Human Nature

, Volume 4, Issue 1, pp 47–79 | Cite as

The evolution of sexuality in chimpanzees and bonobos

  • Richard W. Wrangham
Article

Abstract

The evolution of nonconceptive sexuality in bonobos and chimpanzees is discussed from a functional perspective. Bonobos and chimpanzees have three functions of sexual activity in common (paternity confusion, practice sex, and exchange for favors), but only bonobos use sex purely for communication about social relationships. Bonobo hypersexuality appears closely linked to the evolution of female-female alliances. I suggest that these alliances were made possible by relaxed feeding competition, that they were favored through their effect on reducing sexual coercion, and that they are ultimately responsible for the relaxed social conditions that allowed the evolution of “communication sex.”

Key words

Primate sexuality Bonobos Chimpanzees Communication Social relationships Female Alliances 

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References

  1. Andelman, S.J. 1987 Evolution of Concealed Ovulation in Vervet Monkeys (Cercopithecus aethiops).American Naturalist 129:785–799.CrossRefGoogle Scholar
  2. Baum, M. J. 1983 Hormonal Ovulation of Sexuality in Female Primates.BioScience 33:578–582.CrossRefGoogle Scholar
  3. Beach, F. A. 1976 Sexual Attractivity, Proceptivity and Receptivity in Female Mammals.Hormones and Behavior 7:105–138.CrossRefGoogle Scholar
  4. 1977a Cross-Species Comparisons and the Human Heritage. InHuman Sexuality in Four Perspectives, F. A. Beach, ed. Pp. 296–316. Baltimore: Johns Hopkins University Press.Google Scholar
  5. 1977b Hormonal Control of Sex-Related Behavior. InHuman Sexuality in Four Perspectives, F. A. Beach, ed. Pp. 247–267. Baltimore: Johns Hopkins University Press.Google Scholar
  6. Bielert, C., and C. M. Anderson 1985 Baboon Sexual Swellings and Male Response: A Possible Operational Mammalian Supernormal Stimulus and Response Interaction.International Journal of Primatology 6:377–393.Google Scholar
  7. Birkhead, T. R., L. Atkin, and A. P. Møller 1987 Copulation Behavior of Birds.Behaviour 101:101–138.Google Scholar
  8. Blount, B. G. 1990 Issues in Bonobo (Pan paniscus) Sexual Behavior.American Anthropologist 92:702–714.CrossRefGoogle Scholar
  9. Booth, W. 1988 The Social Lives of Dolphins.Science 240:1273–1274.CrossRefGoogle Scholar
  10. Burt, A. 1992 “Concealed Ovulation” and Sexual Signals in Primates.Folia Primatologica 58:1–6.CrossRefGoogle Scholar
  11. Butler, H. 1974 Evolutionary Trends in Primate Sex Cycles.Contributions to Primatology 3:2–35.Google Scholar
  12. Dahl, J. F., R. D. Nadler, and D. G. Collins 1991 Monitoring the Ovarian Cycles ofPan troglodytes andP. paniscus: A Comparative Approach.American Journal of Primatology 24:195–209.CrossRefGoogle Scholar
  13. de Waal, F. B. 1982Chimpanzee Politics: Power and Sex among Apes. New York: Harper and Row.Google Scholar
  14. 1987 Tension Regulation and Nonreproductive Functions of Sex in Captive Bonobos (Pan paniscus).National Geographic Research 3:318–335.Google Scholar
  15. 1989Peacemaking among Primates. Cambridge: Harvard University Press.Google Scholar
  16. 1990 Sociosexual Behavior Used for Tension Regulation in All Age and Sex Combinations among Bonobos. InPedophilia: Biosocial Dimensions, J. R. Feierman, ed. Pp. 378–393. New York: Springer.Google Scholar
  17. 1992 Appeasement, Celebration and Food Sharing in the TwoPan Species. InHuman Origins, T. Nishida, W. C. McGrew, P. Marler, M. Pickford, and F. de Waal, eds. Pp. 37–50. Tokyo: University of Tokyo Press.Google Scholar
  18. Dixson, A. F. 1983 Observations on the Evolution and Behavioral Significance of “Sexual Skin” in Female Primates.Advances in the Study of Behaviour 13:63–106.Google Scholar
  19. Furuichi, T. 1987 Sexual Swelling, Receptivity, and Grouping of Wild Pygmy Chimpanzee Females at Wamba, Zaïre.Primates 28:309–318.CrossRefGoogle Scholar
  20. 1989 Social Interactions and the Life History of FemalePan paniscus in Wamba, Zaïre.International Journal of Primatology 10:173–197.Google Scholar
  21. Galdikas, B. M. F. 1981 Orangutan Reproduction in the Wild. InReproductive Biology of the Great Apes, C. F. Graham, ed. Pp. 281–299. New York: Academic Press.Google Scholar
  22. Goodall, J. 1968 The Behaviour of Free-Living Chimpanzees in the Gombe Stream Reserve.Animal Behaviour Monographs 1:161–311.Google Scholar
  23. 1986The Chimpanzees of Gombe: Patterns of Behavior. Cambridge: Harvard University Press.Google Scholar
  24. Grabowski, C. T. 1983Human Reproduction and Development. Philadelphia: Saunders College.Google Scholar
  25. Guilford, T., and M. Dawkins 1991 Receiver Psychology and the Evolution of Animal Signals.Animal Behaviour 42:1–14.CrossRefGoogle Scholar
  26. Hamilton, W. J. 1984 Significance of Paternal Investment by Primates to the Evolution of Male-Female Associations. InPrimate Paternalism, D. M. Taub, ed. Pp. 309–335. New York: van Nostrand Reinhold.Google Scholar
  27. Harcourt, A. H., K. J. Stewart, and D. Fossey 1981 Gorilla Reproduction in the Wild. InReproductive Biology of the Great Apes, C. E. Graham, ed. Pp. 265–279. New York: Academic Press.Google Scholar
  28. Harvey, P. H., and A. H. Harcourt 1984 Sperm Competition, Testis Size, and Breeding Systems in Primates. InSperm Competition and the Evolution of Mating Systems, R. L. Smith, ed. Pp. 589–600. New York: Academic Press.Google Scholar
  29. Hasegawa, T., and M. Hiraiwa-Hasegawa 1983 Opportunistic and Restrictive Matings among Wild Chimpanzees in the Mahale Mountains, Tanzania.Journal of Ethology 1:75–85.CrossRefGoogle Scholar
  30. 1990 Sperm Competition and Mating Behavior. InThe Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies, T. Nishida, ed. Pp. 115–132. Tokyo: University of Tokyo Press.Google Scholar
  31. Hausfater, G. 1975Dominance and Reproduction in Baboons (Papio cynocephalus). Contributions to Primatology, Vol. 7. Basel: S. Karger.Google Scholar
  32. Hemelrijk, C. K., G. J. van Laere, and J. A. R. A. M. van Hooff 1992 Sexual Exchange Relationships in Captive Chimpanzees?Behavioral Ecology and Sociobiology 30:269–275.CrossRefGoogle Scholar
  33. Hill, W. C. O. 1958 External Genitalia. InPrimatologia, Vol. 3, H. Hofer, A. H. Schultz, and D. Starck, eds. Pp. 630–704. Basel: S. Karger.Google Scholar
  34. Howell, N. 1979Demography of the Dobe !Kung. New York: Academic Press.Google Scholar
  35. Hrdy, S. B. 1981The Woman That Never Evolved. Cambridge: Harvard University Press.Google Scholar
  36. 1988 The Primate Origins of Human Sexuality. InThe Evolution of Sex, R. Bellig and G. Stevens, eds. Pp. 101–136. San Francisco: Harper and Row.Google Scholar
  37. Hrdy, S. B., and P. L. Whitten 1987 Patterning of Sexual Activity. InPrimate Societies, B. B. Smuts, D. Cheney, R. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, eds. Pp. 370–384. Chicago: University of Chicago Press.Google Scholar
  38. Idani, G. 1991a Cases of Inter-Unit Group Encounters in Pygmy Chimpanzees at Wamba, Zaïre. InPrimatology Today: Proceedings of the XIIIth Congress of the International Primatological Society, A. Ehara, T. Kimura, O. Takenaka, and M. Iwamoto, eds. Pp. 235–238. Amsterdam: Elsevier.Google Scholar
  39. 1991b Social Relationships between Immigrant and Resident Bonobo (Pan paniscus) Females at Wamba.Folia Primatologica 57:83–95.CrossRefGoogle Scholar
  40. Jungers, W. L., and R. L. Susman 1984 Body Size and Skeletal Allometry in African Apes. InThe Pygmy Chimpanzee: Evolutionary Biology and Behavior, R. L. Susman, ed. Pp. 131–178. New York: Plenum Press.Google Scholar
  41. Kano, T. 1982 The Social Group of Pygmy Chimpanzees (Pan paniscus) of Wamba.Primates 23:171–188.CrossRefGoogle Scholar
  42. 1989 The Sexual Behavior of Pygmy Chimpanzees. InUnderstanding Chimpanzees, P. G. Heltne and L. A. Marquardt, eds. Pp. 176–183. Cambridge: Harvard University Press.Google Scholar
  43. 1992The Last Ape: Pygmy Chimpanzee Behavior and Ecology. Stanford, California: Stanford University Press.Google Scholar
  44. Kitamura, K. 1989 Genito-Genital Contacts in the Pygmy Chimpanzees (Pan paniscus).African Study Monographs 10:49–67.Google Scholar
  45. Kuroda, S. 1980 Social Behavior of the Pygmy Chimpanzees.Primates 21:181–197.CrossRefGoogle Scholar
  46. 1984 Interaction over Food among Pygmy Chimpanzees. InThe Pygmy Chimpanzee: Evolutionary Biology and Behavior, R. L. Susman, ed. Pp. 301–324. New York: Plenum Press.Google Scholar
  47. Lipson, S. F., and P. T. Ellison 1992 Normative Study of Age Variation in Salivary Progesterone Profiles.Journal of Biosocial Science 24:233–244.Google Scholar
  48. Malenky, R. K. 1990Ecological Factors Affecting Food Choice and Social Organization in Pan paniscus, Ph.D. dissertation, State University of New York at Stony Brook.Google Scholar
  49. Martin, R. D. 1992 Female Cycles in Relation to Paternity in Primate Societies. InPaternity in Primates: Genetic Tests and Theories, R. D. Martin, A. F. Dixson, and E. J. Wickings, eds. Pp. 238–274. Basel: S. Karger.Google Scholar
  50. McHenry, H. M. 1984 The Common Ancestor: A Study of the Postcranium ofPan paniscus, Australopithecus, and Other Hominoids. InThe Pygmy Chimpanzee: Evolutionary Biology and Behavior, R. L. Susman, ed. Pp. 201–230. New York: Plenum Press.Google Scholar
  51. 1991 Sexual Dimorphism inAustralopithecus afarensis.Journal of Human Evolution 20:21–32.CrossRefGoogle Scholar
  52. Møller, A. P. 1988 Ejaculate Quality, Testes Size and Sperm Competition in Primates.Journal of Human Evolution 17:479–488.CrossRefGoogle Scholar
  53. Mori, A. 1984 An Ethological Study of Pygmy Chimpanzees in Wamba, Zaïre: A Comparison with Chimpanzees.Primates 25:255–278.CrossRefGoogle Scholar
  54. Nishida, T. 1980 The Leaf-clipping Display: A Newly Discovered Expressive Gesture in Wild Chimpanzees.Journal of Human Evolution 9:117–128.CrossRefGoogle Scholar
  55. Nishida, T., ed. 1990The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies. Tokyo: University of Tokyo Press.Google Scholar
  56. Nishida, T., H. Takasaki, and Y. Takahata 1990 Demography and Reproductive Profiles. InThe Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies, T. Nishida, ed. Pp. 63–98. Tokyo: University of Tokyo Press.Google Scholar
  57. Parish, A. 1992 Domestic Affairs: The Balance between Tension Reduction and Bonding in Bonobo Females.Abstracts of the XIVth Congress of the International Primatological Society, p. 162.Google Scholar
  58. Parish, A., and F. de Waal 1992 Bonobos Fish for Sweets: the Female Sex-for-Food Connection.Abstracts of the XIVth Congress of the International Primatological Society, p. 202.Google Scholar
  59. Pusey, A. E. 1978The Physical and Social Development of Wild Adolescent Chimpanzees (Pan troglodytes schweinfurthii). Ph.D. dissertation, Stanford University, Stanford, California.Google Scholar
  60. Rahm, U. 1967 Observations during Chimpanzee Captures in the Congo. InProgress in Primatology, D. Starck, R. Schneider, and H. J. Kuhn, eds. Pp. 195–207. Stuttgart: Fischer.Google Scholar
  61. Riesen, A. H. 1971 Nissen’s Observations of the Development of Sexual Behavior in Captive-Born, Nursery-Raised Chimpanzees. InThe Chimpanzee, Vol. 4, G. Bourne, ed. Pp. 1–18. Basel: S. Karger.Google Scholar
  62. Rodseth, L., R. W. Wrangham, A. Harrigan, and B. B. Smuts 1991 The Human Community as a Primate Society.Current Anthropology 32:221–254.CrossRefGoogle Scholar
  63. Rogers, C. M., and R. K. Davenport 1969 Effects of Restricted Rearing on Sexual Behavior of Chimpanzees.Developmental Psychology 1:200–204.CrossRefGoogle Scholar
  64. Short, R. V. 1979 Sexual Selection and Its Component Parts, Somatic and Genital Selection, as Illustrated by Man and the Great Apes.Advances in the Study of Behaviour 9:131–158.CrossRefGoogle Scholar
  65. Smuts, B. B., and N. Nicolson 1989 Reproduction in Wild Female Olive Baboons.American Journal of Primatology 19:229–246.CrossRefGoogle Scholar
  66. Smuts, B. B., and R. W. Smuts 1991 Male Aggression against Female Primates: Evidence and Theoretical Implications.Advances in the Study of Behaviour, in press.Google Scholar
  67. Smuts, B. B., and J. M. Watanabe 1990 Social Relationships and Ritualized Greetings in Adult Male Baboons (Papio cynocephalus anubis).International Journal of Primatology 11:147–172.CrossRefGoogle Scholar
  68. Stanyon, R., B. Chiarelli, K. Gottlieb, and W. H. Patton 1986 The Phylogenetic and Taxonomic Status ofPan paniscus: A Chromosomal Perspective.American Journal of Physical Anthropology 69:489–498.CrossRefGoogle Scholar
  69. Sugiyama, Y. 1988 Grooming Interactions among Adult Chimpanzees at Bossou, Guinea, with Special Reference to Social Structure.International Journal of Primatology 9:393–407.Google Scholar
  70. 1989 Population Dynamics of Chimpanzees at Bossou, Guinea. InUnderstanding Chimpanzees, P. G. Heltne and L. A. Marquardt, eds. Pp. 134–145. Cambridge: Harvard University Press.Google Scholar
  71. Temerlin, M. K. 1975Lucy: Growing Up Human. Palo Alto, California: Science and Behavior Books.Google Scholar
  72. Thompson-Handler, N., R. K. Malenky, and N. Badrian 1984 Sexual Behavior ofPan paniscus under Natural Conditions in the Lomako Forest, Equateur, Zaire. InThe Pygmy Chimpanzee: Evolutionary Biology and Behavior, R. L. Susman, ed. Pp. 347–368. New York: Plenum Press.Google Scholar
  73. Tratz, E., and H. Heck 1954 Der Afrikanische Anthropoide “Bonobo,” Eine Neue Menschenaffengattung.Sugetierkundige Mitt. 2:97–101.Google Scholar
  74. Tutin, C. E. G. 1976Sexual Behaviour and Mating Patterns in a Community of Wild Chimpanzees (Pan troglodytes schweinfurthii). Ph.D. thesis, University of Edinburgh.Google Scholar
  75. Tutin, C. E. G., and P. R. McGinnis 1981 Chimpanzee Reproduction in the Wild. InReproductive Biology of the Great Apes, C. E. Graham, ed. Pp. 239–264. New York: Academic Press.Google Scholar
  76. Tutin, C. E. G., and W. C. McGrew 1973 Chimpanzee Copulatory Behaviour.Folia Primatologica 19:237–256.Google Scholar
  77. Uehara, S., and T. Nishida 1987 Body Weights of Wild Chimpanzees (Pan troglodytes schweinfurthii) of the Mahale Mountains National Park, Tanzania.American Journal of Physical Anthropology 72:315–321.CrossRefGoogle Scholar
  78. Vrba, E. S. 1988 Late Pliocene Climatic Events and Hominid Evolution. InEvolutionary History of the “Robust” Australopithecines, F. E. Grine, ed. Pp. 405–426. New York: Aldine de Gruyter.Google Scholar
  79. Wallis, J. 1992 Chimpanzee Genital Swelling and Its Role in the Pattern of Sociosexual Behavior.American Journal of Primatology 28:101–113.CrossRefGoogle Scholar
  80. Watts, D. 1990 Mountain Gorilla Life Histories, Reproductive Competition, and Sociosexual Behavior and Some Implications for Captive Husbandry.Zoo Biology 9:185–200.CrossRefGoogle Scholar
  81. White, F. J. 1988 Party Composition and Dynamics inPan paniscus.International Journal of Primatology 9:179–193.Google Scholar
  82. 1989 Social Organization of Pygmy Chimpanzees. InUnderstanding Chimpanzees, P. G. Heltne and L. A. Marquardt, eds. Pp. 194–207. Cambridge: Harvard University Press.Google Scholar
  83. 1992 Pygmy Chimpanzee Social Organization: Variation with Party Size and between Study Sites.American Journal of Primatology 26:203–214.CrossRefGoogle Scholar
  84. White, F. J., and R. W. Wrangham 1988 Feeding Competition and Patch Size in the Chimpanzee SpeciesPan paniscus andPan troglodytes.Behaviour 105:148–164.Google Scholar
  85. Wickler, W. 1967 Sociosexual Signals and Their Intraspecific Imitation among Primates. InPrimate Ethology, D. Morris, ed. Pp. 69–147. New York: Doubleday.Google Scholar
  86. Wrangham, R. W. 1979 On the Evolution of Ape Social Systems.Social Science Information 18:334–368.CrossRefGoogle Scholar
  87. 1986 Ecology and Social Evolution in Two Species of Chimpanzees. InEcology and Social Evolution: Birds and Mammals, D. I. Rubenstein and R. W. Wrangham, eds. Pp. 352–378. Princeton: Princeton University Press.Google Scholar
  88. Wrangham, R. W., and B. B. Smuts 1980 Sex Differences in the Behavioural Ecology of Chimpanzees in Gombe National Park, Tanzania.Journal of Reproduction and Fertility, Supplement 28:13–31.Google Scholar
  89. Wrangham, R. W., A. P. Clark, and G. Isabirye-Basuta 1992 Female Social Relationships and Social Organization of Kibale Forest Chimpanzees. InHuman Origins, T. Nishida, W. C. McGrew, P. Marler, M. Pickford, and F. de Waal, eds. Pp. 81–98. Tokyo: University of Tokyo Press.Google Scholar
  90. Yerkes, R. M. 1943Chimpanzees: A Laboratory Colony. New Haven: Yale University Press.Google Scholar
  91. Yerkes, R. M., and J. H. Elder 1936 Oestrus, Receptivity and Mating in Chimpanzees.Comparative Psychology Monographs 13:1–39.Google Scholar
  92. Zahavi, A. 1977 The Testing of a Bond.Animal Behaviour 25:246–247.CrossRefGoogle Scholar
  93. Zihlman, A. L. 1979 Pygmy Chimpanzees and Early Hominids.South African Journal of Science 75:165–168.Google Scholar
  94. Zihlman, A. L., J. Cronin, D. Cramer, and V. Sarich 1978 Pygmy Chimpanzees as a Possible Prototype for the Common Ancestor of Humans, Chimpanzees, and Gorillas.Nature 275:744–746.CrossRefGoogle Scholar

Copyright information

© Walter de Gruyter, Inc 1993

Authors and Affiliations

  • Richard W. Wrangham
    • 1
  1. 1.Peabody MuseumHarvard UniversityCambridge

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