Skip to main content
SpringerLink
Log in

Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d’Ivoire

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

Abstract

According to sexual selection theory, females should selectively mate with high-quality males to enhance offspring survival and maximize reproductive success. Yet, chimpanzee (Pan troglodytes) females are known to mate promiscuously. Although there is substantial rationale for a promiscuous mating strategy, there is also a strong expectation that females should be selective, and the question arises as to whether promiscuity precludes female choice. The aims of this study are to: (1) compare wild female chimpanzee sexual strategies throughout estrus, and (2) determine whether females exhibit mate preferences for particular males. Over 2,600 h of data were collected on two habituated chimpanzee (Pan troglodytes verus) communities in the Taï National Park, Côte d’Ivoire. Female mate preferences were measured by quantifying proceptivity and receptivity toward males. Results indicate that all females exhibited proceptivity and resistance to male solicitations, but that there was substantial variation in their magnitudes within and among females. Female proceptivity rates were lower and resistance rates were higher in the periovulatory period (POP) when conception is most likely. Females were more selective during POP, and more promiscuous outside of POP, suggesting that females may follow a mixed reproductive strategy, being selective when conception is likely and more promiscuous when conception is unlikely. Results from this study emphasize the importance of considering the fertility window when determining female mate preferences, and of examining female behavior in POP and non-POP phases separately when evaluating hypotheses for multi-male mating.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5 a

Similar content being viewed by others

References

  • Alexander RD, Noonan KM (1979) Concealment of ovulation, parental care, and human social behaviour. In: Chagnon NA, Irons WG (eds) Evolutionary biology and human social behavior. Duxbury, North Scituate, Mass, pp 436–453

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

    CAS  PubMed  Google Scholar 

  • Anderson C, Beilert C (1994) Adolescent exaggeration in female catarrhine primates. Primates 35:283–300

    Google Scholar 

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

  • 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

    Google Scholar 

  • Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Google Scholar 

  • Bercovitch FB (1991) Male selection, consortship formation, and reproductive tactics in adult female savannah baboons. Primates 32:437–452

    Google Scholar 

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

  • Brooks R, Kemp DJ (2001) Can older males deliver the good genes? Trends Ecol Evol 16:308–313

    Article  PubMed  Google Scholar 

  • Butler H (1974) Evolutionary trends in primate sex cycles. In: Luckett WP (ed) Reproductive biology of the primates. Karger, New York, pp 2–35

  • Bygott JD (1979) Agonistic behavior, ‘dominance’, and social structure in wild chimpanzees of the Gombe National Park. In: Hamburg DA, McCown ER (eds) The great apes. Cummings, Menlo Park, Calif

  • Chapais B (1983) Reproductive activity in relation to male dominance and the likelihood of ovulation in rhesus monkeys. Behav Ecol Sociobiol 12:215–228

    Google Scholar 

  • Clutton-Brock TH (1988) Reproductive success. In: Clutton-Brock TH (ed) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 472–485

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

  • Constable JL, Ashley MV, Goodall J, Pusey AE (2001) Noninvasive paternity assignment in Gombe chimpanzees. Mol Ecol 10:1279–1300

    Article  CAS  PubMed  Google Scholar 

  • Cowlishaw G, Dunbar RIM (1991) Dominance rank and mating success in male primates. Anim Behav 41:1045–1056

    Google Scholar 

  • Cox CR, LeBoeuf BJ (1977) Female incitation of male competition: a mechanism in sexual selection. Am Nat 111:317–335

    Article  Google Scholar 

  • Curie-Cohen M, Yoshihara D, Luttrell L, Benforado K, MacCluer JW, Stone WH (1983) The effects of dominance on mating behavior and paternity in a captive troop of rhesus monkeys (Macaca mulatta). Am J Primatol 5:127–138

    Google Scholar 

  • Czekala NM, Mitchell WR, Lasley BL (1987) Direct measurement of urinary estrone conjugates during the normal menstrual cycle of the gorilla (Gorilla gorilla). Am J Primatol 12:223–229

    CAS  Google Scholar 

  • Daly M (1978) The cost of mating. Am Nat 112:771–774

    Article  Google Scholar 

  • Darwin C (1871) The descent of man and selection in relation to sex. Murray, London

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

    Article  Google Scholar 

  • Doran D, Jungers WL, Sugiyama Y, Fleagle JG, Heesy CP (2002) Multivariate and phylogenetic approaches to understanding chimpanzee and bonobo behavioral diversity. In: Boesch C, Hohmann G, Marchant L (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, Cambridge, pp 14–34

  • Duvall SW, Bernstein IS, Gordon TP (1976) Paternity and status in a rhesus monkey group. J Reprod Fertil 47:25–31

    CAS  PubMed  Google Scholar 

  • Elder J, Yerkes R (1936) The sexual cycle of the chimpanzee. Anat Rec 67:119–143

    Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    CAS  PubMed  Google Scholar 

  • Estep DQ, Gordon TP, Wilson ME, Walker ML (1986) Social stimulation and the resumption of copulation in rhesus macaques (Macaca arctoides). Int J Primatol 7:507–515

    Google Scholar 

  • France JT (1981) Overview of the biological aspects of the fertile period. Int J Fertil 26:143–152

    CAS  PubMed  Google Scholar 

  • France JT, Graham FM, Gosling L, Hair P, Knox BS (1992) Characteristics of natural conceptual cycles occurring in a prospective study of sex pre-selection: fertility awareness symptoms, hormone levels, sperm survival, and pregnancy outcome. Int J Fertil 37:244–255

    CAS  PubMed  Google Scholar 

  • Gangestad SW, Thornhill R (1998) Menstrual cycle variation in women’s preferences for the scent of symmetical men. Proc R Soc Lond B 265:927–933

    Article  CAS  PubMed  Google Scholar 

  • Gomendio M, Roldan ERS (1993) Coevolution between male ejaculates and female reproductive biology in eutherian mammals. Proc R Soc Lond B 252:7–12

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Hamai M, Nishida T, Takasaki H, Turner L (1992) New records of within-group infanticide and cannibalism in wild chimpanzees. Primates 33:151–162

    Google Scholar 

  • Hansen TF, Price DK (1995) Good genes and old age: do old mates provide superior genes? J Evol Biol 8:759–778

    Google Scholar 

  • Harvey PH, Bennett PM (1985) Sexual dimorphism and reproductive strategies. In: Ghesquire J, Martin RD, Newcombe F (eds) Human sexual dimorphism. Taylor and Francis, London, pp 43–59

  • Hasegawa T, Hiraiwa-Hasegawa M (1990) Sperm competition and mating behavior. In: Nishida T (ed) The chimpanzees of the Mahale Mountains: sexual and life history strategies. University of Tokyo Press, Tokyo, pp 115–132

  • Hemelrijk CK, Meier C, Martin RD (1999) ‘Friendship’ for fitness in chimpanzees? Anim Behav 58:1223–1229

    Article  PubMed  Google Scholar 

  • Hoogland J (1998) Why do female Gunnison’s prairie dogs copulate with more than one male? Anim Behav 55:351–359

    Article  PubMed  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 (1997) Raising Darwin’s consciousness: female sexuality and the prehominid origins of patriarchy. Hum Nat 8:1–49

    Google Scholar 

  • Hrdy SB, Whitten PL (1987) Patterning of sexual behavior. In: Smuts B, Cheney D, Seyfarth R, Wrangham R, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 370–384

  • Hunter FM, Petrie M, Otronen M, Birkhead T, Møller AP (1993) Why do females copulate repeatedly with one male? Trends Ecol Evol 8:21–26

    Article  Google Scholar 

  • Hurst LD, Atlan A, Bengtsson BO (1996) Genetic conflicts. Q Rev Biol 71:317–364

    Google Scholar 

  • Janson CH (1984) Female choice and mating system of the brown capuchin monkey, Cebus apella (Primates: Cebidae). Z Tierpsychol 65:177–200

    Google Scholar 

  • Jennions MD (1997) Female promiscuity and genetic incompatability. Trends Ecol Evol 12:251–253

    Google Scholar 

  • Keller L (1985) Why do females mate multiply with multiple males? The sexually selected sperm hypothesis. Adv Stud Behav 24:291–315

    Google Scholar 

  • Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38

    Article  Google Scholar 

  • Knott CD (1997) Field collection and preservation of urine in orangutans and chimpanzees. Trop Biodivers 4:95–102

    Google Scholar 

  • Kuester J, Paul A (1992) Influence of male competition and female mate choice on male mating success in Barbary Macaques (Macaca sylvanus). Behaviour 120:192–217

    Google Scholar 

  • Lehmann J, Boesch C (2004) To fission or to fusion: effects of community size on wild chimpanzee (Pan troglodytes verus) social organization. Behav Ecol Sociobiol: 1–19

    Google Scholar 

  • Lindburg DG (1971) The rhesus monkey in north India: an ecological and behavioral study. In: Rosenblum LA (ed) Primate behavior. Academic, New York, pp 1–106

  • Manning JT (1985) Choosy females and correlates of male age. J Theor Biol 116:349–354

    Google Scholar 

  • Manson JH (1997) Does female rank or age affect mate choice in free-ranging rhesus macaques? Folia Primatol 68:366–369

    CAS  PubMed  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 

  • Maynard Smith J (1991) Theories of sexual selection. Trends Ecol Evol 6:146–151

    Article  Google Scholar 

  • Milton K (1985) Mating patterns of woolly spider monkeys, Brachyteles arachnoides: implications for female choice. Behav Ecol Sociobiol 17:53–59

    Article  Google Scholar 

  • Mundry R (1999) Testing related samples with missing values: a permutation approach. Anim Behav 58:1143–1153

    Article  PubMed  Google Scholar 

  • Nishida T (1990) The chimpanzees of the Mahale Mountains. University of Tokyo Press, Tokyo

  • Nishida T (1997) Sexual behavior of adult male chimpanzees of the Mahale Mountains National Park, Tanzania. Primates 38:379–398

    Google Scholar 

  • Nishida T, Takasaki H, Takahata Y (1990) Demography and reproductive profiles. In: Nishida T (ed) The chimpanzees of the Mahale Mountains. University of Tokyo Press, Tokyo, pp 63–98

  • 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 

  • Penton-Voak IS, Perrett DI (2000) Female preference for male faces changes cyclically: further evidence. Evol Hum Behav 21:39–48

    Article  Google Scholar 

  • Pereira ME, McGlynn CA (1997) Special relationships instead of female dominance for red-fronted lemurs, Eulemur fulvus rufus. Am J Primatol 43:239–258

    CAS  PubMed  Google Scholar 

  • Pusey A (1980) Inbreeding avoidance in chimpanzees. Anim Behav 28:543–582

    Google Scholar 

  • Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828–831

    Article  CAS  PubMed  Google Scholar 

  • Ransom TW, Ransom BS (1971) Adult male-infant relations among baboons (Papio anubis). Folia Primatol 16

  • Scheskin D (2000) Handbook of parametric and nonparametric statistical procedures. Chapman & Hall/CRC, New York

  • Siegel S, Castellan NJ Jr (1988) Non-parametric statistics for the behavioral sciences. McGraw-Hill, New York

  • Small MF (1990) Promiscuity in barbary macaques (Macaca sylvanus). Am J Primatol 20:267–282

    Google Scholar 

  • Small MF, Smith DG (1982) The relationship between maternal and paternal rank in rhesus macaques (Macaca mulatta). Anim Behav 30:626–627

    Google Scholar 

  • Smith DG (1987) Generational bias in mating in captive groups of rhesus monkeys (Macaca mulatta). Folia Primatol 49:212–215

    CAS  PubMed  Google Scholar 

  • Smith DG (1994) Male dominance and reproductive success in a captive group of rhesus macaques (Macaca mulatta). Behaviour 129:225–242

    Google Scholar 

  • Smuts BB (1985) Sex and friendship in baboons. Aldine, New York

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

    Google Scholar 

  • Soltis J, Mitsunaga F, Shimizu K, Nozaki M, Yanagihara Y, Domingo-Roura X, Takenaka O (1997) Sexual selection in Japanese macaques. II: Female mate choice and male-male competition. Anim Behav 54:737–746

    Article  PubMed  Google Scholar 

  • Soltis J, Mitsunaga F, Shimizu K, Yanagihara Y, Nozaki M (1999) Female mating strategy in an enclosed group of Japanese macaques. Am J Primatol 47:263–278

    Article  CAS  PubMed  Google Scholar 

  • Strier KB (1997) Mate preferences of wild muriqui monkeys (Brachyteles arachnoides): reproductive and social correlates. Folia Primatol 68:120–133

    Google Scholar 

  • Stumpf RM (2004) Female reproductive strategies in chimpanzees of the Taï National Park, Côte d’Ivoire. PhD Thesis, Stony Brook University, Stony Brook, N.Y.

  • Tabachnik BG, Fidell LS (2001) Using multivariate statistics. Allyn and Bacon, Toronto

  • Takahata Y (1980) The reproductive biology of a free-ranging troop of Japanese monkeys. Primates 21:303–329

    Google Scholar 

  • Takahata Y (1982) The socio-sexual behavior of Japanese monkeys. Z Tierpsychol 59:89–108

    CAS  PubMed  Google Scholar 

  • Takahata Y, Ihobe H, Idani G (1996) Comparing copulations of chimpanzees and bonobos: do females exhibit proceptivity or receptivity? In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 146–155

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine, Chicago, pp 136–179

  • Tutin CEG (1979) Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 6:29–38

    Article  Google Scholar 

  • Tutin CEG, McGinnis PR (1981) Chimpanzee reproduction in the wild. In: Graham CE (ed) Reproductive biology of the great apes. Academic, New York, pp 239–264

  • Tutin CEG, McGrew WC (1973) Chimpanzee copulatory behaviour. Folia Primatol 19:237–256

    CAS  PubMed  Google Scholar 

  • Utami SS, Goossens B, Bruford MW, Ruiter JR de, Hooff JARAM van (2002) Male bimaturism and reproductive success in Sumatran orang-utans. Behav Ecol 13:643–652

    Article  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

  • Vigilant L, Hofreiter M, Seidel H, Boesch C (2001) Paternity and relatedness in wild chimpanzee communities. Proc Natl Acad Sci 98:12890–12895

    Article  CAS  PubMed  Google Scholar 

  • Watts DP, Mitani JC (2000) Infanticide and cannibalism by male chimpanzees at Ngogo, Kibale National Park, Uganda. Primates 41:357–365

    Google Scholar 

  • Wilcox A, Weinberg C, Baird D (1995) Timing of sexual intercourse in relation to ovulation. Neth J Med 333:1517–1521

    CAS  Google Scholar 

  • Wrangham RW (1986) Ecology and social relationships in two species of chimpanzee. In: Rubenstein DI, Wrangham RW (eds) Ecological aspects of social evolution: birds and mammals. Princeton University Press, Princeton, pp 352–378

  • Zeh JA, Zeh DW (1996) The evolution of polyandry. I. Intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263:1711–1717

    Google Scholar 

Download references

Acknowledgements

The authors wish to thank the Centre Suisse de la Recherche Scientifique, the Ministère de la Recherche Scientifique in Côte d’Ivoire, the Ministère de l’Agriculture et des Resources Animales, Côte d’Ivoire and the direction of Taï National Park for permission to conduct this research. R.M.S. would particularly like to thank Diane Doran for her guidance and support throughout all phases of this project. Additional thanks go to John Fleagle, Patricia Wright, Charlie Janson, John Polk, Linda Vigilant, Martha Robbins, Valentin Gagnon, Camille Bolé, Nicaise Oulaï Daurid, Jonas Eriksson, Cathy Crockford, Tobias Deschner, Ilka Herbinger, and Roman Wittig. Daniel Stahl provided invaluable help with statistical analyses. We are very grateful for reviewers’ comments. Quidel Corporation generously donated ovulation and pregnancy test kits. Funding was provided by a National Science Foundation doctoral dissertation grant to R.M.S. and the Max Planck Society for the Advancement of Science. This study complies with Côte d’Ivoire regulations.

Author information

Authors and Affiliations

  1. Department of Anthropology, University of Illinois at Urbana-Champaign, 109 Davenport Hall, Urbana, IL 61801, USA

    R. M. Stumpf

  2. Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

    R. M. Stumpf & C. Boesch

Authors
  1. R. M. Stumpf
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Boesch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. M. Stumpf.

Additional information

Communicated by C. Nunn

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stumpf, R.M., Boesch, C. Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d’Ivoire. Behav Ecol Sociobiol 57, 511–524 (2005). https://doi.org/10.1007/s00265-004-0868-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-004-0868-4

Keywords

Search

Navigation