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:

Female mate-choice drives the evolution of male-biased dispersal in a social mammal

Abstract

Dispersal has a significant impact on lifetime reproductive success1, and is often more prevalent in one sex than the other2. In group-living mammals, dispersal is normally male-biased and in theory this sexual bias could be a response by males to female mate preferences, competition for access to females or resources, or the result of males avoiding inbreeding2,3,4,5,6,7. There is a lack of studies on social mammals that simultaneously assess these factors and measure the fitness consequences of male dispersal decisions. Here we show that male-biased dispersal in the spotted hyaena (Crocuta crocuta) most probably results from an adaptive response by males to simple female mate-choice rules that have evolved to avoid inbreeding. Microsatellite profiling revealed that females preferred sires that were born into or immigrated into the female’s group after the female was born. Furthermore, young females preferred short-tenured sires and older females preferred longer-tenured sires. Males responded to these female mate preferences by initiating their reproductive careers in groups containing the highest number of young females. As a consequence, 11% of males started their reproductive career in their natal group and 89% of males dispersed. Males that started reproduction in groups containing the highest number of young females had a higher long-term reproductive success than males that did not. The female mate-choice rules ensured that females effectively avoided inbreeding without the need to discriminate directly against close kin or males born in their own group, or to favour immigrant males. The extent of male dispersal as a response to such female mate preferences depends on the demographic structure of breeding groups, rather than the genetic relatedness between females and males.

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

Access options

Buy this article

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

Figure 1: The relationship between the age of the mother on the date of conception and the tenure of the father.
Figure 2: Preference of male spotted hyaenas for clans with the highest number of young females.
Figure 3: The influence of the number of young female clan members at clan selection on the long-term reproductive success of male spotted hyaenas.
Figure 4: The fitness benefits of male spotted hyaenas that selected clans with the highest number of young females.

Similar content being viewed by others

References

  1. Alberts, S. C. & Altmann, J. Balancing costs and opportunities: dispersal in male baboons. Am. Nat. 145, 279–306 (1995)

    Article  Google Scholar 

  2. Greenwood, P. J. Mating systems, philopatry and dispersal in birds and mammals. Anim. Behav. 28, 1140–1162 (1980)

    Article  Google Scholar 

  3. Lehmann, L. & Perrin, N. Inbreeding avoidance through kin recognition: choosy females boost male dispersal. Am. Nat. 162, 638–652 (2003)

    Article  Google Scholar 

  4. Dobson, F. S. Competition for mates and predominant juvenile male dispersal in mammals. Anim. Behav. 30, 1183–1192 (1982)

    Article  Google Scholar 

  5. Moore, J. & Ali, R. Are dispersal and inbreeding avoidance related? Anim. Behav. 32, 94–112 (1984)

    Article  Google Scholar 

  6. Cockburn, A., Scott, M. P. & Scotts, D. J. Inbreeding avoidance and male-biased natal dispersal in Antechinus spp. (Marsupialia: Dasyuridae). Anim. Behav. 33, 908–915 (1985)

    Article  Google Scholar 

  7. Johnson, M. L. & Gaines, M. S. Evolution of dispersal: theoretical models and empirical tests using birds and mammals. Annu. Rev. Ecol. Syst. 21, 449–480 (1990)

    Article  Google Scholar 

  8. Smith, R. H. On selection for inbreeding in polygynous animals. Heredity 43, 205–211 (1979)

    Article  Google Scholar 

  9. Parker, G. A. in Mate Choice (ed. Bateson, P. P. G.) 141–166 (Cambridge Univ. Press, Cambridge, 1983)

    Google Scholar 

  10. Parker, G. A. in Sexual Selection and Reproductive Competition in Insects (eds Blum, M. S. & Blum, N. A.) 123–166 (Academic Press, New York, 1979)

    Google Scholar 

  11. Pusey, A. E. & Packer, C. in Primate Societies (eds Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W. & Struhsaker, T. T.) 250–266 (Univ. Chicago Press, Chicago, 1986)

    Google Scholar 

  12. Keane, B. Dispersal and inbreeding avoidance in the white-footed mouse, Peromyscus leucopus. Anim. Behav. 40, 143–152 (1990)

    Article  Google Scholar 

  13. Kruuk, H. The Spotted Hyena. A Study of Predation and Social Behavior (Univ. Chicago Press, Chicago, 1972)

    Google Scholar 

  14. East, M. L. & Hofer, H. Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females. Behav. Ecol. 12, 558–568 (2001)

    Article  Google Scholar 

  15. Höner, O. P., Wachter, B., East, M. L., Runyoro, V. A. & Hofer, H. The effect of prey abundance and foraging tactics on the population dynamics of a social, territorial carnivore, the spotted hyena. Oikos 108, 544–554 (2005)

    Article  Google Scholar 

  16. Matthews, L. H. Reproduction in the spotted hyaena, Crocuta crocuta, (Erxleben). Phil. Trans. R. Soc. Lond. B 230, 1–78 (1939)

    Article  ADS  Google Scholar 

  17. East, M. L., Hofer, H. & Wickler, W. The erect 'penis' is a flag of submission in a female-dominated society: greetings in Serengeti spotted hyaenas. Behav. Ecol. Sociobiol. 33, 355–370 (1993)

    Article  Google Scholar 

  18. East, M. L., Burke, T., Wilhelm, K., Greig, C. & Hofer, H. Sexual conflicts in spotted hyenas: male and female mating tactics and their reproductive outcome with respect to age, social status and tenure. Proc. R. Soc. Lond. B 270, 1247–1254 (2003)

    Google Scholar 

  19. Engh, A. L. et al. Reproductive skew among males in a female-dominated mammalian society. Behav. Ecol. 13, 193–200 (2002)

    Article  Google Scholar 

  20. Hofer, H. & East, M. L. in Serengeti II. Dynamics, Management, and Conservation of an Ecosystem (eds Sinclair, A. R. E. & Arcese, P.) 332–363 (Elsevier, Chicago, 1995)

    Google Scholar 

  21. Trivers, R. L. in Sexual Selection and the Descent of Man (ed. Campbell, B.) 136–179 (Aldine, Chicago, 1972)

    Google Scholar 

  22. Smale, L., Nunes, S. & Holekamp, K. E. in Advances in the Study of Behavior Vol. 26 (eds Slater, P. J. B., Rosenblatt, J. S., Milinski, M. & Snowdon, C. T.) 181–250 (Academic Press, London, 1997)

    Google Scholar 

  23. Kokko, H. & Sutherland, W. J. Optimal floating and queuing strategies: consequences for density dependence and habitat loss. Am. Nat. 152, 345–366 (1998)

    Article  Google Scholar 

  24. Sherman, P. W., Reeve, H. K. & Pfennig, D. W. in Behavioural Ecology—An Evolutionary Approach (eds Krebs, J. R. & Davies, N. B.) 69–96 (Blackwell Science, Oxford, 1997)

    Google Scholar 

  25. East, M. L. & Hofer, H. Loud calling in a female-dominated mammalian society: II. Behavioural contexts and functions of whooping of spotted hyaenas, Crocuta crocuta. Anim. Behav. 42, 651–669 (1991)

    Article  Google Scholar 

  26. Manly, B. F. J., McDonald, L. L. & Thomas, D. L. Resource Selection by Animals. Statistical Design and Analysis for Field Studies (Chapman & Hall, London, 1993)

    Google Scholar 

  27. Albert, R. Genstruktur und Genfluß in ausgewählten Populationen der Tüpfelhyäne (Crocuta crocuta). PhD thesis, Freie Universität Berlin. (2002)

  28. McFadden, D. in Frontiers in Econometrics (ed. Zarembka, P.) 105–142 (Academic Press, New York, 1974)

    Google Scholar 

  29. Wilhelm, K. et al. Characterization of spotted hyena, Crocuta crocuta, microsatellite loci. Mol. Ecol. Notes 3, 360–362 (2003)

    Article  CAS  Google Scholar 

  30. Marshall, T. C., Slate, J., Kruuk, L. E. B. & Pemberton, J. M. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7, 639–655 (1998)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the Tanzania Commission for Science and Technology for permission to conduct the study, the Tanzania Wildlife Research Institute, the Ngorongoro Conservation Area Authority, A. Francis, L. Kimaay, T. Ndooto, G. Orio, H. Richner, D. Thierer, C. Trout, L. Trout, C. Voigt and W. Wickler for their assistance and suggestions. This study was financed by the Leibniz Institute for Zoo and Wildlife Research, the Fritz-Thyssen-Stiftung, the Stifterverband der deutschen Wissenschaft, the Max Planck Society, the German Academic Exchange Service (DAAD) and the Messerli Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. P. Höner.

Ethics declarations

Competing interests

Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Höner, O., Wachter, B., East, M. et al. Female mate-choice drives the evolution of male-biased dispersal in a social mammal. Nature 448, 798–801 (2007). https://doi.org/10.1038/nature06040

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06040

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