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Silk-2008-Social-Preferences.Pdf Provided for non-commercial research and educational use only. Not for reproduction, distribution or commercial use. This chapter was originally published in the book Neuroeconomics: Decision Making and the Brain, published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author’s institution, for non-commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissions From: Neuroeconomics: Decision Making and the Brain Edited by Paul W. Glimcher, Colin F. Camerer, Ernst Fehr and Russell A. Poldrack ISBN: 978-0-12-374176-9 © Copyright 2008 Elsevier Inc. Academic Press. Author’s personal copy CHAPTER 18 Social Preferences in Primates Joan B. Silk OUTLINE Introduction 269 Empirical Evidence for Empathy and Sympathy 275 The Adaptive Challenge of Altruism 270 Social Preferences in Primates 276 Kin Selection 270 Chimps Display Indifference About the Welfare Contingent Reciprocity 271 of Other Group Members 276 Chimps Respond Positively to the Needs of Others 280 The Deployment of Altruism in Primate Groups 271 Reconciling the Results 280 In-group Biases 271 Nepotistic Biases 272 Conclusions 282 Altruism Toward Reciprocating Partners 272 Acknowledgments 283 Primate Policing and Punishment 273 References 283 Cognitive Basis of Social Preferences 274 When I do good, I feel good; when I do bad,I feel bad, individuals to survive and reproduce successfully. and that is my religion. Success in what Charles Darwin (1859) called“ the Abraham Lincoln struggle for existence ” often comes at the expense of others, leaving little scope for the kinds of proso- INTRODUCTION cial sentiments that Lincoln expressed. Darwin him- self was troubled by the fact that his theory could not explain the altruistic existence of sterile workers in Humans, like all of the other organisms on earth, social insect colonies, which spend their lives caring are the product of evolution by natural selection. for the offspring of the queen, but never reproduce Natural selection generally favors traits that enable themselves. In The Origin of Species , he wrote that the Neuroeconomics: Decision Making and the Brain 269 © 2009, Elsevier Inc. Author’s personal copy 270 18. SOCIAL PREFERENCES IN PRIMATES altruism of social insects presented “ one special dif- THE ADAPTIVE CHALLENGE OF ficulty, which at first appeared to me insuperable, ALTRUISM and actually fatal to my theory. ” This conundrum has engrossed evolutionary biologists for the last 40 years, and has generated a large theoretical and empirical lit- Biologists define altruism as any behavior that is erature on the evolution of altruism. This work shows costly to the actor and beneficial to the recipient. By that altruism is widespread in nature, but is typically performing an altruistic behavior, actors incur costs limited to kin and reciprocating partners ( Crozier that reduce their own chance of reproducing success- and Pamilo, 1996; Dugatkin, 1997 ; Kappeler and van fully (fitness), and provide benefits that increase the Schaik, 2006). This literature has also illuminated the recipient’s fitness. If altruists provide benefits to others gap between humans and other animals. Humans indiscriminately, then the benefits will not increase the rely on cooperation to a far greater extent than most relative fitness of altruists. However, altruists always other animals do, and are able to orchestrate coopera- bear the costs. The average fitness of a genetic vari- tion in substantially larger groups. Moreover, humans ant (allele) that increases the likelihood of performing are the only animals that regularly provide aid to the altruistic behavior will therefore be lower than the strangers and impose costly punishment on wrong- average fitness of the non-altruistic allele. In order for doers in anonymous, one-shot interactions ( Fehr and altruism to evolve, there must be some process that Fischbacher, 2003 ; Boyd and Richerson, 2005 ; Henrich allows altruists to direct benefits selectively with other et al. 2006). Cooperation in humans is sustained by a altruists. In nature, two types of processes can produce willingness to impose costly punishment on those this outcome: nepotism and contingent reciprocity. who shirk social obligations. In humans, altruism seems to be motivated at least in part by social pref- Kin Selection erences based on empathy, concern for the welfare of others, and a preference for equity ( Batson, 1991 ; Selection can favor altruism toward close relatives Fehr and Fischbacher, 2003; see also Chapter 19 of this because kinship provides a reliable cue of genetic simi- volume). larity. W.D. Hamilton realized that individuals that are What is the evolutionary source of human proso- descended from the same ancestors have some prob- cial preferences? If our prosocial preferences are based ability of inheriting copies of the same genes. In par- on empathy, which relies on the ability to perceive ticular, individuals who carry genes that are associated the thoughts and feelings of others, then comparative with altruistic behavior are more likely to have relatives studies of the cooperation, cognition, and capacity for who carry copies of the same genes than individuals empathy in humans and and other primates may pro- drawn at random from the population. If individuals vide clues about the origins of prosocial preferences. behave altruistically to their relatives, they have some On the other hand, our prosocial preferences might chance of conferring benefits on individuals who also reflect the evolutionary consequences of the economic carry copies of the the genes that lead to altruistic importance of cooperation in human societies. If that behavior. This is the underlying foundation for the the- is the case, then it might be profitable to examine the ory of kin selection ( Hamilton, 1964 ). What has come to nature of social preferences in other species in which be known as Hamilton’s rule predicts that altruism will cooperation plays an important role. be favored when br Ͼ c . The quantities b and c repre- Here, I review what we know about the evolution- sent the benefits and costs associated with the altruistic ary foundation and deployment, of altruism in non- act. The quantity r measures how much the possession human primate species. I begin with a brief primer of a particular gene in one individual predicts the pres- on the evolution of altruism, and briefly describe the ence of the same gene in a second individual. pattern and scope of altruism among primates in the If there is limited movement in and out of groups, wild, including the deployment of both beneficent levels of genetic relatedness will build up over time. behavior and punishment. Then, I examine what is When this is the case, group membership can provide a known about the cognitive capacities that underlie cue for assortative interaction because genes that gen- empathy, and evidence for empathy and sympathy in erate altruistic behavior are disproportionately likely non-human primates. Finally, I review what we know to be shared by other group members. This holds even about the nature of social preferences that motivate for individuals who do not share recent ancestry. altruistic behavior in non-human primates, focusing Multi-level selection models ( Wilson and Sober, 1994) on recent experimental studies that probe the nature provide an alternative, but equivalent, description of of prosocial preferences in chimpanzees. the same process ( Dugatkin and Reeve, 1994 ; Reeve and III. SOCIAL DECISION MAKING, NEUROECONOMICS, AND EMOTION Author’s personal copy THE DEPLOYMENT OF ALTRUISM IN PRIMATE GROUPS 271 Keller, 1997). In the Hamilton’s rule approach, fitness (see edited volumes by Chapais and Berman, 2004 ; effects are allocated to the bodies in which the genes Kappeler and van Schaik, 2006 ). The most common causing the effects are expressed. In the multi-level form of altruistic behavior in primate groups is social selection approach, fitness effects are partitioned into grooming, which has important hygienic and social within-group and between-group components. The two functions. Other forms of altruistic behaviors that approaches are mathematically equivalent, but their occur in various primate species include coalitionary heuristic value may vary in different circumstances. support, in which one individual intervenes on behalf of another in an ongoing agonistic interaction; alarm- calling, in which one individual signals to others that Contingent Reciprocity a predator is nearby; alloparental care, in which group members help to carry, protect, and care for depend- The basic logic underlying contingent reciprocity, ent offspring; and food-sharing, which ranges from or reciprocal altruism, is the same as the logic underly- active donations of food items to passive tolerance of ing kin selection, but now previous behavior provides others feeding in close proximity. a cue about whether others carry alleles that lead to altruistic behaviors. When individuals interact more than once, contingent altruistic strategies (such as tit- for-tat) can arise. (For example, in the one-shot ver- In-group Biases sion of the prisoner’s dilemma game, two suspects of Virtually all of the New World monkeys (which a crime are apprehended and interrogated separately. range through Central and South America) and Old Each suspect is offered a reduced sentence if he con- World monkeys and apes (which range through fesses, and implicates his partner. Not knowing what Africa and Asia) live in social groups ( Figure 18.1 ). the other suspect will do, each suspect has a strong The size and structure of social groups vary consid- incentive to confess.
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