. Even neighbouring groups may have very different culturally transmitted languages, marriage systems, and so on.

(c) Stable variation among groups leads to group selection In the Origin of species, Darwin famously argued that three conditions are necessary for adaptation by natural selection: first, there must be a ‘struggle for existence’ so that not all individuals survive and reproduce. Second, there must be variation so that some types are more likely to survive and reproduce than others, and finally, variation must be heritable so that the offspring of survivors resemble their parents. As the quote at the beginning of this section illustrates, Darwin thought that the same three postulates apply to groups as well as individuals. Only the first two conditions are satisfied by most other kinds of animal Phil. Trans. R. Soc. B (2009)

(a)

(b)

(c)

Figure 1. An equilibrium behaviour in a 16 16 array of populations linked by stepping stone migration on a torus is shown. There are three binary traits. Each combination of traits is evolutionarily stable when common, and all basins of attraction are the same. Populations are initialized at random. The vector of frequencies at evolutionary equilibrium is plotted as the RGB colour resulting from that mix of red, green and blue. (a) When migration rates are greater than or equal to selection coefficients (m s) all groups have the same behaviour at equilibrium. (b) When migration rates are somewhat less than to selection coefficients (2m ¼ s) simple clines often persist at evolutionary equilibrium. (c) When migration rates are much less than to selection coefficients (10m ¼ s) complex patterns of small scale variation often persist at evolutionary equilibrium.

groups. For example, vervet monkey groups compete with one another, and groups vary in their ability to survive and grow, but, and this is a big but, the causes of group-level variation in competitive ability are not heritable, so there is no cumulative adaptation. Once rapid cultural adaptation in human societies gave rise to stable, between-group differences, the stage was

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Culture and human cooperation set for a variety of selective processes to generate adaptations at the group level. Different human groups have different norms and values, and the cultural transmission of these traits can cause such differences to persist for long periods of time. The norms and values that predominate in a group plausibly affect the probability that the group survives, whether it is economically successful, whether it expands, and whether it is imitated by its neighbours. For example, suppose that groups with norms that promote patriotism are more likely to survive than groups lacking this sentiment. This creates a selective process that leads to the spread of patriotism. Of course, this process may be opposed by an evolved innate psychology that makes us more prone to imitate, remember and invent nepotistic beliefs than patriotic beliefs. The long run evolutionary outcome would then depend on the balance of these two processes. The simplest mechanism is intergroup competition. The spread of the Nuer at the expense of the Dinka in the nineteenth century Sudan provides a good example. During the nineteenth century each consisted of a number of politically independent groups (Kelly 1985). Cultural differences in norms between the two groups meant that the Nuer were able to cooperate in larger groups than the Dinka, and as a consequence defeated their Dinka neighbours, occupied their territories and assimilated tens of thousands of Dinka into their communities. This example illustrates the requirements for cultural group selection by intergroup competition. Contrary to some critics (Palmer et al. 1997), there is no need for groups to be strongly bounded, individual-like entities. The only requirement is that there are persistent cultural differences between groups, and these differences must affect the group’s competitive ability. Losing groups must be replaced by the winning groups. Interestingly, the losers do not have to be killed. The members of losing groups just have to disperse or to be assimilated into the victorious group. Losers will be socialized by conformity or punishment, so even very high rates of physical migration need not result in the erosion of cultural differences This kind of group selection can be a potent force even if groups are very large. Group competition is common in small scale societies. The best data come from New Guinea, which provides the only large sample of simple societies studied by professional anthropologists before they experienced major changes due to contact with Europeans. Joseph Soltis assembled data from the reports of early ethnographers in New Guinea (Soltis et al. 1995). Many studies report appreciable intergroup conflict and about half mention cases of social extinction of local groups. Five studies contained enough information to estimate the rates of extinction of neighbouring groups. The typical pattern is for groups to be weakened over a period of time by conflict with neighbours and finally to suffer a sharp defeat. When enough members become convinced of the group’s vulnerability to further attack, members take shelter with friends and relatives in other groups, and the group becomes socially extinct. At these rates of group extinction, it would take between 20 and Phil. Trans. R. Soc. B (2009)

R. Boyd & P. J. Richerson

3285

40 generations, or 500 to 1000 years, for an innovation to spread from one group to most of the other local groups by cultural group selection. This might seem slow, but the history of the rise of ever larger and more complex societies in the Holocene does have a millennial time scale. A propensity to imitate the successful can also lead to the spread of group beneficial variants. People often know about the norms that regulate behaviour in neighbouring groups. They know that we can marry our cousins here, but over there they cannot; or anyone is free to pick fruit here, while individuals own fruit trees there. Suppose different norms are common in neighbouring groups, and that one set of norms causes people to be more successful. Both theory and empirical evidence suggest that people have a strong tendency to imitate the successful (Henrich & Gil-White 2001; McElreath et al. 2008). Consequently, behaviours can spread from groups at high payoff equilibria to neighbouring groups at lower payoff equilibria because people imitate their more successful neighbours. A mathematical model suggests that this process will result in the spread of group beneficial beliefs over in a wide range of conditions (Boyd & Richerson 2002). The model also suggests that such spread can be rapid. Roughly speaking, it takes about twice as long for a group beneficial trait to spread from one group to another as it does for an individually beneficial trait to spread within a group. Selective migration is a third mechanism that can lead to the spread of some kinds of group beneficial traits. In the modern world streams of migrants flow between societies. The extensive literature on this topic (e.g. Borjas 1994; Alba & Nee 2003; Martin 2005) supports two generalizations: (i) that migrants flow from societies where immigrants find their prospects poor to ones where they perceive them to be better, and (ii) most immigrant populations assimilate to the host culture within a few generations. Ethnographic evidence suggests that selective immigration is not limited to complex modern societies, and thus is likely to be an ancient phenomenon (Knauft 1985; Cronk 2002). The spread of cultural institutions associated with ancient complex societies, such as China, Rome and India supports the idea that this process is not new. Ancient imperial systems often expanded militarily but the durable ones, such as Rome, succeeded by assimilating conquered peoples and by inducing a flow of migrants across their boundaries. Although the Roman Empire as a political entity eventually faded, its most attractive institutions were adapted by successor polities and persist in modified form to this day. Rome, India, China and Islamic civilization stand in stark contrast to pure conquest empires like that of the Mongols, which expanded but did not assimilate. A simple mathematical model of this process (Boyd & Richerson 2009) indicates that it has two qualitatively different evolutionary outcomes. The model assumes that there are two possible evolutionary equilibria in an isolated population, and one equilibrium leads to higher average welfare than the other. The population is subdivided into two subpopulations linked by migration. There is more migration from

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3286

R. Boyd & P. J. Richerson

Review. Culture and human cooperation

low payoff to high payoff subpopulations than the reverse. When local adaptation is strong enough compared with migration to maintain cultural variation among subpopulations, the population as a whole evolves toward a polymorphic equilibrium at which the variants that produce higher average welfare are more common, but the lower payoff variant also persists. Initial subpopulation size and the sizes of the basins of attraction play relatively minor roles. When migration is stronger, however, initial population sizes and sizes of the basins of attraction predominate. The variant that is common in the larger of the two populations tends to spread and the other variant tends to disappear even it yields a higher payoff.

(d) This argument is consistent with an evolved, genetically adaptive psychology The claim that cultural evolution can give rise to forms of novel cooperation is vulnerable to an obvious objection: Cultural evolution can lead to the spread of cooperation in large, weakly related groups only if computational and motivational systems existed in the human brain that allowed people to acquire and perform the requisite behaviours. Given that such behaviours were not favoured by natural selection, why should these systems exist? Like living primates, our ancestors were large brained mammals capable of flexibly responding to a range of biotic and social environments. Natural selection cannot equip such organisms with fixed action patterns; instead it endows them with a complex psychology that causes them to modify their behaviour adaptively in response to environmental cues (Tooby & Cosmides 1992). Cultural evolution can generate novel behaviours by manipulating these cues. For example, cooperation among relatives requires (among other things) a means of assessing costs and benefits, and of identifying relatives and assessing their degree of relatedness. Such systems can be manipulated by culturally transmitted input. Individuals have to learn the costs and benefits of different behaviours in their particular environment. Thus people who learn that sinners suffer an eternity of punishment may be more likely to behave morally than those who only fear the reprisals of their victims. Individuals have to learn who their relatives are in different environments. So the individual who learns that members of his patriclan are brothers may behave quite differently from one who learns that he owes loyalty to the band of brothers in his platoon. Once activated, such computational systems provide input to existing motivational systems which in turn generate behaviour. This account raises an obvious question: If cultural inputs regularly lead to what is, from the genes point of view, maladaptive behaviour, why has not selection modified our psychology so that it is immune to such maladaptive inputs. This is a crucial question, and we have dealt with it at length elsewhere (Richerson & Boyd 2005, ch. 5). In brief, we believe that cumulative cultural evolution creates a novel evolutionary tradeoff. Social learning allows human populations to accumulate adaptive information over many Phil. Trans. R. Soc. B (2009)

generations, leading to the cultural evolution of highly adaptive behaviours and technology. Because this process is much faster than genetic evolution, human populations can evolve cultural adaptations to local environments, an especially valuable adaptation to the chaotic, rapidly changing world of the Pleistocene. However, the same psychological mechanisms that create this benefit necessarily come with a built-in cost. To get the benefits of social learning, humans have to be credulous, for the most part accepting the ways that they observe in their society as sensible and proper, and such credulity opens up human minds to the spread of maladaptive beliefs. This cost can be shaved by tinkering with human psychology, but it cannot be eliminated without also losing the adaptive benefits of cumulative cultural evolution. Culture is a little like breathing. One could reduce the chances of respiratory infections by breathing less, but the costs of doing so would curtail other essential activities. One could learn less from other people in order to avoid getting bad ideas from them. In humans, the optimum in these tradeoffs has led to lots of breathing and lots of cultural transmission.

4. NATURAL SELECTION IN CULTURALLY EVOLVED SOCIAL ENVIRONMENTS MAY HAVE FAVOURED NEW TRIBAL SOCIAL INSTINCTS In regard to the moral qualities, some elimination of the worst dispositions is always in progress even in the most civilized nations. Malefactors are executed, or imprisoned for long periods, so that they cannot freely transmit their bad qualities. (Charles Darwin, The Descent of Man 1871, p. 166)

We hypothesize that this new social world, created by rapid cultural adaptation, led to the genetic evolution of new, derived social instincts. Cultural evolution created cooperative groups. Such environments favoured the evolution of a suite of new social instincts suited to life in such groups including a psychology which ‘expects’ life to be structured by moral norms, and that is designed to learn and internalize such norms. New emotions evolved, like shame and guilt, which increase the chance the norms are followed. Individuals lacking the new social instincts more often violated prevailing norms and experienced adverse selection. They might have suffered ostracism, been denied the benefits of public goods, or lost points in the mating game. Cooperation and group identification in inter-group conflict set up an arms race that drove social evolution to ever-greater extremes of in-group cooperation. Eventually, human populations came to resemble the hunter–gathering societies of the ethnographic record. We think that the evidence suggests that after about 100 000 years ago most people lived in tribal scale societies (Kelly 1995). These societies are based upon in-group cooperation where in-groups of a few hundred to a few thousand people are symbolically marked by language, ritual practices, dress and the like. These societies are egalitarian, and political power is diffuse. People are quite ready to punish others for transgressions of social norms, even when personal interests are not directly at stake.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Review. Culture and human cooperation These new tribal social instincts did not eliminate ancient ones favouring self, kin and friends. The tribal instincts that support identification and cooperation in large groups, are often at odds with selfishness, nepotism and face-to-face reciprocity. People feel deep loyalty to their kin and friends, but they are also moved by larger loyalties to clan, tribe, class, caste and nation. Inevitably, conflicts arise. Families are torn apart by civil war. Parents send their children to war (or not) with painfully mixed emotions. Criminal cabals arise to prey upon the public goods produced by larger scale institutions. Elites take advantage of key locations in the fabric of society to extract disproportionate private rewards for their work. The list is endless. Some of our colleagues in evolutionary psychology have complained to us that this story is too complicated. Wouldn’t it be simpler to assume that culture is shaped by a psychology adapted to small groups of relatives? Well, maybe. But the same people almost universally believe an equally complex co-evolutionary story about the evolution of an innate language acquisition device (Pinker 1994, pp. 111 – 112). Such innate language instincts must have coevolved with culturally transmitted languages in much the same way that we hypothesize that the social instincts coevolved with culturally transmitted social norms. Initially, languages must have been acquired using mechanisms not specifically adapted for language learning. This combination created a new and useful form of communication. Those individuals innately prepared to learn a little more proto-language, or learn it a little faster, would have a richer and more useful communication system than others not so well endowed. Then selection could favour still more specialized language instincts, which allowed still richer and more useful communication, and so on. We think that human social instincts constrain and bias the kind of societies that we construct, but the details are filled in by the local cultural input (Steward 1955; Kelly 1995). When cultural parameters are set, the combination of instincts and culture produces operational social institutions.

5. CONCLUSION The model described above gives a cogent Darwinian explanation for why human societies are so cooperative, and why human psychology seems to include prosocial motivations. The theory of cultural group selection is fairly well worked out, and there are a number of convincing examples of the process at work. We believe that work in this area can profit from two kinds of researches: first, there has been little systematic quantitative empirical work that allows an assessment of the relative importance of cultural group selection compared with other processes that shape cultural variation. We need quantitative empirical estimates of rates of group extinction, and of rates of spread of cultural variants due to differential imitation and differential migration. Quantitative estimates of cultural variation would also be useful. Second, this model predicts that societies should exhibit design at the group level, that we should be able to Phil. Trans. R. Soc. B (2009)

R. Boyd & P. J. Richerson

3287

understand the structure and variation of norms in terms of how they enhance group welfare. Of course there is a long tradition of functionalist explanation in the social sciences, but for the most part this work takes the form of group-level just so stories. What is needed are sharp, testable hypotheses about how group functional behaviours, especially group functional norms, should vary with ecology, group size, and other measurable variables.

REFERENCES Alba, R. & Nee, V. 2003 Remaking the American mainstream: assimilation and the new immigration. Cambridge, MA: Harvard University Press. Alexander, R. D. 1987 The biology of moral systems. New York, NY: Aldine de Gruyter. Axelrod, R. & Hamilton, W. D. 1981 The evolution of cooperation. Science 211, 1390 –1396. (doi:10.1126/ science.7466396) Borjas, G. J. 1994 The economics of immigration. J. Econ. Lit. 32, 1667–1717. Bowles, S. 2006 Group competition, reproductive leveling, and the evolution of human altruism. Science 314, 1569–1572. (doi:10.1126/science.1134829) Boyd, R. & Richerson, P. J. 1988 The evolution of reciprocity in sizable groups. J. Theor. Biol. 132, 337–356. (doi:10. 1016/S0022-5193(88)80219-4) Boyd, R. & Richerson, P. J. 1992 Punishment allows the evolution of cooperation (or anything else) in sizable groups. Ethol. Sociobiol. 13, 171 –195. (doi:10.1016/ 0162-3095(92)90032-Y) Boyd, R. & Richerson, P. J. 1996 Why culture is common, but cultural evolution is rare. Proc. Br. Acad. 88, 77–93. Boyd, R. & Richerson, P. J. 2002 Group beneficial norms spread rapidly in a structured population. J. Theor. Biol. 215, 287–296. (doi:10.1006/jtbi.2001.2515) Boyd, R. & Richerson, P. J. 2009 Voting with your feet: payoff biased migration and the evolution of group beneficial behavior. J. Theor. Biol. 257, 331–339. (doi:10. 1016/j.jtbi.2008.12.007) Boyd, R. & Richerson, P. J. In press. Transmission coupling mechanisms: cultural group selection. Phil. Trans. R. Soc. B. Boyd, R., Gintis, H., Bowles, S. & Richerson, P. J. 2003 The evolution of altruistic punishment. Proc. Natl Acad. Sci. USA 100, 3531– 3535. (doi:10.1073/pnas.0630443100) Bradley, R. S. 1999 Paleoclimatology: reconstructing climates of the quaternary, 2nd edn. San Diego, CA: Academic Press. Cronin, T. M. 1999 Principles of paleoclimatology. New York, NY: Columbia University Press. Cronk, L. 2002 From true Dorobo to Mukogodo Masai: contested ethnicity in Kenya. Ethnology 41, 27–49. Darwin, C. 1871 The descent of man and selection in relation to sex. London, UK: John Murray. Foley, R. & Gamble, C. 2009 The ecology of social transitions in human evolution. Phil. Trans. R. Soc. B 364, 3267–3279. (doi:10.1098/rstb.2009.0136) Foster, K. R., Wenseleers, T. & Ratnieks, F. L. 2005 Kin selection is the key to altruism. Trends Ecol. Syst. 21, 57–60. (doi:10.1016/j.tree.2005.11.020) Gardner, A. & West, S. 2004 Cooperation and punishment, especially in humans. Am. Nat. 164, 753–764. Ghiselin, M. T. 1974 The economy of nature and the evolution of sex. Berkeley, CA: University of California Press. Haley, K. & Fessler, D. 2005 Nobody’s watching? Subtle cues affect generosity in an anonymous economic game. Evol. Hum. Behav. 26, 245–256.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3288

R. Boyd & P. J. Richerson

Review. Culture and human cooperation

Henrich, J. & Boyd, R. 2001 Why people punish defectors: weak conformist transmission can stabilize costly enforcement of norms in cooperative dilemmas. J. Theor. Biol. 208, 79–89. (doi:10.1006/jtbi.2000.2202) Henrich, J. & Gil-White, F. J. 2001 The evolution of prestige—freely conferred deference as a mechanism for enhancing the benefits of cultural transmission. Evol. Hum. Behav. 22, 165 –196. (doi:10.1016/S10905138(00)00071-4) Kelly, R. C. 1985 The Nuer conquest. Ann Arbor, MI: University of Michigan Press. Kelly, R. L. 1995 The foraging spectrum: diversity in hunter – gatherer lifeways. Washington, DC: Smithsonian Institution Press. Knauft, B. M. 1993 South coast New Guinea cultures: history, comparison, dialectic. Cambridge studies in social and cultural anthropology, no. 89. Cambridge, UK: Cambridge University Press. Lamb, H. H. 1977 Climatic history and the future. Princeton, NJ: Princeton University Press. Martin, P. 2005 Migrants in the global labor market, pp. 1– 57. Global Commission on International Migration. See http://www.gcim.org/attachements/TP1.pdf. McElreath, R., Bell, A. V., Efferson, C., Lubell, M., Richerson, P. J. & Waring, T. 2008 Beyond existence and aiming outside the laboratory: estimating frequencydependent and payoff-biased social learning strategies. Phil. Trans. R. Soc. B 363, 3515–3528. (doi:10.1098/ rstb.2008.0131) Nowak, M. A. & Sigmund, K. 2005 Evolution of indirect reciprocity. Nature 437, 1291–1270. (doi:10.1038/ nature04131) Palmer, C. T., Fredrickson, B. E. & Tilley, C. F. 1997 Categories and gatherings: group selection and the mythology of cultural anthropology. Evol. Hum. Behav. 18, 291 –308. (doi:10.1016/S1090-5138(97)00045-7) Panchanathan, K. & Boyd, R. 2004 Indirect reciprocity can stabilize cooperation without the second-order free rider

Phil. Trans. R. Soc. B (2009)

problem. Nature 432, 499– 502. (doi:10.1038/ nature02978) Partridge, T. C., Bond, G. C., Hartnady, C. J. H., deMenocal, P. B. & Ruddiman, W. F. 1995 Climatic effects of Late Neogene tectonism and vulcanism. In Paleoclimate and evolution with emphasis on human origins (eds E. S. Vrba, G. H. Denton, T. C. Partridge & L. H. Burckle), pp. 8–23. New Haven, CT: Yale University Press. Pinker, S. 1994 The language instinct: the new science of language and mind. New York, NY: Penguin. Ratinieks, F. & Wenseleers, T. 2005 Policing insect societies. Science 307, 54–56. Richerson, P. J. & Boyd, R. 2005 Not by genes alone: how culture transformed human evolution. Chicago, IL: University of Chicago Press. Richerson, P. J., Boyd, R. & Bettinger, R. L. 2005 Evolution on a restless planet: were environmental variability and environmental change major drivers of human evolution? In Handbook of evolution, vol. 2 (eds F. M. Wuketits & F. J. Ayala), pp. 223 –242. Weinheim, Germany: John Wiley & Sons. Steward, J. 1955 Theory of culture change. Urbana, IL: University of Illinois Press. Soltis, J., Boyd, R. & Richerson, P. J. 1995 Can groupfunctional behaviors evolve by cultural group selection? An empirical test. Curr. Anthropol. 36, 437 –494. Tooby, J. & Cosmides, L. 1992 The psychological foundations of culture. In The adapted mind: evolutionary psychology and the generation of culture (eds J. H. Barkow, L. Cosmides & J. Tooby), pp. 19–136. New York, NY: Oxford University Press. Tooby, J. & DeVore, I. 1987 The reconstruction of hominid behavioral evolution through strategic modelling. In The evolution of primate behavior: primate models (ed. W. G. Kinsey), pp. 183 –237. New York, NY: SUNY Press. Trivers, R. L. 1971 The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3289–3299 doi:10.1098/rstb.2009.0115

The evolutionary and ecological roots of human social organization Hillard S. Kaplan1,*, Paul L. Hooper1 and Michael Gurven2 1

Department of Anthropology, University of New Mexico, Albuquerque, NM 87131, USA Department of Anthropology, University of California Santa Barbara, Santa Barbara, CA 93106, USA

2

Social organization among human foragers is characterized by a three-generational system of resource provisioning within families, long-term pair-bonding between men and women, high levels of cooperation between kin and non-kin, and relatively egalitarian social relationships. In this paper, we suggest that these core features of human sociality result from the learning- and skill-intensive human foraging niche, which is distinguished by a late age-peak in caloric production, high complementarity between male and female inputs to offspring viability, high gains to cooperation in production and risk-reduction, and a lack of economically defensible resources. We present an explanatory framework for understanding variation in social organization across human societies, highlighting the interactive effects of four key ecological and economic variables: (i) the role of skill in resource production; (ii) the degree of complementarity in male and female inputs into production; (iii) economies of scale in cooperative production and competition; and (iv) the economic defensibility of physical inputs into production. Finally, we apply this framework to understanding variation in social and political organization across foraging, horticulturalist, pastoralist and agriculturalist societies. Keywords: intergenerational transfers; sexual division of labour; cooperation; economic defensibility; egalitarianism; leadership

1. INTRODUCTION This paper considers the evolutionary and ecological bases of human social organization and is designed to provide a broad overview of the topic. It offers a general theory based on two central theses. The first is that there is an evolved, modal pattern of traditional human social organization that has co-evolved with the characteristics of our species’ specialized foraging niche. This pattern is characterized by a threegenerational system of resource provisioning within families, long-term pair-bonding between men and women, high levels of cooperation between kin and non-kin and relatively egalitarian social relationships. We suggest that these features of human sociality are a function of the learning- and skill-intensive human foraging niche, which is distinguished by a late age-peak in caloric production, high complementarity between male and female inputs to offspring viability, high gains to cooperation in production and risk-reduction, and a lack of economically defensible resources. The second thesis is that major shifts away from this modal pattern of social organization are driven by changes in four key ecological and economic variables: (i) the role of skill in resource production; (ii) the degree of complementarity in male and female inputs into production; (iii) economies of scale in cooperative production and competition; and (iv) the economic defensibility of physical inputs into production. We * Author for correspondence ([email protected]). One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

propose that the interaction of these four factors explains both why human social organization is distinctive in a comparative species context, and also much of the variation in social organization across human societies. 2. THE SOCIAL ORGANIZATION OF FORAGERS IN RELATION TO OTHER PRIMATES This section addresses the social organization of human foragers with respect to other primates in terms of a larger set of coevolved traits, which we refer to as the human adaptive complex (Kaplan et al. 2009). Compared with other primates, the human life history exhibits a number of remarkable characteristics: (i) an exceptionally long lifespan; (ii) a large brain relative to body size; (iii) an extended period of juvenile dependence, resulting in families with multiple dependent children of different ages; (iv) multigenerational resource flows and support of reproduction by post-reproductive individuals; (v) male support of reproduction through the provisioning of women and their offspring; and (vi) substantial cooperation in production and food-sharing between kin and non-kin. Our theory is that these extreme life-history characteristics and extensive cooperative relationships within and between nuclear families are co-evolved responses to an equally extreme commitment to learningintensive foraging strategies and a dietary shift towards high-quality, nutrient-dense and difficult-to-acquire food resources (Kaplan 1997; Kaplan et al. 2000; Kaplan & Robson 2002). The following logic underlies our proposal.

3289

This journal is q 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3290

H. S. Kaplan et al.

Human social organization

First, high levels of knowledge, skill, coordination and strength are required to exploit the suite of highquality, difficult-to-acquire resources humans consume. The time investment in skill acquisition and knowledge leads to selection for lowered mortality rates and greater longevity, because the returns on the investments in development occur at older ages. The extended learning phase during which productivity is low is compensated for by higher productivity during the adult period, with an intergenerational flow of food from old to young. Second, the feeding niche specializing in the capture of large, valuable food packages—particularly through hunting—promotes cooperation between men and women and high levels of male parental investment, because it favours sex-specific specialization in skill investments and generates a complementarity between male and female inputs. Third, the returns to cooperative production and food-sharing promote cooperative relationships within and between families. Food-sharing reduces the risk of food shortfalls due both to the vagaries of foraging luck and to stochastic variance in family size due to mortality and fertility. In addition, we propose that the relative egalitarianism and lack of clearly delineated dominance hierarchies in most forager groups (Boehm 1999) is primarily the result of the same socio-ecological factors; we suggest that this egalitarianism results mainly from the importance of pair-bonding and voluntarily cooperative relationships (especially between non-kin), and a lack of easily defensible resources in the human foraging niche. The following subsections present the logic and evidence for each component of this socio-ecological framework in sequence.

(a) Age-specific production and intergenerational transfers The age-profiles of net food production (food produced minus food consumed) differ dramatically between chimpanzees (Pan troglodytes) and human foragers (figure 1). Among chimpanzees, net production before age 5 is negative, representing complete, then partial, dependence upon mother’s milk. The second phase is independent juvenile growth, lasting until adulthood, during which net production is zero. The third phase is reproductive, during which females, but not males, produce a surplus of calories that they allocate to nursing. The slow-growth, learningintensive human life history, in contrast, generates large calorie deficits until age 20, followed by great calorie surpluses later in life. Humans produce less than they consume for some 15– 22 years, depending on the population. Adult net production in humans is about five times as high as in chimpanzees and peaks at about 35– 45 years of age. The human age-pattern of production, with its long period of dependency and late peak in productivity, could only be evolutionarily viable with substantial transfers from producers to consumers. Unlike other mammals, for which transfers from mothers to offspring are limited largely to lactation during infancy, human parents provision their children until adulthood. Moreover, the sharing of food between human Phil. Trans. R. Soc. B (2009)

parents and their children continues bi-directionally until death in traditional non-market societies. Men, who produce a majority of calories in foraging economies (Kaplan et al. 2001) play a particularly active role in provisioning offspring. Post-reproductive individuals also contribute significant resources towards offspring and grand-offspring fertility and survivorship. The possibility of high-volume transfers from older to younger generations in fact obviates the tight linkage between the age-schedules of fertility and survival that constrains other mammalian life histories, allowing the evolution of significant post-reproductive (i.e. post-menopausal) lifespan (Kaplan & Robson 2002; Lee 2003; Kaplan & Robson 2009). These contributions to offspring fitness may also come in the form of non-material resources, such as help in childcare or the transfer of knowledge and skills. To realize this transfer of resources, human societies exhibit a three-generational residential pattern including offspring, parents and grandparents. Figure 2 shows the implications of this pattern of age-specific production and co-residence for food transfers among Tsimane’ forager–horticulturalists. This figure displays net food transfers between parents and children and between grandparents and grandchildern. It shows that for both males and females, parents give more to children than children give to parents, even into old age, and that flows from grandparents to grandchildren become increasingly significant during the post-reproductive period.

(b) Pair-bonding and the sexual division of labour The human foraging niche, and particularly hunting, promotes cooperation between men and women and high levels of male parental investment because it favours sex-specific economic specialization and generates a complementarity between male and female inputs. Unlike most other mammals, men in foraging societies provide the majority of the energy necessary to support reproduction. Among the 10 foraging societies for which quantitative data are available; on an average men acquire 68 per cent of the calories and almost 88 per cent of the protein; women acquire the remaining 32 per cent of calories and 12 per cent of protein (Kaplan et al. 2001). Hunting game, as opposed to gathering animal protein in small packets (e.g. insects), is largely incompatible with the evolved commitment among primate females to intensive mothering, carrying of infants and lactation-on-demand. First, it is often risky, involving rapid travel and encounters with dangerous prey. Second, it is often most efficiently practised over relatively long periods of time rather than in short stretches, due to search and travel costs. Third, it is extremely skill-intensive, with improvements in return rate occurring over two decades of daily hunting (Kaplan et al. 2000; Walker et al. 2002; Gurven et al. 2006). The first two qualities make hunting a high-cost activity for pregnant and lactating females. The third quality, in interaction with the first and second, generates life-course effects such that gathering is a better option for females, even

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Human social organization

H. S. Kaplan et al.

1.0

3291

2000 1750

0.9

1500 1250

0.8

1000 0.7

500

survival

0.6

250 0.5

0 –250

0.4

–500

net production (kcal)

750

–750

0.3

–1000 0.2

–1250 –1500

0.1

–1750 –2000 0

5

10

15

20

25

30

35

40

45

50

55

60

65

70

75

age Figure 1. Net food production and survival in human foragers and chimpanzees (adapted from Kaplan et al. 2000). Broken lines, human survival; dotted lines, chimpanzee survival; thick solid line, net production humans; thin solid lines, net production chimpanzees. 3500 3000

kcal d–1

2500 2000 1500 1000 500 0 15–19

20–29

30–39

40–49 age

50–59

60–69

70+

Figure 2. Net caloric resource flows from parents, grandparents and husbands among Tsimane forager–horticulturalists (adapted from Gurven & Kaplan 2008). Filled circles, mother ! children; filled squares, father ! children; open circles, grandmother ! grandchildren; open squares, grandfather ! grandchildren; crosses, husband ! wife.

when they are not lactating, and hunting is a better option for males. Since women spend a majority of their reproductive lives either nursing or more than three months pregnant, it would not pay to hunt, and they therefore never get enough practice to make it worthwhile, even when they are not nursing or pregnant, or are post-reproductive (Kaplan et al. 2001). This sex-specific specialization in hunting (for men) and gathering and childcare (for women) yields a Phil. Trans. R. Soc. B (2009)

complementarity between male and female roles, increasing the returns to economic and reproductive cooperation between men and women and encouraging the formation of long-term pair bonds. The fact that humans are unique in raising multiple dependent offspring of different ages additionally reduces the payoffs to desertion and increases the benefits for men and women to link their economic and reproductive lives over the long run (Kaplan et al. 2003; Winking et al. 2007). Men and women who divorce and remarry

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3292

H. S. Kaplan et al.

Human social organization

during the time they are raising offspring will face conflicts of interest with new spouses over the division of resources. Those conflicts increase the benefits of spouses staying together and having all or most of their children together. As a result, monogamy is the predominant form of marriage across human foraging societies (Kaplan & Lancaster 2003). (c) Cooperation in production and risk-reduction While many other animals actively share food—including eusocial insects, social carnivores and some species of birds and bats—the volume and complexity of foodsharing among humans is unique. In addition to within-family food transfers, food-sharing in human foraging societies often extends beyond the nuclear family. Widespread pooling of large game animals, for example, is common among the Hadza (Hawkes et al. 2001), Dobe !Kung (Lee 1979), G/wi (Silberbauer 1981), Ifaluk (Sosis 2000), Ache (Kaplan & Hill 1985) and Gunwinggu (Altman 1987). Because foragers specialize on the largest, highest quality, most nutrient-dense foods available in their environments, they experience high variance in foraging luck due to the difficulty in acquiring these items. For example, individual Ache hunters return emptyhanded on 40 per cent of days they hunt, but some days return with several hundred thousand calories of meat (Hill et al. 1987). Hunting success is even more sporadic among large-game hunters, such as the Hadza, who only acquire meat on less than 3 per cent of hunting days (Hawkes et al. 1991). Since there are diminishing returns to consumption of large quantities of food, especially in environments where spoilage is a problem, and because food portions are very valuable to hungry individuals, reciprocal sharing can significantly reduce variation in day-to-day consumption and maximize the intertemporal utility of food. Reciprocal altruism therefore allows people to devote time and energy to the pursuit of large, asynchronously acquired, high-quality packages (Smith 1988). Widespread sharing of game and other foods may also signal one’s quality as a social partner or mate and indebt others to you during critical periods of disability, injury or sickness (Gurven 2004). Human foragers also experience high gains to cooperation in other aspects of economic production. Many species can be prevented from escaping predation by groups of cooperating hunters. By coordinating their approach, for example, a group of two to five Ache hunters can corral and kill a full troop of capuchin monkeys. Across Amazonia groups of men, women and children can extract large volumes of fish by collectively damming a section of river and intoxicating the fish with plant-derived poisons. Marine hunters, such as the Inuit of North Alaska and Lamalera of Indonesia, work together in 8- to 12-man boats to secure whales that can yield several tons of protein and fat (Spencer 1959; Alvard & Nolin 2002). (d) Forager egalitarianism The human feeding niche—with its high returns to cooperation between men and women and between Phil. Trans. R. Soc. B (2009)

producers—also drives the relative egalitarianism characteristic of foraging societies. This egalitarianism contrasts with both the clearly recognized hierarchies typical of the other apes, as well as the political and economic inequalities characteristic of many postagricultural human societies. We suggest that forager egalitarianism results primarily from the interaction of (i) the lack of economically defensible resources; (ii) the returns to male provisioning; and (iii) the importance of long-term cooperative partners in human foraging economies. The key productive resources of foraging economies—game, honey, fruits, nuts and tubers—are rarely concentrated in stable, predictable patches across the landscape, and are difficult to monopolize as a result. Although there are often territorial delineations and non-trivial clashes between neighbouring groups, there is generally open access to foraging sites within a group’s territory (Dyson-Hudson & Smith 1978). Because men’s productive ability is determined by work effort and ability rather than material wealth, there is comparatively low variance in men’s production. The central importance of cooperative relationships in the human foraging economy further limits overt dominance behaviour and exploitation (Cashdan 1980; Wiessner 1996). The mobility of foragers across largely homogeneous landscapes allows dissatisfied social partners to easily escape the reach of selfish aggrandizers. Would-be dominants must take into account the loss of future cooperation that would result from an intolerably selfish division of cooperatively produced resources. This social accounting becomes more critical as the value of cooperation increases relative to the solitary, non-cooperative alternative. An additional hypothesis for the evolution of forager egalitarianism that has received significant attention is that humans, more than chimpanzees or other primates, can more effectively form levelling coalitions that counter exploitation by physically dominant individuals (Boehm 1999; Pandit & van Schaik 2003). While this is most often phrased in terms of collective aggression against dominants, we suggest that the ability to coordinate collective emigration away from dominants may be a more important and commonly exercised strategy for imposing costs on aggrandizing and anti-social personalities.

(e) Evolved modal human social organization Synthesizing these themes, there are four distinctive features of the evolved human production system that have direct implications for social organization: (i) First, it is skill-based, resulting in a long period of net negative production during infancy, childhood and adolescence, and then a long period of net positive production during adulthood and post-reproductive old age. This results in a three-generational system of wealth flows. (ii) Second, there is sex-based complementarity in skill acquisition in both production and reproduction. This results in cooperation between males and females in food production and childrearing and relatively stable nuclear

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Human social organization families where the reproductive careers of husbands and wives are effectively linked. (iii) Third, gains from risk-reduction and cooperative resource pursuits generate linkages between nuclear families, based on voluntary labour inputs and resource redistributions. (iv) Fourth, for the most part, inputs into resource production are not economically defensible, since foraging territories are large and the most important inputs are labour. This—in combination with the gains to monogamous pair-bonding and the importance of voluntarily cooperating partners—leads to relatively egalitarian, dominance-free social relationships. Together, these social ties produce the basic unit of human social organization: small-scale bands or residential clusters of nuclear families, related through consanguinal and affinal ties, and engaging in cooperative production, altruistic provisioning, and reciprocal sharing in the relative absence of dominance. We refer to this as the evolved modal human social organization, since we propose that most human social groups over the last several tens of thousands of years lived this way. However, we also expect that variation in each of the ecological factors highlighted here has existed throughout human evolutionary history As a result, some groups may have diverged significantly from this basic pattern, and there is much room for subtle variation in social formations within this overall structure (see Foley & Gamble in press, for a discussion of the long-term evolutionary history of human social organization).

3. MAJOR ECOLOGICAL SHIFTERS AWAY FROM THE MODAL PATTERN Important changes in social organization occur as the result of changes in the production system of human societies. The introduction of new inputs into production—such as land for agriculture or cattle for pastoralism—can affect social organization through changes in the relative importance of skill-based labour inputs, the nature of male – female complementarity, returns-to-scale in cooperative production and competition, and the ability to establish relations of coercive social dominance (table 1). In the subsequent sections, we discuss some of the important variations in production and their implications for human social organization across foraging, horticulturalist, pastoralist and agrarian societies. (a) Forager variation The economies of foraging peoples vary on each of the four dimensions discussed above. (i) Skill The importance of resources requiring high levels of skill varies seasonally, and from place to place. When there are valuable resources, such as fruits and fish, that are abundant and easy to harvest, children are more productive and less dependent on resource flows from parents and grandparents (Bliege Bird & Bird 2002; Tucker & Young 2005). Nevertheless, there Phil. Trans. R. Soc. B (2009)

H. S. Kaplan et al.

3293

appear to be no cases in which the basic pattern of three-generational families is not fundamental. (ii) Complementarity There are specific examples of deviations from the basic pattern of male – female complementarity in production and reproduction. In Australia, high rates of polygyny are found in the Northern Territories and Queensland, with the most extreme case being the Tiwi, where 51 per cent of marriages are polygynous. In a sense, they are the exception that proves the rule because Tiwi women are actively involved in hunting and fishing (Hart & Pilling 1960; Goodale 1971). In that coastal environment, there are fishing and small-game hunting opportunities that are more like gathering than hunting—for example, catching small animals such as lizards, snakes, opossums, rats and bandicoots—and women can be more economically self-sufficient. (iii) Scale of cooperation The scale of cooperation also varies ecologically among foragers, across seasons and from one place to another. For example, Shoshoni foragers of the Great Basin in eastern California spent large parts of the year in isolated nuclear families, due to a diet based on pine nuts and scarce game (Steward 1938). On the other hand, game drives and the hunting of large mammals often involve the cooperation of many individuals. In the case of large-scale cooperation, leaders sometimes emerge, whose power derives from the benefits they provide to fellow group members. We suggest that leadership effort, by encouraging pro-sociality, facilitating coordination and mitigating conflict, can reduce the likelihood that cooperation fails due to free-riding or coordination errors. When the gains to collective action in production, aggression or defence are high but untenable in an unsupervised group, group members will sometimes prefer to cooperate under the direction of a leader and take on the costs he or she might impose rather than operate solitarily (Smith & Choi 2007; Hooper et al. submitted). Among marine hunters, Lamalera and Inuit boat managers provide cases of leadership arising in response to economies of scale when many individuals are required to successfully hunt whales (Spencer 1959; Alvard & Nolin 2002). (iv) Dominance in production The nature of resource patches appears to be critical in producing deviations from the standard forager pattern. In general, the resources pursued by human foragers tend to either be mobile or distributed widely in space. However, when there are superabundant patches of resources, such as oak groves and salmon runs in rivers, those inputs into production can become ‘economically defensible’ (Brown 1964; Dyson-Hudson & Smith 1978; Boone 1992). Resource patches tend to be owned, defended with force, and inherited from parents to offspring. Associated with ownership are differences in status, power and wealth with implications for differential survival and reproduction

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3294

H. S. Kaplan et al.

Human social organization

Table 1. Subsistence ecology and major dimensions of social organization. subsistence system (resource base)

intergenerational relations

male– female relations

foragers (mobile prey and widely distributed gathered resources)

intergenerational provisioning, little inheritance

predominant cooperative production relative egalitarianism monogamy, bride and risk reduction, service small-scale leadership

stratified foragers intergenerational (concentrated and provisioning, predictable foraging sites) inheritance of foraging sites

scale of cooperation, leadership

inequality

some polygyny, bride capture

cooperation and leadership in production and warfare

stratification, slavery, unequal access to prime foraging sites

cooperative field labour, relative egalitarianism big men manage conflict over land

horticulturalists (labour-limited cultivation)

intergenerational provisioning, little inheritance

some polygyny, bride capture

pastoralists (livestock)

intergenerational provisioning, inheritance of herds

significant polygyny, cooperative husbandry, bride wealth and chiefs manage bride capture conflict over herds and grazing land

significant inequality in herd-based wealth

agriculturalists (concentrated, highquality land)

intergenerational provisioning, inheritance of land, primogeniture

significant polygyny, cooperation and female leadership in largeclaustration and scale warfare and dowry public works

stratification, slavery, high inequality in land-based wealth

(Sellen & Hruska 2004). In such cases, societies are socially stratified (sometimes including slave classes) and are more similar to land-based agricultural societies. Examples can be found throughout the Pacific coast of North America, being particularly elaborate in British Columbia (Ames 2003). Forager social organization was also transformed in western North America during the relatively short period during which men maintained herds of horses to hunt bison (Ewers 1958). Because these groups engaged in animal husbandry, their social organization more closely resembled that of pastoral societies, including bride price in the form of ponies, bride capture and frequent warfare. (b) Tribal horticulture Subsistence based on horticulture rests on landextensive, slash-and-burn cultivation or polyculture without significant use of irrigation, terracing, ploughs or draft animals (Bates 2001). People reside together in small villages, larger than hunter– gatherer bands but similarly scaled in terms of face-to-face, kinshipladen interactions. Contemporary examples include the manioc and plantain farmers of South America (such as the Tsimane’ and Yanomomo¨), the millet farmers of sub-Saharan Africa, and the island horticulturalists of Oceana. (i) Skill The relative importance of skill in the horticulturalist subsistence strategy varies. For example, among South American forager– horticulturalists, skill development remains highly important for two reasons. First, the same foraging skills that hunter – gatherers employ must still be learned (Gurven et al. 2006); Phil. Trans. R. Soc. B (2009)

second, the yearly clearing of forest and field preparation are also demanding. In contrast, economies that depend more exclusively on horticulture and in which fields are cleared less frequently because the soil remains fertile, as in many African horticulturalists, the relative importance of skill may be diminished. (ii) Complementarity Local ecology affects complementarity in the male and female division of labour in horticultural societies. Garden production by women using the dibble and hoe can provide the carbohydrate and caloric base of the diet and is easily combined with childcare (Boserup 1970; Goody 1976). Males contribute their labour in clearing fields, in provisioning animal protein through hunting and fishing, and in protection of the village resource base through defence. The relative contribution of male help, however, varies by ecological context. More productive soils can be cultivated for longer periods before abandonment, decreasing the yearly demand for strength- and skill-intensive clearing effort. The availability of vegetable protein can also decrease the demand for male hunting effort. As a result of these two factors, gardening based on millet and sorghum that is high in protein and farmed on riverine alluvial soils—as in much of village Africa— is very different from subsistence based on manioc in the thin, lateritic soils of South America. In the African case, each wife is more capable of supporting herself and her children through her own labour, leading to a high frequency of sororal polygyny as sisters form collaborative horticultural work groups (Colson 1960; Lancaster 1981). In the South American case, frequent clearing is necessary and male hunting is critical to acquiring dietary protein, resulting in lower levels of polygyny (Lancaster & Kaplan 1992).

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Human social organization Where the men’s primary complementary input is defence, rather than productive labour, it can be supplied as an ‘umbrella’ benefit to multiple women. As a result, males do not have to consider so much whether they can afford to provision additional wives and children, but rather how they can acquire and keep them (Kaplan & Lancaster 2003). The returns to bride capture and threat of bride capture by other groups can create conditions of endemic raiding (Ayres 1974; Low 2000). Polygyny based on bride capture can be understood as harem-defence polygyny in Orians’ (1969) distinction between harem-defence and resource-defence polygyny. (iii) Scale of cooperation While there are some returns to cooperative in horticultural labour, particularly in clearing and harvesting fields, warfare for bride capture and over land yield the highest returns to scale in horticulturalist societies. In highland New Guinea, the endemic need for military coherence and for diplomacy with both hostile and collaborative groups encouraged the rise of war leaders and big men (Meggitt 1977). These leaders held considerable social power based on their ability to help realize the group’s interests, but were relatively constrained compared with the elites of large-scale agricultural societies. (iv) Dominance in production The distribution of high-quality land is generally less patchy in horticultural than agricultural systems. Access to land is generally defended by males against outsiders. Within the group, a usufruct system of land tenure gives group members direct rights to the means of production and reproduction (Boserup 1970; Goody 1976). The returns to competition for land within and between groups increase where productive soil is concentrated in high-quality patches, as in the lower alluvial Amazon, or where land becomes the limiting input to production due to population pressure, as in the highlands of New Guinea (Meggitt 1977). (c) Tribal pastoralism Pastoral economies are those based on domesticated herd animals such as cattle, camels, horses and sheep. Contemporary examples include the Maasai of East Africa, the Tuareg of North Africa and the Altaic peoples of Inner Asia. The introduction of livestock as the key input to economic production has multiple effects on social and political organization. The importance of competition for grazing lands and the ability to dominate the resources of neighbouring agricultural settlements add additional dimensions affecting variability among pastoral societies. (i) Skill While successful herd management requires skill and knowledge of animal husbandry and local ecology, the daily supervision of herding animals is often accomplished by boys and adolescent males (Spencer 1998). An adult male’s productivity becomes determined more by the size of his herd than his inputs of time and labour. Because cattle are generally inherited Phil. Trans. R. Soc. B (2009)

H. S. Kaplan et al.

3295

(if they are not obtained through warfare), this affords parents more control of their offspring, since offspring require parental transfers to marry and make a living (Borgerhoff Mulder 1988; Spencer 1998). Thus, the three-generational system of wealth flows is still intact, but children are beholden to their parents, which is not true in foraging societies, where individual freedom often extends to family relationships as well. (ii) Complementarity The products of herds require intensive processing of meat, milk and hides, labour provided by women. Men contribute their wealth of animal stock and protection from raiding by other groups. The facts that men’s contribution to production is limited by herd size—the distribution of which may be highly unequal—and that defence may be offered as an umbrella benefit to multiple wives allows high levels of polygyny in most pastoral economies (Spencer 1998; Kaplan & Lancaster 2003). Because males compete for the resources that females require for successful reproduction, this mating system can be understood as resource-defence polygyny. One expression of the importance of male extra-somatic wealth in the mating process is the institution of bride wealth, by which men provide a significant payment of resources as a preferred substitute for bride service (Borgerhoff Mulder 1988). Thus, among pastoralists, the complementarity in sex roles interacts with the inheritance system and wealth differences among men to produce higher inequalities in male reproductive success and greater asymmetries in male–female relationships than in economies limited by men’s labour. (iii) Scale of cooperation The frequency and intensity of warfare and the need for diplomacy in negotiating grazing rights creates a demand for significant leadership roles among pastoralists. The prominence of pastoralist chiefs probably reflects both these increased demands for organization in intergroup conflict, as well as the inequalities in social power that accompany the large inequalities in resource holdings possible in pastoral economies. Within pastoralists, some groups—such as the mounted pastoralists of Inner Asia and North Africa—evidence stronger tendencies toward largerscale political integration than others—such as the pastoralists of sub-Saharan Africa—perhaps due to the former’s proximity to resource-rich and militarily tempting agrarian communities (M. Borgerhoff Mulder 2009, personal communication; Turchin 2009). (iv) Dominance in production The nature of pastoral resources—individually controllable but easily stolen—plus the returns to bride capture drive the chronic warfare common to pastoralists (White & Burton 1988; Keeley 1996). Here the ‘warrior complex’ is full-blown, with chronic internal warfare, blood feuds, social segregation of a male warrior age class, fraternal interest groups, a geographical flow of women from subordinate to dominant groups, and expansionist, segmentary lineages based on the male

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3296

H. S. Kaplan et al.

Human social organization

line (DiVale & Harris 1976; White & Burton 1988). The differential accumulation and loss of livestock promotes asymmetries in male wealth and reproductive success both within- and between-groups. Variation in both the degree of status inequality and the scale of warfare may also be determined by the importance of high quality grazing lands as an input into livestock production. Where grazing lands are poor, cattle must move extensively, land is often held communally and status differentials may be modest; when they are rich and patchily distributed, larger scale wars and differentials in status and power tend to be found.

value on the table in order to access a desirable groom or move a daughter up in the social hierarchy. These extra payments included actual wealth in the form of dowry, as well as guarantees of paternity confidence. Guarantees of a daughter’s virginity and chastity took the form of female seclusion and incapacitation—special women’s quarters, chaperones, foot-binding, corseting, clitoridectomy and infibulation—and could be substantially costly, barring women from the outside world of productive labour (Dickemann 1979, 1981; Gaulin & Boster 1990).

(d) Agrarian states and despotism The rise of the first large-scale agrarian states, beginning about 6000 years ago in Mesopotamia and later in East Asia and the Americas, marked a critical shift in how humans organized themselves in relation to each other and their environments. These early civilizations share a number of common characteristics: (i) the presence of large, stratified social groupings settled on particularly concentrated, high-quality resource patches; (ii) the appearance of social despots, men who use political and military power to defend their wealth and reproduction and warfare to acquire more resource patches and slaves; and (iii) the advent of formal systems of social governance and law (Betzig 1986; Betzig 1993; Diamond 1997; Summers 2005). We argue that these characteristics of agrarian social organization flow from the nature of the territorial resources that provided the primary input into large-scale agricultural production.

(iii) Scale of cooperation In addition to the first-order shift in social inequality and stratification due to the patchiness of territorial resources, the returns to scale in territorial competition and agricultural intensification—and the more general need for peaceful coexistence in large, dense settlements—may have driven the emergence of prominent leadership roles and top-down governance structures typical of agrarian states. Returns to cooperation in expansionist or defensive warfare may have especially encouraged the acceptance of politically ‘legitimate’ elite leadership (Hooper et al. submitted). The Epic of Gilgamesh, in which Gilgamesh consolidates political control by establishing the defensive walls of Uruk, provides an early narrative of this theme (Adams 1966). The advent of formal systems of law—such as the Code of Hammurabi in Mesopotamia—probably reflected both the effort of ruling elites to control subordinate behaviour to their personal advantage, as well as popular demand for the regulation of social life in large-scale politics. While centralized social control was often an instrument of exploitation, the formal definition and punishment of crime, management of property rights and enforced contributions to public goods may have yielded benefits to non-elites as well (Smith & Choi 2007; Hooper et al. submitted).

(i) Skill As in the inheritance of livestock in pastoralism, the inheritance of land as an important input into production affects the relative importance of skill in production. Children are more beholden to their parents, who control their primary source of wealth. Because land and other rival sources of wealth can yield greater economic and social returns when kept intact rather than divided, there were sometimes efforts to reduce the number of claimants to the reproductive estate; this was accomplished through distinctions between legitimate and illegitimate offspring and differential inheritance to first-born sons (Goody 1976; Hrdy & Judge 1993). (ii) Complementarity For access to the mating market, men must have brought wealth, power and land in order to be favourably placed, or else get wives as high-risk booty in warfare against other groups (Low 2000; Clarke & Low 2001). These despotic males provide an extreme example of resource-defence polygyny; i.e. they controlled access to the resource base for reproduction that females required and, with few competitors, polygynous marriage to them became the only reproductive option for many women. While women in stratified systems continued to bring their health, fertility and labour to the mating market, the extreme variance in male quality sometimes forced women’s families to put down more Phil. Trans. R. Soc. B (2009)

(iv) Dominance in production The patches upon which the first agricultural civilizations were settled were highly productive, but set in environments where there was a rapid fall off to unproductive lands such as desert or forest. Intensification of production through irrigation or terracing tended to further increase patchiness in land quality (Adams 1966). Competition for access to high-quality, defensible patches drove both social stratification within groups as well as territorial warfare between competing settlements. Families that were unable to produce on their own land became labourers and share-croppers under socially dominant lineages (Boone 1992; Smith & Choi 2007). Political and military control of resources in these societies was maintained almost exclusively by the power of men. Although nonhuman primate females often form alliances with their female kin to protect and control access to the resources necessary for their reproduction (Isbell 1991; Sterck et al. 1997), women are not in a position to do so; the very nature of the sexual division of labour and the dependency of multiple children

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Human social organization means that women cannot band together and contest men for control of resources. Variance in male resource holdings in agrarian states was probably the greatest it has ever been in human history (Betzig 1986, 1992, 1993). Despotic males yielded tremendous social power, with the ability to eliminate rivals and their families through edicts, to acquire land, wealth and slaves for labour and reproduction, and to determine political succession for favoured sons. An outcome of such major variance in male quality and male mating success was that many men remained unmarried or had only one wife, so that male celibacy or at least non-marital sex was a prominent feature of the mating-pool structure for men. This extreme variance in male resource-holdings inevitably led to political instability from the creation of too many potential heirs and too many males without access to the means of reproduction (Turchin & Nefedov 2009).

4. CONCLUSIONS To summarize, we propose that details of the resource production system explain much of human social organization, both accounting for our distinctiveness among primates, as well as explaining variation in human sociality across space and time. Investment in skill and knowledge is the hallmark of human foraging. Such investments diminish in importance when other inputs, especially defensible and inheritable resources such as land and cattle, become important in determining total production. Nevertheless, the three-generational system of downward wealth flows appears to be a universal feature of human social organization. A principal difference when inheritable wealth becomes an important input in production is that differential inheritance within and among families also emerges, and members of the older generation often exert greater power over their descendents. Complementarity among the inputs of men and women into production and reproduction is another hallmark of our species. This complementarity derives from the forager diet of mobile prey—which requires both skill and dangerous pursuit—and stationary extracted plant resources. Complementarity, coupled with the existence of multiple offspring of different ages, tends to link the reproductive careers of husbands and wives. Thus, among foragers, where wealth variance is general minimal, monogamy is the dominant marital form. As additional material inputs into production become important, however, the nature of complementarity between males and females also changes because males tend to control those physical inputs through dominance, warfare and inheritance. Wealth in the form of defensible, storable and inheritable resources tends to increase the variance among males in what they have to offer females, and the rate and extent of polygyny increases as well. This is true of stratified foragers, and becomes more extreme with pastoralism and agrarian states. Risk-reduction, food-sharing and cooperative production tend to be nearly universal among foragers (although varying in extent both seasonally and crossculturally). This is due to the large and highly variable Phil. Trans. R. Soc. B (2009)

H. S. Kaplan et al.

3297

packages acquired by human foragers, and the skillbased production strategy that puts a premium on cooperative pursuits. The mix of cooperation, returns to monogamy, and the lack of defensible inputs into production tends to limit the formation of dominance hierarchies among foragers. There is still some debate as to whether this relative lack of dominance is due to social levelling strategies, or whether, since the major input into production is voluntary skilled labour, the opportunities for coercion are limited. The importance of defensible material inputs into production and intensification are almost always associated with greater inequality, social stratification and more prominent political elites. The roles of despotic motives versus the demand for group leadership in driving greater stratification in such situations are difficult to disentangle, however. In our view, it is principally the incorporation of defensible assets into production that generates exploitative dominance hierarchies and despotism, whereas it is economies of scale that produce patterns of managerial leadership. It is just that as economies tend to be based on defensible resources that the scale of production and conflict increases as well. Therefore, managerial leadership and dominance relations usually co-occur. Finally, we suggest that the same principles may explain the transitions in social organization accompanying the shift to modern developed economies. The transition from despotic agrarian states to more representative forms of government appears to involve the rise of commerce in Europe with a new emphasis on managerial and technological skills. This created a transition from an economy based largely on defendable agricultural land to one based on fungible capital and skill-based labour. The efficiency of private, as opposed to state-mandated, economic production led ruling classes to release direct control of the means of production (McNeill 1982). This tipped the balance of economic and political bargaining power, traditionally held firmly by land-based elites, toward a growing commercial middle class, which demanded expanded social and political rights. This trend continued with the industrial revolution and the efficiency of labour markets—with their attendant mobility—in contrast to slavery, peonage and patron – client bonds characteristic of feudal Europe and the plantation economies of the Americas. In some respects, modern skill-based economies and the skill-based economies of foragers share some fundamental similarities, both resulting in more egalitarian political and social institutions and more individual freedom. Jane Lancaster contributed significantly to the development of many of the ideas in this paper. Thanks also to Sam Bowles, Jim Boone, Paul Seabright, Ann Caldwell, Robert Foley and Monique Borgerhoff Mulder for helpful discussions and feedback, to Jeff Winking for the preparation of Tsimane data and to Tim Clutton-Brock for organizing the Royal Society discussion meeting. H.K., P.H. and M.G. were supported by the National Science Foundation (BCS-0422690) and the National Institute on Ageing (R01AG024119-01). P.H. received additional support from the Howard Hughes Medical Institute through the Program in Interdisciplinary Biological and Biomedical Sciences at UNM.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3298

H. S. Kaplan et al.

Human social organization

REFERENCES Adams, R. M. 1966 The evolution of urban society: early Mesopotamia and prehispanic Mexico. Chicago, IL: Aldine. Altman, J. C. 1987 Hunter –gatherers today: an aboriginal economy of north Australia. Canberra, Australia: Australian Institute of Aboriginal Studies. Alvard, M. S. & Nolin, D. A. 2002 Rousseau’s whale hunt? Coordination among big-game hunters. Curr. Anthropol. 43, 533 –559. (doi:10.1086/341653) Ames, K. 2003 The northwest coast. Evol. Anthropol. 12, 19–33. (doi:10.1002/evan.10102) Ayres, B. 1974 Bride theft and raiding for wives in crosscultural perspective. Anthropol. Quart. 47, 238 –252. (doi:10.2307/3316978) Bates, D. G. 2001 Human adaptive strategies: ecology culture and politics, 2nd edn. Boston, MA: Allyn and Bacon. Betzig, L. 1986 Despotism and differential reproduction: a Darwinian view of history. Hawthorne, NY: Aldine de Gruyter. Betzig, L. 1992 Roman polygyny. Ethol. Sociobiol. 13, 309 –349. (doi:10.1016/0162-3095(92)90008-R) Betzig, L. 1993 Sex, succession and stratification in the first six civilizations: how powerful men reproduced, passed power on to their sons, and used their power to defend their wealth, women and children. In Social stratification and socioeconomic inequality (ed. L. Ellis), pp. 37– 74. New York, NY: Praeger. Bliege Bird, R. & Bird, D. 2002 Constraints of knowing or constraints of growing? Fishing and collecting by the children of Mer. Human Nat. 13, 239 –267. Boehm, C. 1999 Hierarchy in the forest: the evolution of egalitarian behavior. Cambridge, UK: Harvard University Press. Boone, J. L. 1992 Competition, conflict, and the development of social hierarchies. In Evolutionary ecology and human behavior (eds E. A. Smith & B. Winterhalder), pp. 301 –337. Hawthorne, NY: Aldine de Gruyter. Borgerhoff Mulder, M. 1988 Kipsigis bridewealth payments. In Human reproductive behavior: a Darwinian perspective (eds L. Betzig, M. Borgerhoff Mulder & P. Turke), pp. 65–82. Cambridge, UK: Cambridge University Press. Boserup, E. 1970 Women’s role in economic development. London, UK: Allen and Unwin. Brown, J. L. 1964 The evolution of diversity in avian territorial systems. Wilson Bull. 76, 160–169. Cashdan, E. A. 1980 Egalitarianism among hunters and gatherers. Am. Anthropol. 82, 116 –120. (doi:10.1525/aa. 1980.82.1.02a00100) Clarke, A. L. & Low, B. S. 2001 Testing evolutionary hypotheses with demographic data. Popul. Dev. Rev. 27, 633 –660. (doi:10.1111/j.1728-4457.2001.00633.x) Colson, E. 1960 Social organization of the Gwembe Tonga. Manchester, UK: Rhodes-Livingstone Institute. Diamond, J. 1997 Guns, germs, and steel: the fates of human societies. New York, NY: Norton. Dickemann, M. 1979 The ecology of mating systems in hypergynous dowry societies. Soc. Sci. Inform. 18, 163 –195. (doi:10.1177/053901847901800201) Dickemann, M. 1981 Paternal confidence and dowry competition: a biocultural analysis of purdah. In Natural selection and social behavior (eds R. D. Alexander & D. W. Tinkle), pp. 417–438. New York, NY: Chiron Press. DiVale, W. & Harris, M. 1976 Population, warfare, and the male supremacist complex. Am. Anthropol. 80, 21 –41. Dyson-Hudson, R. & Smith, E. A. 1978 Human territoriality: an ecological reassessment. Am. Anthropol. 80, 21–41. (doi:10.1525/aa.1978.80.1.02a00020) Ewers, J. C. 1958 The Blackfeet: raiders on the northwestern plains. Norman, OK: University of Oklahoma Press. Phil. Trans. R. Soc. B (2009)

Foley, R. & Gamble, C. In press. The ecology of social transitions in human evolution. Phil. Trans. R. Soc. B. (doi:10.1098/rstb.2009.0136) Gaulin, S. & Boster, J. 1990 Dowry as female competition. Am. Anthropol. 92, 994 –1005. (doi:10.1525/aa.1990.92. 4.02a00080) Goodale, J. C. 1971 Tiwi wives. Seattle, WA: University of Washington Press. Goody, J. 1976 Production and reproduction: a comparative study of the domestic domain. Cambridge, UK: Cambridge University Press. Gurven, M. 2004 To give or give not: the evolutionary ecology of human food transfers. Behav. Brain Sci. 27, 543 –583. Gurven, M. & Kaplan, H. 2008 Beyond the grandmother hypothesis: evolutionary models of human longevity. In The cultural context of aging: worldwide perspectives (ed. J. Sokolovsky), pp. 53–60, 3rd edn. Santa Barbara, CA: Greenwood Press. Gurven, M., Kaplan, H. & Guitierrez, M. 2006 How long does it take to become a proficient hunter? Implications on the evolution of delayed growth. J. Human Evol. 51, 454 –470. (doi:10.1016/j.jhevol.2006.05.003) Hart, C. W. M. & Pilling, A. R. 1960 The Tiwi of north Australia. New York, NY: Holt, Rinehart and Winston. Hawkes, K., O’Connell, J. F., Blurton Jones, N. G., Oftedal, O. T. & Blumenschine, R. J. 1991 Hunting income patterns among the Hadza: big game, common goods, foraging goals and the evolution of the human diet. Phil. Trans. R. Soc. Lond. B 334, 243 –251. (doi:10. 1098/rstb.1991.0113) Hawkes, K., O’Connell, J. F. & Blurton Jones, N. 2001 Hadza meat sharing. Evol. Human Behav. 22, 113–142. (doi:10.1016/S1090-5138(00)00066-0) Hill, K., Hawkes, K., Kaplan, H. & Hurtado, M. 1987 Foraging decisions among Ache hunter –gatherers: new data and implications for optimal foraging models. Ethol. Sociobiol. 8, 1–36. (doi:10.1016/0162-3095(87) 90055-0) Hooper, P. L., Kaplan, H. S. & Boone, J. L. Submitted. A theory of leadership in human cooperative groups. Hrdy, S. B. & Judge, D. 1993 Darwin and the puzzle of primogeniture: an essay on biases in parental investment after death. Human Nat. 4, 1– 45. (doi:10.1007/ BF02734088) Isbell, L. A. 1991 Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav. Ecol. 2, 143–155. (doi:10.1093/beheco/2.2.143) Kaplan, H. S. 1997 The evolution of the human life course. Between Zeus and Salmon: the biodemography of aging (eds K. Wachter & C. Finch), pp. 175 –211. Washington, DC: National Academy of Sciences. Kaplan, H. S. & Hill, K. 1985 Food-sharing among Ache foragers: tests of explanatory hypotheses. Curr. Anthropol. 26, 223–245. (doi:10.1086/203251) Kaplan, H. & Robson, A. 2002 The co-evolution of intelligence and longevity and the emergence of humans. Proc. Natl Acad. Sci. USA 99, 10221–10226. (doi:10. 1073/pnas.152502899) Kaplan, H. S. & Lancaster, J. B. 2003 An evolutionary and ecological analysis of human fertility, mating patterns, and parental investment. In Offspring: human fertility behavior in biodemographic perspective (eds K. W. Wachter & R. A. Bulatao), pp. 270–223. Washington, DC: National Academies Press. Kaplan, H. S. & Robson, A. 2009 We age because we grow. Proc. R. Soc. B 276, 1837–1844. (doi:10.1098/ rspb.2008.1831) Kaplan, H., Hill, K., Lancaster, J. B. & Hurtado, A. M. 2000 A theory of human life history evolution: diet,

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Human social organization intelligence, and longevity. Evol. Anthropol. 9, 156–185. (doi:10.1002/1520-6505(2000)9:4,156::AID-EVAN5.3. 0.CO;2-7) Kaplan, H. S., Hill, K., Hurtado, A. M. & Lancaster, J. B. 2001 The embodied capital theory of human evolution. In Reproductive ecology and human evolution (ed. P. T. Ellison), pp. 293 –317. Hawthorne, NY: Aldine de Gruyter. Kaplan, H., Robson, A. & Lancaster, J. B. 2003 Embodied capital and the evolutionary economics of the human lifespan. In Lifespan: evolutionary, ecology and demographic perspectives (eds J. R. Carey & S. Tuljapaur), Population and Development Review 29(Supplement), 152–182. New York, NY: The Population Council. Kaplan, H. S., Gurven, M. & Winking, J. 2009 An evolutionary theory of human lifespan: Embodied capital and the human adaptive complex. In Handbook of theories of aging (eds V. L. Bengtson, D. Gans, N. M. Putney & M. Silverstein), pp. 53 – 60. 2nd edn. New York: Springer. Keeley, L. H. 1996 War before civilization: the myth of the peaceful savage. Oxford, UK: Oxford University Press. Lancaster, C. S. 1981 The Goba of the Zambezi: sex roles, economics, and change. Norman, OK: University of Oklahoma Press. Lancaster, J. B. & Kaplan, H. 1992 Human mating and family formation strategies: the effects of variability among males in quality and the allocation of mating effort and parental investment. In Topics in primatology: human origins, vol. 1 (eds T. Nishida, W. C. McGrew, P. Marler, M. Pickford & F. de Waal), pp. 21–33. Tokyo, Japan: University of Tokyo Press. Lee, R. B. 1979 The !Kung San: men, women, and work in a foraging society. Cambridge, UK: Cambridge University Press. Lee, R. 2003 Rethinking the evolutionary theory of aging: transfers, not births, shape senescence in social species. Proc. Natl Acad. Sci. 100, 9637–9642. (doi:10.1073/ pnas.1530303100) Low, B. S. 2000 Why sex matters: a Darwinian look at human behavior. Princeton, NJ: Princeton University Press. McNeill, W. H. 1982 The pursuit of power: technology, armed force, and society since A.D. 1000. Chicago, IL: University of Chicago Press. Meggitt, M. 1977 Blood is their argument: warfare among the Mae Enga tribesmen of the New Guinea Highlands. Mountain View, CA: Mayfield. Orians, G. H. 1969 On the evolution of mating systems in birds and mammals. Am. Nat. 103, 589 –603. (doi:10. 1086/282628) Pandit, S. A. & van Schaik, C. P. 2003 A model for leveling coalitions among primate males: toward a theory of egalitarianism. Behav. Ecol. Sociobiol. 55, 161–168. (doi:10.1007/s00265-003-0692-2) Sellen, D. W. & Hruska, D. J. 2004 Extractedfood resource-defense polygyny in native western North

Phil. Trans. R. Soc. B (2009)

H. S. Kaplan et al.

3299

America. Curr. Anthropol. 45, 707 –714. (doi:10.1086/ 425637) Silberbauer, G. 1981 Hunter and habitat in the Central Kalahari Desert. Cambridge, UK: Cambridge University Press. Smith, E. A. 1988 Risk and uncertainty in the ‘original affluent society’: evolutionary ecology of resource-sharing and land tenure. In Hunter gatherers. Vol. 1: History, evolution and social change (eds T. Ingold, D. Riches & J. Woodburn), pp. 222 –251. New York, NY: Berg. Smith, E. A. & Choi, J. K. 2007 The emergence of inequality in small-scale societies: simple scenarios and agent-based simulations. In The model-based archaeology of socio-natural systems (eds S. van der Leeuw & T. Kohler). Santa Fe, NM: SAR Press. Sosis, R. 2000 The emergence and stability of cooperative fishing on Ifaluk Atoll. In Human behavior and adaptation: an anthropological perspective (eds L. Cronk, N. Chagnon & W. Irons), pp. 437 –472. Hawthorne, NY: Aldine de Gruyter. Spencer, P. 1998 The pastoral continuum. Oxford, UK: Oxford University Press. Spencer, R. 1959 The north Alaskan Eskimo: a study in ecology and society. Washington, DC: Smithsonian Institution. Sterck, E. H. M., Watts, D. P. & van Schaik, C. P. 1997 The evolution of female social relationships in nonhuman primates. Behav. Ecol. Sociobiol. 41, 291 –309. (doi:10.1007/ s002650050390) Steward, J. 1938 Basin-plateau aboriginal sociopolitical groups. Washington, DC: Smithsonian Institution. Summers, K. 2005 The evolutionary ecology of despotism. Evol. Human Behav. 26, 106 –135. (doi:10.1016/j.evol humbehav.2004.09.001) Tucker, B. & Young, A. G. 2005 Growing up Mikea: children’s time allocation and tuber foraging in southwestern Madagascar. In Hunter– gatherer childhoods (eds B. Hewlett & M. Lamb), pp. 147 –171. New York, NY: Aldine de Gruyter. Turchin, P. 2009 A theory for formation of large empires. J. Glob. Hist. 4, 191 –217. Turchin, P. & Nefedov, S. A. 2009 Secular cycles. Princeton, NJ: Princeton University Press. Walker, R., Hill, K., Kaplan, H. & McMillan, G. 2002 Age-dependency in skill, strength and hunting ability among the Ache of eastern Paraguay. J. Human Evol. 42, 639 –657. (doi:10.1006/jhev.2001.0541) White, D. R. & Burton, M. L. 1988 Causes of polygyny: ecology, economy, kinship, and warfare. Am. Anthropol. 90, 871 –887. (doi:10.1525/aa.1988.90.4.02a00060) Wiessner, P. 1996 Leveling the hunter: constraints on the status quest in foraging societies. In Food and the status quest: an interdisciplinary perspective (eds P. Wiessner & W. Schiefenho¨vel), pp. 171– 192. Providence, RI: Berghahn Books. Winking, J., Kaplan, H., Gurven, M. & Rucas, S. 2007 Why do men marry and why do they stray? Proc. R. Soc. B 274, 1643–1649. (doi:10.1098/rspb.2006.0437)

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Phil. Trans. R. Soc. B (2009) 364, 3301–3309 doi:10.1098/rstb.2009.0123

Trust and cooperation among economic agents Partha Dasgupta1,2,* 1

Faculty of Economics and Politics, University of Cambridge, Cambridge, UK Sustainable Consumption Unit and Brooks World Poverty Institute, University of Manchester, UK

2

The units that are subject to selection pressure in evolutionary biology are ‘strategies’, which are conditional actions (‘Do P if X occurs, otherwise do Q’). In contrast, the units in economics select strategies from available menus so as to further their projects and purposes. As economic agents do not live in isolation, each agent’s optimum choice, in general, depends on the choices made by others. Because their projects and purposes involve the future, not just the present, each agent reasons about the likely present and future consequences of their respective choices. That is why beliefs, about what others may do and what the consequences of those choices could be, are at the basis of strategy selection. A catalogue of social environments is constructed in which agents not only promise each other’s cooperation, but also rationally believe that the promises will be kept. Unfortunately, non-cooperation arising from mistrust can be the outcome in those same environments: societies harbour multiple ‘equilibria’ and can skid from cooperation to noncooperation. Moreover, a pre-occupation among analysts with the Prisoners’ Dilemma game has obscured the fact that cooperative arrangements can harbour not only inequality, but also exploitation. The analysis is used to discuss why international cooperation over the use of global public goods has proved to be so elusive. Keywords: negotiation; culture; rational beliefs; tipping points; exploitation

1. INTRODUCTION The units that are subject to selection pressure in evolutionary biology are ‘strategies’ (Maynard Smith 1982; Nowak 2006), which are conditional actions, such as ‘Do P if X occurs, otherwise do Q’. In contrast, the units in economics select strategies from available menus so as to further their projects and purposes. As agency assumes a central role in the social sciences, economic units are called ‘agents’ or ‘parties’. Sometimes, economists even call them ‘people’. Robinson Cruso aside, people do not live in isolation. So, an agent’s optimum choice depends on the choices made by others. Moreover, as their projects and purposes involve not just the present but the future too, every agent reasons about the likely present and future consequences of their respective choices, while recognizing that all others are engaged in similar reasoning. That is why beliefs, about what others may do and what the consequences of those choices could be, are at the basis of strategy selection. Economic environments are therefore inter-temporal games, in the sense of the theory of games (Binmore & Dasgupta 1986). Notice, we are not pre-judging that agents cooperate so as to improve their lot. Whether they do depends on the ease with which they have access to a cooperative ‘infrastructure’ (e.g. commitment devices that can be used to make the promises agents make to one another *[email protected] One contribution of 16 to a Discussion Meeting Issue ‘The evolution of society’.

credible; see §3).Various social environments in which cooperation is possible are studied. That the basis of cooperation is mutual trust is a banality, the deeper point is that trust in turn is based on beliefs. However, if the trust is not to be ‘blind’, it has to be based on rational beliefs. In §§1–3, I develop these arguments in a sequence of increasing complexity. In §4, I study why cooperation is often very fragile. In §5, I show that cooperation among members of a group is not always benign and that it can harbour inequality, even exploitation. In §6, I apply the theoretical framework of §§3 and 4 to ask why, in contrast to the cooperation that is frequently observed among members of local communities over the use of geographically confined natural resources (Dasgupta & Heal 1979; Ostrom 1990; Baland & Platteau 1996) and among people engaged in transactions in well-functioning markets, international cooperation in the management of global public goods (e.g. the atmosphere as a sink for pollutants, the oceans) has proved to be so elusive. Section 7 concludes. 2. TRUST Imagine that a group of people have discovered a mutually advantageous course of actions. At the grandest level, it could be that citizens see the benefits of adopting a constitution for their country. At a more local level, the undertaking could be to: share the costs and benefits of maintaining a communal resource (irrigation system, grazing field and coastal fishery); construct a jointly useable asset (drainage channel in a watershed), collaborate in political activity (civic engagement, lobbying); do business when the purchase

3301

This journal is q 2009 The Royal Society

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3302

P. Dasgupta Trust and cooperation

and delivery of goods cannot be synchronized (credit, insurance and wage labour); enter marriage, create a rotating saving and credit association (as in the institution of iddir in Ethiopia); initiate a reciprocal arrangement (I help you, now that you are in need, with the understanding that you will help me when I am in need); adopt a convention (send one another Christmas cards); create a partnership to produce goods for the market; conduct an instantaneous transaction (purchase something across the counter) and so on. Then there are mutually advantageous courses of action that involve being civil to one another. They range from such forms of civic behaviour as not disfiguring public spaces and obeying the law more generally, to respecting the rights of others. Imagine next that the parties have agreed to share the benefits and costs in a certain way. The agreement could involve some members making side payments to others. Again, at the grandest level, the agreement could be a social contract among citizens to observe their Constitution. Or it could be a tacit agreement to be civil to one another, such as respecting the rights of others to be heard, to get on with their lives and so forth. Here we will be thinking of agreements over transactions in goods and services. There would be situations where the agreement was based on a take-it-or-leave-it offer one party makes with another (as when a purchaser accepts the terms and conditions in a supermarket). In other contexts, bargaining may have been involved (as in a Middle-Eastern bazaar). Here we will not ask how agreements have been reached, nor look for principles of equity that might have been invoked during negotiation (but see §5). We ask instead: under what circumstances would the parties who have reached agreement trust one another to keep their word? Because one’s word must be credible if it is to be believed, mere promises would not be enough. (Witness that we caution others, and ourselves too, not to trust people ‘blindly’.) If the parties are to trust one another to keep their promise, matters must be so arranged that: (1) at every stage of the agreed course of actions, it would be in the interest of each party to plan to keep his or her word if all others were to plan to keep their word and (2) at every stage of the agreed course of actions, each party would believe that all others would keep their word. If the two conditions are met, a system of beliefs that the agreement will be kept would be self-confirming. Notice that condition (2) on its own wouldn’t do. Beliefs need to be justified. Condition (1) provides the justification. It offers the basis on which everyone could in principle believe that the agreement will be kept. A course of actions, one per party, satisfying condition (1) is called a Nash equilibrium, in honour of the mathematician John Nash (he of The beautiful mind ) who proved that it is not a vacuous concept (Nash 1950). By their very definition, Nash equilibria (there can be more than one equilibrium; see below) are self-enforcing, which is why the parties in question would seek to identify them. Notice that condition (1) on its own would not do either. It could be that it is in each agent’s interest to behave opportunistically if everyone believed that Phil. Trans. R. Soc. B (2009)

everyone else would behave opportunistically. In that case, non-cooperation is also a Nash equilibrium, meaning that a set of mutual beliefs that the agreement will not be kept would also be self-confirming, and so, non-cooperation would be self-enforcing. Stated formally, a Nash equilibrium is a set of strategies, one per agent, such that no agent would have any reason to deviate from his or her course of actions if all other agents were to pursue their courses of actions. As we have just seen, generally speaking, societies harbour multiple Nash equilibria (see Maynard Smith 1982; Nowak 2006; Osborne 2004 for specific examples). Some yield desirable outcomes, others do not. The famous Prisoners’ Dilemma (PD) is a game that has a unique Nash equilibrium in which all parties are worse off than they could have been if a suitable cooperative infrastructure had been in place (§6). The fundamental problem facing a society is to create institutions where conditions (1) and (2) apply to engagements that protect and promote its members’ interests. Conditions (1) and (2), taken together, require an awful lot of coordination among the parties. In order to probe the question of which Nash equilibrium can be expected to be reached, if a Nash equilibrium is expected to be reached at all, economists study human behaviour that are not Nash equilibria. The idea is to model the way people form beliefs about the way the world works, the way people behave in response to those beliefs, and the way they revise their beliefs on the basis of what they observe. The idea is to track the consequences of those patterns of belief formation so as to check whether the model economy moves towards a Nash equilibrium over time or whether it moves about in some fashion or other but not towards an equilibrium. Because beliefs (and their revisions) play a strong role in the evolution of cooperation among humans, evolutionary dynamics in economic environments involves a somewhat different set of drivers from the ones that are studied in evolutionary biology.1 Theoretical research on the evolution of beliefs and the concomitant evolution of strategies has yielded one general conclusion: suppose the economic environment in a certain place harbours multiple Nash equilibria. Which equilibrium should be expected to be approached, if the economy approaches an equilibrium at all, will depend on the beliefs that people held at some point in the past. It also depends on the way people have revised their beliefs on the basis of observations since that past date. This is another way of saying that history matters. Model building, statistical tests on data relating to the models, and historical narratives have to work together synergistically if we are to make progress in understanding our social world. Unfortunately, the study of disequilibrium behaviour would lengthen this paper greatly. We shall see though that, fortunately, a study of equilibrium behaviour takes us a long way.

3. CREDIBLE PROMISES We began by observing that mutual trust is the basis of cooperation. In view of the multiplicity of Nash

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Trust and cooperation equilibria and the possible awfulness of equilibria in those social environments where a cooperative infrastructure is absent, we look for environments in which cooperation is possible. To do that, it proves useful to classify the social environments in which the promises people make to one another are credible. Five come to mind (Dasgupta 2000, 2005, 2007).2 (a) Mutual affection Promises would be credible if the parties care about one another sufficiently. Innumerable transactions take place only because the people involved care about one another and rationally believe that they care about one another (each knows that the others know that they care about one another, each knows that the others know that each knows that they care about one another and so on) and thus trust one another to carry out their obligations. The household best exemplifies institutions based on care and affection. (The corresponding notion in evolutionary biology is ‘kin selection’ (Hamilton 1964). Humans of course do not confine their affection to their kin.) Because people who cohabit are able to observe and know one another, they can be sanguine that members will not be unduly opportunistic. The problem is that, being few in number, members of a household, as a group, are unable to engage in those enterprises that require large numbers of people of varied talents and locations. That is why mutual affection is not the basis of cooperation in most other contexts. (b) Pro-social disposition Promises would be credible if it was common knowledge that those making the promises were trustworthy or that they reciprocated by keeping their promise if others displayed trust in them. The new behavioural economics emphasizes this aspect of human character (e.g. Rabin 1993; Fehr & Fischbacher 2002). Nature and nurture play a still little-understood combined role in developing in us a general disposition to reciprocate (Hinde & Groebel 1991; Ehrlich 2000). Our capacity to have such feelings as shame, affection, anger, elation, obligation, benevolence and jealousy would appear to have emerged under selection pressure. No doubt culture helps to shape preferences, expectations and thus, behaviour, which are known to differ widely across societies. But cultural coordinates enable us to identify the locus of points upon which shame, affection, anger, elation, obligation, benevolence and jealousy are put to work; they do not displace the centrality of those capacities in the human make-up. The thought I am pursuing here is that as adults we not only have a disposition for such behaviour as paying our dues, helping others at some cost to ourselves and returning a favour, we also practise norms such as those that prescribe that we punish those who have hurt us intentionally, and even such higher order norms as shunning those who break agreements, on occasion frowning on those who socialize with people who have broken agreements and so forth. Often enough, the disposition to be honest would be towards members of some particular group, not others. This Phil. Trans. R. Soc. B (2009)

P. Dasgupta

3303

amounts to group loyalty. The underlying group could be one’s neighbours or clan or nation. The glue that binds could also be religion or ethnicity (Ehrlich 2000 has an excellent discussion on these matters). By internalizing specific norms, persons enable the springs of their actions to include them. They therefore feels shame or guilt in violating the norm, and this prevents them from doing so, or at the very least it puts a break on them, unless other considerations are found by them to be overriding. In short, their upbringing ensures that they have a disposition to obey the norm, be it moral or social. When they do violate it, neither guilt nor shame would typically be absent, but frequently the act will have been rationalized by them. For such persons, making a promise is a commitment, and it is essential for them that others recognize it to be so (Arrow 1974). Although trustworthiness is not alien to human nature, people do not have their inherent trustworthiness stamped on their forehead. So they cannot be expected to know in advance whom to trust. In any event, if relative to the gravity of the misdemeanour the pecuniary benefits of opportunistic behaviour were high, transgression could be expected. The problem is that one would not know in advance who would be likely to transgress. Punishment assumes its role as deterrence because of these agency problems. As someone’s trustworthiness is not publicly observable, punishment is usually tailored to the ‘crime’. In the next section, we study the remaining three contexts in which people are able to trust one another to keep their promises. We will confirm that, by looking into someone’s personal history, it becomes possible to tailor punishment not only to the crime, but also their past behaviour and circumstances.

4. INCENTIVES TO KEEP PROMISES The promises the parties have made to one another to keep to their agreement would be credible if they could devise an institution in which keeping promises would be in the interest of each party if everyone else were to keep them. The problem therefore is to devise an institution in which keeping to the agreement is a Nash equilibrium. Recall that a strategy is a sequence of conditional actions. Strategies assume the forms, ‘I shall choose X if you choose Y’ or ‘I shall do P if Q occurs’ and so on. If promises are to be credible, it must be in the interest of those making promises to carry them out if and when the relevant occasions arise. Societies everywhere have constructed solutions to the credibility problem, but in different ways. What all solutions have in common, however, is the imposition of collective sanctions on those who intentionally do not comply with agreements. Of course, a credible threat of punishment for misdemeanours would be an effective deterrence only if future costs and benefits are not discounted at too high a rate relative to other parameters of the social environment, a matter to which I return presently. Broadly speaking, there are three types of situation where parties to an agreement could expect everyone

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3304

P. Dasgupta Trust and cooperation

to keep to their words. Of course, none may be potent in a particular context, in which case people would find themselves in a hole they cannot easily get out of, and what could have been mutually beneficial agreements will not take place. (The behaviour reported in the Mezzogiorno by Banfield (1958) is an illustration of this possibility.) Each gives rise to a set of institutions that capitalize on its particular features. In practice, of course, the types would be expected to shade into one another, but it pays to study them separately. So, in §4a – c, I assume that the discount rates agents apply to their future costs and benefits are low relative to other parameters of the social environment.

(a) External enforcement It could be that the agreement is translated into an explicit contract and enforced by an established structure of power and authority, that is, an external enforcer. By an external enforcer, I imagine here, for simplicity, the state. (Depending on the social environment, the ‘external enforcer’ could be the tribal chieftain, the warlord, the priest, or the village elders.) Consider that the rules governing transactions in the formal market place are embodied in the law. So markets are supported by a legal structure. Firms, for example, are legal entities. Even when you go to a supermarket, your purchases (paid in cash or by card) involve the law, which provides protection for both parties (the grocer, in case the cash is counterfeit or the card is void; the purchaser, in case the product turns out on inspection to be substandard). The law is enforced by the coercive power of the state. Transactions involve legal contracts backed by an external enforcer, namely, the state. It is because you and the supermarket owner are confident that the state has the ability and willingness to enforce contracts that you and the owner of the supermarket are willing to transact. What is the basis of that confidence? After all, the state apparatus is run by people, which means a further agency problem. In any event, the contemporary world has shown that there are states and there are states. Simply to invoke an external enforcer for solving the credibility problem would not do. For why should the parties trust the state to carry out its tasks in an honest and effective manner? A possible answer is that the government worries about its reputation (§3b). So, for example, a free and inquisitive press in a democracy helps to sober the government into believing that incompetence or malfeasance would mean an end to its rule when the time comes for the next election. Because voters know that the government worries, they trust their government to enforce agreements. Even if senior members of the ruling party are getting on in years and do not much care what happens in the future, younger members would worry that the party’s reputation would suffer if the government were not to behave. The above argument involves a system of interlocking beliefs about one another’s abilities and intentions. Consider that millions of households in many parts of the world trust their government (more or less!) to Phil. Trans. R. Soc. B (2009)

enforce contracts, because they know that government leaders know that not to enforce contracts efficiently would mean being thrown out of office. In their turn, each side of a contract trusts the other not to renege (again, more or less!), because each knows that the other knows that the government can be trusted to enforce contracts and so on. Trust is maintained by the threat of punishment (a fine, a jail term, dismissal or whatever) for anyone who breaks a contract. We are in the realm of equilibrium beliefs, held together by their own bootstraps. Unfortunately, cooperation is not the only possible outcome. Non-cooperation can also be held together by its own bootstrap. At a non-cooperative equilibrium, the parties do not trust one another to keep their promises, because the external enforcer cannot be trusted to enforce agreements. To ask whether cooperation or non-cooperation would prevail is to ask which system of beliefs is adopted by the parties about one another’s intentions. Social systems harbour multiple equilibria. (b) Reputation as capital asset Political parties are not the only entities that view reputation as a capital asset. Individuals and firms view it that way too. Consider someone who does not care what his or her reputation will be after death. Even he or she would care to build a reputation for honest dealing if by doing so he or she could cash in that reputation at the time of retirement. Brand names are an instance of such cases. The person owning the brand name no doubt changes over time, but the name itself remains. Consider a firm whose dishonest behaviour has been exposed. Suppose too that customers deal only with firms that have an unsullied reputation. On retirement, the owner would find no buyer for the firm. If the owners knew that in advance, they may well wish to maintain the firm’s reputation for honesty. If the owners cared sufficiently about their quality of life after retirement, honesty would be an equilibrium strategy, just as boycotting ill-reputed firms would be a corresponding equilibrium strategy for customers (Kreps 1990). Of course, even in situations where reputation can be accumulated as a capital asset, it may be that agents do not accumulate reputations for honesty. It cannot be repeated often enough that social systems possess multiple equilibria. The formal analysis of reputation as capital asset is similar to one where the parties expect to face transaction opportunities repeatedly in the future. Let us study those situations. (c) Long-term relationships Suppose the agents expect to face similar transaction opportunities in each period over an indefinite future. Imagine too that the parties cannot depend on the law of contracts because the nearest courts are far from their residence. There may even be no lawyers in sight. In rural parts of sub-Saharan Africa, for example, much economic life is shaped outside a formal legal system. But even though no external enforcer may be available, people there do transact. Credit involves saying, ‘I lend to you now with your

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Trust and cooperation promise that you will repay me’ and so on. But why should the parties be sanguine that the agreements would not turn sour on account of opportunistic behaviour? They would be sanguine if agreements were mutually enforced. The basic idea is this: a credible threat by members of a community that stiff sanctions would be imposed on anyone who broke an agreement could deter everyone from breaking it. (The corresponding mechanism in evolutionary biology is called ‘reciprocal altruism’; Trivers 1971.) The problem then is to make the threat credible. The solution to the credibility problem in this case is achieved by recourse to social norms of behaviour. By a social norm, we mean a rule of behaviour, or a strategy, that is followed by members of a community. For a rule of behaviour to be a social norm, it must be in the interest of everyone to act in accordance with the rule if all others were to act in accordance with it. Social norms are (Nash) equilibrium rules of behaviour. To see how social norms work, imagine that the gain to a party from breaking the agreement unilaterally during a period is less than the discounted value of the losses she or he would suffer if all other parties were to punish her or him subsequently. The punishment could involve all others refusing to engage in any transactions with the erring party in the following period, shunning her or him for suitable numbers of periods and so on. Call a party ‘conformist’ if she or he cooperates with parties who are conformists but punishes those who are non-conformists. That sounds circular, but it is not, because the social norm we are studying here requires all parties to start the process by keeping their agreement. It would then be possible for any party in any period to determine which party is conformist and which party is not. For example, if ever someone were to break the original agreement, he or she would be judged to be non-conformist; so, the norm would require all parties to punish the non-conformist. Moreover, the norm would require that punishment be inflicted not only upon those in violation of the original agreement (first-order violation), but also upon those who fail to punish those in violation of the agreement (secondorder violation), upon those who fail to punish those who fail to punish those in violation of the agreement (third-order violation) and so on, indefinitely. This infinite chain makes the threat of punishment for errant behaviour credible because, if all others were to conform to the norm, it would not be worth any party’s while to violate the norm. Keeping one’s agreement would then be self-enforcing.3 All traditional societies appear to have sanctions in place for first-order violations. Anthropologists and novelists have noted the use of sanctions for second-order violations. The fact that sanctions against higher order violations have not been documented much may be because they are not needed to be built into social norms if it is commonly recognized that people feel a strong emotional urge to punish those who have broken agreements. Anger facilitates cooperation by making the threat of retaliation credible.4 Phil. Trans. R. Soc. B (2009)

P. Dasgupta

3305

Social norms that are enshrined in the culture of a community depend not only on the character of the agreements themselves, but also on the relative ease with which prospects are expected to arise for opportunistic behaviour. Sanctions can range from the punitive and unforgiving (‘one strike and you are out!’—known in the literature as the ‘grim strategy’), which have been observed in places where tempting short-term outside economic opportunities appear from time to time. However, many rural communities (e.g. in the mountains of Nepal) are like enclaves: they live far from established markets. Adopting ‘grim’ would prove counter-productive there. That is why sanctions there have been found to be graduated: the first misdemeanour is met by a small punishment, subsequent ones by stiffer punishments, persistent ones by punishments that are stiffer still (Ostrom 1992). Where information is imperfect, a small penalty for the first misdemeanour would be warning that others were watching or it could be that others signal their acknowledgement that the misdemeanour could have been an error on the part of the offender and that he should try harder next time. And so on. It can be shown that the scope for cooperation can be increased by tying several agreements (e.g. agreements over the mutual provision of credit, insurance and labour, respectively), so that the norm has it that violation of any one agreement is met by withdrawal of cooperation in all other engagements (Dasgupta 2007). When separate agreements (whether among the same set of individuals or among different groups of individuals) are tied, the long-run benefits of cooperation become larger than the (short-run) gains from defection even at larger values of the rates at which individuals discount their future benefits than they would be if agreements were not tied. So, tying agreements makes cooperation robust against defection. Interestingly, tied relationships are a common feature of traditional societies in the contemporary world (Baland & Platteau 1996). Greif (2006) has argued that tied relationships among Maghreb merchants who were engaged in long-distance trade fuelled economic growth in medieval southern Europe. Unfortunately, even when cooperation is a possible equilibrium, non-cooperation is an equilibrium too. To see why, imagine that each party believes that all others will renege on the agreement. It would then be in each one’s interest to renege at once, meaning that there would be no cooperation. Failure to cooperate could be due simply to an unfortunate pair of self-confirming beliefs, nothing else. No doubt, it is mutual suspicion that ruins their chance to cooperate, but the suspicions are internally self-consistent. In short, even when people do not discount future costs and benefits at a high rate and appropriate institutions are in place to enable people to cooperate, it can be that they do not cooperate. Whether they cooperate depends on mutual beliefs, nothing more. I have known this result for many years, but still find it a surprising and disturbing fact about social life. Remark. In their review of the theoretical literature on the emergence of cooperation and altruism in behavioural ecology and game theory, Lehmann &

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3306

P. Dasgupta Trust and cooperation

Keller (2006) report that the models assume that one or more of the following four conditions need to be fulfilled (provided of course that the benefits of cooperation exceed the short run gains from defection): (i) direct benefits to the individual to the focal individual performing a cooperative act, (ii) direct or indirect information allowing a better than random guess about whether a given individual will behave cooperatively in repeated reciprocal interactions, (iii) preferential interactions between related individuals, and (iv) genetic correlation between genes coding for altruism and phenotypic traits that can be identified. Notice that (i) is pre-supposed in the latter four social environments in our five-way classification, (ii) is involved in all five of our social environments (but, obviously, in different manners), while (iii) and (iv) are implicit in, respectively, the first and second social environments in our five-way classification.

5. DARK MATTERS: BREAKDOWN OF COOPERATION We have so far assumed that the discount rates people apply to their future gains and losses are small. It is, of course, obvious that if the rates were large, cooperation would not be possible (the present discounted value of the flow of future private benefits of cooperation would fall short of the short-term gains from defection). So we now have in hand a tool to explain how a community where members have been cooperating can skid to a state of affairs where they cease to cooperate. Ecological stress (caused, for example, by high population growth and prolonged droughts) often leads people to fight over land and natural resources (Homer-Dixon 1999; Diamond 2005). More generally, political instability (in the extreme, civil war) would be a reason why people discount the future benefits of cooperation at a high rate, if for no other reason than a heightened fear that their community will not survive in its present shape. For whatever reason, if discount rates were to increase sufficiently relative to the parameters characterizing the social environment, cooperation would cease. Mathematicians call the points at which those switches occur ‘bifurcations’, sociologists call them ‘tipping points’. Social norms work only when people have reasons to value the future benefits of cooperation. Contemporary examples illustrate this. Local institutions have been observed to deteriorate in the unsettled regions of sub-Saharan Africa. Communal management systems that once protected Sahelian forests from unsustainable use were destroyed by governments keen to establish their authority over rural people. But Sahelian officials had no expertise at forestry, nor did they have the resources to observe who took what from the forests. Many were corrupt. Rural communities were unable to switch from communal governance to governance based on the law: the former was destroyed and the latter did not really get going. The collective vacuum has had a terrible impact on people whose lives had been built round their forests and woodlands (Dasgupta in press). Ominously, there are subtler pathways by which societies can tip from a state of mutual trust to one Phil. Trans. R. Soc. B (2009)

of mutual distrust. We have seen that when discount rates are low, both cooperation and non-cooperation are equilibrium outcomes. So, a society could tip over from cooperation to non-cooperation simply because of a change in beliefs. The tipping may have nothing to do with any discernable change in circumstances; the entire shift in behaviour could be triggered in people’s minds. The switch could occur quickly and unexpectedly, which is why it would be impossible to predict and why it would cause surprise and dismay. People who woke up in the morning as friends would discover at noon that they are at war with one another. Of course, in practice, there are usually cues to be found. False rumours and propaganda create pathways by which people’s beliefs can so alter that they tip a society where people trust one another to one where they do not. The reverse can happen too, but it takes a lot longer. Rebuilding a community that was previously racked by civil strife involves building trust. Noncooperation does not require as much coordination as cooperation does. Not to cooperate usually means to withdraw. To cooperate, people must not only trust one another to do so, they must also coordinate on a social norm that everyone understands. That is why it is a lot easier to destroy a society than to build it. How does an increase or decrease in cooperation translate into macroeconomic performance? Consider two communities that are identical in all respects, excepting that in one people have coordinated at an equilibrium state of affairs where they trust one another, while people in the other have coordinated at an equilibrium where they do not trust one another. The difference between the two economies would be reflected in the productivity of their assets, which would be higher in the community where people trust one another than in the one where they do not. Enjoying greater incomes, individuals in the former economy are able to put aside more of their income to accumulate capital assets, other things being equal. So it would become relatively wealthier. Mutual trust would be interpreted from the statistics as a driver of economic growth, but the statistics would not reveal how that trust was created and maintained.

6. MORE DARK MATTER: EXPLOITATION IN LONG-TERM RELATIONSHIPS Both theory and empirics tell us that cooperation can harbour inequality (see Dasgupta in press for a review). Unhappily, it can also harbour exploitation, a far worse state of affairs. We began by considering a group of people who have not only discovered a mutually beneficial course of actions, but have also agreed to follow that course. We identified circumstances in which people would be able to enter long-term relationships in which they would trust one another to do what they are required to under the terms of the agreement. In studying long-term relationships, we assumed that all who enter them benefit (although not perhaps equally). I now want to show that long-term relationships can be bad for

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Trust and cooperation some members of a cooperative; in that there are circumstances where some people are worse off being part of a long-term relationship than they would have been if a long-term relationship had not been entered into. If that sounds implausible, it may be because in studying cooperation and the benefits that accrue from it, we are used to drawing on the PD game. Indeed, the PD game has been used almost universally to illustrate the problem of collective action people face in producing public goods (e.g. flood barriers) or managing common property resources (CPRs) (e.g. local woodlands). However, societal problems involving the production of public goods and the management of CPRs are not reflected in the PD game (Dasgupta & Heal 1979; Dasgupta 2008). To see why, recall that the PD game, when played once, has two distinguishing features: (i) every agent has a dominant strategy, that is, a strategy that is best for her no matter what strategies are chosen by the others and (ii) there is a set of strategies, one for each agent, which, if it were chosen, would lead to an outcome that is better for all than the outcome that is obtained when each agent plays her dominant strategy. In the absence of a cooperative infrastructure, agents would choose their dominant strategies. So, the dominant strategies constitute the unique Nash equilibrium. Moreover the equilibrium is collectively suboptimal. That is the dilemma. Recall from the theory of games that an agent’s min – max payoff is the payoff she can guarantee for herself even if all others were bent on making her life as miserable as possible. The reason we are interested in the concept of min – max payoffs in the present context is that in the PD game agents receive their min – max payoffs when they play their dominant strategies. So, at the unique Nash equilibrium of the PD game, agents’ payoffs are their min – max payoffs. Dasgupta & Heal (1979, ch. 3) showed that in the absence of a cooperative infrastructure, the production of public goods and the management of CPRs involve games in which (the unique) Nash equilibrium is indeed collectively suboptimal; but the authors also showed that agents’ equilibrium payoffs are not their min – max payoffs. This means that in public-goods games and CPR games, there is a gap between the equilibrium payoff of an agent and her min – max payoff: ‘the former exceeds the latter’. Now consider a long-term relationship among people engaged in the management of a CPR. Suppose the social norm they use in order to maintain cooperation instructs members to punish non-conformists by pushing them down to their min – max payoffs for a suitable number of periods. Using results from the theory of repeated games (e.g. Mailath & Samuelson 2006), Dasgupta (2000, 2008) showed that if the agents discount their future payoffs at a low enough rate, such a norm would support outcomes in which the payoffs over time to some agents are less than their respective Nash equilibrium payoffs, but in excess of their min – max payoffs. Those unfortunate agents accept the conditions of the long-term relationship only because not to do so would mean that they are driven down to their min – max payoffs for an extended Phil. Trans. R. Soc. B (2009)

P. Dasgupta

3307

period of time. Plainly, those agents would have been better off if there had been no long-term relationship. This is the sense in which cooperation can involve exploitation. Thus far, theory. Unearthing exploitation from data will prove to be fiendishly difficult, because they would involve answering a counterfactual question: what would life have been like for those who are suspected of being exploited had long-term relationships not been entered into? Nevertheless, there are informal grounds for thinking that long-term relationships can give rise to exploitation. Under the caste system in India, for example, ‘untouchables’ in rural areas are frequently barred from drawing water from the village well, whose use is restricted to caste Hindus. And there are many other similar restrictions on untouchables besides. To be sure, untouchables are members of the village community, but each group has its assigned role. Can one prove that untouchables are exploited in village India, in the precise sense in which I am using the term? Probably not, but the theory I am appealing to is suggestive. And that is a virtue of the theory.

7. INTERNATIONAL COOPERATION Several of the pre-conditions for cooperation would be found to be missing if we consider the prospects of international cooperation in the management of global public goods (e.g. the global climate). In §§2–4, we assumed that the parties have discovered a mutually advantageous course of actions and have reached an agreement over the way the costs and benefits are to be shared. Sadly, that cannot be assumed in the international context. Consider international negotiations over climate change. Nations (by which, of course, I mean national leaders) differ greatly in their assessment of the costs and benefits to them from continuing increases in carbon concentration: some nations are small, while others are large; some are rich, while others are poor; some are in the tropics, others in temperate zones; some are governed by leaders who take science seriously, others are less fortunate; and so on. Side payments would be needed if all nations were to sign a treaty, but the promise of such payments may not be credible. For a treaty to be believable, it must be self-enforcing. Among the possible outcomes of international negotiations over climate change is the ‘null treaty’, meaning global non-cooperation, commonly referred to as ‘business as usual’. Moreover, it can be that the negotiations harbour more than one self-enforcing treaty. Treaties would differ in their efficiency and in the distribution of benefits and burdens among nations. Carraro (2002), Barrett (2003) and Dutta & Radner (2004), among others, have shown that not all countries should be expected to sign a potential treaty on climate change. Some (among them many small countries) would free ride. Among the choices to be made in designing a treaty are adaptation and mitigation measures. The costs and benefits involving the two kinds of investment would be expected to differ among countries. So, economists who study the political economy of climate change face the

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

3308

P. Dasgupta Trust and cooperation

problem of having to explain which equilibrium would be selected. Factors outside theoretical models would be particularly relevant here. The power of rich countries could be expected to tilt the selection towards their favour. As the Kyoto Protocol did not lay the groundwork for a self-enforcing treaty on climate change (Barrett 2003; Dutta & Radner 2004), it has been a failure. On the other hand, the Montreal Protocol on the emission of chlorofluorocarbons (CFCs) has been a success. Why? Barrett (2003) has argued that if, relative to the costs of curbing emissions, the perceived benefits are large, it is possible for large numbers of nations to reach an agreement. In effect, very little in the way of side-payments needs to be made in order for signatories to enjoy the benefits. This was the case with curbing CFCs. Carbon emissions are a problem of a different order of magnitude. The costs of controlling emissions to any significant degree are huge, while the benefits of controlling them are likely to be diffuse. Unlike radiation arriving through holes in the Ozone layer, global climate change does not kill people in a direct, identifiable and immediate way. It is easy to go into denial over climate change. Barrett (2008) observes that although in discussions on global climate change it is frequently claimed that adaptation and mitigation are complementary activities, they are more like substitutes. As countries invest more in the former, they suffer less from climate change and find mitigation less attractive. But mitigation is a global public good (‘windmills’), whereas adaptation is a national public good (‘dikes’). One can imagine a situation where the globally optimal investment policy would have every country invest in windmills, but where under non-cooperation each nation constructs only dikes. Imagine that the ideal international treaty (with appropriate, credible side payments) sustains a high level of participation and requires so many windmills to be built that no one needs to construct dikes. Barrett constructs examples where, nevertheless, the treaties that are signed are ones under which rich countries construct dikes and pollute the atmosphere, leaving poor countries not so much high and dry, as ‘low and wet’. Such an ominous possibility cannot yet be ruled out.

8. CONCLUSIONS In this article, I have identified five social environments where cooperation is possible. They range from environments where people care about one another to those where people are to a greater or lesser extent self-seeking but laws and/or social norms are in place to make cooperation self-enforcing. The bad news is that in all but the social environment where the fact that people care about one another is common knowledge, non-cooperation is also selfenforcing. Societies harbour multiple equilibria. The beliefs people hold about one another and about the way behaviour translates into social consequences would appear to be central to the possibilities of cooperation. Alarmingly, societies can tip from cooperation to conflict because of a mere change in beliefs. Our analysis showed why it is a lot easier for Phil. Trans. R. Soc. B (2009)

a society to destroy itself than to re-build. Creating trust is no easy matter. I have also shown that longterm relationships, which can sustain cooperation, have a dark side to them. They can not only sustain inequality among people engaged in cooperation; they can involve exploitation too. We used our findings on the possibilities of cooperation to explain why international cooperation over the use of global public services, such as the ecological services that are provided by the atmosphere and the stratosphere, has proved to be so uneven: the Montreal Protocol over the emission of CFCs was a success, but the Kyoto Protocol over carbon emissions was a failure. The answer would seem to be that the social infrastructures that are necessary for cooperation are all too fragile in the international sphere. Unlike the Montreal Protocol, the Kyoto Protocol did not form the basis of a self-enforcing treaty. The prospects that humanity will be able to contain carbon concentrations in the atmosphere within reasonable limits are not large. I am grateful to the referees for their suggestions on an earlier draft of the paper and to Kenneth Arrow, Scott Barrett, Patrick Bateson, Paul Ehrlich and Robert Hinde for discussions over the years on the matter of trust.

ENDNOTES 1

Fudenberg & Levine (1998) and Evans & Honkapohja (2001) are key theoretical treatises on the evolution of beliefs in social systems. Axelrod & Hamilton (1981) and Nowak (2006) offer the evolutionary biologist’s account of the emergence of cooperation in animal populations. Beliefs play no role there. 2 The five-way classification that follows does not presume that the social environments in question are distinct. For example, mutual affection, pro-social disposition, reputation and mutual enforcement (see below in the text) overlap in many contexts. I offer the classification nonetheless because, for conceptual purposes, it is useful to regard them as distinct. Lehmann & Keller (2006) have offered a related classification in evolutionary biology. I remark on their work below in the text. 3 The literature on repeated games is huge. Mailath & Samuelson (2006) is the definitive treatise on the subject and contains a comprehensive list of references to original papers. 4 On a riverboat ride in Australia’s Kakadu National Park some years ago, my wife and I were informed by the guide, a young Aborigine, that his tribe traditionally practiced a form of punishment that involved spearing the thigh muscle of the errant party. When I asked him what would happen if the party obliged to spear an errant party were to balk at doing so, the young man’s reply was that he in turn would have been speared. When I asked him what would happen if the person obliged to spear the latter miscreant were to balk, he replied that he too would have been speared! I asked him if the chain he was describing would go on indefinitely. Our guide said he didn’t know what I meant by ‘indefinitely’, but as far as he knew, there was no end to the chain.

REFERENCES Arrow, K. J. 1974 The limits of organization. New York, NY: W.W. Norton. Axelrod, R. & Hamilton, W. D. 1981 The evolution of cooperation. Science 211, 1390–1396. (doi:10.1126/ science.7466396) Baland, J.-M. & Platteau, P. 1996 Halting degradation of natural resources: is there a role for rural communities? Oxford, UK: Clarendon Press. Banfield, E. 1958 The moral basis of a backward society. Chicago, IL: Free Press.

Downloaded from rstb.royalsocietypublishing.org on October 31, 2010

Trust and cooperation Barrett, S. 2003 Environment & statecraft: the strategy of environmental treaty-making. New York, NY: Oxford University Press. Barrett, S. 2008 Dikes vs. windmills: climate treatise and adaptation. Discussion Paper, The Johns Hopkins University. Binmore, K. & Dasgupta, P. 1986 Game theory: a survey. In Economic environments as games (eds K. Binmore & P. Dasgupta), pp. 1 –48. Oxford, UK: Basil Blackwell. Carraro, C. 2002 Climate change policy: models, controversies, and strategies. In The international yearbook of environmental and resource economics 2002/2003 (eds T. Tietenberg & H. Folmer), pp. 1 –65. Cheltenham, UK: Edward Elgar. Dasgupta, P. 2000 Economic progress and the idea of social capital. In Social capital: a multifaceted perspective (eds P. Dasgupta & I. Serageldin), pp. 325–424. Washington, DC: World Bank. Dasgupta, P. 2005 The economics of social capital. Econ. Rec. 81(Suppl. 255), S2 –S21. (doi:10.1111/j.14754932.2005.00245.x) Dasgupta, P. 2007 Economics: a very short introduction. Oxford, UK: Oxford University Press. Dasgupta, P. 2008 Common property resources: economic analytics. In Promise, trust, and evolution: managing the commons of South Asia (eds R. Ghate, N. S. Jodha & P. Mukhopadhyay), pp. 19–51. Oxford, UK: Oxford University Press. Dasgupta, P. In press. The role of nature in economic development. In Handbook of development economics, vol. 5 (eds D. Rodrik & M. Rosenzweig). Amsterdam, The Netherlands: North Holland. Dasgupta, P. & Heal, G. 1979 Economic theory and exhaustible resources. Cambridge, UK: Cambridge University Press. Diamond, J. 2005 Collapse: how societies choose to fail or survive. London, UK: Allen Lane. Dutta, P. K. & Radner, R. 2004 Self-enforcing climate change treatise. Proc. Natl Acad. Sci. USA 101, 5174– 5179. (doi:10.1073/pnas.0400489101) Ehrlich, P. R. 2000 Human natures: genes, culture, and the human prospect. Washington, DC: Island Press. Evans, G. W. & Honkapohja, S. 2001 Learning and expectations in macroeconomics. Princeton, NJ: Princeton University Press. Fehr, E. & Fischbacher, U. 2002 Why social preferences matter: the impact of non-selfish motives on competition,

Phil. Trans. R. Soc. B (2009)

P. Dasgupta

3309

cooperation and incentives. Econ. J. 112, C1–C33. (doi:10.1111/1468-0297.00027) Fudenberg, D. & Levine, D. K. 1998 The theory of learning in games. Cambridge, MA: MIT Press. Greif, A. 2006 Institutions and the path to the modern economy: lessons from medieval trade. New York, NY: Cambridge University Press. Hamilton, W. D. 1964 The general evolution of social behavior. J. Theor. Biol. 7, 1–55. (doi:10.1016/00225193(64)90038-4) Hinde, R. A. & Groebel, J. (eds) 1991 Cooperation and prosocial behaviour. Cambridge, UK: Cambridge University Press. Homer-Dixon, T. E. 1999 Environment, scarcity, and violence. Princeton, NJ: Princeton University Press. Kreps, D. 1990 Corporate culture and economic theory. In Perspectives on positive political economy (eds J. E. Alt & K. A. Shepsle), pp. 90–143. New York, NY: Cambridge University Press. Lehmann, L. & Keller, L. 2006 The evolution of cooperation and altruism: a general framework and classification of models. J. Evol. Biol. 19, 1365– 1378. (doi:10. 1111/j.1420-9101.2006.01119.x) Mailath, G. & Samuelson, L. 2006 Repeated games and reputation: long-run relationships. New York, NY: Oxford University Press. Maynard Smith, J. S. 1982 Evolution and the theory of games. Cambridge, UK: Cambridge University Press. Nash, J. F. 1950 Equilibrium points in N-person games. Proc. Natl Acad. Sci. USA 36, 48–49. (doi:10.1073/ pnas.36.1.48) Nowak, M. A. 2006 Evolutionary dynamics: exploring the equations of life. Cambridge, MA: The Belkamps Press. Osborne, M. J. 2004 An introduction to game theory. New York. NY: Oxford University Press. Ostrom, E. 1990 Governing the commons: the evolution of institutions for collective action. Cambridge, UK: Cambridge University Press. Ostrom, E. 1992 Crafting institutions for self-governing irrigation systems. San Francisco, CA: International Center for Self-Governance Press. Rabin, M. 1993 Incorporating fairness into game theory and economics. Am. Econ. Rev. 83, 1281– 1302. Trivers, R. L. 1971 The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57. (doi:10.1086/406755)

RSTB_364_1533_Cover.qxd

09/26/09

12:15 PM

Page 2

GUIDANCE FOR AUTHORS

Editor Professor Georgina Mace Publishing Editor Claire Rawlinson Editorial Board Neuroscience and Cognition Dr Brian Billups Dr Andrew Glennerster Professor Bill Harris Professor Trevor Lamb Professor Obaid Siddiqi Professor Andrew Whiten Cell and developmental biology Professor Julie Ahringer Dr Buzz Baum Dr Louise Cramer Dr Anne Donaldson Professor Richard Gardner Professor John Gray Professor Keith Gull Professor Laurence Hurst Professor Fotis Kafatos Professor Elliot Meyerowitz Dr Tanja van Mourik Publishing Editor: Claire Rawlinson (tel: +44 (0)20 7451 2602; fax: +44 (0)20 7976 1837; [email protected])

Production Editor: Jessica Mnatzaganian

6–9 Carlton House Terrace, London SW1Y 5AG, UK rstb.royalsocietypublishing.org

Professor Anthony Pawson Dr Stephen Tucker Organismal, environmental and evolutionary biology Dr Will Cresswell Professor Georgina Mace Professor Yadvinder Malhi Professor Manfred Milinski Professor Peter Mumby Professor Peter Raven Professor Karl Sigmund Professor Monkombu Swaminathan Health and Disease Professor Zhu Chen Professor Mark Enright Professor Peter Goodfellow Professor Michael Malim Professor Lap-Chee Tsui Professor Nicholas Wald Professor Joanne Webster

Selection criteria The criteria for selection are scientific excellence, originality and interest across disciplines within biology. The Editors are responsible for all editorial decisions and they make these decisions based on the reports received from the referees and/or Editorial Board members. Many more good proposals and articles are submitted to us than we have space to print, we give preference to those that are of broad interest and of high scientific quality. Publishing format Phil. Trans. R. Soc. B articles are published regularly online and in print issues twice a month. Along with all Royal Society journals, we are committed to archiving and providing perpetual access. The journal also offers the facility for including Electronic Supplementary Material (ESM) to papers. Contents of the ESM might include details of methods, derivations of equations, large tables of data, DNA sequences and computer programs. However, the printed version must include enough detail

Conditions of publication Articles must not have been published previously, nor be under consideration for publication elsewhere. The main findings of the article should not have been reported in the mass media. Like many journals, Phil. Trans. R. Soc. B employs a strict embargo policy where the reporting of a scientific article by the media is embargoed until a specific time. The Executive Editor has final authority in all matters relating to publication.

Electronic Submission details For full submission guidelines and access to all journal content please visit the Phil. Trans. R. Soc. B website at rstb.royalsocietypublishing.org.

AIMS AND SCOPE Each issue of Phil. Trans. R. Soc. B is devoted to a specific area of the biological sciences. This area will define a research frontier that is advancing rapidly, often bridging traditional disciplines. Phil. Trans. R. Soc. B is essential reading for scientists working across the biological sciences. In particular, the journal is focused on the following four cluster areas: neuroscience and cognition; organismal and evolutionary biology; cell and developmental biology; and health and disease. As well as theme issues, the journal publishes papers from the Royal Society’s biological discussion meetings. For information on submitting a proposal for a theme issue, consult the journal‘s website at rstb.royalsocietypublishing.org. Reviews. The journal also publishes reviews in the broad areas of research listed above. Review articles will often be commissioned, but the Editor is happy to consider suggestions / proposals for unsolicited review articles. Please submit an abstract and a covering letter to the Editorial Office for approval for consideration. 6000 words is usually a maximum length for reviews.

The Royal Society is an independent scientific academy founded in 1660 and self-governing under Royal Charter. The Society has three roles, as the scientific academy of the United Kingdom, as a learned society, as a funding body. The objectives of the Royal Society are to

• recognise excellence in science • support leading-edge scientific research and its applications

ISBN: 978-0-85403-780-3

Copyright © 2009 The Royal Society

• stimulate international interaction

Except as otherwise permitted under the Copyright, Designs and Patents Act, 1988, this publication may only be reproduced, stored or transmitted, in any form or by any other means, with the prior permission in writing of the publisher, or in the case of reprographic reproduction, in accordance with the terms of a licence issued by the Copyright Licensing Agency. In particular, the Society permits the making of a single photocopy of an article from this issue (under Sections 29 and 38 of this Act) for an individual for the purposes of research or private study.

• further the role of science, engineering

SUBSCRIPTIONS In 2010 Phil. Trans. R. Soc. B (ISSN 0962-8436) will be published twice a month. Full details of subscriptions and single issue sales may be obtained either by contacting our journal fulfilment agent, Portland Customer Services, Commerce Way, Colchester CO2 8HP; tel: +44 (0)1206 796351; fax: +44 (0)1206 799331; email: [email protected] or by visiting our website at http://royalsocietypublishing.org/info/subscriptions. The Royal Society is a Registered Charity No. 207043.

to satisfy most non-specialist readers. Supplementary data up to 10Mb is placed on the Society's website free of charge. Larger datasets must be deposited in recognised public domain databases by the author.

• promote the public’s understanding of science • provide independent authoritative advice on • encourage research into the history of science

printed version plus electronic access

Europe

USA & Canada

All other countries

£2145/€2788

$4058

£2317/US$4153

Typeset in India by Techset Composition Limited, Salisbury, UK. Printed by Latimer Trend, Plymouth. This paper meets the requirements of ISO 9706:1994(E) and ANSI/NISO Z39.48-1992 (Permanence of Paper) effective with volume 335, issue 1273, 1992. Philosophical Transactions of the Royal Society B (ISSN: 0962-8436) is published twice a month for $4058 per year by the Royal Society, and is distributed in the USA by Pitney Bowes International Mailing Services Inc. as mailing agent. Periodicals postage paid at Kearny, NJ. and additional mailing offices. POSTMASTER: Send address changes to PB International Mailing Services Inc. 500 US Hwy 46, Clifton, NJ, 07011.

Research Support (UK grants and fellowships) Research appointments: 2547 Research grants: 2539 Conference grants: 2540 Science Advice General enquiries: 2585 Science Communication General enquiries: 2572

and technology in society

matters relating to science, engineering and technology

Subscription prices 2010 calendar year

For further information on the Society’s activities, please contact the following departments on the extensions listed by dialling +44 (0)20 7839 5561, or visit the Society’s Web site (www.royalsociety.org).

International Exchanges (for grants enabling research visits between the UK and most other countries (except the USA)) General enquiries: 2550 Library and Information Services Library/archive enquiries: 2606

Cover image: Cooperation in micro-organisms. Clockwise from top left: A cooperating swarm of Pseudomonas aeruginosa cells (left) envelops a group of non-cooperating cheats. (Image courtesy of Edgar Lissel and Stephen Diggle.) Guards at the nest entrance of the neotropical bee Tetragonisca angustula, known in Brazil as Jatai. Jatai is unique in having both standing (shown) and hovering guards. Hovering guards detect intruders of different species, by their different colour or volatile odour. Standing guards detect intruders from other Jatai colonies. (Photo courtesy of F. Ratnieks.) Pied babblers (Turdoides bicolor) live in stable groups of 5–10 consisting of a single breeding pair and natal helpers of both sexes that assist in rearing their young. (Image courtesy of T. H. Clutton-Brock.) Cooperative breeding also occurs in a number of mammals. Meerkats (Suricata suricatta) live in groups of 5–50, consisting of a single dominant individual of each sex and a variable number of helpers of both sexes that contribute to rearing their offspring. Dominants are the parents of most juveniles born in the group and subordinate females rarely breed successfully. Field studies show that breeding success rises with helper number. (Image courtesy of T. H. Clutton-Brock.) Allo-grooming in Barbary macaques (Macaca sylvanus) plays an important role in maintaining relationships between non-kin as well as between kin. (Image courtesy of Robert Foley.) Human societies differ from those of most other animals in regularly involving cooperative behaviour between unrelated individuals maintained by cultural norms. (Image courtesy of Mehdi Moussaïd and Simon Gariner from Proceedings of the Royal Society B 2009;276: 2755–2762, doi:10.1098/rspb.2009.0405.)

Neuroeconomics (Philosophical Transactions of the Royal Society series B)

The Neurobiology of Social Recognition, Attraction and Bonding (Philosophical Transactions of the Royal Society series B)

Mechanisms and Functions of Brain and Behavioural Asymmetries (Philosophical Transactions of the Royal Society series B)

Predictions in the brain: using our past to prepare for the future (Philosophical Transactions of the Royal Society series B)

The Nature of Mathematical Proof (Philosophical Transactions of the Royal Society A)

Scientific Discourse in Sociohistorical Context: The Philosophical Transactions of the Royal Society of London, 1675-1975 (Rhetoric, Knowledge, and Society)

Evolution of Society (Philosophical Transactions of the Royal Society series B)

Neuroeconomics (Philosophical Transactions of the Royal Society series B)

Cultural Transmission and the Evolution of Human Behaviour (Philosophical Transactions of the Royal Society series B)

Evolution and Human Behavioural Diversity (Philosophical Transactions of the Royal Society series B)

Cooperation and Deception: From Evolution to Mechanisms (Philosophical Transactions of the Royal Society series B)

The Neurobiology of Social Recognition, Attraction and Bonding (Philosophical Transactions of the Royal Society series B)

Mechanisms and Functions of Brain and Behavioural Asymmetries (Philosophical Transactions of the Royal Society series B)

Rationality and Emotions (Philosophical Transactions of the Royal Society series B)

Culture Evolves (Philosophical Transactions of the Royal Society series B) issue 1567

Transactions of the American Philosophical Society

Group decision making in humans and animals (Philosophical Transactions of the Royal Society series B)

Cultural and Linguistic Diversity: Evolutionary Approaches (Philosophical Transactions of the Royal Society series B)

The Sapient Mind: Archaeology Meets Neuroscience (Philosophical Transactions of the Royal Society B)

Social intelligence: from brain to culture (Philosophical Transactions of the Royal Society B)

Predictions in the brain: using our past to prepare for the future (Philosophical Transactions of the Royal Society series B)

The Nature of Mathematical Proof (Philosophical Transactions of the Royal Society A)

Babylonian Horoscopes (Transactions of the American Philosophical Society)

Isaiah Berlin's Counter-Enlightenment (Transactions of the American Philosophical Society)

Scientific Discourse in Sociohistorical Context: The Philosophical Transactions of the Royal Society of London, 1675-1975 (Rhetoric, Knowledge, and Society)

The Logic of Society: A Philosophical Study

Communication and the Evolution of Society

Communication and the Evolution of Society

The Society (The Society Series, Book 1)

Royal Entomological Society Book of British Insects

Prehistoric Settlement of the Pacific (Transactions of the American Philosophical Society)

Transactions of the Royal Society of Edinburgh, Volume 6 (Latin Edition)

Aquatic Insects (Royal Entomological Society)

The Science of Bakery Products (Royal Society of Chemistry Paperbacks)

The Evolution Of Talk And The Emergence Of Complex Society

The Society of S

The Future of Society

Evolution of Society (Philosophical Transactions of the Royal Society series B)

Neuroeconomics (Philosophical Transactions of the Royal Society series B)

Cultural Transmission and the Evolution of Human Behaviour (Philosophical Transactions of the Royal Society series B)

Evolution and Human Behavioural Diversity (Philosophical Transactions of the Royal Society series B)

Cooperation and Deception: From Evolution to Mechanisms (Philosophical Transactions of the Royal Society series B)

The Neurobiology of Social Recognition, Attraction and Bonding (Philosophical Transactions of the Royal Society series B)

Mechanisms and Functions of Brain and Behavioural Asymmetries (Philosophical Transactions of the Royal Society series B)

Rationality and Emotions (Philosophical Transactions of the Royal Society series B)

Culture Evolves (Philosophical Transactions of the Royal Society series B) issue 1567

Transactions of the American Philosophical Society

Group decision making in humans and animals (Philosophical Transactions of the Royal Society series B)

Cultural and Linguistic Diversity: Evolutionary Approaches (Philosophical Transactions of the Royal Society series B)

The Sapient Mind: Archaeology Meets Neuroscience (Philosophical Transactions of the Royal Society B)

Social intelligence: from brain to culture (Philosophical Transactions of the Royal Society B)

Predictions in the brain: using our past to prepare for the future (Philosophical Transactions of the Royal Society series B)

The Nature of Mathematical Proof (Philosophical Transactions of the Royal Society A)

Babylonian Horoscopes (Transactions of the American Philosophical Society)

Isaiah Berlin's Counter-Enlightenment (Transactions of the American Philosophical Society)

Scientific Discourse in Sociohistorical Context: The Philosophical Transactions of the Royal Society of London, 1675-1975 (Rhetoric, Knowledge, and Society)

The Logic of Society: A Philosophical Study

Communication and the Evolution of Society

Communication and the Evolution of Society

The Society (The Society Series, Book 1)

Royal Entomological Society Book of British Insects

Prehistoric Settlement of the Pacific (Transactions of the American Philosophical Society)

Transactions of the Royal Society of Edinburgh, Volume 6 (Latin Edition)

Aquatic Insects (Royal Entomological Society)

The Science of Bakery Products (Royal Society of Chemistry Paperbacks)

The Evolution Of Talk And The Emergence Of Complex Society

The Society of S

The Future of Society

Recommend Documents