On the psychology of cooperation in humans and other primates: combining the natural history and experimental evidence of prosociality

In any given species, cooperation involves prosocial acts that usually return a fitness benefit to the actor. These acts are produced by a set of psychological rules, which will be similar in related species if they have a similar natural history of cooperation. Prosocial acts can be (i) reactive, i.e. in response to specific stimuli, or (ii) proactive, i.e. occur in the absence of such stimuli. We propose that reactive prosocial acts reflect sensitivity to (i) signals or signs of need and (ii) the presence and size of an audience, as modified by (iii) social distance to the partner or partners. We examine the evidence for these elements in humans and other animals, especially non-human primates, based on the natural history of cooperation, quantified in the context of food sharing, and various experimental paradigms. The comparison suggests that humans share with their closest living relatives reactive responses to signals of need, but differ in sensitivity to signs of need and cues of being watched, as well as in the presence of proactive prosociality. We discuss ultimate explanations for these derived features, in particular the adoption of cooperative breeding as well as concern for reputation and costly signalling during human evolution.

[1]  T. Clutton‐Brock,et al.  Contributions to cooperative rearing in meerkats , 2001, Animal Behaviour.

[2]  B. Chapais Kinship, competence and cooperation in primates , 2006 .

[3]  M. Manser,et al.  The effect of pup vocalisations on food allocation in a cooperative mammal, the meerkat (Suricata suricatta) , 2000, Behavioral Ecology and Sociobiology.

[4]  F. D. de Waal,et al.  Prosocial primates: selfish and unselfish motivations , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  A. Pusey Chimpanzee Politics: Power and Sex among Apes, France de Waal. Harper & Row, New York (1982), 223, Price $16.50 , 1984 .

[6]  A. Thornton,et al.  Teaching in Wild Meerkats , 2006, Science.

[7]  S. Gächter Behavioral Game Theory , 2008, Encyclopedia of Evolutionary Psychological Science.

[8]  Frans B. M. de Waal,et al.  Attitudinal reciprocity in food sharing among brown capuchin monkeys , 2000, Animal Behaviour.

[9]  R. Trivers The Evolution of Reciprocal Altruism , 1971, The Quarterly Review of Biology.

[10]  Joseph de Acosta,et al.  The natural history , 2009 .

[11]  J. Henrich,et al.  Markets, Religion, Community Size, and the Evolution of Fairness and Punishment , 2010, Science.

[12]  J. Silk Practicing Hamilton’s rule: kin selection in primate groups , 2006 .

[13]  M. Tomasello,et al.  What's in it for me? Self-regard precludes altruism and spite in chimpanzees , 2006, Proceedings of the Royal Society B: Biological Sciences.

[14]  Terence C Burnham,et al.  Engineering Human Cooperation , 2007, Human nature.

[15]  Laurie R Santos,et al.  Capuchin monkeys are sensitive to others' welfare , 2008, Current Biology.

[16]  L. Birch,et al.  Preschool Children's Food Sharing with Friends and Acquaintances. , 1986 .

[17]  G. Hohmann,et al.  How bonobos handle hunts and harvests : Why share food? , 2002 .

[18]  Ian C. Gilby,et al.  Meat sharing among the Gombe chimpanzees: harassment and reciprocal exchange , 2006, Animal Behaviour.

[19]  L. Rapaport,et al.  Social influences on foraging behavior in young nonhuman primates: Learning what, where, and how to eat , 2008 .

[20]  R. Earley Social eavesdropping and the evolution of conditional cooperation and cheating strategies , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[21]  M. Beran,et al.  Trading behavior between conspecifics in chimpanzees, Pan troglodytes. , 2009, Journal of comparative psychology.

[22]  T. Matsuzawa,et al.  Social influences on ant-dipping acquisition in the wild chimpanzees (Pan troglodytes verus) of Bossou, Guinea, West Africa , 2009, Animal Cognition.

[23]  M. Hauser,et al.  Why be nice? Psychological constraints on the evolution of cooperation , 2004, Trends in Cognitive Sciences.

[24]  J. Mitani,et al.  Behavioural Diversity in Chimpanzees and Bonobos: Hunting and meat sharing by chimpanzees at Ngogo, Kibale National Park, Uganda , 2002 .

[25]  B. Chapais Primeval Kinship: How Pair-Bonding Gave Birth to Human Society , 2008 .

[26]  B. Rockenbach,et al.  Egalitarianism in young children , 2008, Nature.

[27]  S. Takagi,et al.  Natural History , 2019, Nature.

[28]  J. Stevens Donor payoffs and other-regarding preferences in cotton-top tamarins (Saguinus oedipus) , 2010, Animal Cognition.

[29]  C. Schaik,et al.  The socioecology of fission-fusion sociality in Orangutans , 2007, Primates.

[30]  Katherine A. Cronin,et al.  The effects of unequal reward distributions on cooperative problem solving by cottontop tamarins, Saguinus oedipus , 2008, Animal Behaviour.

[31]  Carol M. Lauer,et al.  Hierarchy in the forest: The evolution of egalitarian behavior , 2001 .

[32]  Klaus E. Liebold,et al.  A Method for Studying Altruism in Monkeys , 1969 .

[33]  F. Marlowe Hadza Cooperation , 2009 .

[34]  K. Bard,et al.  Intentional behavior and intentional communication in young free-ranging orangutans. , 1992, Child development.

[35]  Kevin E. Langergraber,et al.  Kinship and social bonds in female chimpanzees (Pan troglodytes) , 2009, American journal of primatology.

[36]  Philip Kitcher,et al.  VARIETIES OF ALTRUISM , 2010, Economics and Philosophy.

[37]  R. Bshary,et al.  Image scoring and cooperation in a cleaner fish mutualism , 2006, Nature.

[38]  R. Kurzban,et al.  Mysteries of morality , 2009, Cognition.

[39]  David W. Macdonald,et al.  Biology and Conservation of Wild Felids , 2010 .

[40]  D. Povinelli,et al.  Chimpanzees are indifferent to the welfare of unrelated group members , 2005, Nature.

[41]  S. Gächter,et al.  Culture and cooperation , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[42]  G. Anzenberger,et al.  Costs of infant carrying in common marmosets, Callithrix jacchus: an experimental analysis , 2001, Animal Behaviour.

[43]  M. Gurven,et al.  Why Do Men Hunt? , 2009, Current Anthropology.

[44]  M. Erpino Evolution teaching. , 1996, Science.

[45]  J. Vonk,et al.  Do chimpanzees learn reputation by observation? Evidence from direct and indirect experience with generous and selfish strangers , 2008, Animal Cognition.

[46]  Nancy Eisenberg,et al.  The roots of prosocial behavior in children , 1989 .

[47]  T. Clutton‐Brock,et al.  Offspring food allocation by parents and helpers in a cooperative mammal , 2001 .

[48]  Katherine A. Cronin,et al.  Prosocial behaviour emerges independent of reciprocity in cottontop tamarins , 2010, Proceedings of the Royal Society B: Biological Sciences.

[49]  Celia A. Brownell,et al.  To share or not to share: When do toddlers respond to another's needs? , 2009, Infancy : the official journal of the International Society on Infant Studies.

[50]  J. Mitani,et al.  Reciprocal exchange in chimpanzees and other primates , 2006 .

[51]  Katherine A. Cronin,et al.  Cooperative breeders do cooperate , 2007, Behavioural Processes.

[52]  N. Bardsley Dictator game giving: altruism or artefact? , 2008 .

[53]  Robin I. M. Dunbar,et al.  Intergroup Aggression in Chimpanzees and Humans [and Comments and Replies] , 1991, Current Anthropology.

[54]  R. Bshary,et al.  Cooperation and deception: from evolution to mechanisms , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[55]  Shinya Yamamoto,et al.  The influence of kin relationship and reciprocal context on chimpanzees' other-regarding preferences , 2010, Animal Behaviour.

[56]  Charlotte K. Hemelrijk,et al.  Support for being groomed in long-tailed macaques, Macaca fascicularis , 1994, Animal Behaviour.

[57]  W. Hamilton The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[58]  H. Schaub Testing kin altruism in long-tailed macaques (Macaca fascicularis) in a food-sharing experiment , 1996, International Journal of Primatology.

[59]  C. Boesch Cooperative hunting in wild chimpanzees , 1994, Animal Behaviour.

[60]  M. Gurven To give and to give not: The behavioral ecology of human food transfers , 2004, Behavioral and Brain Sciences.

[61]  M. Milinski,et al.  Reputation helps solve the ‘tragedy of the commons’ , 2002, Nature.

[62]  Judith M Burkart,et al.  Other-regarding preferences in a non-human primate: Common marmosets provision food altruistically , 2007, Proceedings of the National Academy of Sciences.

[63]  S. Pika,et al.  Referential gestural communication in wild chimpanzees (Pan troglodytes) , 2006, Current Biology.

[64]  D. Povinelli,et al.  Chimpanzees do not take advantage of very low cost opportunities to deliver food to unrelated group members , 2008, Animal Behaviour.

[65]  S. Wich,et al.  Social learning of diet and foraging skills by wild immature Bornean orangutans: implications for culture , 2010, American journal of primatology.

[66]  Sarah F. Brosnan,et al.  A proximate perspective on reciprocal altruism , 2002, Human nature.

[67]  Alison R Hwong,et al.  Mothers and Others: The Evolutionary Origins of Mutual Understanding , 2010 .

[68]  Robin I. M. Dunbar,et al.  Image scoring in great apes , 2008, Behavioural Processes.

[69]  Yuko Hattori,et al.  Cooperative problem solving by tufted capuchin monkeys (Cebus apella): spontaneous division of labor, communication, and reciprocal altruism. , 2005, Journal of comparative psychology.

[70]  Judith M Burkart,et al.  Cooperative breeding and human cognitive evolution , 2009 .

[71]  C. V. van Schaik,et al.  Begging for information: mother–offspring food sharing among wild Bornean orangutans , 2008, American journal of primatology.

[72]  F. D. Waal,et al.  Payment for labour in monkeys , 2000, Nature.

[73]  L. Rapaport Parenting Behaviour: Babbling Bird Teachers? , 2006, Current Biology.

[74]  L. Rapaport Food Transfer Among Adult Lion Tamarins: Mutualism, Reciprocity or One-Sided Relationships? , 2001, International Journal of Primatology.

[75]  C. Boesch,et al.  Hunting behavior of wild chimpanzees in the Taï National Park. , 1989, American journal of physical anthropology.

[76]  Rui F. Oliveira,et al.  Hormonal mechanisms of cooperative behaviour , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[77]  C. Boesch,et al.  Altruism in Forest Chimpanzees: The Case of Adoption , 2010, PloS one.

[78]  E. Lonsdorf What is the role of mothers in the acquisition of termite-fishing behaviors in wild chimpanzees (Pan troglodytes schweinfurthii)? , 2005, Animal Cognition.

[79]  Carel P. van Schaik,et al.  Cognitive consequences of cooperative breeding in primates? , 2009, Animal Cognition.

[80]  Anita D. Laton,et al.  A life history , 1943 .

[81]  F. D. Waal The Chimpanzee's service economy: Food for grooming , 1997 .

[82]  Keith Jensen,et al.  Punishment and spite, the dark side of cooperation , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[83]  Gabriele Schino,et al.  Grooming and agonistic support: a meta-analysis of primate reciprocal altruism , 2007 .

[84]  C. V. van Schaik,et al.  Tolerant food sharing and reciprocity is precluded by despotism among bonobos but not chimpanzees. , 2010, American journal of physical anthropology.

[85]  A. Chamove,et al.  High motivation toward food increases food-sharing in cotton-top tamarins. , 1986, Developmental psychobiology.

[86]  J. Silk Empathy, sympathy, and prosocial preferences in primates , 2007 .

[87]  Laurie R Santos,et al.  Helping behaviour and regard for others in capuchin monkeys (Cebus apella) , 2008, Biology Letters.

[88]  R. Trivers Reciprocal altruism: 30 years later , 2006 .

[89]  Shinya Yamamoto,et al.  How did altruism and reciprocity evolve in humans?: Perspectives from experiments on chimpanzees ( Pan troglodytes ) , 2009 .

[90]  Andrew M. Colman,et al.  Moral sentiments and material interests: The foundations of cooperation in economic life , 2006 .

[91]  A. Melis,et al.  How is human cooperation different? , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[92]  F. Marlowe WHAT EXPLAINS HADZA FOOD SHARING , 2004 .

[93]  D. Watts RECIPROCITY AND INTERCHANGE IN THE SOCIAL RELATIONSHIPS OF WILD MALE CHIMPANZEES , 2002 .

[94]  Kevin E. Langergraber,et al.  From the Cover : The limited impact of kinship on cooperation in wild chimpanzees , 2007 .

[95]  Y. V. Bergen,et al.  Begging, stealing, and offering : food transfer in nonhuman primates , 2004 .

[96]  E. Visalberghi,et al.  The Complete Capuchin: The Biology of the Genus Cebus , 2004 .

[97]  S. Stewart,et al.  Cultural Influences on Sharer and Recipient Behavior , 1999 .

[98]  M. Tomasello,et al.  Altruistic Helping in Human Infants and Young Chimpanzees , 2006, Science.

[99]  S. Meier,et al.  The Impact of Group Membership on Cooperation and Norm Enforcement: Evidence Using Random Assignment to Real Social Groups , 2006, SSRN Electronic Journal.

[100]  F. Waal Complementary Methods and Convergent Evidence in the Study of Primate Social Cognition1) , 1991 .

[101]  Filippo Aureli,et al.  Trade-offs in primate grooming reciprocation: testing behavioural flexibility and correlated evolution , 2008 .

[102]  Carel P. van Schaik,et al.  Mind the Gap: Cooperative Breeding and the Evolution of Our Unique Features , 2010 .

[103]  S. Kuroda Interaction over Food among Pygmy Chimpanzees , 1984 .

[104]  J. Henrich,et al.  Chimpanzees (Pan troglodytes) do not develop contingent reciprocity in an experimental task , 2009, Animal Cognition.

[105]  A. Dickson On Evolution , 1884, Science.

[106]  A. Feistner,et al.  Cross-generic Food Sharing in Tamarins , 1999, International Journal of Primatology.

[107]  B. Majolo,et al.  Human friendship favours cooperation in the Iterated Prisoner's Dilemma , 2006 .

[108]  T. Matsuzawa,et al.  Food transfer between chimpanzee mothers and their infants , 2004, Primates.

[109]  Berry M. Spruijt,et al.  Generous Leaders and Selfish Underdogs: Pro-Sociality in Despotic Macaques , 2010, PloS one.

[110]  Robert M. Seyfarth,et al.  Hierarchical Classification by Rank and Kinship in Baboons , 2003, Science.

[111]  C. Boehm,et al.  Hierarchy in the Forest. The Evolution of Egalitarian Behavior. Cambridge, MA (Harvard University Press) 1999. , 1999 .

[112]  J. Grisham Biology and Conservation of Wild Canids, D.W. Macdonald, C. Sillero-Zubiri (Eds.). Oxford University Press, Oxford (2004), Pp. xiv+450. Price $74.50 paper , 2005 .

[113]  Maura L. Celli,et al.  Role of mothers in the acquisition of tool-use behaviours by captive infant chimpanzees , 2003, Animal Cognition.

[114]  C. Boesch What makes us human (Homo sapiens)? The challenge of cognitive cross-species comparison. , 2007, Journal of comparative psychology.

[115]  D. Macdonald,et al.  The biology and conservation of wild canids , 2004 .

[116]  M. Tomasello,et al.  Varieties of altruism in children and chimpanzees , 2009, Trends in Cognitive Sciences.

[117]  Michael Tomasello,et al.  Chimpanzees are more skilful in competitive than in cooperative cognitive tasks , 2004, Animal Behaviour.

[118]  G. Schino,et al.  Reciprocal Altruism in Primates: Partner Choice, Cognition, and Emotions , 2009 .

[119]  R. Bshary,et al.  The interplay of cognition and cooperation , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[120]  F. Marlowe,et al.  Hunting and Gathering , 2007 .

[121]  G. Schino,et al.  Chapter 2 Reciprocal Altruism in Primates , 2009 .

[122]  P. Kitcher Psychological Altruism, Evolutionary Origins, and Moral Rules , 1998 .

[123]  S. Kitayama,et al.  Minimal Social Cues in the Dictator Game , 2009 .

[124]  S. Brosnan,et al.  Cebus apella Tolerate Intermittent Unreliability in Human Experimenters , 2009, International Journal of Primatology.

[125]  M. Bateson,et al.  Cues of being watched enhance cooperation in a real-world setting , 2006, Biology Letters.

[126]  W. Kühme Communal Food Distribution and Division of Labour in African Hunting Dogs , 1965, Nature.

[127]  K. Fujita,et al.  Capuchin monkeys (Cebus apella) are sensitive to others’ reward: an experimental analysis of food-choice for conspecifics , 2010, Animal Cognition.

[128]  Joan B. Silk,et al.  USING THE ' F' -WORD IN PRIMATOLOGY , 2002 .

[129]  E. Fehr,et al.  Eyes are on us, but nobody cares: are eye cues relevant for strong reciprocity? , 2009, Proceedings of the Royal Society B: Biological Sciences.

[130]  R. Wittig,et al.  Baboons eavesdrop to deduce mating opportunities , 2007, Animal Behaviour.

[131]  Shinya Yamamoto,et al.  Do chimpanzees (Pan troglodytes) spontaneously take turns in a reciprocal cooperation task? , 2009, Journal of comparative psychology.

[132]  Tim Clutton-Brock,et al.  Breeding together: kin selection and mutualism in cooperative vertebrates. , 2002, Science.

[133]  Paul L. Hooper,et al.  The evolutionary and ecological roots of human social organization , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[134]  John H. Hollis,et al.  Communication between young rhesus monkeys , 1962 .

[135]  M. Hauser,et al.  Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[136]  M. Tomasello,et al.  Spontaneous Altruism by Chimpanzees and Young Children , 2007, PLoS biology.

[137]  Michael Gurven,et al.  The Natural History of Human Food Sharing and Cooperation: A Review and a New Multi-Individual Approach to the Negotiation of Norms , 2001 .

[138]  F. D. de Waal,et al.  Giving is self-rewarding for monkeys , 2008, Proceedings of the National Academy of Sciences.

[139]  Katherine A. Cronin,et al.  Cooperatively breeding cottontop tamarins (Saguinus oedipus) do not donate rewards to their long-term mates. , 2009, Journal of comparative psychology.

[140]  D. Fessler,et al.  Nobody's watching? Subtle cues affect generosity in an anonymous economic game. , 2005 .

[141]  C. Snowdon,et al.  Socially biased learning in the acquisition of a complex foraging task in juvenile cottontop tamarins, Saguinus oedipus , 2008, Animal Behaviour.

[142]  Robin I. M. Dunbar Gossip in Evolutionary Perspective , 2004 .

[143]  M. Tomasello,et al.  Does the chimpanzee have a theory of mind? 30 years later , 2008, Trends in Cognitive Sciences.

[144]  Shinya Yamamoto,et al.  Chimpanzees Help Each Other upon Request , 2009, PloS one.

[145]  Laurent Lehmann,et al.  How life history and demography promote or inhibit the evolution of helping behaviours , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.