Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Promiscuity and the evolutionary transition to complex societies

Abstract

Theory predicts that the evolution of cooperative behaviour is favoured by low levels of promiscuity leading to high within-group relatedness1,2,3,4,5. However, in vertebrates, cooperation often occurs between non-relatives and promiscuity rates are among the highest recorded. Here we resolve this apparent inconsistency with a phylogenetic analysis of 267 bird species, demonstrating that cooperative breeding is associated with low promiscuity; that in cooperative species, helping is more common when promiscuity is low; and that intermediate levels of promiscuity favour kin discrimination. Overall, these results suggest that promiscuity is a unifying feature across taxa in explaining transitions to and from cooperative societies.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The monogamy hypothesis.
Figure 2: Making sense of the diversity.
Figure 3: Promiscuity and cooperation.
Figure 4: Promiscuity and the transition to and from cooperative breeding.
Figure 5: Kin discrimination and rates of promiscuity.

Similar content being viewed by others

References

  1. Boomsma, J. J. Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17, R673–R683 (2007)

    Article  CAS  PubMed  Google Scholar 

  2. Boomsma, J. J. Lifetime monogamy and the evolution of eusociality. Phil. Trans. R. Soc. B 364, 3191–3207 (2009)

    Article  PubMed  PubMed Central  Google Scholar 

  3. Hamilton, W. D. The genetical evolution of social behaviour. I. J. Theor. Biol. 7, 1–16 (1964); The genetical evolution of social behaviour. II. J. Theor. Biol. 7, 17–52 (1964)

    Article  CAS  PubMed  Google Scholar 

  4. Charnov, E. L. Evolution of eusocial behaviour: offspring choice or parental parasitism? J. Theor. Biol. 75, 451–465 (1978)

    Article  CAS  PubMed  Google Scholar 

  5. Charnov, E. L. Kin selection and helpers at the nest: effects of paternity and biparental care. Anim. Behav. 29, 631–632 (1981)

    Article  Google Scholar 

  6. Maynard Smith, J. & Szathmary, E. The Major Transitions in Evolution 6–10 (Freeman, 1995)

    Google Scholar 

  7. Queller, D. C. Relatedness and the fraternal major transitions. Phil. Trans. R. Soc. Lond. B 355, 1647–1655 (2000)

    Article  CAS  Google Scholar 

  8. Queller, D. C. & Strassmann, J. E. Kin selection and social insects. Bioscience 48, 165–175 (1998)

    Article  Google Scholar 

  9. Hamilton, W. D. Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3, 193–232 (1972)

    Article  Google Scholar 

  10. West, S. A. & Gardner, A. Altruism, spite, and greenbeards. Science 327, 1341–1344 (2010)

    Article  CAS  ADS  PubMed  Google Scholar 

  11. 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)

    Article  CAS  ADS  PubMed  Google Scholar 

  12. Cockburn, A. Evolution of helping behavior in cooperatively breeding birds. Annu. Rev. Ecol. Syst. 29, 141–177 (1998)

    Article  Google Scholar 

  13. Hatchwell, B. J. & Komdeur, J. Ecological constraints, life history traits and the evolution of cooperative breeding. Anim. Behav. 59, 1079–1086 (2000)

    Article  CAS  PubMed  Google Scholar 

  14. Clutton-Brock, T. Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69–72 (2002)

    Article  CAS  ADS  PubMed  Google Scholar 

  15. Mulder, R. A., Dunn, P. O., Cockburn, A., Lazenby-Cohen, K. A. & Howell, M. J. Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proc. R. Soc. Lond. B 255, 223–229 (1994)

    Article  ADS  Google Scholar 

  16. Krebs, J. R. & Davies, N. B. Behavioural Ecology: An Evolutionary Approach 291–317 (Blackwell Scientific, 1993)

    Google Scholar 

  17. Bennett, P. M. & Owens, I. P. F. Evolutionary Ecology of Birds (Oxford Univ. Press, 2002)

    Google Scholar 

  18. Arnold, K. E. & Owens, I. P. F. Cooperative breeding in birds: the role of ecology. Behav. Ecol. 10, 465–471 (1999)

    Article  Google Scholar 

  19. Arnold, K. E. & Owens, I. P. F. Cooperative breeding in birds: a comparative test of life history hypothesis. Proc. R. Soc. Lond. B 265, 739–745 (1998)

    Article  Google Scholar 

  20. Hadfield, J. D. & Nakagawa, S. General quantitative genetic methods for comparative biology: phylogenies, taxonomies, and multi-trait models for continuous and categorical characters. J. Evol. Biol. 23, 494–508 (2010)

    Article  CAS  PubMed  Google Scholar 

  21. Pagel, M. & Meade, A. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167, 808–825 (2006)

    PubMed  Google Scholar 

  22. Griffin, A. S. & West, S. A. Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302, 634–636 (2003)

    Article  CAS  ADS  PubMed  Google Scholar 

  23. Cornwallis, C. K., West, S. A. & Griffin, A. S. Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal. J. Evol. Biol. 22, 2445–2457 (2009)

    Article  CAS  PubMed  Google Scholar 

  24. Gardner, A., West, S. A. & Buckling, A. Bacteriocins, spite and virulence. Proc. R. Soc. Lond. B 271, 1529–1535 (2004)

    Article  CAS  Google Scholar 

  25. Boomsma, J. J. & Ratnieks, F. L. W. Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. Lond. B 351, 947–975 (1996)

    Article  ADS  Google Scholar 

  26. Wilson, E. O. Sociobiology: The New Synthesis 155 (Harvard Univ. Press, 1975)

    Google Scholar 

  27. Davies, N. B. Dunnock Behaviour and Social Evolution 117–130 (Oxford Univ. Press, 1992)

    Google Scholar 

  28. Komdeur, J. Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358, 493–495 (1992)

    Article  ADS  Google Scholar 

  29. Griffith, S. C., Owens, I. P. F. & Thuman, K. A. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11, 2195–2212 (2002)

    Article  CAS  PubMed  Google Scholar 

  30. Spottiswoode, C. & Moller, A. P. Extrapair paternity, migration, and breeding synchrony in birds. Behav. Ecol. 15, 41–57 (2004)

    Article  Google Scholar 

  31. Cockburn, A. Prevalence of different modes of parental care in birds. Proc. R. Soc. B 273, 1375–1383 (2006)

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hatchwell, B. J. The evolution of cooperative breeding in birds: kinship, dispersal and life history. Phil. Trans. R. Soc. B 364, 3217–3227 (2009)

    Article  PubMed  PubMed Central  Google Scholar 

  33. Goloboff, P. A., Farris, J. S. & Nixon, K. C. TNT, a free program for phylogenetic analysis. Cladistics 24, 774–786 (2008)

    Article  Google Scholar 

  34. R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna) 〈http://www.r-project.org〉 (2010)

  35. Hadfield, J. D. MCMC methods for multi-response generalised linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010)

    Article  Google Scholar 

  36. Plummer, M., Best, N., Cowles, K. & Vines, K. Convergence diagnosis and output analysis for MCMC. R News 6, 7–11 (2006)

    Google Scholar 

  37. Raftery, A. E. & Lewis, S. M. One long run with diagnostics: Implementation strategies for Markov chain Monte Carlo. Stat. Sci. 7, 493–497 (1992)

    Article  Google Scholar 

  38. Geweke, J. in Bayesian Statistics (eds Bernado, J. M., Berger, J. O. Dawid, A. P. & Smith, A. F. M.) 169–194 (Clarendon, 1992)

    Google Scholar 

  39. Heidelberger, P. & Welch, P. D. Simulation run length control in the presence of an initial transient. Oper. Res. 31, 1109–1144 (1983)

    Article  Google Scholar 

  40. Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999)

    Article  CAS  ADS  PubMed  Google Scholar 

  41. Raudenbush, S. W. in The Handbook of Research Synthesis (eds Cooper, H. & Hedges, L. V.) 301–321 (Russell Sage Foundation, 1994)

    Google Scholar 

  42. de Magalhães, J. P. & Costa, J. A database of vertebrate longevity records and their relation to other life-history traits. J. Evol. Biol. 22, 1770–1774 (2009)

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank J. Hadfield for statistical advice, K. Boomsma, S. Nakagawa and B. Sheldon for comments and discussion, M. Nelson-Flower and P. Brennan for access to unpublished data, and the ERC and Royal Society for funding. The compilation of our data set was made possible by access to the collections of the Alexander Library.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed extensively to the work presented in this paper.

Corresponding author

Correspondence to Ashleigh S. Griffin.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary model code, Supplementary Figure 1 with legend, Supplementary Tables 1-15 and References. (PDF 1455 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cornwallis, C., West, S., Davis, K. et al. Promiscuity and the evolutionary transition to complex societies. Nature 466, 969–972 (2010). https://doi.org/10.1038/nature09335

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature09335

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing