Skip to main content
Log in

Sexual coercion by male chimpanzees shows that female choice may be more apparent than real

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

The extent to which active female mating preferences influence male reproductive success in mammals is unclear, particularly for promiscuously breeding species like chimpanzees (Pan troglodytes). Previous studies from multiple long-term study sites have shown that female chimpanzees mate more restrictively around ovulation, and this has been taken as evidence for female choice. However, none of these studies rigorously evaluated the alternative hypothesis that restrictive mating results not from unconstrained choice, but in response to coercive mate guarding, in which males use punishment and intimidation to reduce female promiscuity and promote their own mating interests. Nor did they consider evidence for the potential genetic or phenotypic benefits that females might be choosing. Using 11 years of data from the Kanyawara community in Kibale National Park, Uganda, we previously demonstrated that males achieve elevated mating success with those females toward whom they direct high levels of aggression. Here we extend those findings to show that even female copulatory approaches, which have previously been attributed to female choice, are correlated with male aggression. Specifically, individual females at our site initiated periovulatory copulations most frequently with the males who were most aggressive toward them throughout their cycles. Those males showed high rates of aggression toward females throughout estrus, despite achieving high copulation rates, demonstrating a continuing conflict of interest over the exclusivity of mating access. Because sexual coercion is potentially widespread in primates and other mammals, our results stress the importance of considering the influence of male aggression in studies of female choice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altmann J (1974) Observational study of behavior: sampling methods. Behav 49:227–267

    Article  CAS  Google Scholar 

  • Andersson M (1994) Sexual Selection. Princeton University Press, Princeton

    Google Scholar 

  • Arcadi AC, Wrangham RW (1999) Infanticide in chimpanzees: review of cases and a new within-group observation from the Kanyawara study group in Kibale National Park. Primates 40:337–351

    Article  Google Scholar 

  • Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Tai Forest: behavioral ecology and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Boesch C, Kohou G, Néné H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Taï forest. Am J Phys Anthropol 130:103–115

    Article  PubMed  Google Scholar 

  • Brewer Marsden S, Marsden D, Emery Thompson M (2006) Demographic and female life history parameters of free-ranging chimpanzees at the Chimpanzee Rehabilitation Project, River Gambia National Park. Int J Primatol 27:321–410

    Google Scholar 

  • Byers JA, Waits L (2006) Good genes sexual selection in nature. PNAS 103:16343–16345

    Article  PubMed  CAS  Google Scholar 

  • Clarke P, Pradhan G, van Schaik CP (2009) Intersexual conflict in primates: infanticide, paternity allocation, and the role of coercion. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, pp 42–77

    Google Scholar 

  • Clutton-Brock T, McAuliffe K (2009) Female mate choice in mammals. Q Rev Biol 84:3–27

    Article  PubMed  Google Scholar 

  • Clutton-Brock TH, Harvey PH (1976) Evolutionary rules and primate societies. In: Bateson PP, Hinde RA (eds) Growing points in ethology. Cambridge University Press, Cambridge, pp 195–237

    Google Scholar 

  • Clutton-Brock TH, Parker GA (1995) Sexual coercion in animal societies. Anim Behav 49:1345–1365

    Article  Google Scholar 

  • Deschner T, Heistermann M, Hodges K, Boesch C (2003) Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Anim Behav 66:551–560

    Article  Google Scholar 

  • Dixson AF (1998) Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press, New York

    Google Scholar 

  • Duffy KG, Wrangham RW, Silk J (2007) Male chimpanzees exchange political support for mating opportunities. Curr Biol 17:586–587

    Article  Google Scholar 

  • Emery Thompson M (2005) Reproductive endocrinology of wild female chimpanzees (Pan troglodytes schweinfurthii): methodological considerations and the role of hormones in sex and conception. Am J Primatol 67:137–158

    Article  PubMed  Google Scholar 

  • Emery Thompson M, Wrangham RW (2008) Male mating interest varies with female fecundity in chimpanzees. Int J Primatol 29:885–905

    Article  Google Scholar 

  • Emery Thompson M, Muller MN, Kahlenberg S, Wrangham RW (2010) Social and ecological correlates of stress in wild female chimpanzees. Horm Behav 58:440–449

    Article  PubMed  Google Scholar 

  • Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge

    Google Scholar 

  • Hemelrijk C (1990) A matrix partial correlation test used in investigations of reciprocity and other social interaction patterns at group level. J Theoret Biol 143:405–420

    Article  Google Scholar 

  • Hill GE (2006) Female mate choice for ornamental coloration. In: Hill GE, McGraw KJ (eds) Bird coloration: function and evolution. Harvard University Press, Cambridge, pp 137–200

    Google Scholar 

  • Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13–40

    Article  Google Scholar 

  • Hrdy SB (1981) The woman that never evolved. Harvard Press, Cambridge

    Google Scholar 

  • Johnson MH, Everitt BJ (1988) Essential reproduction. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Kappeler P, van Schaik CP (2004) Sexual selection in primates: review and selective preview. In: Kappeler P, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 3–23

    Chapter  Google Scholar 

  • Matsumoto-Oda A (1999) Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale. Behav Ecol Sociobiol 46:258–266

    Article  Google Scholar 

  • Mays HL, Albrecht T, Liu M, Hill GE (2008) Female choice for genetic complementarity in birds: a review. Genetica 134:147–158

    Article  PubMed  Google Scholar 

  • Mays HLJ, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554–559

    Article  PubMed  Google Scholar 

  • Muller MN (2002) Agonistic relations among Kanyawara chimpanzees. In: Boesch C, Hohmann G, Marchant L (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, Cambridge, pp 112–124

    Chapter  Google Scholar 

  • Muller MN, Emery Thompson M, Wrangham RW (2006) Male chimpanzees prefer mating with old females. Curr Biol 16:2234–2238

    Article  PubMed  CAS  Google Scholar 

  • Muller MN, Kahlenberg SM, Emery Thompson M, Wrangham RW (2007) Male coercion and the costs of promiscuous mating for females chimpanzees. Proc Biol Sci 274:1009–1014

    Article  PubMed  CAS  Google Scholar 

  • Muller MN, Kahlenberg SM, Wrangham RW (2009a) Male aggression against females and sexual coercion in chimpanzees. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, pp 184–217

    Google Scholar 

  • Muller MN, Kahlenberg SM, Wrangham RW (2009b) Male aggression and sexual coercion of females in primates. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, pp 3–22

    Google Scholar 

  • Muller MN, Wrangham RW (2004) Dominance, aggression and testosterone in wild chimpanzees: a test of the “Challenge Hypothesis”. Anim Behav 67:113–123

    Article  Google Scholar 

  • Muller MN, Wrangham RW (2009) Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge

    Google Scholar 

  • Murray CM, Wroblewski E, Pusey AE (2007) New case of intragroup infanticide in the chimpanzees of Gombe National Park. Int J Primatol 28:23–37

    Article  Google Scholar 

  • Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38

    Article  PubMed  CAS  Google Scholar 

  • Nikitopoulos E, Heistermann M, de Vries H, van Hoof JARAM, Sterck EM (2005) A pair choice test to identify female mating pattern relative to ovulation in longtailed macaques, Macaca fascicularis. Anim Behav 70:1283–1296

    Article  Google Scholar 

  • Nishida T, Kawanaka K (1985) Within-group cannibalism by adult male chimpanzees. Primates 26:274–284

    Article  Google Scholar 

  • Nunn CL (1999) The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim Behav 58:229–246

    Article  PubMed  Google Scholar 

  • Paul A (2002) Sexual selection and mate choice. Int J Primatol 23:877–904

    Article  Google Scholar 

  • Pieta K (2008) Female mate preferences among Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park, Uganda. Int J Primatol 29:845–864

    Article  Google Scholar 

  • Roof KA, Hopkins WD, Izard MK, Hook M, Schapiro SJ (2005) Maternal age, parity, and reproductive outcome in captive chimpanzees (Pan troglodytes). Am J Primatol 67:199–207

    Article  PubMed  Google Scholar 

  • Royston J (1982) Basal body temperature, ovulation, and the risk of conception, with special reference to the lifetimes of sperm and egg. Biometrics 38:397–406

    Article  PubMed  CAS  Google Scholar 

  • Schwensow N, Eberle M, Sommer S (2008) Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. Proc Biol Sci 275:555–564

    Article  PubMed  Google Scholar 

  • Setchell JM (2005) Do female mandrills prefer brightly colored males. Int J Primatol 26:715–735

    Article  Google Scholar 

  • Sicotte P (1993) Inter-group encounters and female transfer in mountain gorillas: influence of group composition on male behavior. Am J Primatol 30:21–36

    Article  Google Scholar 

  • Smuts BB, Smuts RW (1993) Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv Study Behav 22:1–63

    Article  Google Scholar 

  • Stumpf R (2004) Female Reproductive Strategies in Chimpanzees of the Taï Forest, Côte d’Ivoire. Ph.D. dissertation. Anthropology. Stony Brook University, Stony Brook, NY

  • Stumpf R, Boesch C (2005) Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Taï National Park, Cote d'Ivoire. Behav Ecol Sociobiol 57:511–524

    Article  Google Scholar 

  • Stumpf R, Boesch C (2006) The efficacy of female choice in chimpanzees of the Taï Forest, Côte d’Ivoire. Behav Ecol Sociobiol 60:749–765

    Article  Google Scholar 

  • Swedell L, Schreier A (2009) Male aggression toward females in hamadryas baboons: conditioning, coercion, and control. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, pp 244–268

    Google Scholar 

  • Tutin CEG (1979) Mating patterns and reproductive strategies in a community of wild chimpanzees. Behav Ecol Sociobiol 6:39–48

    Article  Google Scholar 

  • van Noordwijk MA, van Schaik CP (2000) Reproductive patterns in eutherian mammals: adaptations against infanticide? In: van Schaik CP, Janson CH (eds) Infanticide by Males and Its Implications. Cambridge University Press, Cambridge, pp 322–360

    Chapter  Google Scholar 

  • van Schaik CP, Hodges JK, Nunn CL (2000) Paternity confusion and the ovarian cycles of female primates. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge pp 361–387

    Chapter  Google Scholar 

  • van Schaik CP, Janson CH (2000) Infanticide by males and its implications. Cambridge University Press, Cambridge, p 569

    Book  Google Scholar 

  • van Schaik CP, Pradhan GR, van Noordwijk MA (2004) Mating conflict in primates: infanticide, sexual harassment and female sexuality. In: Kappeler P, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 131–150

    Chapter  Google Scholar 

  • Wilcox AJ, Weinberg CR, Baird DD (1995) Timing of sexual intercourse in relation to ovulation: effects on the probability of conception, survival of the pregnancy, and sex of the baby. N Engl J Med 333:1517–1521

    Article  PubMed  CAS  Google Scholar 

  • Wrangham RW (2002) The cost of sexual attraction: is there a tradeoff in female Pan between sex appeal and received coercion? In: Boesch C, Hohmann G, Marchant L (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, Cambridge, pp 204–215

    Chapter  Google Scholar 

  • Wrangham RW, Muller MN (2009) Sexual coercion in humans and other primates: the road ahead. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, pp 451–468

    Google Scholar 

  • Zinner DP, Nunn CL, van Schaik CP, Kappeler PM (2004) Sexual selection and exaggerated sexual swellings of female primates. In: Kappeler P, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 71–78

    Chapter  Google Scholar 

Download references

Acknowledgments

Research at Kibale was supported by grants from the US National Science Foundation (awards 9807448 and 0416125), the L.S.B. Leakey Foundation, the National Geographic Society, and the Wenner-Gren Foundation. For sponsoring long-term research in Kibale National Park, we thank the Uganda Wildlife Authority and Makerere University Biological Field Station. We thank Gilbert Isabirye-Basuta, John Kasenene, and Jerry Lwanga for their continuing support, and Emily Otali for research oversight. For assistance in the field, we thank the late John Barwogeza, the late Joseph Basagara, Deo Kateeba, Christopher Katongole, Francis Mugurusi, the late Donor Muhangyi, the late Christopher Muruuli, Solomon Musana, Dennis Sebugwawo, and Peter Tuhairwe. Special thanks to Zarin Machanda for assistance with the KCP database.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin N. Muller.

Additional information

Communicated by J. Silk

Rights and permissions

Reprints and permissions

About this article

Cite this article

Muller, M.N., Thompson, M.E., Kahlenberg, S.M. et al. Sexual coercion by male chimpanzees shows that female choice may be more apparent than real. Behav Ecol Sociobiol 65, 921–933 (2011). https://doi.org/10.1007/s00265-010-1093-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-010-1093-y

Keywords

Navigation