Promiscuity and the evolutionary transition to complex societies

Journal name:
Date published:

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.

At a glance


  1. The monogamy hypothesis.
    Figure 1: The monogamy hypothesis.

    a, Monogamy, or low levels of promiscuity, leads to high relatedness in family groups that favours the transition to cooperative societies (increasing the relatedness term, r, in Hamilton’s rule3, which states that cooperation will be favoured if rb>c, where b is the benefit in terms of reproductive success to the recipient of aid and c is the cost to the performer of a cooperative behaviour). High levels of promiscuity lead to a low relatedness in family groups that favours the loss of cooperative breeding. b, Promiscuity and relatedness. Female promiscuity (number of mates) is plotted against the mean genetic relatedness between potential helpers and either their siblings or their offspring. An individual is always related to its offspring with r = 0.5. In contrast, as the number of males its mother mates with increases, the relatedness to siblings decreases from r = 0.5 to r = 0.25 (full-siblings to half-siblings). Across 11 species of cooperative breeders, we found this expected negative relationship between helper–offspring relatedness and female promiscuity (Supplementary Fig. 1).

  2. Making sense of the diversity.
    Figure 2: Making sense of the diversity.

    Helping may be facultative, as in the Seychelles warbler, Acrocephalus sechellensis28 (a), or obligate: the chicks in the nest of the white-winged chough, Corcorax melanorhamphos (b), have no chance of survival if their parents do not receive assistance from helpers. Promiscuity can be high in cooperative breeders but low in species without cooperative care—cooperative breeding is unknown in seabirds such as the puffin, Fratercula arctica (c), which are either strictly monogamous or have extremely low rates of promiscuity. In contrast, the superb fairy-wren, Malurus cyaneus (d), is a cooperative breeder with one of the highest extra-pair paternity rates ever recorded15. To make helping pay, the benefits have to outweigh the costs of breeding independently, and this depends on ecological as well as genetic factors. (Photos courtesy M. Hammers (a), N. Beck (b), S. Patrick (c), G. Dabb (d).)

  3. Promiscuity and cooperation.
    Figure 3: Promiscuity and cooperation.

    a, Rates of promiscuity (percentage of broods with one or more offspring sired by an extra-group male) in cooperative and non-cooperative species. Promiscuity was significantly higher in non-cooperative than in cooperative species (Supplementary Tables 2 and 3). Data shown, mean±s.e. b, The relationship between levels of cooperation (population with the lowest percentage of nest with helpers throughout the species range) and promiscuity in cooperative species. Helpers were present in a lower percentage of nests in species with higher rates of promiscuity (Supplementary Table 9). The line is the log-linear regression curve.

  4. Promiscuity and the transition to and from cooperative breeding.
    Figure 4: Promiscuity and the transition to and from cooperative breeding.

    a, The phylogenetic distribution of cooperative breeding and ancestral rates of female promiscuity. Red species labels and branches represent cooperative breeding, and black species labels and branches indicate non-cooperative species. Blue circles indicate ancestral values of rates of promiscuity (larger circles correspond to higher promiscuity). Petroica are a poorly constrained group and have been split in the phylogeny. The resulting transitions make no difference to the results (Supplementary Tables 11–14). b, Promiscuity in non-cooperative and cooperative ancestral species that gave rise to only non-cooperative descendants (black bars), only cooperative descendants (dark-grey bars), or both non-cooperative and cooperative descendants (light-grey bars). Non-cooperative ancestors that lead to cooperative descendants had lower promiscuity than those that produced non-cooperative descendants (Supplementary Table 7). Similarly, cooperative ancestors that produced non-cooperative descendants were more promiscuous than those that produced cooperative descendants (Supplementary Table 7). c, The changes in promiscuity associated with transitions to and from cooperative breeding. Rates of promiscuity decreased during transitions to cooperation, but decreased when cooperation broke down. Data shown, mean±s.e. of ancestral values.

  5. Kin discrimination and rates of promiscuity.
    Figure 5: Kin discrimination and rates of promiscuity.

    There was a significant quadratic relationship between kin discrimination (correlation between relatedness and help provided) and promiscuity (measured as in Fig. 3a), indicating that kin discrimination was strongest in species with intermediate rates of promiscuity (Supplementary Table 8).


  1. Boomsma, J. J. Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17, R673R683 (2007)
  2. Boomsma, J. J. Lifetime monogamy and the evolution of eusociality. Phil. Trans. R. Soc. B 364, 31913207 (2009)
  3. Hamilton, W. D. The genetical evolution of social behaviour. I. J. Theor. Biol. 7, 116 (1964); The genetical evolution of social behaviour. II. J. Theor. Biol. 7, 1752 (1964)
  4. Charnov, E. L. Evolution of eusocial behaviour: offspring choice or parental parasitism? J. Theor. Biol. 75, 451465 (1978)
  5. Charnov, E. L. Kin selection and helpers at the nest: effects of paternity and biparental care. Anim. Behav. 29, 631632 (1981)
  6. Maynard Smith, J. & Szathmary, E. The Major Transitions in Evolution 610 (Freeman, 1995)
  7. Queller, D. C. Relatedness and the fraternal major transitions. Phil. Trans. R. Soc. Lond. B 355, 16471655 (2000)
  8. Queller, D. C. & Strassmann, J. E. Kin selection and social insects. Bioscience 48, 165175 (1998)
  9. Hamilton, W. D. Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3, 193232 (1972)
  10. West, S. A. & Gardner, A. Altruism, spite, and greenbeards. Science 327, 13411344 (2010)
  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, 12131216 (2008)
  12. Cockburn, A. Evolution of helping behavior in cooperatively breeding birds. Annu. Rev. Ecol. Syst. 29, 141177 (1998)
  13. Hatchwell, B. J. & Komdeur, J. Ecological constraints, life history traits and the evolution of cooperative breeding. Anim. Behav. 59, 10791086 (2000)
  14. Clutton-Brock, T. Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 6972 (2002)
  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, 223229 (1994)
  16. Krebs, J. R. & Davies, N. B. Behavioural Ecology: An Evolutionary Approach 291317 (Blackwell Scientific, 1993)
  17. Bennett, P. M. & Owens, I. P. F. Evolutionary Ecology of Birds (Oxford Univ. Press, 2002)
  18. Arnold, K. E. & Owens, I. P. F. Cooperative breeding in birds: the role of ecology. Behav. Ecol. 10, 465471 (1999)
  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, 739745 (1998)
  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, 494508 (2010)
  21. Pagel, M. & Meade, A. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167, 808825 (2006)
  22. Griffin, A. S. & West, S. A. Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302, 634636 (2003)
  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, 24452457 (2009)
  24. Gardner, A., West, S. A. & Buckling, A. Bacteriocins, spite and virulence. Proc. R. Soc. Lond. B 271, 15291535 (2004)
  25. Boomsma, J. J. & Ratnieks, F. L. W. Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. Lond. B 351, 947975 (1996)
  26. Wilson, E. O. Sociobiology: The New Synthesis 155 (Harvard Univ. Press, 1975)
  27. Davies, N. B. Dunnock Behaviour and Social Evolution 117130 (Oxford Univ. Press, 1992)
  28. Komdeur, J. Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358, 493495 (1992)
  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, 21952212 (2002)
  30. Spottiswoode, C. & Moller, A. P. Extrapair paternity, migration, and breeding synchrony in birds. Behav. Ecol. 15, 4157 (2004)
  31. Cockburn, A. Prevalence of different modes of parental care in birds. Proc. R. Soc. B 273, 13751383 (2006)
  32. Hatchwell, B. J. The evolution of cooperative breeding in birds: kinship, dispersal and life history. Phil. Trans. R. Soc. B 364, 32173227 (2009)
  33. Goloboff, P. A., Farris, J. S. & Nixon, K. C. TNT, a free program for phylogenetic analysis. Cladistics 24, 774786 (2008)
  34. R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna) left fencehttp://www.r-project.orgright fence (2010)
  35. Hadfield, J. D. MCMC methods for multi-response generalised linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 122 (2010)
  36. Plummer, M., Best, N., Cowles, K. & Vines, K. Convergence diagnosis and output analysis for MCMC. R News 6, 711 (2006)
  37. Raftery, A. E. & Lewis, S. M. One long run with diagnostics: Implementation strategies for Markov chain Monte Carlo. Stat. Sci. 7, 493497 (1992)
  38. Geweke, J. in Bayesian Statistics (eds Bernado, J. M., Berger, J. O. Dawid, A. P. & Smith, A. F. M.) 169194 (Clarendon, 1992)
  39. Heidelberger, P. & Welch, P. D. Simulation run length control in the presence of an initial transient. Oper. Res. 31, 11091144 (1983)
  40. Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877884 (1999)
  41. Raudenbush, S. W. in The Handbook of Research Synthesis (eds Cooper, H. & Hedges, L. V.) 301321 (Russell Sage Foundation, 1994)
  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, 17701774 (2009)

Download references

Author information

  1. These authors contributed equally to this work.

    • Charlie K. Cornwallis &
    • Ashleigh S. Griffin


  1. Edward Grey Institute, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK

    • Charlie K. Cornwallis &
    • Ashleigh S. Griffin
  2. Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK

    • Stuart A. West
  3. Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK

    • Katie E. Davis


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

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

Author details

Supplementary information

PDF files

  1. Supplementary Information (1.4M)

    This file contains Supplementary model code, Supplementary Figure 1 with legend, Supplementary Tables 1-15 and References.

Additional data