Behavioral Ecology and Sociobiology

, Volume 59, Issue 3, pp 333–343 | Cite as

The evolution of female copulation calls in primates: a review and a new model

  • Gauri R. Pradhan
  • Antje Engelhardt
  • Carel P. van Schaik
  • Dario Maestripieri


Female copulation calls are mating-associated vocalizations that occur in some species of Old World monkeys and apes. We argue that copulation calls have two immediate functions: to encourage mating attempts by other males and to increase mate guarding by the consort male. We hypothesize that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition. When male mate guarding is effective, copulation calls allow females to concentrate paternity in dominant males and benefit from their protection against the risk of infanticide. When mate guarding is ineffective, copulation calls may bring genetic benefits to females through facilitation of sperm competition. We present a quantitative model in which interspecific variation in females' promiscuity predicts their tendency to use copulation calls in conjunction with mating. The model predicts that in species with little female promiscuity, copulation calls should be rare and exhibited only in association with mating with dominant males. In species in which females are highly promiscuous, copulation calls should be frequent and unrelated to male dominance rank. The limited data available to test the model support its main predictions as well as the predicted relation between copulation calls and male dominance rank.


Sexual selection Infanticide Sperm competition Copulation calls Primates 



This research was supported by NIH grants R01-MH62577 and K02-MH63097. We thank Sagar Pandit and Stephen Pruett-Jones for helpful discussion and comments on this manuscript.


  1. Aich H, Moos-Heilen R, Zimmermann E (1990) Vocalizations on adult gelada baboons (Theropithecus gelada): acoustic structure and behavioural context. Folia Primatol 55:109–132PubMedGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJGoogle Scholar
  3. Aujard F, Heistermann M, Thierry B, Hodges JK (1998) Functional significance of behavioral, morphological, and endocrine correlates across the ovarian cycle in semifree ranging female tonkean macaques. Am J Primatol 46:285–309CrossRefPubMedGoogle Scholar
  4. Birkhead TR, Pizzari T (2002) Postcopulatory sexual selection. Nat Rev Gen 3:262–273CrossRefGoogle Scholar
  5. Blake BH (1992) Estrous calls in captive Asian chipmunks, Tamias sibiricus. J Mammal 73:597–603CrossRefGoogle Scholar
  6. Cheng MF (1992) For whom does the female dove coo? A case for the role of vocal self-stimulation. Anim Behav 43:1035–1044CrossRefGoogle Scholar
  7. Cox CR, LeBoeuf BJ (1977) Female incitation of male competition: a mechanism in sexual selection. Am Nat 111:317–335CrossRefGoogle Scholar
  8. Deputte BL, Goustard M (1980) Copulatory vocalisations of female macaques (Macaca fascicularis): variability factors analysis. Primates 21:83–89CrossRefGoogle Scholar
  9. Dixson AF (1998) Primate sexuality: comparative studies of the prosimians, monkeys, apes and human beings. Oxford University Press, OxfordGoogle Scholar
  10. Gouzoules H, Gust DA, Donaghey B, St. Andre E (1998) Estrus vocalizations in two primate species (Cercocebus torquatus atys and Macaca nemestrina): evidence for an effect of intrasexual competition. Evol Comm 2:189–215Google Scholar
  11. Gust DA, Gordon TP (1991) Male age and reproductive behaviour in sooty mangabeys, Cercocebus torquatus atys. Anim Behav 41:277–283CrossRefGoogle Scholar
  12. Hall KRL, DeVore I (1965) Baboons social behavior. In: DeVore I (ed) Primate behavior. Field studies of monkeys and apes. Holt, Rinehart and Winston, New York, pp 53–110Google Scholar
  13. Hamilton WJ III, Arrowood PC (1978) Copulatory vocalizations of chacma baboons (Papio ursinus), gibbons (Hylobates hoolock), and humans. Science 200:1405–1409PubMedCrossRefGoogle Scholar
  14. Hasegawa T, Hirawa-Hasegawa M (1990) Sperm competition and mating behavior. In: Nishida T (ed) Chimpanzees of Mahale mountains: sexual and life history strategies. University of Tokyo Press, Tokyo, pp 115–132Google Scholar
  15. Hauser MD (1990) Do chimpanzee copulatory calls incite male–male competition? Anim Behav 39:596–597CrossRefGoogle Scholar
  16. Hauser MD (1993) Rhesus monkey (Macaca mulatta) copulation calls: honest signals for female choice? Proc R Soc Lond B 254:93–96CrossRefGoogle Scholar
  17. Henzi SP (1996) Copulation calls and paternity in chacma baboons. Anim Behav 51:233–234CrossRefGoogle Scholar
  18. Hohmann GM, Herzog MO (1985) Vocal communication in lion-tailed macaques (Macaca silenus). Folia Primatol 45:148–178PubMedCrossRefGoogle Scholar
  19. Hrdy SB (1974) Male–male competition and infanticide among the langurs (Presbytis entellus) of Abu, Rajasthan. Folia Primatol 22:19–58PubMedGoogle Scholar
  20. Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13–40CrossRefGoogle Scholar
  21. Hsu MJ, Lin JF, Chen LM, Agoramoorthy G (2002) Copulation calls in male Formosan macaques: honest signals of male quality? Folia Primatol 73:220–223CrossRefPubMedGoogle Scholar
  22. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64CrossRefPubMedGoogle Scholar
  23. Lindburg DG (1990) Proceptive calling by female lion-tailed macaques. Zoo Biol 9:437–446CrossRefGoogle Scholar
  24. Maestripieri DM, Roney JR (2005) Primate copulation calls and postcopulatory female choice. Behav Ecol 16:106–113CrossRefGoogle Scholar
  25. Maestripieri DM, Leoni M, Raza SS, Hirsch EJ, Whitham JC (2005) Female copulation calls in Guinea baboons: evidence for post-copulatory female choice? Int J Primatol 26:737–758CrossRefGoogle Scholar
  26. Manson JH (1996) Rhesus macaque copulation calls: re-evaluating the “honest signal” hypothesis. Primates 37:145–154CrossRefGoogle Scholar
  27. Milton K (1985) Mating patterns of woolly spider monkeys, Brachyteles arachnoides-implications for female choice. Behav Ecol Sociobiol 17:53–59CrossRefGoogle Scholar
  28. Montgomerie R, Thornhill R (1989) Fertility advertisement in birds: a means of inciting male–male competition? Ethology 81:209–220Google Scholar
  29. Moos-Heilen R, Sossinka R (1990) The influence of oestrus on the vocalizations of female gelada baboons (Theropithecus gelada). Ethology 84:35–46CrossRefGoogle Scholar
  30. Nikitopoulos E (2004) What a girl wants, what a girl needs. Ph.D. Thesis. Utrecht University, Utrecht, The NetherlandsGoogle Scholar
  31. Nikitopoulos E, Arnhem E, van Hooff J, Sterck E (2004) Influence of female copulation calls on male sexual behavior in captive Macaca fascicularis. Int J Primatol 25:659–677CrossRefGoogle Scholar
  32. O'Connell SM, Cowlishaw G (1994) Infanticide avoidance, sperm competition and mate choice: the function of copulation calls in female baboons. Anim Behav 48:687–694CrossRefGoogle Scholar
  33. Oda R, Masataka N (1992) Functional significance of female Japanese macaque copulatory calls. Folia Primatol 58:146–149PubMedGoogle Scholar
  34. Oda R, Masataka N (1995) Function of copulatory vocalizations in mate choice by female Japanese macaques (Macaca fuscata). Folia Primatol 64:132–139PubMedGoogle Scholar
  35. Oi T (1996) Sexual behavior and mating system of wild pig-tailed macaque in West Sumatra. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaque societies. Cambridge University Press, Cambridge, pp 342–368Google Scholar
  36. Saayman GS (1970) The menstrual cycle and sexual behaviour in a troop of free ranging chacma baboons (Papio ursinus). Folia Primatol 12:81–100PubMedGoogle Scholar
  37. Semple S (1998a) Female copulation calls in primates. Ph.D. Dissertation. University of Sussex, Sussex, UKGoogle Scholar
  38. Semple S (1998b) The function of Barbary macaque copulation calls. Proc R Soc Lond B 265:287–291CrossRefGoogle Scholar
  39. Semple S, McComb K (2000) Perception of female reproductive state from vocal cues in a mammal species. Proc R Soc Lond B 267:707–712CrossRefGoogle Scholar
  40. Semple S, McComb K, Alberts S, Altmann J (2002) Information content of female copulation calls in yellow baboons. Am J Primatol 56:43–56CrossRefPubMedGoogle Scholar
  41. Sterling EJ, Richard AF (1995) Social organization in the aye-aye (Daubentonia madagascariensis) and the perceived distinctiveness of nocturnal primates. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Plenum Press, New York, pp 439–451Google Scholar
  42. Todt D, Hammerschmidt K, Ansorge V, Fischer J (1995) The vocal behavior of Barbary macaques (Macaca sylvanus): call features and their performance in infants and adults. In: Zimmermann E, Newman JD, Juergens U (eds) Current topics in primate vocal communications. Plenum Press, New York, pp 141–160Google Scholar
  43. van Noordwijk MA (1985) Sexual behaviour of Sumatran long-tailed macaques (Macaca fascicularis). Z Tierpsychol 70:277–296Google Scholar
  44. van Schaik CP (2000) Infanticide by male primates: the sexual selection hypothesis revisited. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 27–60Google Scholar
  45. van Schaik CP, van Noordwijk M, Nunn CL (1999) Sex and social evolution in primates. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, pp 204–240Google Scholar
  46. van Schaik CP, Pradhan GR, van Noordwijk M (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 131–150Google Scholar
  47. Viljoen S (1977) Factors affecting breeding synchronization in an African bush squirrel (Paraxerus cepapi cepapi). J Reprod Fertil 50:125–127PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Gauri R. Pradhan
    • 1
  • Antje Engelhardt
    • 2
  • Carel P. van Schaik
    • 3
  • Dario Maestripieri
    • 1
    • 4
  1. 1.Animal Behavior Research GroupThe University of ChicagoChicagoUSA
  2. 2.German Primate CenterGottingenGermany
  3. 3.Anthropological Institute and MuseumUniversity of ZurichZurichSwitzerland
  4. 4.The University of ChicagoChicagoUSA

Personalised recommendations