Behavioral Ecology and Sociobiology

, Volume 60, Issue 6, pp 749–765 | Cite as

The efficacy of female choice in chimpanzees of the Taï Forest, Côte d’Ivoire

Original Article

Abstract

Male–male competition has historically been considered the major force driving sexual selection. However, female choice and inter-sexual conflict are increasingly recognized as important influences affecting differential mating and reproductive success. Many females exhibit preferences for particular males; however, male strategies may conflict with females’ ability to obtain their mate preferences. To influence paternity, females must affect both (1) whether or not sexual interactions occur, particularly during the periovulatory period (POP) and (2) the outcome of sexual interactions. This study focuses on the effectiveness of female choice in wild chimpanzees (Pan troglodytes verus). Over 2,600 h of data were collected on two habituated chimpanzee communities in the Taï National Park, Côte d’Ivoire. Female mate preferences were measured by quantifying proceptive and resistance behavior toward males in both the periovulatory period and non-POP phases of estrus. The efficacy of female preference was measured both (1) by measuring success rates of female proceptivity and resistance behaviors and (2) by determining how well measures of female mate preference (proceptivity and resistance rates) predict male mating success. Though male chimpanzees are clearly dominant to females, the results indicate that females could effectively resist male solicitations and, in most cases, unwanted copulations were averted. Both female proceptivity and resistance rates correlate (positively and inversely, respectively) with male mating success in POP. Outside POP, female proceptivity rates corresponded with male mating success, but resistance rates did not. Males (irrespective of rank) that were preferred by females obtained higher mating success compared to other males during the POP, suggesting that females were effective in their mate choice and that, despite clear male dominance, female choice influences paternity in wild chimpanzees.

Keywords

Chimpanzees Pan troglodytes verus Female choice Sexual conflict 

Notes

Acknowledgements

The authors wish to thank the Centre Suisse de la Recherche Scientifique, the Ministèere de la Recherche Scientifique in Côte d’Ivoire, the Ministèere 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-Sheehy, John Fleagle, Patricia Wright, Charlie Janson, John Polk, Daniel Stahl, Charles Roseman, Germán Bollero, all members of the Taï Chimpanzee Project, particularly Valentin Gagnon, Camille Bolé, Nicaise Oulaï Daurid, Cathy Crockford, Tobias Deschner, Ilka Herbinger, and Roman Wittig, as well as helpful comments from two anonymous reviewers. 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.

References

  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267PubMedGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Bercovitch F (1991) Mate selection, consortship formation, and reproductive tactics in adult female savanna baboons. Primates 32:437–452Google Scholar
  4. Birky WA (2002) Mating patterns and social structure in a wild group of Formosan macaques. Ph.D. thesis, Department of Anthropology, Rutgers UniversityGoogle Scholar
  5. Boesch C, Boesch-Achermann H (2000) The chimpanzees of the Taï Forest: behavioral ecology and evolution. Oxford University Press, OxfordGoogle Scholar
  6. Boesch C, Kohou G, Nene H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Taï forest. A J Phys Anthropol 130(1):103–15Google Scholar
  7. Boinski S (1987) Mating patterns in squirrel monkeys (Saimiri oerstedii). Behav Ecol Sociobiol 21:13–21Google Scholar
  8. Brown WD (1997) Female remating and the intensity of female choice in black-horned tree crickets, Oecanthus nigricornis. Behav Ecol 8:66–74Google Scholar
  9. Buck MR (1998) Female mate choice in sooty mangabeys: social constraints on mating behaviour. Ph.D. thesis, Department of Anthropology, Emory UniversityGoogle Scholar
  10. Burley NT, Parker PG, Lundy K (1996) Sexual selection and extra-pair fertilization in a socially monogamous passerine, the zebra finch (Taeniopygia guttata). Behav Ecol 7:218–226Google Scholar
  11. Bygott JD (1979) Agonistic behavior, ‘dominance’, and social structure in wild chimpanzees of the Gombe National Park. In: Hamburg B, McCown E (eds) The great apes. Benjamin/Cummings, Menlo Park, CAGoogle Scholar
  12. Chapman T, Hutchings J, Partridge L (1993) No reduction in the cost of mating Drosophila melanogaster females with spermless males. Proc R Soc Lond 153:211–217Google Scholar
  13. Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47Google Scholar
  14. Clutton-Brock TH, Parker GA (1995) Sexual coercion in animal societies. Anim Behav 49:1345–1365Google Scholar
  15. Cords M, Mitchell BJ, Tsingalia HM, Rowell TA (1986) Promiscuous mating amongst blue monkeys in the Kakamega forest, Kenya. Ethology 72:214–226Google Scholar
  16. Cowlishaw G, Dunbar RIM (1991) Dominance rank and mating success in male primates. Anim Behav 41:1045–1056Google Scholar
  17. Cunningham M (1986) Measuring the physical in physical attractiveness: quasi-experiments on the sociobiology of female facial beauty. J Pers Soc Psychol 50:925–935Google Scholar
  18. Cunningham EJA (2003) Female mate preferences and subsequent resistance to copulation in the mallard. Behav Ecol 14:326–333Google Scholar
  19. Cunningham EJA, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77PubMedGoogle Scholar
  20. 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 12:223–229Google Scholar
  21. Darwin C (1871) The descent of man, and selection in relation to sex. Murray, LondonGoogle Scholar
  22. de Waal FMB (1982) Chimpanzee politics: power and sex among apes. Allen & Unwin, LondonGoogle Scholar
  23. 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 66:551–560Google Scholar
  24. Drickamer LC, Gowaty PA, Holmes CM (2000) Free female mate choice in house mice affects reproductive success and offspring viability and performance. Anim Behav 59:71–378Google Scholar
  25. Drickamer LC, Gowaty PA, Wagner DM (2003) Free mutual mate preferences in house mice affect reproductive success and offspring performance. Anim Behav 65:105–114Google Scholar
  26. Dunbar RIM (1984) Reproductive decisions: an economic analysis of gelada baboon social strategies. Princeton University Press, Princeton, NJGoogle Scholar
  27. East ML, Burke T, Wilhelm K, Greig C, Hofer H (2003) 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 Ser B Biol Sci 270:1247–1254Google Scholar
  28. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, NJGoogle Scholar
  29. Elder J, Yerkes R (1936) The sexual cycle of the chimpanzee. Anat Rec 67:119–143Google Scholar
  30. Enomoto T (1981) Male aggression and the sexual behavior of Japanese monkeys. Primates 1:15–23Google Scholar
  31. Fox EA (1998) The function of female mate choice in the Sumatran orangutan (Pongo pygmaeus abelii). Ph.D. thesis, Department of Biological Anthropology and Anatomy, Duke UniversityGoogle Scholar
  32. Fox EA (2002) Female tactics to reduce sexual harassment in the Sumatran orangutan (Pongo pygmaeus abelii). Behav Ecol Sociobiol 52:93–101Google Scholar
  33. France JT (1981) Overview of the biological aspects of the fertile period. Int J Fertil 26:143–152PubMedGoogle Scholar
  34. France JT, Graham FM, Gosling L, Hair P, Knox BS (1992) Characteristics of natural conceptual cycles occurring in a prospective study of sex preselection—fertility awareness symptoms, hormone levels, sperm survival, and pregnancy outcome. Int J Fertil 37:244–255PubMedGoogle Scholar
  35. Galdikas B (1985) Subadult male orangutan sociality and reproductive behavior at Tanjung Puting. Am J Primatol 8:87–99Google Scholar
  36. Gomendio M, Roldan ERS (1993) Mechanisms of sperm competition: linking physiology and behavioral ecology. Trends Ecol Evol 8:95–100Google Scholar
  37. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge, MAGoogle Scholar
  38. Gowaty PA, Steinichen R, Anderson WW (2002) Mutual interest between the sexes and reproductive success in Drosophila pseudoobscura. Evolution 56:2537–2540PubMedCrossRefGoogle Scholar
  39. Halliday TR (1983) The study of mate choice. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 3–22Google Scholar
  40. Harcourt AH (1989) Environment, competition, and reproductive performance of female monkeys. Trends Ecol Evol 4:101–105Google Scholar
  41. 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 115–132Google Scholar
  42. Hemelrijk CK, Meier C, Martin RD (1999) ‘Friendship’ for fitness in chimpanzees? Anim Behav 58:1223–1229PubMedGoogle Scholar
  43. Hine E, Lachish S, Higgie M, Blows MW (2002) Positive genetic correlation between female preference and offspring fitness. Proc R Soc Lond Ser B Biol Sci 269:2215–2219Google Scholar
  44. Howard RD, Moorman RS, Whiteman HH (1997) Differential effects of mate competition and mate choice on eastern tiger salamanders. Anim Behav 53:1345–1356PubMedGoogle Scholar
  45. Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13–40Google Scholar
  46. Huffman MA (1987) Consort intrusion and female mate choice in Japanese macaques. Ethology 75:221–234CrossRefGoogle Scholar
  47. Huffman MA (1991) Mate selection and partner preference in female Japanese macaques. In: Fedigan LM, Asquith PJ (eds) The monkeys of Arashiyama: thirty-five years of study in the East and the West. State University of New York Press, New York, pp 101–122Google Scholar
  48. Janson CH (1984) Female choice and mating system of the brown capuchin monkey, Cebus apella (Primates: Cebidae). Z Tierpsychol 65:177–200Google Scholar
  49. Keddy AC (1986) Female mate choice in vervet monkeys (Cercopithecus aethiops). Am J Primatol 10:125–143Google Scholar
  50. Knott CD (1997) Field collection and preservation of urine in orangutans and chimpanzees. Trop Biodivers 4:95–102Google Scholar
  51. Kolm N (2001) Females produce larger eggs for large males in a paternal mouthbrooding fish. Proc R Soc Lond B 268:2229–2234Google Scholar
  52. Lehmann J, Boesch C (2003) Social influences on ranging patterns among chimpanzees (Pan troglodytes verus) in the Taï National Park, Côte d’Ivoire. Behav Ecol 14(5):642–649Google Scholar
  53. LeBoeuf B (1978) Sex and evolution. In: McGill T, Dewsbury D, Sachs B (eds) Sex and behavior. Plenum, New YorkGoogle Scholar
  54. Manly BFJ (1997) Randomization, bootstrap, and Monte Carlo methods in biology. London: Chapman & HallGoogle Scholar
  55. Manson JH (1992) Measuring female mate choice in Cayo Santiago rhesus macaques. Anim Behav 44:405–416Google Scholar
  56. Matsumoto-Oda A (1998) Injuries to the sexual skin of female chimpanzees at Mahale and their effect on behaviour. Folia Primatol 69:400–404PubMedGoogle Scholar
  57. Matsumoto-Oda A (1999) Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale. Behav Ecol Sociobiol 46:258–266Google Scholar
  58. Milton K (1985) Mating patterns of Woolly spider monkeys, Brachyteles arachnoides: implications for female choice. Behav Ecol Sociobiol 17:53–59Google Scholar
  59. Mitani J (1985) Mating behavior of male orangutans in the Kutai reserve. Anim Behav 33:392–402Google Scholar
  60. Nishida T (1997) Sexual behavior of adult male chimpanzees of the Mahale Mountains National Park, Tanzania. Primates 38:379–398Google Scholar
  61. Nishida T, Hiraiwa-Hasegawa M, Hasegawa T, Takahata Y (1985) Group extinction and female transfer in wild chimpanzees in the Mahale Mountains. Z Tierpsychol 67:284–301Google Scholar
  62. 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 63–98Google Scholar
  63. Norris K (1993) Heritable variation in a plumage indicator of viability in male great tits, Parus major. Nature 362:537–539Google Scholar
  64. Nunn CL (1999) The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim Behav 58:229–246PubMedGoogle Scholar
  65. Parker G (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic, New York, pp 123–166Google Scholar
  66. Partridge L (1980) Mate choice increases a component of offspring fitness in fruit flies. Nature 283:290–291Google Scholar
  67. Partridge L, Hurst LD (1998) Sex and conflict. Science 281:2003–2008PubMedGoogle Scholar
  68. Paul A (2002) Sexual selection and mate choice. Int J Primatol 23:877–904Google Scholar
  69. Pereira ME, Weiss ML (1991) Female mate choice, male migration, and the threat of infanticide in ringtailed lemurs. Behav Ecol Sociobiol 28:141–152Google Scholar
  70. Perloe SI (1992) Male mating competition, female choice and dominance in a free ranging troop of Japanese macaques. Primates 33:289–304Google Scholar
  71. Petrie M (1994) Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371:598–599Google Scholar
  72. Promislow DEL, Smith EA, Pearse L (1998) Adult fitness consequences of sexual selection in Drosophila melanogaster. Proc Natl Acad Sci USA 95:10687–10692PubMedGoogle Scholar
  73. Pusey A (1980) Inbreeding avoidance in chimpanzees. Anim Behav 28:543–582Google Scholar
  74. Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277:828–831PubMedGoogle Scholar
  75. Rabe-Hasketh S, Everitt B (2004) A handbook of statistical analysis using Stata, 3rd edn. Chapman & Hall/CRC Boca Raton, USAGoogle Scholar
  76. Reynolds JD, Gross MR (1992) Female mate preference enhances offspring growth and reproduction in a fish, Poecilia reticulata. Proc R Soc Lond Ser B Biol Sci 250:57–62Google Scholar
  77. Richard A (1992) Aggressive competition between males, female-controlled polygyny and sexual monomorphism in a Malagasy primate, Propithecus verreauxi. J Hum Evol 22:395–406Google Scholar
  78. Rice W (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232–243PubMedGoogle Scholar
  79. Rodman P, Mitani J (1987) Orangutans: sexual dimorphism in a solitary species. In: Smuts B, Cheney D, Seyfarth R, Wrangham R, TT Struhsacker (eds) Primate societies. University of Chicago Press, Chicago, pp 146–54Google Scholar
  80. Schürmann CL, van Hooff JARAM (1986) Reproductive strategies of the orang-utan: new data and a consideration of existing socio-sexual models. Int J Primatol 7:265–287Google Scholar
  81. Sicotte P (2001) Female mate choice in mountain gorillas. In: Robbins MM, Sicotte P, Stewart KJ (eds) Mountain gorillas: three decades of research at Karisoke. Cambridge University Press, CambridgeGoogle Scholar
  82. Setchell JM, Kappleler PM (2003) Selection in relation to sex in primates. Adv Study Behav 33:87–173CrossRefGoogle Scholar
  83. Siegel S, Castellan NJ Jr (1988) Non-parametric statistics for the behavioral sciences. McGraw-Hill, New YorkGoogle Scholar
  84. Small MJ (1989) Female choice in non-human primates. Yearb Phys Anthropol 32:103–127Google Scholar
  85. Small MF (1990) Promiscuity in Barbary macaques (Macaca sylvanus). Am J Primatol 20:267–282Google Scholar
  86. Smuts BB, Smuts RW (1993) Male aggression and sexual coercion of females in non-human primates and other mammals: evidence and theoretical implications. Adv Study Behav 22:1–63Google Scholar
  87. Soltis J, Mitsunaga F, Shimizu K, Yanagihara Y, Nozaki M (1997) Sexual selection in Japanese macaques I: female mate choice or male sexual coercion? Anim Behav 54:725–736PubMedGoogle Scholar
  88. 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(4):263–278PubMedGoogle Scholar
  89. Soltis J, Thomsen R, Takenaka O (2001) The interaction of male and female reproductive strategies and paternity in wild Japanese macaques, Macaca fuscata. Anim Behav 62:485–494Google Scholar
  90. Strier KB (1992) Causes and consequences of nonaggression in the woolly spider monkey, or muriqui (Brachyteles arachnoides). In: Silverberg J, Gray JP (eds) Aggression and peacefulness in humans and other primates. Oxford University Press, New York, pp 100–116Google Scholar
  91. Strier K (1997) Mate preference of wild muriqui monkeys (Brachyteles arachnoides): reproductive and social correlates. Folia Primatol 68:120–133CrossRefGoogle Scholar
  92. Stumpf RM (2004) Female reproductive strategies in chimpanzees of the Taï National Park, Cote d’Ivoire. Ph.D. thesis, Stony Brook University, Stony Brook, NYGoogle Scholar
  93. Stumpf RM, Boesch C (2005) Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees of the Taï Forest, Côte d’Ivoire. Behav Ecol Sociobiol 57:511–524Google Scholar
  94. Tabachnik BG, Fidell LS (2001) Using multivariate statistics. Allyn and BaconGoogle Scholar
  95. 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 146–155Google Scholar
  96. Takasaki H (1985) Female life history and mating patterns among the M group chimpanzees in Mahale National Park, Tanzania. Primates 26:121–129Google Scholar
  97. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine, Chicago, pp 136–179Google Scholar
  98. Tutin CEG (1979) Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 6:29–38Google Scholar
  99. Tutin CEG (1980) Reproductive behaviour of wild chimpanzees in the Gombe National Park, Tanzania. J Reprod Fertil Suppl Suppl 18:43–57Google Scholar
  100. Tutin CEG, McGinnis PR (1981) Chimpanzee reproduction in the wild. In: Graham CE (ed) Reproductive biology of the great apes. Academic, New York, pp 239–264Google Scholar
  101. Utami SS, Goossens B, Bruford MW, de Ruiter JR, van Hooff JARAM (2002) Male bimaturism and reproductive success in sumatran orang-utans. Behav Ecol 13:643–652Google Scholar
  102. 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 361–387Google Scholar
  103. Van Schaik CP, Pradhan GR, van Noordwijk MA (2004) Mating conflict in primates: infanticide, sexual harassment and female sexuality. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. pp 131–150Google Scholar
  104. Wallen K, Winston LA (1984) Social complexity and hormonal influences on sexual behavior in rhesus monkeys (Macaca mulatta). Physiol Behav 32:629–637PubMedGoogle Scholar
  105. Wallis J (1992) Chimpanzee genital swelling and its role in the pattern of sociosexual behavior. Am J Primatol 28:101–113Google Scholar
  106. Watson PJ, Arnqvist G, Stallman RR (1998) Sexual conflict and the energetic costs of mating and mate choice in water striders. The Am Nat 151:46–58Google Scholar
  107. Wilcox A, Weinberg C, Baird D (1995) Timing of sexual intercourse in relation to ovulation. New Engl J Med 333:1517–1521PubMedGoogle Scholar
  108. Wiley RH, Poston J (1996) Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution 50:1371–1381Google Scholar
  109. Wrangham R (2002) The cost of sexual attraction: is there a trade-off in female Pan between sex appeal and received coercion? In: Hohmann G, Boesch C, Marchant L (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, CambridgeGoogle Scholar
  110. Wrangham RW, Smuts BB (1980) Sex difference in the behavioral ecology of chimpanzees in the Gombe national park, Tanzania. J Reprod Fertil Suppl Suppl 28:13–31PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  2. 2.Max Planck Institute for Evolutionary AnthropologyLeipzigGermany

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