Abstract
Cooperation among non-kin has been attributed sometimes to reciprocal altruism: Two or more individuals exchange behaviour that benefits the respective partner. According to direct reciprocity, cooperation is based on past behaviour of a known partner. In contrast, in generalised reciprocity, cooperation is based on anonymous social experience where the identity of the partner is irrelevant. In a previous study, female Norway rats (Rattus norvegicus) were found to cooperate according to a generalised reciprocity mechanism. In this study, we tested whether Norway rats would also cooperate as predicted by a direct reciprocity mechanism and whether direct reciprocity would cause a higher propensity to cooperate than generalised reciprocity. Focal animals were experimentally manipulated to receive social experience from known or unknown, helpful or defecting partners in an instrumental cooperative task. Our first experiment shows that rats are more helpful towards a partner from which they had received help before than towards a partner that had not helped (i.e. direct reciprocity). Our second experiment revealed that after receiving help by others, rats were more helpful towards a partner from which they had received help before than towards a new partner (i.e. direct reciprocity generated a higher cooperation propensity than generalised reciprocity). We conclude that in female Norway rats, the tendency to cooperate is influenced by partner-specific information. To our knowledge, this is the first study to demonstrate direct reciprocity in rodents, and it is the first study testing direct vs generalised reciprocity in animals.
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Alexander RD (1987) The biology of moral systems. Aldine de Gruyter, New York
Axelrod R, Hamilton WD (1981) The evolution of cooperation. Science 211:1390–1396
Barrett L, Henzi SP, Weingrill T, Lycett JE, Hill RA (2000) Female baboons do not raise the stakes but they give as good as they get. Anim Behav 59:763–770
Berkowitz L, Daniels L (1964) Affecting the salience of the social responsibility norm: effects of past help on the response to dependency relationships. J Abnorm Soc Psychol 68:275–281
Boyd R, Richerson PJ (1989) The evolution of indirect reciprocity. Soc Netw 11:213–236
Brosnan SF, de Waal FBM (2002). A proximate perspective on reciprocal altruism. Hum Nat 13:129–152 (An Interdisciplinary Biosocial Perspective)
Bshary R, Grutter AS (2006) Image scoring and cooperation in a cleaner fish mutualism. Nature 441:975–978
Burman OHP, Mendl M (2000) Short-term social memory in the laboratory rat: its susceptibility to disturbance. Appl Anim Behav Sci 67:241–254
Clements KC, Stephens DW (1995) Testing models of non-kin cooperation: mutualism and the Prisoner’s Dilemma. Anim Behav 50:527–535
De Waal FBM (1997) Food transfers through mesh in brown capuchins. J Comp Psychol 111:370–378
De Waal FBM, Berger ML (2000) Payment for labour in monkeys. Nature 404:563
Dugatkin A (1997) Cooperation among animals. Oxford University Press, Oxford
Dugatkin LA, Alfieri M (1991) Guppies and the TIT FOR TAT strategy: preference based on past interaction. Behav Ecol Sociobiol 28:243–246
Gheusi G (1997) Individually distinctive odours represent individual conspecifics in rats. Anim Behav 53:935–944
Gheusi G, Bluthé R-M, Goodall G, Dantzer R (1994) Social and individual recognition in rodents: methodological aspects and neurobiological bases. Behav Processes 33:59–88
Godard R (1993) Tit for tat among neighbouring hooded warblers. Behav Ecol Sociobiol 33:45–50
Hamilton IM, Taborsky M (2005) Contingent movement and cooperation under generalized reciprocity. Proc R Soc B 272:2259–2267
Hauser MD, Chen MK, Chen F, Chuang E (2003) Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back. Proc R Soc B 270:2363–2370
Hsu Y, Wolf LL (1999) The winner and loser effect: integrating multiple experiences. Anim Behav 57:903–910
Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E (2005) Oxytocin increases trust in humans. Nature 435:673–676
Krams I, Krama T (2002) Interspecific reciprocity explains mobbing behaviour of the breeding chaffinches, Fringilla coelebs. Proc R Soc Lond B 269:2345–2350
Leimar O, Hammerstein P (2001) Evolution of cooperation through indirect reciprocity. Proc R Soc B 268:745–753
Milinski M, Wedekind C (1998) Working memory constrains human cooperation in the Prisoner’s Dilemma. Proc Natl Acad Sci 95:13755–13758
Milinski M, Pfluger D, Külling D, Kettler R (1990) Do sticklebacks cooperate repeatedly in reciprocal pairs? Behav Ecol Sociobiol 27:17–21
Milinski M, Semmann D, Bakker TCM, Krambeck HJ (2001) Cooperation through indirect reciprocity: image scoring or standing strategy? Proc R Soc B 268:2495–2501
Nowak MA, Sigmund K (1994) The alternating Prisoner’s Dilemma. J Theor Biol 168:219–356
Nowak MA, Sigmund K (1998) The dynamics of indirect reciprocity. J Theor Biol 194:561–574
Nowak MA, Sigmund K (2005) Evolution of indirect reciprocity. Nature 437:1291–1298
Olendorf R, Getty T, Scribner K (2004) Cooperative nest defence in red-winged blackbirds: reciprocal altruism, kinship or by-product mutualism? Proc R Soc Lond B 271:177–182
Pfeiffer T, Rutte C, Killingback T, Taborsky M, Bonhoeffer S (2005) Evolution of cooperation through generalized reciprocity. Proc R Soc B 272:1115–1120
Rilling JK, Gutman DA, Zeh TR, Pagnoni G, Berns GS, Kilts CD (2002) A neural basis for social cooperation. Neuron 35:395–405
Rutte C, Taborsky M (2007) Generalized reciprocity in rats. PLoS PLoS Biol 5(7):e196
Rutte C, Brinkhof MWG, Taborsky M (2006) What sets the odds of winning and losing? Trends Ecol Evol 21:16–21
Schuster R (2002) Cooperative coordination as a social behavior—experiments with an animal model. Hum Nat 13:47–83 (An Interdisciplinary Biosocial Perspective)
Schuster R, Perelberg A (2004) Why cooperate? An economic perspective is not enough. Behav Processes 66:261–277
Semmann D, Krambeck HJ, Milinski M (2005) Reputation is valuable within and outside one’s own social group. Behav Ecol Sociobiol 57:611–616
Stephens DW, Anderson JP, Benson KE (1997) On the spurious occurrence of Tit for Tat in pairs of predator-approaching fish. Anim Behav 53:113–131
Stevens JR, Hauser MD (2004) Why be nice? Psychological constraints on the evolution of cooperation. Trends Cogn Sci 8:60–65
Stevens JR, Cushman FA, Hauser MD (2005) Evolving the psychological mechanisms for cooperation. Ann Rev Ecolog Syst 36:499–518
Telle H-J (1966) Beitrag zur Kenntnis der Verhaltensweise von Ratten, vergleichend dargestellt bei Rattus norvegicus und Rattus rattus. Z für Angewandte Zoologie 53:129–196
Trivers R (1971) The evolution of reciprocal altruism. Quart Rev Biol 46:35–57
Uvnas-Moberg K (1998) Oxytocin may mediate the benefits of positive social interaction and emotions. Psychoneuroendocrinology 23:819–835
Wedekind C, Milinski M (2000) Cooperation through image scoring in humans. Science 288:850–852
White NM, Hiroi N (1998) Preferential localization of self-stimulation sites in striosomes/patches in the rat striatum. Proc Natl Acad Sci USA 95:6486–6491
Wilkinson GS (1984) Reciprocal food sharing in the vampire bat. Nature 308:181–184
Acknowledgements
We are grateful to anonymous referees for helpful comments on an earlier version of the manuscript. The housing of the rats and the experimental procedure adhered to the Association for the Study of Animal Behaviour Guidelines for the Use of Animals in Research and were approved by the Swiss Federal Veterinary Office.
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Communicated by F. Trillmich.
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Rutte, C., Taborsky, M. The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct vs generalised reciprocity. Behav Ecol Sociobiol 62, 499–505 (2008). https://doi.org/10.1007/s00265-007-0474-3
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DOI: https://doi.org/10.1007/s00265-007-0474-3