The Evolution of Primate Societies available in Paperback
In 1987, the University of Chicago Press published Primate Societies, the standard reference in the field of primate behavior for an entire generation of students and scientists. But in the twenty-five years since its publication, new theories and research techniques for studying the Primate order have been developed, debated, and tested, forcing scientists to revise their understanding of our closest living relatives.
Intended as a sequel to Primate Societies, The Evolution of Primate Societies compiles thirty-one chapters that review the current state of knowledge regarding the behavior of nonhuman primates. Chapters are written by the leading authorities in the field and organized around four major adaptive problems primates face as they strive to grow, maintain themselves, and reproduce in the wild. The inclusion of chapters on the behavior of humans at the end of each major section represents one particularly novel aspect of the book, and it will remind readers what we can learn about ourselves through research on nonhuman primates. The final section highlights some of the innovative and cutting-edge research designed to reveal the similarities and differences between nonhuman and human primate cognition. The Evolution of Primate Societies will be every bit the landmark publication its predecessor has been.
John C. Mitani is the James N. Spuhler Collegiate Professor of Anthropology at the University of Michigan. Josep Call is a senior scientist and director of the Wolfgang Kohler Primate Research Centre at the Max Planck Institute for Evolutionary Anthropology. Peter M. Kappeler is head of the Department of Behavioral Ecology and Sociobiology/Anthropology at the University of Gottingen. Ryne A. Palombit is associate professor of anthropology at Rutgers, the State University of New Jersey. Joan B. Silk is professor in the Department of Anthropology and the Institute for Society and Genetics at the University of California, Los Angeles.
|Publisher:||University of Chicago Press|
|Edition description:||New Edition|
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About the Author
John C. Mitani is the James N. Spuhler Collegiate Professor of Anthropology at the University of Michigan.
Josep Call is a senior scientist and director of the Wölfgang Kohler Primate Research Centre at the Max Planck Institute for Evolutionary Anthropology.
Peter M. Kappeler is head of the Department of Behavioral Ecology and Sociobiology/Anthropology at the University of Göttingen.
Ryne A. Palombit is associate professor of anthropology at Rutgers, the State University of New Jersey.
Joan B. Silk is professor in the Department of Anthropology and the Institute for Society and Genetics at the University of California, Los Angeles.
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The Evolution of Primate Societies
The University of Chicago PressCopyright © 2012 The University of Chicago
All right reserved.
Goals of This Book
The study of nonhuman primates and their behavior generates considerable scientific interest. Anthropologists use information about primates to make inferences about the evolution of our hominin ancestors, while psychologists and biologists study them to glean insights into the behavioral, anatomical, physiological, and genetic factors that make us uniquely human. Most importantly, there are now many primatologists who study primates because they represent a highly diverse and ecologically successful radiation of socially complex mammals with unusual life histories.
For an entire generation of students and scientists, Primate Societies (Smuts et al. 1987) served as the standard reference in the field of primate behavior. But in the 25 years since it was published, much has been learned. New theoretical paradigms to understand the behavioral differences between nonhuman primates and humans have been developed, debated, and tested. Field and laboratory studies of an increasing number of species continue to add to our knowledge of the diversity of adaptations within the Primate order. For example, there has been an explosion of interest in and field research on the strepsirrhine primates, and as a result, we now have a much clearer picture of their behavior. Some of the well known long-term field studies of baboons, macaques, and chimpanzees have amassed quantitative data spanning multiple generations, which are of great value in understanding patterns of life history and behavior. These have now been joined by exemplary studies of species such as mouse lemurs, capuchin monkeys, and muriquis. Experiments conducted with wild and captive animals have furnished novel insights into primate cognition. New methods, such as PCR-enabled DNA sequencing and noninvasive hormonal monitoring, have greatly amplified our understanding of the proximate and ultimate causes of behavior. While data from recent research have sometimes reinforced what we knew 25 years ago, they have also forced us to revise and alter our thinking. And as new findings accumulate, it has become increasingly difficult for researchers inside and outside the discipline to keep abreast of recent advances and to synthesize results across the entire field.
With these issues in mind, The Evolution of Primate Societies compiles 31 chapters that review the current state of our knowledge regarding the behavior of nonhuman primates. Like Primate Societies, this book has the primary goal of providing an up-to-date synthesis that will serve as a standard reference for advanced undergraduates, graduate students, and the diverse community of scientists who are interested in the behavior of our closest living relatives. As the study of primate behavior has grown, it has changed from an inductive, taxon-oriented scientific discipline into a mature problem-oriented one that relies on observations and experiments to test evolutionary hypotheses. As one measure of this change, most chapters in the first major compilation of primate field studies, Primate Behavior: Field Studies of Monkeys and Apes (DeVore 1965), described the behavior of specific taxa (12/18 = 67%). In contrast, the predecessor to this volume, Primate Societies (Smuts et al. 1987) contained considerably fewer (14/40 = 35%). We continue that trend here by minimizing the number of taxon-specific chapters and organizing this volume around a set of four broad adaptive problems primates encounter as they attempt to grow, survive, and reproduce in their natural habitats. In this fashion we move away from descriptions of the behavior of specific taxa, and instead emphasize questions, focus on concepts, and evaluate theory with empirical evidence.
A second goal of this book is to integrate research on nonhuman and human behavior through the inclusion of chapters that specifically address the behavior of the human primate. Primatology is uniquely situated at the interface between the biological and social sciences. A long series of pioneers in the field—Robert Yerkes, Wolfgang Kohler, Ray Carpenter, Kinji Imanishi, David Hamburg, and Sherwood Washburn—recognized that the findings from primate research are of central importance for understanding human behavior. As our closest living relatives, primates provide the standard for defining human uniqueness and inform us about the changes that must have taken place during the course of our own evolution. This logic provided the impetus for some of the earliest field studies of primates, and it continues to act as the intellectual glue that bonds primatology with the social sciences. By illuminating the similarities and differences between humans and our closest living relatives, primate behavioral research still has much to tell us about our place in nature.
Primatology will continue to furnish insights into human behavior only if the field remains firmly rooted within the biological sciences. Major advances in the study of primate behavior during the past 40 years have relied heavily on theoretical and methodological breakthroughs in other areas in biology. For example, the melding of evolution, behavior, and ecology into the new subfield of behavioral ecology in the 1960s and 1970s provided the theoretical rationale for many of the subsequent primate field studies that were summarized in Primate Societies. To maintain their vitality and rigor, modern primate field studies must continue to assimilate recent developments in the biological sciences. An effective dialogue between the two disciplines will have important consequences for the behavioral sciences.
We believe that there has never been a better time for the study of primate behavior to achieve its integrative potential and serve as a unifying force to link its sister disciplines in the social and biological sciences. By synthesizing the findings of primate behavioral research, the chapters in this volume promise to highlight the significance of primatology to several fields, including animal behavior, anthropology, cognitive science, economics, genetics, and psychology.
Contents and Organization of This Book
With the preceding goals in mind, we have divided this book into five parts. Part 1, "Primate Behavioral Diversity," will introduce readers to the animals that constitute the order. Five taxa are considered in chapters on strepsirrhines and tarsiers, platyrrhines, colobines, cercopithecines, and apes. These introductory chapters adhere to a standard format, reviewing the ecology, life history, and social systems of primates in each taxon. The aim is to summarize salient aspects of the behavior of primates across the order. Taken together, these chapters furnish taxon-specific background information for the topical chapters that follow in the rest of the book.
Parts 2 through 5 form the central part of this volume. As noted above, chapters in these sections deal with four adaptive problems primates face in the wild. Part 2, "Surviving and Growing Up in a Difficult and Dangerous World," comprises seven chapters that focus on the ways in which primates respond to ecological challenges, such as finding food and avoiding predators, and how these ecological pressures have shaped the evolution of primate sociality, life history, and development. The penultimate chapter in this section reviews how these same ecological forces, through their effects on sociality, influence the genetic composition of populations; the concluding chapter employs the comparative data furnished by primate studies to evaluate human survival and life history in evolutionary perspective.
Reproduction is the evolutionary currency of import, and part 3, "Mating and Rearing Offspring," comprises eight chapters that deal with this crucial facet of primate life. Chapters in this section examine female and male reproductive strategies, the sources and magnitude of variation in female reproduction and male mating success, female choice, parenting, and sexual conflict in the form of infanticide by males. The final chapter in part 3 reviews aspects of human reproduction, highlighting points of divergence from and convergence with nonhuman primates.
Primates are unusually social animals. As a consequence, they must interact successfully with conspecifics to grow, survive, and reproduce. Part 4, "Getting Along," considers the forces that shape the evolution of primate social behavior and social relationships. Chapters in this section highlight research on the evolution of cooperation between kin and between nonkin, the mechanisms maintaining relationships, the adaptive consequences of social bonds, the nature of social preferences, and human social behavior.
The final part of this book, "Cognitive Strategies for Coping with Life's Challenges," considers how natural selection has shaped the cognitive abilities of primates. Five chapters review how nonhuman primates have evolved cognitive solutions to problems related to ecological challenges, their knowledge of social relations and the minds of others, their communication strategies, and their social learning, traditions, and culture. Like the other parts of the book, this part concludes with a chapter devoted exclusively to humans and the issue of human cognition.
Chapter TwoThe Behavioral Ecology of Strepsirrhines and Tarsiers
Peter M. Kappeler
Phylogenetic analyses of morphological and genetic data unequivocally identify strepsirrhines (Lemuriformes and Lorisiformes) as a monophyletic suborder of Primates (Yoder 1997). Strepsirrhines have sometimes been allied with tarsiers (Tarsiiformes) because of some plesiomorphic traits, but the corresponding taxon Prosimii is clearly paraphyletic (Schmitz et al. 2001; Roos et al. 2004) and should not be used (Fleagle 1999). Instead, tarsiers are grouped with the platyrrhines (New World monkeys) and catarrhines (Old World monkeys, apes, and humans) into the haplorrhines. However, because of some phenotypic convergences between tarsiers and nocturnal strepsirrhines, and because this numerically small primate taxon is still understudied, tarsiers will be treated here together with strepsirrhines rather than in a separate chapter.
Phenotypically, various shared primitive features of the life histories, reproductive biology, and nervous systems of strepsirrhines and tarsiers affect and constrain the way in which these basal primates have adapted to particular ecological and social challenges. An appreciation of these and other characteristic traits is therefore helpful for understanding the socioecological adaptations of these animals. Because the number of studies of the behavioral ecology of these basal primates has increased disproportionally more than that of corresponding studies of anthropoids (monkeys, apes and humans) in the past 25 years (Bearder 1987; Richard 1987), it is no longer possible to provide a complete review. The specific aim of this chapter, therefore, is to summarize selected, relevant facts about strepsirrhine and tarsier diversity, ecology, life history, and social systems to provide taxon-specific background information for the topical reviews constituting the core of this volume.
Diversity and Biogeography
Strepsirrhines and tarsiers make up about a third of all living primates. The lemurs of Madagascar (Lemuriformes) represent the largest group among strepsirrhines. Molecular methods and increased sampling in the field have resulted in a drastic increase in the number of recognized lemur species. While there are doubts about the scientific standards used to identify and describe some new species (Tattersall 2007; Markolf et al. 2011), there is an emerging consensus among taxonomic experts that lemur diversity is much higher than the 20 species recognized during most of the previous century (cf. Richard 1987). Today, there is broad consensus that the living lemurs can be divided into 5 families and 15 genera, with about 100 known species (Mittermeier et al. 2010; table 2.1). In addition, 17 species from an additional 8 genera and 3 families went extinct only during the past 500 to 2,000 years and were clearly part of the contemporary fauna (Godfrey & Jungers 2003). The remains of these animals are so recent that they have not yet fossilized; hence they are referred to as the subfossil lemurs.
Lemurs are endemic to Madagascar. About 150 million years ago, during the breakup of Gondwana, Madagascar was separated from the African mainland. It remained attached to today's Indian subcontinent for about 60 million years. Because molecular methods have estimated the time of the single successful lemur colonization of Madagascar as around 65 to 75 million years ago (Horvath et al. 2008; Matsui et al. 2009), the first lemurs presumably rafted across the Mozambique Channel (Kappeler 2000a; Roos et al. 2004; but see Stankiewicz et al. 2006 for evidence suggesting an Asian origin). Following the early divergence of the ancestral Daubentoniidae, the remaining four lineages with living representatives diverged about 24 to 40 million years ago after the emergence of the first rain forests on Madagascar (Horvath et al. 2008).
Today, lemurs inhabit a wide range of different habitats. Madagascar's north and east are dominated by wet forests, the west is covered by dry deciduous forests, and the arid south is dominated by spiny forests; only the mostly treeless central plateau is largely devoid of lemurs. All major Malagasy rivers have their source in the central highlands. They divide the island into smaller biogeographic regions, which presumably acted as natural barriers for range expansions of many species (Wilmé et al. 2006; Vences et al. 2009). Interestingly, some species have ranges covering almost the length of the island (e.g., the gray mouse lemur, Microcebus murinus; the western fat-tailed dwarf lemur, Cheirogaleus medius), whereas others have some of the smallest known ranges among living primates (e.g., Madame Berthe's mouse lemur, Microcebus berthae; Perrier's sifaka, Propithecus perrieri; the northern sportive lemur, Lepilemur septentrionalis). Accordingly, some lemur species with small remaining ranges are among the most threatened primates.
The Lorisiformes are found in Africa and Asia. Based on morphological and molecular data, two clades can be distinguished at the family level (Roos et al. 2004; Masters et al. 2005). The bush babies, or galagos (Galagidae), are the most diverse members of this monophyletic group, with representatives of five genera found in most suitable habitats of sub-Saharan Africa, ranging from West African rain forest to South African acacia woodlands, including secondary habitats (Nash et al. 1987; Nekaris & Bearder 2007). The true diversity of galagos remains unknown as new taxa continue to be discovered and remain undescribed (Grubb et al. 2003). It is therefore difficult to precisely characterize their geographic ranges and, hence, the ecological success of individual taxa. Some species (e.g., Rondo dwarf galago, Galagoides rondoensis; fig. 2.1) are known to have small, fragmented ranges, however, and are also among the most endangered primates.
Lorises (Lorisidae) are found in both Africa and Asia. One gracile and one robust genus exists on each continent: Arctocebus and Perodicticus in Africa, and Loris and Nycticebus in Asia. They remain poorly studied in the field, so that their exact ranges and local densities are not well known. According to molecular estimates, the Galagidae and Lorisidae separated about 35 million years ago (Matsui et al. 2009). The historical phylogeography of the Lemuriformes and Lorisiformes continues to be debated as additional molecular data and lorisid fossils emerge, along with new information about the relative positions of India and Madagascar during the breakup of Gondwana (Masters et al. 2005; Stevens & Heesy 2006; Ali & Huber 2010).
Tarsiers are an enigmatic group of Southeast Asian primates with a present-day distribution limited to the Indonesian archipelago and Phillippine islands. They are the sole survivors of a much more diverse and widespread group of Eocene tarsiiforms. As with other small nocturnal primates, new species continue to be discovered (Merker & Groves 2006), bringing the current species count to at least 10 (Shekelle et al. 2008; Groves & Shekelle 2010), some of which are separated by remarkably narrow acoustic and genetic boundaries (Merker et al. 2009). Recent analyses of morphometric and genetic data have suggested that a separation into three distinct genera is warranted (Groves & Shekelle 2010). The affiliation of tarsiers with either strepsirrhines or haplorrhines has been the topic of a controversy for more than two centuries (Gursky 2007a), but molecular analyses clearly support the monophyly of the haplor rhines—that is, the anthropoids (New and Old World monkeys, apes, and humans) and tarsiers (Schmitz et al. 2001).
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Table of Contents
Part 1. Primate Behavioral Diversity
Table A.1 Taxonomy of Living Primates
2. The Behavioral Ecology of Strepsirrhines and Tarsiers
Peter M. Kappeler
3. The Behavior, Ecology, and Social Evolution of New World Monkeys
Eduardo Fernandez-Duque, Anthony Di Fiore, and Maren Huck
4. The Behavioral Ecology of Colobine Monkeys
Elisabeth H. M. Sterck
5. The Behavior, Ecology, and Social Evolution of Cercopithecine Monkeys
6. The Apes: Taxonomy, Biogeography, Life Histories, and Behavioral Ecology
David P. Watts
Part 2. Surviving and Growing Up in a Difficult and Dangerous World
7. Food as a Selective Force in Primates
Colin A. Chapman, Jessica M. Rothman, and Joanna E. Lambert
9. Ecological and Social Influcences on Sociality
Oliver Schülke and Julia Ostner
10. Life-History Evolution
Carel P. van Schaik and Karin Isler
11. Socialization and Development of Behavior
Elizabeth V. Lonsdorf and Stephen R. Ross
12. Genetic Consequences of Primate Social Organization
Anthony Di Fiore
13 Human Survival and Life History in Evolutionary Perspective
Part 3. Mating and Rearing Offspring
14. From Maternal Investment to Lifetime Maternal Care
Maria A. van Noordwijk
15. Magnitude and Sources of Variation in Female Reproductive Performance
16. Mate Choice
Peter M. Kappeler
17. Mating, Parenting, and Male Reproductive Strategies
Martin N. Muller and Melissa Emery Thompson
18. Magnitude and Sources of Variation in Male Reproductive Performance
Susan C. Alberts
19. Infanticide: Male Strategies and Female Counterstrategies
Ryne A. Palombit
20. The Socioecology of Human Reproduction
Frank W. Marlowe
Part 4. Getting Along
21. Cooperation Among Kin
Kevin A. Langergraber
22. Cooperation among Non-kin: Reciprocity, Markets, Mutualism
Ian C. Gilby
23. The Regulation of Social Relationships
Filippo Aureli, Orlaith N. Fraser, Colleen M. Schaffner, and Gabriele Schino
24. The Adaptive Value of Sociality
Joan B. Silk
25. Social Regard: Evolving a Psychology of Cooperation
26. Human Sociality
Part 5. Cognitive Strategies for Coping with Life's Challenges
27. Solving Ecological Problems
28. Knowledge of Social Relations
Robert M. Seyfarth and Dorothy L. Cheney
29. Communication Strategies
30. Understanding Other Minds
Josep Call and Laurie R. Santos
31. Social Learning, Traditions, and Culture
32. Human Cultural Cognition
Esther Herrmann and Michael Tomasello