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Image scoring and cooperation in a cleaner fish mutualism

Nature volume 441, pages 975–978 (2006)Cite this article

Abstract

Humans are highly social animals and often help unrelated individuals that may never reciprocate the altruist's favour1,2,3,4,5. This apparent evolutionary puzzle may be explained by the altruist's gain in social image: image-scoring bystanders, also known as eavesdroppers, notice the altruistic act and therefore are more likely to help the altruist in the future5,6,7. Such complex indirect reciprocity based on altruistic acts may evolve only after simple indirect reciprocity has been established, which requires two steps. First, image scoring evolves when bystanders gain personal benefits from information gathered, for example, by finding cooperative partners8,9,10. Second, altruistic behaviour in the presence of such bystanders may evolve if altruists benefit from access to the bystanders. Here, we provide experimental evidence for both of the requirements in a cleaning mutualism involving the cleaner fish Labroides dimidiatus. These cleaners may cooperate and remove ectoparasites from clients or they may cheat by feeding on client mucus11,12. As mucus may be preferred over typical client ectoparasites13, clients must make cleaners feed against their preference to obtain a cooperative service. We found that eavesdropping clients spent more time next to ‘cooperative’ than ‘unknown cooperative level’ cleaners, which shows that clients engage in image-scoring behaviour. Furthermore, trained cleaners learned to feed more cooperatively when in an ‘image-scoring’ than in a ‘non-image-scoring’ situation.

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Figure 1: Experimental set-up to test for image scoring.
Figure 2: Client fish conduct image scoring.
Figure 3: Experimental set-up to test for indirect reciprocity.
Figure 4: Indirect reciprocity because of image scoring.

References

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

    Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  ADS  PubMed  Google Scholar 

  5. Nowak, M. A. & Sigmund, K. Evolution of indirect reciprocity. Nature 437, 1291–1298 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Zahavi, A. Altruism as a handicap–the limitations of kin selection and reciprocity. J. Avian Biol. 26, 1–3 (1995)

    Article  Google Scholar 

  9. Roberts, G. Competitive altruism: from reciprocity to the handicap principle. Proc. R. Soc. Lond. B 265, 427–431 (1998)

    Article  Google Scholar 

  10. Lotem, A., Fishman, M. A. & Stone, L. From reciprocity to unconditional altruism through signaling benefits. Proc. R. Soc. Lond. B 270, 199–205 (2003)

    Article  Google Scholar 

  11. Grutter, A. S. Spatio-temporal variation and feeding selectivity in the diet of the cleaner fish Labroides dimidiatus. Copeia 1997, 346–355 (1997)

    Article  Google Scholar 

  12. Arnal, C. & Côté, I. M. Diet of broadstrip cleaning gobies on a Barbadian reef. J. Fish Biol. 57, 1075–1082 (2000)

    Article  Google Scholar 

  13. Grutter, A. S. & Bshary, R. Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions. Proc. R. Soc. Lond. B 270 (suppl.), 242–244 (2003)

    Google Scholar 

  14. McGregor, P. K. Signalling in territorial systems: a context for individual identification, ranging and eavesdropping. Phil. Trans. R. Soc. Lond. B 340, 237–244 (1993)

    Article  ADS  Google Scholar 

  15. McGregor, P. K. (ed.) Animal Communication Networks (Cambridge Univ. Press, Cambridge, 2005)

  16. Johnstone, R. A. Eavesdropping and animal conflict. Proc. Natl Am. Soc. 98, 9177–9180 (2001)

    Article  ADS  CAS  Google Scholar 

  17. Johnstone, R. A. & Bshary, R. The evolution of spiteful behaviour. Proc. R. Soc. Lond. B 271, 1917–1922 (2004)

    Article  Google Scholar 

  18. Sherratt, T. N. & Roberts, G. The role of phenotypic defectors in stabilizing reciprocal altruism. Behav. Ecol. 12, 313–317 (2001)

    Article  Google Scholar 

  19. Matos, R. J. & Schlupp, I. In Animal Communication Networks (ed. McGregor, P. K.) 84–113 (Cambridge Univ. Press, Cambridge, 2005)

    Google Scholar 

  20. Bshary, R. & Bronstein, J. L. Game structures in mutualisms: what can the evidence tell us about the kind of models we need? Adv. Stud. Behav. 34, 59–101 (2004)

    Article  Google Scholar 

  21. Bshary, R. & Noë, R. In Genetic and Cultural Evolution of Cooperation (ed. Hammerstein, P.) 167–184 (MIT Press, Cambridge, 2003)

    Google Scholar 

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

    Article  Google Scholar 

  23. Bshary, R. In Economics in Nature (eds Noë, R., van Hooff, J. A. R. A. M. & Hammerstein, P.) 146–172 (Cambridge Univ. Press, Cambridge, 2001)

    Book  Google Scholar 

  24. Dugatkin, L. A. Cooperation Among Animals: An Evolutionary Perspective (Oxford Univ. Press, Oxford, 1997)

    Google Scholar 

  25. Bshary, R. Biting cleaner fish use altruism to deceive image scoring clients. Proc. R. Soc. Lond. B 269, 2087–2093 (2002)

    Article  Google Scholar 

  26. Bshary, R. & D'Souza, A. In Communication Networks (ed. McGregor, P.) 521–539 (Cambridge Univ. Press, Cambridge, 2005)

    Google Scholar 

  27. Bshary, R. & Grutter, A. S. Punishment and partner switching cause cooperative behaviour in a cleaning mutualism. Biol. Lett. 1, 396–399 (2005)

    Article  PubMed  PubMed Central  Google Scholar 

  28. Dutreland, C., McGregor, P. K. & Oliveira, R. F. The effect of an audience on intrasexual communication in male Siamese fighting fish, Betta splendens. Behav. Ecol. 12, 283–286 (2001)

    Article  Google Scholar 

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Acknowledgements

We thank the Lizard Island Research Station for their continuous support and friendship, and W. Wickler for his support and for discussions on this topic. R. Bergmüller, K. Cheney, P. Munday and M. Blows provided substantial comments on earlier drafts. Funding was provided by NERC (R.B) and the Australian Research Council (A.S.G.).

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Authors and Affiliations

  1. Department of Zoology, University of Neuchâtel, Neuchâtel, Rue Emile-Argand 11, Case postale 158, 2009, Switzerland

    Redouan Bshary

  2. University of Queensland, School of Integrative Biology, St Lucia, QLD, 4072, Australia

    Alexandra S. Grutter

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  1. Redouan Bshary
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  2. Alexandra S. Grutter
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Correspondence to Redouan Bshary.

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Bshary, R., Grutter, A. Image scoring and cooperation in a cleaner fish mutualism. Nature 441, 975–978 (2006). https://doi.org/10.1038/nature04755

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