Explanations of cooperation between non-kin in animal societies often suggest that individuals exchange resources or services and that cooperation is maintained by reciprocity. But do cooperative interactions between unrelated individuals in non-human animals really resemble exchanges or are they a consequence of simpler mechanisms? Firm evidence of reciprocity in animal societies is rare and many examples of cooperation between non-kin probably represent cases of intra-specific mutualism or manipulation.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Scientific Reports Open Access 24 November 2022
The portrayal of animal interactions in nature documentaries by David Attenborough and Bernhard Grzimek
Evolution: Education and Outreach Open Access 15 September 2022
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Darwin, C. The Origin of Species Ch. VIII (The Modern Library, 1859/, 1958)Although Darwin did not confront the problem of altruistic behaviour directly, he was aware of the challenge posed by the development of sterile castes in some social insects and, in Chapter VIII of The Origin of Species , he describes how he thought, at first, that this was fatal to the whole theory of natural selection.
Kropotkin, P. Mutual Aid (William Heineman, 1908)
Wynne-Edwards, V. C. Animal Dispersion in Relation to Social Behaviour (Oliver and Boyd, 1962)
Hamilton, W. D. The genetical evolution of social behaviour. I. II. J. Theor. Biol. 7, 1–52 (1964)Although they are usually cited as an explanation of the role of kin selection in maintaining cooperative behaviour, Hamilton’s papers and Hamilton’s Rule (see Box 1) also provide the basis for explaining cooperation between non-kin.
Axelrod, R. The Evolution of Cooperation (Basic Books, 1984)
Nowak, M. A. Five rules for the evolution of cooperation. Science 314, 1560–1565 (2006)
Trivers, R. L. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57 (1971)The theoretical interest generated by Trivers’ theory caused explanations of cooperation between non-kin based on reciprocity to eclipse all other explanations for more than thirty years.
von Neumann, J. & Morgenstein, O. Theory of Games and Economic Behaviour (Princeton Univ. Press, 1953)
Nowak, M. A. & Sigmund, K. Evolution of indirect reciprocity. Nature 437, 1295–1297 (2005)
Suzuki, S. & Akiyama, E. Evolution of indirect reciprocity in groups of various sizes and comparison with direct reciprocity. J. Theor. Biol. 245, 539–552 (2007)
Roberts, G. Evolution of direct and indirect reciprocity. Proc. R. Soc. Lond. B 275, 173–179 (2008)
Pfeiffer, T., Rutte, C., Killingback, T., Taborsky, M. & Benhoeffer, S. Evolution of cooperation by generalized reciprocity. Proc. R. Soc. B 272, 1115–1120 (2005)
Rankin, D. J. & Taborsky, M. Assortment and the evolution of generalized reciprocity. Evolution 63, 1913–1922 (2009)
Kokko, H., Johnstone, R. A. & Clutton-Brock, T. H. The evolution of cooperative breeding through group augmentation. Proc. R. Soc. Lond. B 268, 187–196 (2001)Kokko’s model shows that shared fitness benefits can maintain costly cooperation between non-kin in small groups—but that their capacity to do so is greatly enhanced if r exceeds 0.
Brown, J. S. & Vincent, T. L. Evolution of cooperation with shared costs and benefits. Proc. R. Soc. Lond. B 275, 1985–1994 (2008)
Bowles, S. & Gintis, H. in Genetic and Cultural Evolution of Cooperation (ed. Hammerstein, P.) 429–444 (Dahlem Univ. Press, 2003)
Paxton, M. Foraging associations between pale chanting goshawks, honey badgers and slender mongooses. Gabar 3, 82–93 (1988)As Trivers pointed out, cooperative interactions between members of different species cannot be attributed to kin selection—but this does not necessarily suggest that they represent examples of reciprocity.
Bshary, R., Hohner, A., Ait-el-Djoudi, K. & Fricke, H. Interspecific communicative and coordinated hunting between groupers and giant Moray eels in the Red Sea. PLoS Biol. 4, 2393–2398 (2006)
McMahon, B. F. & Evans, R. M. Foraging strategies of American white pelicans. Behaviour 120, 69–89 (1992)
West, S. A., Griffin, A. S. & Gardiner, A. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415–432 (2007)West et al. prefer to use mutualism to refer only to interactions between species, whereas I use it here to refer to all +/+ interactions, where the behaviour of individuals is adapted to generating benefits to their partners, whether they involve heterospecifics or conspecifics.
Clutton-Brock, T. H. & Parker, G. A. Punishment in animal societies. Nature 373, 209–216 (1995)
Cant, M. A. & Johnstone, R. A. Self-serving punishment and the evolution of cooperation. Evol. Biol. 19, 1383–1385 (2006)
Connor, R. C. Pseudoreciprocity: investing in mutualism. Anim. Behav. 34, 1652–1654 (1986)
Leimar, O. & Connor, R. C. in Genetic and Cultural Evolution of Cooperation (ed. Hammerstein, P.) 202–222 (MIT Press, 2003)The models of pseudo-reciprocity produced by Connor and Leimar have attracted less attention than models of reciprocity but the processes they capture may help to explain many examples of cooperation between non-kin in animals.
Zahavi, A. & Zahavi, A. The Handicap Principle: a Missing Piece of Darwin's Puzzle (Oxford Univ. Press, 1997)
Wright, J., Berg, E., de Kort, S. R., Khazin, V. & Maklakov, A. A. Cooperative sentinel behaviour in the Arabian babbler. Animal Behav. 61 10.1006/anbe.2001.1838 (2001)
Brown, J. L. Helping and Communal Breeding in Birds (Princeton Univ. Press, 1987)
Clutton-Brock, T. H. Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69–72 (2002)
Russell, A. F. in Ecology and Evolution of Cooperative Breeding in Birds (eds Koenig, W. & Dickinson, J.) 210–227 (Cambridge Univ. Press, 2004)
Lehmann, L. & Keller, L. The evolution of cooperation and altruism: a general framework and classification of models. J. Evol. Biol. 19, 1365–1378 (2006)
Bergmuller, R., Russell, A. F., Johnstone, R. A. & Bshary, R. Integrating cooperative breeding into theoretical concepts of cooperation. Behav. Process. 76, 61–72 (2007)Bergmuller’s review provides a comprehensive classification of types of reciprocity.
West, S. A., Griffin, A. S. & Gardner, A. Evolutionary explanations for cooperation. Curr. Biol. 17, R661–R672 (2007)
Taborsky, M. Cooperation built the Tower of Babel. Behav. Process. 76, 95–99 (2007)
Packer, C. Reciprocal altruism in olive baboons (Papio anubis). Nature 265, 441–443 (1977)
Wilkinson, G. S. Reciprocal food sharing in the vampire bats. Nature 308, 181–184 (1984)
Milinski, M. No alternative to Tit for Tat in sticklebacks. Anim. Behav. 39, 989–991 (1990)
Noë, R. & Hammerstein, P. Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behav. Ecol. Sociobiol. 35, 1–11 (1994)Market theory provides important predictions concerning the magnitude of costs and benefits that apply as much to explanations of cooperation based on mutualistic interactions or manipulative tactics as to those based on reciprocity, so evidence that its predictions are confirmed does not necessarily support the interpretation of cooperative interactions as exchanges.
de Waal, F. B. M. & Berger, M. L. Payment for labour in monkeys. Nature 404, 563 (2000)
Watts, D. P. Reciprocity and interchange in the social relationships of wild male chimpanzees. Behaviour 139, 343–370 (2002)
Gumert, M. D. Payment for sex in a macaque mating market. Anim. Behav. 74, 1655–1667 (2007)
Barras, C. A biological market for monkey prostitution. New Sci. 197, 6 (2008)This article represents an extreme example of the tendency to emphasise similarities between cooperative interactions between non-kin in animals and exchanges in human societies—but there are many others.
Hammerstein, P. in Genetic and Cultural Evolution of Cooperation (ed. Hammerstein, P.) 83–93 (Berlin Univ. Press, 2003)
Smuts, B. B. & Watanabe, J. M. Social relationships and ritualized greetings in adult male baboons Papio cynocephalus . Int. J. Primatol. 11, 147–172 (1990)
McNamara, J. M., Gasson, I. E. & Houston, A. I. Incorporating rules for responding to evolutionary games. Nature 401, 368–371 (1999)
Enquist, M. & Leimar, O. Evolution of cooperation in mobile organisms. Anim. Behav. 45, 747–757 (1993)
Clements, K. C. & Stephens, D. W. Testing models of non-kin cooperation: mutualism and the prisoner's dilemma. Anim. Behav. 50, 527–535 (1995)
Hauser, M. D., Chen, M. K. & Chen, F. Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back. Proc. R. Soc. Lond. B 270, 2363–2370 (2003)
Rutte, C. & Taborsky, M. The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct versus generalised reciprocity. Behav. Ecol. Sociobiol. 62, 499–505 (2008)Rutte and Taborsky provide convincing evidence that prior experience of cooperative interactions in rats affects their tendency to respond cooperatively to other individuals.
Bercovitch, F. B. in Reproductive Ecology and Human Evolution (ed. Ellison, P. T.) 369–396 (Aldine de Gruyter, 2001)
Dawkins, R. The God Delusion (Bantam, 2006)
Wilkinson, G. S. Reciprocal altruism in bats and other mammals. Ethol. Sociobiol. 9, 85–100 (1988)Wilkinson’s study of blood sharing in vampire bats is commonly cited as the classic example of reciprocity but his results do not exclude the possibility that cooperation is maintained by kin selection, mutualism or manipulation.
Gilby, I. C. Meat sharing among the Gombe chimpanzees: harassment and reciprocal exchange. Anim. Behav. 71, 953–963 (2006)
Hart, B. L. & Hart, L. Reciprocal allogrooming in impala. Anim. Behav. 44, 1073–1083 (1992)
Barrett, L., Henzi, S. P., Weingrill, T., Lycett, J. E. & Hill, R. A. Market forces predict grooming reciprocity in female baboons. Proc. R. Soc. Lond. B 266, 665–670 (1999)Barrett and Henzi’s studies of grooming in wild baboons provide some of the most sophisticated evidence that grooming affects the extent of tolerance and the frequency of aggression in natural populations, but can be interpreted as examples of pseudo-reciprocity (or manipulation) as well as of evidence of reciprocity.
Barrett, L. & Henzi, S. P. in Cooperation in Primates and Humans (eds Kappeler, P. M. & Schaik, C. P. v.) 209–232 (Springer, 2006)
Connor, R. C. Impala allogrooming and the parceling model of reciprocity. Anim. Behav. 49, 528–530 (1995)
Creel, S. & Creel, N. M. The African Wild Dog: behavior, ecology and conservation (Princeton Univ. Press, 2001)
Wrangham, R. W. An ecological model of female-bonded primate groups. Behaviour 75, 262–300 (1980)
Clutton-Brock, T. H. in Cooperation in Primates and Humans (eds Kappeler, P. M. & van Schaik, C. P.) 173–190 (Springer, 2006)
de Waal, F. B. M. Chimpanzee Politics (Allen and Unwin, 1982)
Smuts, B. B. Sex and Friendship in Baboons (Aldine, 1985)
Mitani, J. C. Male chimpanzees form enduring and equitable social bonds. Anim. Behav. 77, 633–640 (2009)
Gomes, C. M., Mundry, R. & Boesch, C. Long-term reciprocation of grooming in wild West African chimpanzees. Proc. R. Soc. Lond. B 276, 699–706 (2009)
Seyfarth, R. M. & Cheney, D. L. Grooming alliances and reciprocal altruism in vervet monkeys. Nature 308, 541–543 (1984)
Hemelrijk, C. K. Support for being groomed in long-tailed macques Macaca fascicularis . Anim. Behav. 48, 479–481 (1994)
Silk, J. B., Alberts, S. C. & Altmann, J. Social bonds of female baboons enhance infant survival. Science 302, 1331–1334 (2003)
Boyd, R. & Richerson, P. J. The evolution of reciprocity in sizeable groups. J. Theor. Biol. 132, 337–356 (1988)
Dugatkin, L. A. Cooperation Among Animals: An Evolutionary Perspective (Oxford Univ. Press, 1997)Dugatkin’s comprehensive review of cooperative behaviour in animals provides an important synthesis of theory and evidence.
Wilson, D. S. & Wilson, E. O. Rethinking the theoretical foundation of sociobiology. Q. Rev. Biol. 82, 327–348 (2007)
West, S. A., Griffin, A. S. & Gardiner, A. Social semantics: how useful has group selection been? J. Evol. Biol. 21, 374–385 (2007b)
Gardiner, A. & Grafen, A. Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. 22, 659–671 (2009)
Hauser, M. D. Costs of deception: cheaters are punished in rhesus monkeys Macaque mulatta . Proc. Natl Acad. Sci. USA 89, 12137–12139 (1992)
Connor, R. C. Altruism among non-relatives: alternatives to the 'prisoner's dilemma'. Trends Ecol. Evol. 10, 84–86 (1995)
Bourke, A. F. G. in Behavioural Ecology: an Evolutionary Approach (eds Krebs, J. R. & Davies, N. B.) 203–227 (Blackwell, 1997)
Barrett, L., Gaynor, D. & Henzi, S. P. A dynamic interaction between aggression and grooming reciprocity among female chacma baboons. Anim. Behav. 63, 1047–1053 (2002)
Cheney, D. L. & Seyfarth, R. M. Baboon Metaphysics: the Evolution of a Social Mind (Univ. Chicago Press, 2007)
Henzi, S. P. & Barrett, L. Infants as a commodity in a baboon market. Anim. Behav. 63, 915–921 (2002)
de Waal, F. B. M. The integration of dominance and social bonding in primates. Q. Rev. Biol. 61, 459–479 (1986)
Aureli, F., van Schaik, C. P. & van Hoof, J. Functional aspects of reconciliation among captive long-tailed macaques. Am. J. Primatol. 19, 39–51 (1989)
Aureli, F. Post-conflict behaviour among wild long-tailed macaques Macaca fascicularis . Behav. Ecol. Sociobiol. 31, 329–337 (1992)
Seed, A. M., Clayton, N. S. & Emery, N. J. Postconflict third-party affiliation in rooks, Corvus frugilegus . Curr. Biol. 17, 1–7 (2007)
Turchin, P. War and Peace and War: the Rise and Fall of Empires (Pi Press, 2005)
Richerson, P. J. & Boyd, R. Not By Genes Alone: How Culture Transformed Human Evolution (Univ. Chicago Press, 2005)
Smith, E. A. in Genetic and Cultural Evolution of Cooperation (ed. Hammerstein, P.) 401–428 (Dahlem Univ. Press, 2003)
Stevens, J. R. & Hauser, M. D. Why be nice? Psychological constraints on the evolution of cooperation. Trends Cogn. Sci. 8, 60–65 (2004)
Boyd, R., Gintis, H., Bowles, S. & Richerson, P. J. The evolution of altruistic punishment. Proc. Natl Acad. Sci. USA 100, 3531–3535 (2003)
Grafen, A. How not to measure inclusive fitness. Nature 298, 425–426 (1982)
Grafen, A. in Behavioural Ecology: an Evolutionary Approach (eds Krebs, J. R. & Davies, N. B.) 62–84 (Blackwell, 1984)
Trivers, R. L. & Hare, H. Haplo-diploidy and the evolution of the social insects. Science 191, 249–263 (1976)
Bourke, A. F. G. & Franks, N. R. Social Evolution in Ants (Princeton Univ. Press, 1995)
Solomon, N. G. & French, J. A. Cooperative Breeding in Mammals (Cambridge Univ. Press, 1997)
Koenig, W. & Dickinson, J. Ecology and Evolution of Cooperative Breeding in Birds (Cambridge Univ. Press, 2004)
Boomsma, J. J. Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17, R673–R683 (2007)
Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216 (2008)
Emlen, S. T. & Wrege, P. H. The role of kinship in helping decisions among white-fronted bee-eaters. Behav. Ecol. Sociobiol. 23, 305–315 (1988)
Hatchwell, B. J., Ross, D. J., Fowlie, M. K. & McGowan, A. Kin discrimination in cooperatively breeding long-tailed tits. Proc. R. Soc. Lond. B 268, 885–890 (2001b)
Boncoraglio, G. & Saino, N. Barn swallow chicks beg more loudly when brood mates are unrelated. J. Evol. Biol. 21, 256–262 (2007)
Packer, C. et al. in Reproductive Success (ed. Clutton-Brock, T. H.) 363–383 (Univ. Chicago Press, 1988)
Heinsohn, R. G. & Packer, C. Complex cooperative strategies in group-territorial African lions. Science 269, 1260–1262 (1995)
Rood, J. P. Banded mongoose rescues back member from eagle. Anim. Behav. 31, 1261–1262 (1983)
Young, P. in Genetic and Cultural Evolution of Cooperation (ed. Hammerstein, P.) (Dahlem Univ. Press, 2003)
I thank M. Bell, S. Bowles, R. Boyd, M. Cant, A. Cockburn, N. Davies, A. Gardner, S. Hodge, R. Johnstone, A. Russell, S. Sharp, J. Silk, J. Stevens, M. Taborsky and S. West for discussions or for comments on this manuscript. I also thank C. R. Packer and R. Woodroffe for the use of their photographs.
About this article
Cite this article
Clutton-Brock, T. Cooperation between non-kin in animal societies. Nature 462, 51–57 (2009). https://doi.org/10.1038/nature08366
This article is cited by
Behavioral Ecology and Sociobiology (2023)
The portrayal of animal interactions in nature documentaries by David Attenborough and Bernhard Grzimek
Evolution: Education and Outreach (2022)
Scientific Reports (2022)
Integrative Psychological and Behavioral Science (2022)
Kin-structured cooperatively breeding groups due to limited dispersal in the obligate shell-brooding cichlid Neolamprologus meeli
Behavioral Ecology and Sociobiology (2022)