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.

Sexual swellings advertise female quality in wild baboons

Abstract

The females of many Old World primate species produce prominent and conspicuous swellings of the perineal skin around the time of ovulation. These sexual swellings have been proposed to increase competition among males for females1 or to increase the likelihood of a female getting fertilized, by signalling either a female's general reproductive status1,2,3,4,5, or the timing of her ovulation6. Here we show that sexual swellings in wild baboons reliably advertise a female's reproductive value over her lifetime, in accordance with a theoretical model of honest signalling7. Females with larger swellings attained sexual maturity earlier, produced both more offspring and more surviving offspring per year than females with smaller swellings, and had a higher overall proportion of their offspring survive. Male baboons use the size of the sexual swelling to determine their mating effort, fighting more aggressively to consort females with larger swellings, and spending more time grooming these females. Our results document an unusual case of a sexually selected ornament in females, and show how males, by mating selectively on the basis of the size of the sexual swelling, increase their probability of mating with females more likely to produce surviving offspring.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1

References

  1. Clutton-Brock, T. & Harvey, P. in Growing Points in Ethology (eds Bateson, P. & Hinde, R.) 195–237 (Cambridge Univ. Press, Cambridge, 1976).

    Google Scholar 

  2. Hrdy, S. & Whitten, P. in Primate Societies (eds Smuts, B., Cheney, D., Seyfarth, R., Wrangham, R. & Strusaker, T.) 370–384 (Univ. Chicago Press, Chicago, 1987).

    Google Scholar 

  3. Hrdy, S. in The Evolution of Sex (eds Bellig, R. & Stevens, G.) 101–136 (Harper and Row, New York, 1988).

    Google Scholar 

  4. Sillen-Tullberg, B. & Moller, A. The relationship between concealed ovulation and mating systems in anthropoid primates: a phylogenetic analysis. Am. Nat. 141, 1–25 (1993).

    Article  CAS  Google Scholar 

  5. Nunn, C. The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Anim. Behav. 58, 229–246 (1999).

    Article  CAS  Google Scholar 

  6. Hamilton, W. J. in Primate Paternalism (ed. Taub, D.) 309–335 (Van Nostrand Reinhold, New York, 1984).

    Google Scholar 

  7. Pagel, M. The evolution of conspicuous oestrous advertisement in Old World monkeys. Anim. Behav. 47, 1333–1341 (1994).

    Article  Google Scholar 

  8. Packer, C. Male transfer in olive baboons. Nature 255, 219–220 (1975).

    Article  ADS  Google Scholar 

  9. Packer, C. Inter-troop transfer and inbreeding avoidance in Papio anubis. Anim. Behav. 27, 1–36 (1979).

    Article  Google Scholar 

  10. Packer, C. Male dominance and reproductive activity in Papio anubis. Anim. Behav. 27, 37–45 (1979).

    Article  Google Scholar 

  11. Nash, L. Troop fissioning in free-ranging baboons in the Gombe Stream National Park. Am. J. Phys. Anthrop. 44, 63–77 (1976).

    Article  CAS  Google Scholar 

  12. Owens, N. The development of sociosexual behavior in free-living baboons, Papio anubis. Behaviour 57, 241–259 (1976).

    Article  Google Scholar 

  13. Ransom, T. Beach Troop of the Gombe (Associated Univ. Press, New Jersey, 1981).

    Google Scholar 

  14. Collins, D., Busse, C. & Goodall, J. in Infanticide: A Comparative and Evolutionary Perspective (eds Hausfater, G. & Hrdy, S.) 193–215 (Aldine, Hawthorne, New York, 1984).

    Google Scholar 

  15. Packer, C., Collins, D. A., Sindimwo, A. & Goodall, J. Reproductive constraints on aggressive competition in female baboons. Nature 373, 60–63 (1995).

    Article  ADS  CAS  Google Scholar 

  16. Packer, C., Tatar, M. & Collins, D. Reproductive cessation in female mammals. Nature 392, 807–811 (1998).

    Article  ADS  CAS  Google Scholar 

  17. Ellison, P. Developmental influences on adult ovarian hormonal function. Am. J. Hum. Biol. 8, 725–734 (1996).

    Article  Google Scholar 

  18. Ryder, N. & Westoff, C. Reproduction in the United States (Princeton Univ. Press, Princeton, 1971).

    Google Scholar 

  19. Critescu, M. Differential fertility depending on the age of puberty. J. Human Evol. 4, 521–524 (1975).

    Article  Google Scholar 

  20. Heistermann, M., Mohle, U., Vervaecke, H., van Elsacker, L. & Hodges, J. K. Application of urinary and fecal steroid measurements for monitoring ovarian function and pregnancy in the bonobo (Pan paniscus) and evaluation of perineal swelling patterns in relation to endocrine events. Biol. Reprod. 55, 844–853 (1996).

    Article  CAS  Google Scholar 

  21. Thompson, J. et al. The Sulawesi crested black macaque (Macaca nigra) menstrual cycle: Changes in perineal tumescence and serum estradiol, progesterone, follicle-stimulating hormone, and luteinizing hormone levels. Biol. Reprod. 46, 879–884 (1992).

    Article  Google Scholar 

  22. Whitten, P. & Russell, E. Information content of sexual swellings and fecal steroids in sooty mangabeys (Cercocebus torquatus atys). Am. J. Primatol. 40, 67–82 (1996).

    Article  Google Scholar 

  23. Borgerhoff-Mulder, M. Early maturing Kipsigis women have higher reproductive success than late maturing women and cost more to marry. Behav. Ecol. Sociobiol. 24, 145–153 (1989).

    Article  Google Scholar 

  24. David, P., Bjorksten, T., Fowler, K. & Pomiankowski, A. Condition-dependent signalling of genetic variation in stalk-eyed flies. Nature 406, 186–188 (2000).

    Article  ADS  CAS  Google Scholar 

  25. Ryan, M. Sexual selection, sensory systems, and sensory exploitation. Oxford Surv. Evol. Biol. 5, 156–195 (1990).

    Google Scholar 

  26. Bielert, C. & Busse, C. Influence of ovarian hormones on the food intake and feeding of captive and wild female chacma baboons (Papio ursinus). Physiol. Behav. 30, 103–111 (1983).

    Article  CAS  Google Scholar 

  27. Strusaker, T. The Red Colobus Monkey (Univ. Chicago Press, Chicago, 1975).

    Google Scholar 

  28. Hausfater, G. Dominance and reproduction in baboons (Papio cynocephalus): a quantitative analysis. Contrib. Primatol. 7, 1–150 (1975).

    CAS  PubMed  Google Scholar 

  29. Alberts, S., Altmann, J. & Wilson, M. Mate guarding constrains foraging activity of male baboons. Anim. Behav. 51, 1269–1277 (1996).

    Article  Google Scholar 

Download references

Acknowledgements

We thank C. Packer and D. A. Collins for providing access to the reproductive histories of the females in this study; the Government of Tanzania for permission to carry out this study; K. Hawkes, C. Packer, R. Wrangham and D. A. Collins for comments on this work; and A. Sindimwo, M. Bwenda, I. Rukamata, M. Omari, S. Hamisi, R. Mkono, J. Bushingwa, F. Juma. and D. A. Collins for assistance in data collection at Gombe National Park. L.G.D.'s field work was supported by National Science Foundation and Wenner-Gren Foundation for Anthropological Research. Data collection at Gombe was supported by the Jane Goodall Institute. M.P. is supported by the Leverhulme Trust and the Natural Environment Research Council.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leah G. Domb.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Domb, L., Pagel, M. Sexual swellings advertise female quality in wild baboons. Nature 410, 204–206 (2001). https://doi.org/10.1038/35065597

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35065597

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