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Evolution of indirect reciprocity

Abstract

Natural selection is conventionally assumed to favour the strong and selfish who maximize their own resources at the expense of others. But many biological systems, and especially human societies, are organized around altruistic, cooperative interactions. How can natural selection promote unselfish behaviour? Various mechanisms have been proposed, and a rich analysis of indirect reciprocity has recently emerged: I help you and somebody else helps me. The evolution of cooperation by indirect reciprocity leads to reputation building, morality judgement and complex social interactions with ever-increasing cognitive demands.

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Figure 1: Direct and indirect reciprocity.
Figure 2: Building a reputation.
Figure 3: Two problems with indirect reciprocity. B has defected in previous rounds and therefore has a low reputation.

References

  1. Trivers, R. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57 (1971)

    Article  Google Scholar 

  2. Alexander, R. D. The Biology of Moral Systems (Aldine de Gruyter, New York, 1987)

    Google Scholar 

  3. Binmore, K. G. Game Theory and the Social Contract (MIT Press, Cambridge, Massachusetts, 1994)

    MATH  Google Scholar 

  4. Seabright, P. The Company of Strangers: A Natural History of Economic Life (Princeton Univ. Press, Princeton, 2004)

    Google Scholar 

  5. Bolton, G. E., Katok, E. & Ockenfels, A. How effective are electronic reputation mechanisms? An experimental investigation. Manage. Sci. 50, 1587–1602 (2004)

    Article  Google Scholar 

  6. Keser, C. Trust and reputation building in e-commerce. IBM Watson Research Center, CIRANO working paper no. 2002s-75 http://www.cirano.qc.ca/en/publication_detail.php?id=2002s-75 (2002).

  7. Dellarocas, C. Sanctioning reputation mechanisms in online trading environments with moral hazard. MIT Sloan School of Management working paper no. 4297–03 http://ssrn.com/abstract=393043 (2003).

  8. Bolton, G., Katok, E. & Ockenfels, A. in Applications of Supply Chain Management and e-Commerce Research (eds Geunes, J., Akcali, E., Pardalos, P. M., Romeijn, H. E. & Shen, Z.-J.) 195–216 (Springer, Dordrecht, 2005)

    Book  Google Scholar 

  9. Resnick, P., Zeckhauser, R., Friedman, E. & Kuwabara, K. Reputation systems. Commun. ACM 43, 45–48 (2000)

    Article  Google Scholar 

  10. Lucking-Reiley, D., Bryan, D., Prasad, N. & Reeves, D. Pennies from eBay: The Determinants of Price in Online Auctions. Vanderbilt Univ., Univ. Arizona working paper (1999).

  11. Maynard Smith, J. & Szathmary, E. The Major Transitions in Evolution (Oxford Univ. Press, Oxford, 1997)

    Google Scholar 

  12. Wilson, E. O. Sociobiology (Harvard Univ. Press, Cambridge, Massachusetts, 1975)

    Google Scholar 

  13. Trivers, R. Social Evolution (Benjamin Cummings, Menlo Park, 1985)

    Google Scholar 

  14. Hamilton, W. D. Narrow Roads of Gene Land Vol. 1 (Freeman, New York, 1996)

    Google Scholar 

  15. Sanfey, A. G., Rilling, J. K., Aronson, J. A., Nystrom, L. E. & Cohen, J. D. The neural basis of economic decision-making in the ultimatum game. Science 300, 1755–1758 (2003)

    ADS  CAS  Article  Google Scholar 

  16. Rilling, J. K. et al. A neural basis for social cooperation. Neuron 35, 395–405 (2002)

    CAS  Article  Google Scholar 

  17. Fehr, E. The neural basis of altruistic punishment. Science 305, 1254–1258 (2004)

    ADS  Article  Google Scholar 

  18. Dunbar, R. Grooming, Gossip and the Evolution of Language (Harvard Univ. Press, Cambridge, Massachusetts, 1996)

    Google Scholar 

  19. Brown, D. E. Human Universals (McGraw-Hill, New York, 1991)

    Google Scholar 

  20. Whiten, A. & Byrne, R. W. (eds) Machiavellian Intelligence II: Extensions and Evaluations (Cambridge Univ. Press, Cambridge, UK, 1997)

  21. Axelrod, R. The Evolution of Cooperation (Reprinted by Penguin, Harmondsworth, 1989.) (Basic Books, New York, 1984)

    MATH  Google Scholar 

  22. Nowak, M. A. & Sigmund, K. The alternating prisoner's dilemma. J. Theor. Biol. 168, 219–226 (1994)

    Article  Google Scholar 

  23. Frean, M. R. The prisoner's dilemma without synchrony. Proc. R. Soc. Lond. B 257, 75–79 (1994)

    ADS  CAS  Article  Google Scholar 

  24. Berg, J., Dickhaut, J. & McCabe, K. Trust, reciprocity and social history. Games Econ. Behav. 10, 122–142 (1995)

    Article  Google Scholar 

  25. Fudenberg, D. & Maskin, E. The folk theorem in repeated games with discounting or with incomplete information. Econometrica 50, 533–554 (1986)

    MathSciNet  Article  Google Scholar 

  26. Binmore, K. Fun and Games: A Text on Game Theory (Heath, Lexington, Massachusetts, 1992)

    MATH  Google Scholar 

  27. Rosenthal, R. W. Sequences of games with varying opponents. Econometrica 47, 1353–1366 (1979)

    MathSciNet  Article  Google Scholar 

  28. Kandori, M. Social norms and community enforcement. Rev. Econ. Stud. 59, 63–80 (1992)

    MathSciNet  Article  Google Scholar 

  29. Ellison, G. Cooperation in the prisoner's dilemma with anonymous random matching. Rev. Econ. Stud. 61, 567–588 (1994)

    MathSciNet  Article  Google Scholar 

  30. Okuno-Fujiwara, M. & Postlewaite, A. Social norms in matching games. Games Econ. Behav. 9, 79–109 (1995)

    Article  Google Scholar 

  31. Nowak, M. A. & Sigmund, K. Evolutionary dynamics of biological games. Science 303, 793–799 (2004)

    ADS  CAS  Article  Google Scholar 

  32. Nowak, M. A. & Sigmund, K. Tit for tat in heterogeneous populations. Nature 355, 250–253 (1992)

    ADS  Article  Google Scholar 

  33. Nowak, M. A., Sasaki, A., Taylor, C. & Fudenberg, D. Emergence of cooperation and evolutionary stability in finite populations. Nature 428, 646–650 (2004)

    ADS  CAS  Article  Google Scholar 

  34. Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981)

    ADS  MathSciNet  CAS  Article  Google Scholar 

  35. Nowak, M. A. & Sigmund, K. A strategy of win-stay, lose-shift that outperforms tit-for-tat in the prisoner's dilemma game. Nature 364, 56–58 (1993)

    ADS  CAS  Article  Google Scholar 

  36. Nowak, M. A. & Sigmund, K. Evolution of indirect reciprocity by image scoring. Nature 393, 573–577 (1998)

    ADS  CAS  Article  Google Scholar 

  37. Wedekind, C. Give and ye shall be recognized. Science 280, 2070–2071 (1998)

    CAS  Article  Google Scholar 

  38. Ferrière, R. Help and you shall be helped. Nature 393, 517–519 (1998)

    ADS  Article  Google Scholar 

  39. Leimar, O. & Hammerstein, P. Evolution of cooperation through indirect reciprocation. Proc. R. Soc. Lond. B 268, 745–753 (2001)

    CAS  Article  Google Scholar 

  40. Panchanathan, K. & Boyd, R. A tale of two defectors: The importance of standing for evolution of indirect reciprocity. J. Theor. Biol. 224, 115–126 (2003)

    MathSciNet  Article  Google Scholar 

  41. Nowak, M. A. & Sigmund, K. The dynamics of indirect reciprocity. J. Theor. Biol. 194, 561–574 (1998)

    CAS  Article  Google Scholar 

  42. Ohtsuki, H. & Iwasa, Y. How should we define goodness? Reputation dynamics in indirect reciprocity. J. Theor. Biol. 231, 107–120 (2004)

    MathSciNet  Article  Google Scholar 

  43. Dawes, R. M. Social dilemmas. Annu. Rev. Psychol. 31, 169–193 (1980)

    Article  Google Scholar 

  44. Fehr, E. & Gächter, S. Cooperation and punishment in public goods experiments. Am. Econ. Rev. 90, 980–994 (2000)

    Article  Google Scholar 

  45. Fehr, E. & Gächter, S. Altruistic punishment in humans. Nature 415, 137–140 (2002)

    ADS  CAS  Article  Google Scholar 

  46. Fehr, E. & Fischbacher, U. The nature of human altruism. Nature 425, 785–791 (2003)

    ADS  CAS  Article  Google Scholar 

  47. Sigmund, K., Hauert, C. & Nowak, M. A. Reward and punishment. Proc. Natl Acad. Sci. USA 98, 10757–10762 (2001)

    ADS  CAS  Article  Google Scholar 

  48. Sugden, R. The Economics of Rights, Cooperation and Welfare (Blackwell, Oxford, 1986)

    Google Scholar 

  49. Ohtsuki, H. & Iwasa, Y. The leading eight: social norms that can maintain cooperation by indirect reciprocity. J. Theor. Biol.(in the press)

  50. Lotem, A., Fishman, M. A. & Stone, L. Evolution of cooperation between individuals. Nature 400, 226–227 (1999)

    ADS  CAS  Article  Google Scholar 

  51. Lotem, A., Fishman, M. A. & Stone, L. Evolution of unconditional altruism through signalling benefits. Proc. R. Soc. Lond. B 270, 199–205 (2002)

    Article  Google Scholar 

  52. Fishman, M. A., Lotem, A. & Stone, L. Heterogeneity stabilises reciprocal altruism interaction. J. Theor. Biol. 209, 87–95 (2001)

    CAS  Article  Google Scholar 

  53. Fishman, M. A. Indirect reciprocity among imperfect individuals. J. Theor. Biol. 225, 285–292 (2003)

    Article  Google Scholar 

  54. Brandt, H. & Sigmund, K. The logic of reprobation: Assessment and action rules for indirect reciprocity. J. Theor. Biol. 231, 475–486 (2004)

    Article  Google Scholar 

  55. Mohtashemi, M. & Mui, L. Evolution of indirect reciprocity by social information: The role of trust and reputation in evolution of altruism. J. Theor. Biol. 223, 523–531 (2003)

    MathSciNet  Article  Google Scholar 

  56. Brandt, H. & Sigmund, K. Indirect reciprocity, image scoring, and moral hazard. Proc. Natl Acad. Sci. USA 102, 2666–2670 (2005)

    ADS  CAS  Article  Google Scholar 

  57. Takahashi, N. & Mashima, R. The emergence of indirect reciprocity: Is the standing strategy the answer? Hokkaido Univ. working paper no. 29 http://lynx.let.hokudai.ac.jp/COE21/pdf/029.zip (2003).

  58. Wilson, D. S. A theory of group selection. Proc. Natl Acad. Sci. USA 72, 143–146 (1975)

    ADS  CAS  Article  Google Scholar 

  59. Wedekind, C. & Milinski, M. Cooperation through image scoring in humans. Science 288, 850–852 (2000)

    ADS  CAS  Article  Google Scholar 

  60. Seinen, I. & Schram, A. Social status and group norms: Indirect reciprocity in a repeated helping experiment. Eur. Econ. Rev. (in the press)

  61. Haley, K. J. & Kessler, D. M. T. Nobody is watching?: Subtle cues affect generosity in an anonymous economic game. Evol. Hum. Behav. 26, 245–256 (2005)

    Article  Google Scholar 

  62. Bolton, G. E., Katok, E. & Ockenfels, A. Cooperation among strangers with limited information about reputation. J. Public Econ. 89, 1457–1468 (2005)

    Article  Google Scholar 

  63. Wedekind, C. & Braithwaite, V. A. The long-term benefits of human generosity in indirect reciprocity. Curr. Biol. 12, 1012–1015 (2002)

    CAS  Article  Google Scholar 

  64. Engelmann, D. & Fischbacher, U. Indirect reciprocity and strategic reputation building in an experimental helping game. Univ. Zürich working paper no. 132 http://www.iew.unizh.ch/wp/iewwp132.pdf (2002).

  65. Milinski, M., Semmann, D., Bakker, T. C. M. & Krambeck, H. J. Cooperation through indirect reciprocity: Image scoring or standing strategy? Proc. R. Soc. Lond. B 268, 2495–2501 (2001)

    CAS  Article  Google Scholar 

  66. Greiner, B. & Levati, M. V. Indirect reciprocity in cyclical networks: An experimental study. Max Planck Institute, Jena, working paper no. 2003-15 ftp://papers.mpiew-jena.mpg.de/esi/discussionpapers/2003-15.pdf (2003).

  67. Dufwenberg, M., Gneezy, U., Güth, W. & van Damme, E. Direct vs indirect reciprocity: An experiment. Homo Oecon. 18, 19–30 (2001)

    Google Scholar 

  68. Güth, W., Königstein, M., Marchand, N. & Nehring, K. Trust and reciprocity in the investment game with indirect reward. Homo Oecon. 18, 241–262 (2001)

    Google Scholar 

  69. Pollock, G. B. & Dugatkin, L. A. Reciprocity and the evolution of reputation. J. Theor. Biol. 159, 25–37 (1992)

    Article  Google Scholar 

  70. Gintis, H. Game Theory Evolving: A Problem-Centered Introduction to Modeling Stategic Interaction (Princeton Univ. Press, Princeton, 2000)

    MATH  Google Scholar 

  71. Fehr, E. & Fischbacher, U. Social norms and human cooperation. Trends Cogn. Sci. 8, 185–190 (2004)

    Article  Google Scholar 

  72. Fehr, E. & Fischbacher, U. Third party punishment and social norms. Evol. Hum. Behav. 25, 63–87 (2004)

    Article  Google Scholar 

  73. Milinski, M., Semmann, D. & Krambeck, H. J. Donors in charity gain in both indirect reciprocity and political reputation. Proc. R. Soc. Lond. B 269, 881–883 (2002)

    Article  Google Scholar 

  74. Milinski, M., Semmann, D. & Krambeck, H. J. Reputation helps solve the ‘tragedy of the commons’. Nature 415, 424–426 (2002)

    ADS  Article  Google Scholar 

  75. Panchanathen, K. & Boyd, R. Indirect reciprocity can stabilize cooperation without the second-order free-rider problem. Nature 432, 499–502 (2004)

    ADS  Article  Google Scholar 

  76. Fehr, E. Don't lose your reputation. Nature 432, 449–450 (2004)

    ADS  CAS  Article  Google Scholar 

  77. Boyd, R. & Richerson, P. J. The evolution of indirect reciprocity. Soc. Networks 11, 213–236 (1989)

    MathSciNet  Article  Google Scholar 

  78. Pfeiffer, T., Rutte, C., Killingback, T., Taborsky, M. & Bonhoeffer, S. Evolution of cooperation by generalized reciprocity. Proc. R. Soc. B 272, 1115–1120 (2005)

    Article  Google Scholar 

  79. Brandt, H. & Sigmund, K. The good, the bad and the discriminator. J. Theor. Biol. (in the press)

  80. Imhof, L., Fudenberg, D. & Nowak, M. A. Evolutionary cycles of cooperation and defection. Proc. Natl Acad. Sci. USA 102, 10797–10800 (2005)

    ADS  CAS  Article  Google Scholar 

  81. Camerer, C. E. Behavioral Game Theory (Princeton Univ. Press, Princeton, 2003)

    MATH  Google Scholar 

  82. Colman, A. M. Game Theory and its Applications in the Social and Biological Sciences (Butterworth-Heinemann, Oxford, 1995)

    Google Scholar 

  83. Arrow, K. The Limits of Organization (Norton, New York, 1974)

    Google Scholar 

  84. Kosfeld, M., Heinrichs, M., Zak, P., Fischbacher, U. & Fehr, E. Oxytocin increases trust in humans. Nature 435, 673–676 (2005)

    ADS  CAS  Article  Google Scholar 

  85. Milgrom, P., North, D. & Weingast, B. The role of institutions in the revival of trade: The law merchant, private judges, and the champagne fairs. Econ. Politics 2, 1–23 (1990)

    Article  Google Scholar 

  86. Suzuki, Y. & Toquenaga, Y. Effects of information and group structure on evolution of altruism: Analysis of two-score model by covariance and contextual analyses. J. Theor. Biol. 232, 191–203 (2005)

    MathSciNet  Article  Google Scholar 

  87. Fudenberg, D. & Maskin, E. Evolution of cooperation in noisy repeated games. American Economic Reviewl. 80, 274–279 (1990)

    Google Scholar 

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Acknowledgements

Support from the John Templeton Foundation is gratefully acknowledged. The Program for Evolutionary Dynamics at Harvard University is sponsored by Jeffrey Epstein.

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Correspondence to Karl Sigmund.

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Nowak, M., Sigmund, K. Evolution of indirect reciprocity. Nature 437, 1291–1298 (2005). https://doi.org/10.1038/nature04131

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