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Mammal Societies

Tim Clutton-Brock

Department of Zoology

University of Cambridge

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Preface

The core of Darwin's theory of natural selection is the realisation (based on Malthus's demographic projections) that the rate of population increase will inevitably lead to competition between individuals for resources and reproductive opportunities, and that competition will favour individuals that are well adapted to the environments they live in, with the result that their heritable characteristics will increase in future generations. Empirical research on population ecology since Malthus has provided extensive evidence to support Darwin's argument, while research in evolutionary biology and population genetics has confirmed that favourable mutations are likely to spread.

Natural selection adapts animals to the ecological niches that they occupy. Early explorations of animal adaptation mostly examined relationships between anatomical traits and the challenges imposed on different species by their physical environments. More recently, research has documented the impact of the social environment on the selection pressures operating on both sexes and on the evolution of behavioural, physiological and anatomical adaptations. In addition, an increasing range of studies have explored the consequences of contrasts in social organisation and the adaptations they generate for ecological processes within and between species, as well as for other areas of biology, including population genetics, epidemiology and conservation biology.

While there have been excellent reviews of the social behaviour of particular Orders of mammals, there have been few attempts to integrate research across mammalian groups and more extensive reviews of social organisation are available for ants and birds than for mammals. My aim in writing this book was to produce an integrated account of the evolution of mammalian societies within the framework provided by theoretical and empirical research on social evolution. As one of the main reasons for studying animal societies is to provide a general perspective on studies of the evolution of human societies, I particularly wanted to integrate research on primates with studies of other mammalian groups in order to explore the extent to which studies of non-human mammals (including non-primates as well as primates) provide insight into the evolution of hominin societies and human behaviour. Finally, as well as exploring the evolution of variation in the structure and organisation of mammalian societies, I wanted to examine what is known of the consequences of variation in social behaviour and breeding systems for ecological processes.

In contrast to birds, most mammals are polygamous and the structure of mating systems has important effects on the selection pressures operating on females and males and the distribution of sex differences in anatomy, physiology and behaviour. In many mammalian species, different factors determine the distribution of the two sexes: while the need to maintain access to adequate resources and to avoid predation commonly structures the distribution and behaviour of females, selection to maximise access to females often has a more important influence on the distribution and behaviour of males. As a result, although the behaviour of the two sexes coevolves, it is often useful to consider the behaviour of females and males separately. I have consequently organised the book to focus first on the behaviour and reproductive strategies of females and then on those of males. The first chapter provides a brief review of the body of theory relevant to the evolution of social behaviour that has built up over the last 40 years. Chapters 2–9 deal with different aspects of female behaviour in non-human mammals, including sociality, the kinship structure of female groups, mate choice, maternal care, social development, communication and the distribution of competition and cooperation. Subsequently, Chapters 10–16 cover similar topics in males. Chapter 17 then examines the evolution of cooperative breeding systems and Chapter 18 explores the evolution of sex differences in behaviour, physiology and anatomy. Finally, Chapters 19 and 20 provide an introduction to related research on the evolution of breeding systems and social behaviour in hominins and humans.

Acknowledgements

I owe an enormous debt to the large number of people that contributed in different ways to this book. In particular, I am deeply indebted to my wife, Dafila Scott, who has provided continuous support and encouragement; to Katy McAuliffe, who produced syntheses of material for six chapters and comments on others as well as vital encouragement at a time when progress had stalled; and to Penny Roth, who has typed, corrected and retyped all chapters multiple times.

For reading and for generous commenting on drafts that allowed me to improve them, I am grateful to Matt Bell (Chapter 2), Monique Borgerhoff Mulder (Chapters 19 and 20), Andrew Bourke (Chapter 1), Mike Cant (Chapter 17), Alecia Carter (Chapter 6), Ben Dantzer (Chapters 5 and 6), Alan Dixson (Chapter 18), Claudia Feh (Chapter 15), Robert Foley (Chapter 19), Sarah Hrdy (Chapters 9, 19 and 20), Elise Huchard (Chapters 8–11 and 18), Dieter Lukas (Chapters 9, 10 and 14), Katy McAuliffe (Chapters 6 and 20), Karen McComb (Chapter 7), Marta Manser (Chapter 7), Martin Muller (Chapter 16), Ryne Palombit (Chapter 15), Oliver Schülke (Chapter 14), Joan Silk (Chapters 9 and 19), Chuck Snowdon (Chapter 16) and Stuart West (Chapter 1). Any mistakes that remain are, of course, my own. I am also grateful to a large number of people for helping me to locate suitable photographs or for allowing me to use their images.

Dieter Lukas regularly provided relevant papers and useful discussion. In the later stages of production, Bonnie Metherell, Rebecca Stanley, Alex Thompson, Tom Houslay, Gabrielle Davidson, Samantha Leivers and Andrew Szopa-Comley helped me to find photographs and references, and obtain permissions to use images and figures. A large number of colleagues helped me to locate relevant photographs, including Karen Strier, John Hoogland, Carel van Schaik, Tim Caro, Sarah Hrdy, Nigel Bennett, Elise Huchard, Robert Seyfarth, Claudia Fichtel, Dan Rubenstein and Kelvin Matthews. At Wiley-Blackwell, I am grateful to Ward Cooper who originally commissioned the book; to Jolyon Phillips for his meticulous copy-editing; to Kelvin Matthews for his role in organising permissions and in guiding the development of the manuscript; to Kathy Syplywczak for organising the text; and to Emma Strickland for arranging the cover design.

My academic debts extend widely in time and space and I am well aware of how much I owe to my colleagues, collaborators and students. Over the last 35 years while I have been a member of the Zoology Department at Cambridge my work has been supported by the Heads of Department (Gabriel Horn, Pat Bateson, Malcolm Burrows and Michael Akam) and several Departmental Secretaries (including John Andrews, Milly Bodfish and Julian Jacobs). Colleagues on the staff of the Department (including Nick Davies, William Foster, Bill Amos, Andrew Balmford, Bryan Grenfell, Andrea Manica, Claire Spottiswoode and Rebecca Kilner) all contributed in one way or another to its inception and development. So, too, did colleagues at the University of Zurich, where I spent half a year working on the manuscript, including Marta Manser, Barbara Koenig, Gustl Anzenberger and Gerald Kerth.

My debts extend beyond the UK and beyond Europe. For the last 20 years, I have been involved in research on the evolution and ecology of cooperative breeding systems in the southern Kalahari. The late John Skinner and Nigel Bennett have both provided generous help, while Marta Manser has co-directed the meerkat project with me for the last 10 years. Research on meerkats in the Kalahari has involved a substantial number of students, post-docs and collaborators including Christine Drea, Dave Gaynor, Andrew Bateman, Ben Dantzer, Elise Huchard, Alecia Carter, Kirsty MacLeod, Peter Santema, Sinead English, Johanna Nielsen, Raff Mares, Matt Bell, Stu Sharp, Sarah Leclaire, Dom Cram, Constance Dubuc, Ashleigh Griffin, Jack Thorley, Joah Madden, Alex Thornton, Sarah Hodge, Andrew Young, Nobu Kutsukake, Tom Flower, Arpat Ozgul, Julian Drewe, Goran Spong, Neil Jordan, Lynda Sharpe, Andy Russell, Anne Carlson, Pete Brotherton, Andrew MacColl, Michael Scantlebury, Justin O'Riain, Ruth Kansky and Franck Courchamp, as well as a large number of volunteers. Josephine Pemberton and Loeske Kruuk have also been continuously involved.

Over the same period we began work on other cooperative breeders. Rosie Woodroffe, Mike Cant, Jason Gilchrist, Matt Bell and Sarah Hodge joined me to establish and run a long-term comparative study of banded mongooses in Uganda which now continues under Mike Cant's leadership. Markus Zottl, Philippe Vullioud and Jack Thorley joined me to work on Damaraland mole-rats, in conjunction with Nigel Bennett at Pretoria. Amanda Ridley came to work on Arabian babblers in Israel and then, with Nikki Raihani, came to work on pied babblers in the Kalahari. All of these people have left an indelible mark on my research, my thinking – and this book.

So, too, have the large number of students, post-docs and collaborators that worked with me previously on red deer and Soay sheep or on lek-breeding ungulates, including fallow deer, Uganda kob and Kafue lechwe. My involvement with research on red deer began soon after I had finished my PhD in 1972 when, with support and guidance from Roger Short, Gerald Lincoln and John Fletcher, Fiona Guinness and I started a long-term project that continues today under the leadership of Josephine Pemberton and Loeske Kruuk. Over the 38 years that I led the red deer project, many PhD students and post-docs contributed to the development of the work including Fiona Guinness, Steve Albon, Marion Hall, Rosemary Cockerill, Michael Reiss, Robert Gibson, Michael Appleby, Iain Gordon, Chris Thouless, Callan Duck, Glen Iason, Paul Marrow, Tim Coulson, Owen Price, Martin Major, Karen Rose, Karen McComb, Larissa Conradt, Kelly Moyes, Kathreen Ruckstuhl, Josephine Pemberton, Loeske Kruuk and Dan Nussey. The research on red deer on Rum led on to related projects on Soay sheep on St Kilda in collaboration with Peter Jewell, Steve Albon, Josephine Pemberton, Loeske Kruuk, Mick Crawley, Ken Wilson, Frances Gulland, Bryan Grenfell and Ian Stevenson, as well as to research on fallow deer and other lek-breeding ungulates with Andrew Balmford, Mariko Hiraiwa-Hasegawa, Karen McComb, David Green, James Deutsch, Rory Nefdt, Richard Stillman, Marco Apollonio and Bill Sutherland. Some of the results of these projects are described in relevant chapters but whether I have included them or not, all played some role in the development of my perception of mammal societies and their ecological consequences. So, too, did a range of other collaborators and students: Geoff Parker, Michael Taborsky, Petr Komers, Virpi Lummaa, Claudia Feh, Marco Festa-Bianchet, Andrew Illius, Peter Langley, Amanda Vincent, Sigal Balshine, Márcio Ayres, Kavita Isvaran, Anthony Rylands and Peter Kappeler.

It is also a pleasure to thank people who helped me at the beginning of my career and gave me opportunities without which I would never have been able to make progress. As an undergraduate reading anthropology at Cambridge, I was lucky to be supervised by David Pilbeam who kindled my interest in human evolution and primate societies. I remain enormously grateful to Robert Hinde who agreed to take me on as a PhD student despite my lack of formal scientific qualifications, helped me to make the transition from anthropology to zoology, and taught me to tackle academic questions head-on. Like many others in the field, my interest in the causes and consequences of variation in animal societies was stimulated by the work of John Crook at Bristol and David Lack at Oxford. Subsequently, when I moved to the University of Sussex, John Maynard Smith and Paul Harvey introduced me to evolutionary biology and population genetics.

Finally, I am grateful to the bodies that have funded my long-term research projects, including the Natural Environment Research Council and the Biotechnology and Biological Sciences Research Council of the UK, the Newton Trust and the European Research Council. This book was completed as one component of an ERC Advanced Grant (No. 294494) which supported our long-term research on cooperative breeding systems.