TREE OF ORIGIN What Primate Behavior Can Tell Us about Human Social Evolution Frans B. M. de Waal, Editor HARVARD UNIVERSITV PRESS Cambridge, Massachusetts, and London, England Unless othenvise noted, illustrations by Margaret C. Nelson Copyright © 2001 by the President and Fellows of Harvard College AU rights reserved Printed in the United States of America Designed by Marianne Perlak Second printing, 2002 First Harvard University Press paperback edition, 2002 Library o/Congress Cataloging-in-Publication Data Tree of origin: what primate behavior can tell us about hwnan social evolution / Frans B.M. de Waal, editor. p.em. Includes bibliographical references and index. ISBN 0-674-00460-4 (cloth) ISBN 0-674-01004-3 (pbk.) 1. Primate Behavior. 2. Human evolution. 3. Social evolution. I. Waal, F. B. M. de (Frans B. M.), 1948- QL737.P91752001 599.8'15-dc21 00-050581 ~-\l@@)u 2005/08 Contents Frans B . M . de Waal Introduction 1 1 Anne E . Pusey Of Genes and Apes: Chimpanzee Social Organization and Reproduction 9 2 Frans B. M. de Waal Apes from Venus: Bonobos and Human Social Evolution 39 3 Karen B. Strier Beyond the Apes: Reasons to Consider the Entire Primate Order 69 4- Craig B . Stanford The Ape's Gift: Meat-eating, Meat-sharing, and Human Evolution 95 S Richard W. Wrangham Out of the Pan, Into the Fire: How Our Ancestors' Evolution Depended on What They Ate 119 6 Richard W. Byrne Social and Technical Forms of Primate Intelligence 145 7 Robin I. M . Dunbar Brains on Two Legs: Group Size and the Evolution of Intelligence 173 8 Charles T. Snowdon From Primate Communication to Human Language 193 !J William C. McGrew The Nature of Culture: Prospects and Pitfalls of Cultural Primatolo81J 229 Notes 257 Contributors 301 Bibliography 277 Index 303 Frans B. M. de Waal Introduction I T IS READILY APPARENT that comparisons between humans and other animals take two basic forms, depending on whether the main objec tive is to confirm human identity or to stress the common thread that fillS through all forms of life. The first approach is still commonplace in the social sciences and the humanities, where the importance of any particu lar subject is underlined by claims that ours is the only species to which the topic could possibly apply. The second approach-at least as old received strong impetus from Darwin's theory of evolution by natural se lection. Especially in the last couple of decades, the view of human behav ior as the product of evolution, hence subject to the same explanatory framework as animal behavior, has gained ground and respectability. It has been transformed from a controversial minority view to one that today is widely applied. This transformation was made possible by major theoretical develop ments in the field of animal behavior-such as the explanations of cooper ative behavior at the heart of sociobiology and behavioral ecology-and by the courage of a few scientists who in the 1970s began sending wake-up calls to those sections of the academic community traditionally favoring nurture over nature. The evidence for a connection between genes and behavior is mow1t ing rapidly. Twins-reared-apart studies have reached the status of com mon knowledge, and almost every week newspapers report a new human gene-those involved in schizophrenia, epilepsy, and Alzheimer's disease, even in behavioral traits such as thrill-seeking. We are also learning more about genetic and neurological differences between men and women. Not that there is a simple one-on-one relation between genes and behavior: our sound-bite culture tends to tum findings into a gene-for-this and a gene for-that language, whereas in reality behavioral variability is only partly explained by genetic factors (the other part being attributable to the envi- 1 2 . Frans B. M. de Waal ronment}. Nevertheless, the list of scientific advances implying genetic in fluences is getting longer by the day, resulting in a critical mass of evidence that is impossible to ignore. Understandably, academics who have spent a lifetime condemning the idea that biology influences human behavior are reluctant to change course, but they are being overtaken by the general public, which seems to have accepted that genes are involved in just about everything we do and are. Another development that has influenced the way we look at our place in nature, and that has particular relevance to the present volume, is the proliferation of research on monkeys and apes. In terms of genetics, neu rology, cognition, and social behavior, many cherished assumptions in support of human/ animal dualism have fallen by the wayside. DNA shld ies have placed the apes far closer to us than anyone deemed possible at the beginning of the twentieth cenrury. Not only are chimpanzees and bonobos genetically our closest relatives, the reverse is also true; that is, chimpanzees and bonobos are closer to us than to, say, gorillas. • Millions of Years Ago o 35 30 25 20 15 10 5 I I I I I I I I Hwnans Chimpanzees ~~-:"'- Bonobos Gorillas Orangutans ()Id World Printates Old World Monkeys ~~------------~~----------~~---------Baboons Macaques ...... ""-=~--- Capuchins MlUiquis Squirrel Monkeys Figure 1.1 Evolutionary tree showing the main branches of the primate order (ex cept for the prosimians): the New World monkeys, the ()Id World monkeys, and the hominoid lineage that produced our own species. The diagram reflects advances in DNA analysis that place the African apes (gorillas, bonobos, and chimpanzees) much closer to hlUl1ans than previously suspected. Introduction . 3 People have a tendency to lump all two hUlldred primate species Ullder the rubric of "monkeys," but the great apes (only four species: chimpan zee, bonobo, gorilla, and orangutan) together with gibbons and humans are a distinct group, the Hominoids, not to be confused with the Old World monkeys (such as baboons and macaques), which in turn are not to be con fused with New World monkeys (such as capuchins and marmosets). Fig ure I.1 and Table I.1 offer help with the classification. Readers are referred to MacDonald (1984) and Napier and Napier (1985) for more detailed pri mate taxonomies. So, after a period in which human behavior has been freely interpreted in light of what we know about pigeons (such as the research of the learn ing psycholOgist B. F. Skinner), geese (Konrad Lorenz), social insects (E. O. Wilson), and rodents (Robert Ardrey, who compared people in inner cities with crowded rats), comparisons increasingly focus on species that are a lot closer and more similar to us than any of the above. Such comparisons have captured public attention ever since Desmond Table 1.1 The hominoid family is characterized by flat chests, rotational ability in the shoulders, absence of tails, and relatively large body size. It includes the Asian gibbons and siamangs (the so-called lesser apes), the Pongidae (great apes) of Africa and Asia, and modern humans. With the exception of the gibbon family, this table delineates the species and subspecies of extant humans and apes, customarily divided into five different species belonging to four genera. Genus Species Subspecies Common name Gorilla gorilla beringei Mountain gorilla graueri Eastern lowland gorilla gorilla Western lowland gorilla Pongo pygmaeus pygmaeus Bornean orangutan abelii Sumatran orangutan Pan troglodytes verus Masked or pale-faced dlimpanzee (west Africa) troglodytes Black-faced chimpanzee (central Africa) seh weinfurthii Long-haired chimpanzee (eastern Africa) paniseus Bonobo (previously: pygmy chimpanzee) Homo sapiens sapiens Modern human 4 . Frans B. M. de Waal Morris in 1967 published The Naked Ape, followed in 1971 by Jane Good all's In the Shadow of Man. Both books relied on direct ape-human compari sons-the former from the human perspective; the second, more subtly, via an in-depth account of chimpanzee social life with the implicit message that these animals are a great deal like us. These two early books are only the tip of the iceberg, however. A steady stream of scholarly and popular publications have appeared since, detailing numerous parallels between human and ape behavior. Often the implication has been that these paral lels represent homologies; that is, they derive from the common ancestor of humans and apes. Some of the contributors to the present volume have been in the forefront of this literature. The growing influence of primate research has forced lingUists to look more closely at their definitions of language, and anthropologists to con sider nonhuman culture. Ape studies have also triggered the current fasci nation with self-awareness and so-called Theory of Mind in child psychol ogy. Even the origins of human politics, warfare, and morality are now being discussed in the light of primate observations. What is the objective of such comparisons? Is it just to show that we are not alone in being cognitively and SOcially complex, or does it go deeper? If humans and other primates show similar behavior, does that make the apes look smarter, assuming that they put as much cognition into their ac tions as we do? Or does it make us look dumber? Do similarities prove that we are instinctive creatures held on a leash by our biology? These are the sorts of questions that fueled many debates in the 1970s. There were accu sations directed at biologists of genetic determinism and questions about their application of human concepts to animal behavior (for instance, Sher wood Washburn's 1978 essay "What We Can't Learn about People from Apes"). The current generation of primatologists, however, is quite averse to attempts to squeeze behavior into a simple "learned versus innate" di chotomy. We assume that all behavior in all primates, including our own species, derives from a combination of evolved tendencies, environmen tal modification, development, learning, and cognition. The word instinct, with its connotation of a purely genetic derivation, has indeed become out dated except in usage such as a "language instinct," where the concept has been broadened to stand for learning predisposition. In sum, this book is not about our species as a preprogrammed robot destined by its biology to act one way or another. The contributors have far too high an opinion of the behavioral flexibility of their primary research Introduction . 5 subjects, which in all cases are nonhuman primates, to embrace such a view. If they see monkeys and apes as mentally complex, socially skilled, even cultural beings, why would they want to simplify human behavior? Rather, the goal is to understand human social evolution from the per spective of what we know about the social organization, commwlication, learned habits, subsistence, reproduction, and cognition of other extant primates. This is no simple task, and it certainly has no simple answers. The genesis of our book goes back to October 1997, when a conference on Human Evolution was held at the well-known Cold Spring Harbor Laboratory in New York State. A well-attended and well-received session, organized by the writer, was entitled "Primate Behavior and the Recon struction of Human Social Evolution." Six of the nine contributors to this volume participated. All the other sessions, except for one on paleontol ogy, dealt with molecular genetics. It was felt that a symposium topic such as primate behavior deserved its own volume; not since Warren Kinzey's 1987 book, The Evolution ofH uman Behavior: Primate Models, has anyone brought together primatologists spe cificallyarOlmd the question of human evolution. Most primatologists stay close to their data without venturing too far into speculation about the ori gins of human behavior. Even if some of our contributors are known ex ceptions, there are no works juxtaposing their views with those of others. In putting this volume together, we followed three simple rules: 1. All authors are behavioral primatologists-psychologists, anthropolo gists, or zoologists extensively familiar with the behavior of monkeys and apes. Informed opinions about human evolution are to be fOlmd in many quarters (neuroscience, paleontology, linguistics), but we wished to pre sent the primate perspective straight from the pen of people with intimate, firsthand knowledge of the natural or naturalistic behavior of this special taxonomic group. 2. All contributors speculate about the origins of human evolution. How is our species similar to or different from other primates, and which selec tion pressures may have forced our ancestors to evolve in the direction they took. Some authors address this issue more explicitly than others, but all present an aspect of what primate behavior can tell us about human so cial evolution. 3. Contributors were asked to write in an accessible, jargon-free style. Only the notes provide technical background. The authors should be for- 6 . Frans B. M. de Waal given for not citing each and every relevant study, and for not mentioning every angle of a problem. Even though all contributors are recognized ex perts in their field, there is no mainsh·eam view on the topic of human evo lution. Hence this book should be supplemented with other readings, in cluding altemative views by other scholars. No attempt has been made here to reconcile differences of opinion. It would be surprising if any treahnent of this topic at this stage could pro vide lasting answers. Our hope, rather, is that this book will make readers rethink hlUnan evolution, and consider peculiarities of our species or lines of argument that they have not taken into account before. Even if what one author considers obvious is questioned by another, it is the underlying problem that matters most. For example, Robin Dunbar follows many other primatologists in argu ing for social complexity as the driving force behind the evolution of intel ligence, whereas Richard Byme thinks that, at least in the apes, planning of action chains played a significant role-and Craig Stanford sees the poli tics surrounding meat-sharing as yet another factor. All three authors try to come up with reasons why primate brains expanded so much more, rel ative to body size, than the brains of other land mammals. The reader need not choose among these points of view to recognize that an evolutionary explanation is needed, which at the same time may tell us something about our own species, which has the largest brain of all. Other differences of opinion are evident too. Richard Wrangham regards the chimpanzee as the best model of the last common ancestor of hun1ans and apes, whereas Frans de Waal argues that the bonobo is at least as good a candidate. Stanford emphasizes hunting and meat-sharing in human evolution, in contrast to Wrangham's focus on plant foods. Charles Snow don looks for continuities between primate communication and human language, whereas Dunbar emphasizes the social bonding function of lan guage and places it functionally closer to grooming. Finally, whereas many authors emphasize the behavior and cognitive capacities of our closest rel atives, Karen Strier urges us to look beyond the apes. This final point relates to two different approacl1es to the matter of hu man evolution. One involves development of general principles that apply to a great variety of species, from insects to birds to humans. Primates are a not particularly numerous or varied group of organisms to consider when we investigate how the distribution of food affects social organization, or the conditions under whicl1 animals increase in body size, or how competi-