Primates

, Volume 41, Issue 1, pp 1–16 | Cite as

Primate sexual swellings as coevolved signal systems

  • Robert R. Stallmann
  • Jeffery W. Froehlich
Article

Abstract

Many female catarrhine primates possess visually conspicuous organs that apparently function to increase the sexual interest of adult male conspecifics around the time the female is ovulating—i.e. sexual swellings. The hypothesized functional benefits for both sexes of these sexual swellings are reviewed (honest signaling; paternity confusion; paternity confidence and paternal investment; protection; incitement of precopulatory male-male competition; and postcopulatory sexual selection), as well as an additional hypothesis that has not yet been applied to this problem (sensory exploitation). Currently available evidence is presented that supports or fails to support each of these hypotheses. Predictions associated with broad groupings of these hypotheses, which could be tested in noninvasive field studies, are then presented. Ecological circumstances are discussed that could have led to differential mating success among female primates, and hence to sexual selection on females and directional evolution of sexual swellings. It is concluded that the available evidence does not support the paternity confidence-paternal investment hypothesis; that the paternity confusion hypothesis lacks empirical support, but could still be viable; and that insufficient data exists at present to rigorously test the other hypotheses. The ecological factors that may have led to differential reproductive success among females as a function of mating frequency or mate choice likewise require further empirical investigation.

Key Words

Sexual swellings Sexual conflict Sexual selection Mate choice Multiple mating 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alberts, S. C.;Sapolsky, R. M.;Altmann, J. 1992. Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group.Horm. Behav., 26: 167–178.PubMedCrossRefGoogle Scholar
  2. Altmann, J. 1997. Mate choice and intrasexual reproductive competition: contributions to reproduction that go beyond acquiring more mates. In:Feminism and Evolutionary Biology: Boundaries, Intersections, and Frontiers,Gowaty,P. A. (ed.), Chapman & Hall, New York, pp. 320–333.Google Scholar
  3. Andersson, M. 1994.Sexual Selection. Princeton Univ. Press, Princeton.Google Scholar
  4. Arnqvist, G.;Rowe, L. 1995. Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect.Proc. R. Soc. Lond. B, 261: 123–127.CrossRefGoogle Scholar
  5. Basolo, A. L. 1990. Female preference predates the evolution of the sword in swordtail fish.Science, 250: 808–810.CrossRefPubMedGoogle Scholar
  6. Beach, F. A. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals.Horm. Behav., 7: 105–138.PubMedCrossRefGoogle Scholar
  7. Bielert, C.;Anderson, C. M. 1985. Baboon sexual swellings and male response: a possible operational supernormal stimulus and response interaction.Int. J. Primatol. 6: 377–393.Google Scholar
  8. Birkhead, T. R.;Fletcher, F.;Pellatt, E. J.;Staples, A. 1995. Ejaculate quality and the success of extra-pair copulations in the zebra finch.Nature, 377: 422–423.CrossRefGoogle Scholar
  9. Birkhead, T. R.;Møller, A. P. (eds.), 1998a)Sperm Competition and Sexual Selection. Academic Press, New York.Google Scholar
  10. Birkhead, T. R.;Møller, A. P. 1998b. Sperm competition, sexual selection and different routes to fitness. In:Sperm Competition and Sexual Selection,Birkhead,T. R.;Møller,A. P. (eds.), Academic Press, New York, pp. 757–781.Google Scholar
  11. Clark, A. G.;Begun, D. J.;Prout, T. 1999. Female x male interactions inDrosophila sperm competition.Science, 283: 217–220.PubMedCrossRefGoogle Scholar
  12. Clutton-Brock, T. H.;Harvey, P. H. 1976. Evolutionary rules and primate societies. In:Growing Points in Ethology,Bateson,P. P. G.;Hinde,R. A. (eds.), Cambridge Univ. Press, Cambridge, pp. 195–237.Google Scholar
  13. Cowlishaw, G.;O'Connell, S. M. 1996. Male-male competition, paternity certainty and copulation calls in female baboons.Anim. Behav., 51: 235–238.CrossRefGoogle Scholar
  14. Cox, C. R.;LeBoeuf, B. J. 1977. Female incitation of male competition: a mechanism in sexual selection.Amer. Naturalist, 111: 317–335.CrossRefGoogle Scholar
  15. Cunningham, E. J. A.;Birkhead, T. R. 1998. Sex roles and sexual selection.Anim. Behav., 56: 1311–1321.PubMedCrossRefGoogle Scholar
  16. Curtsinger, J. W. 1991. Sperm competition and the evolution of multiple mating.Amer. Naturalist, 138: 93–102.CrossRefGoogle Scholar
  17. Dahl, J. F. 1986. Cyclic perineal swelling during the intermenstrual intervals of captive female pygmy chimpanzees (Pan paniscus).J. Human Evol., 15: 369–385.CrossRefGoogle Scholar
  18. Devsbury, D. A. 1982. Ejaculate cost and mate choice.Amer. Naturalist, 119: 601–610.CrossRefGoogle Scholar
  19. Dixson, A. F. 1998a.Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Human Beings. Oxford Univ. Press, Oxford.Google Scholar
  20. Dixson, A. F. 1998b. Sexual selection and evolution of the seminal vesicles in primates.Folia Primatol., 69: 300–306.PubMedCrossRefGoogle Scholar
  21. Eberhard, W. G. 1996.Female Control: Sexual Selection by Cryptic Female Choice. Princeton Univ. Press, Princeton.Google Scholar
  22. Eberhard, W. G. 1998. Female roles in sperm competition. In:Sperm Competition and Sexual Selection,Birkhead,T. R.;Møller,A. P. (eds.), Academic Press, New York, pp. 91–116.Google Scholar
  23. Estep, D. Q.;Nieuwenhuijsen, K.;Bruce, K. E. M.;De Neef, K. J.;Walters, P. A.;Baker, S. C.;Slob, A. K. 1988. Inhibition of sexual behaviour among subordinate stumptail macaques,Macaca arctoides.Anim. Behav., 36: 854–864.CrossRefGoogle Scholar
  24. Fleagle, J. G. 1999.Primate Adaptation and Evolution (2nd ed.). Academic Press, San Diego.Google Scholar
  25. Gagneux, P.;Woodruff, D. S.;Boesch, C. 1997. Furtive mating in female chimpanzees.Nature, 387: 358–359.PubMedCrossRefGoogle Scholar
  26. Glick, B. B. 1980. Ontogenetic and psychobiological aspects of the mating activities of maleMacaca radiata. In:The Macaques: Studies in Ecology, Behavior and Evolution,Lindburg,D. G. (ed.), Van Nostrand Reinhold, New York, pp. 345–369.Google Scholar
  27. Goldfoot, D. A. 1971. Hormonal and social determinants of sexual behavior in pigtail monkeys (Macaca nemestrina). In:Normal and Abnormal Development of Brain and Behavior,Stoelinga,G. B. A.;van der Werfften Bosch,J. J. (eds.), Leiden Univ. Press, Leiden, pp. 325–342.Google Scholar
  28. Gomendio, M.;Harcourt, A. H.;Roldan, E. R. S. 1998. Sperm competition in mammals. In:Sperm Competition and Sexual Selection,Birkhead,T. R.;Møller,A. P. (eds.), Academic Press, San Diego, pp. 667–756.Google Scholar
  29. Goodall, J. 1986.The Chimpanzees of Gombe: Patterns of Behavior. Harvard Univ. Press, Cambridge, Massachusetts.Google Scholar
  30. Gould, S. J.;Lewontin, R. C. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme.Proc. R. Soc. Lond. B, 205: 581–598.PubMedGoogle Scholar
  31. Hamilton, W. D.;Zuk, M. 1982. Heritable true fitness and bright birds: a role for parasites?Science, 218: 384–387.PubMedCrossRefGoogle Scholar
  32. Hamilton, W. J. 1984. Significance of paternal investment by primates to the evolution of male-female associations. In:Primate Paternalism,Taub,D. M. (ed.), Van Nostrand Reinhold, New York, pp. 309–335.Google Scholar
  33. Harcourt, A. H. 1989. Environment, competition and reproductive performance of female monkeys.Trends Ecol. Evol., 4: 101–105.CrossRefGoogle Scholar
  34. Harcourt, A. H. 1995. Sexual selection and sperm competition in primates: what are male genitalia good for?Evol. Anthropol., 4: 121–129.CrossRefGoogle Scholar
  35. Harvey, P. H.;May, R. M. 1989. Out for the sperm count.Nature, 337: 508–509.PubMedCrossRefGoogle Scholar
  36. Hill, R. A.;Dunbar, R. I. M. 1998. An evaluation of the roles of predation rate and predation risk as selective pressures on primate grouping behaviour.Behaviour, 135: 411–430.Google Scholar
  37. Hiraiwa-Hasegawa, M. 1988. Adaptive significance of infanticide in primates.Trends Ecol. Evol., 3: 102–105.CrossRefGoogle Scholar
  38. Hiraiwa-Hasegawa, M.;Hasegawa, T. 1994. Infanticide in nonhuman primates: sexual selection and local resource competition. In:Infanticide and Parental Care,Parmigiani,S.;vom Saal,F. S. (eds.), Harwood, New York, pp. 137–154.Google Scholar
  39. Hoogland, J. L. 1998. Why do female Gunnison's prairie dogs copulate with more than one male?Anim. Behav., 55: 351–359.PubMedCrossRefGoogle Scholar
  40. Hrdy, S. B. 1979. Infanticide among animals: a review, classification and examination of the implications for the reproductive strategies of females.Ethol. Sociobiol., 1: 13–40.CrossRefGoogle Scholar
  41. Hrdy, S. B. 1981.The Woman That Never Evolved. Harvard Univ. Press, Cambridge, Massachusetts.Google Scholar
  42. Hrdy, S. B.;Whitten, P. L. 1987. Patterns of sexual activity. In:Primate Societies,Smuts,B. B.;Cheney,D. L.;Seyfarth,R. M.;Wrangham,R. W.;Struhsaker,T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 370–384.Google Scholar
  43. Johnstone, R. A. 1995. Sexual selection, honest advertisement and the handicap principle: reviewing the evidence.Biol. Rev., 70: 1–65.PubMedCrossRefGoogle Scholar
  44. Kuester, J.;Paul, A. 1996. Female-female competition and male mate choice in Barbary macaques (Macaca sylvanus).Behaviour, 133: 763–790.Google Scholar
  45. Madsen, T.;Shine, R.;Loman, J.;Håkansson, T. 1992. Why do female adders copulate so frequently?Nature, 355: 440–441.CrossRefGoogle Scholar
  46. Manson, J. H. 1992. Measuring female mate choice in Cayo Santiago rhesus macaques.Anim. Behav., 44: 405–416.CrossRefGoogle Scholar
  47. Manson, J. H. 1994. Male aggression: a cost of female choice in Cayo Santiago rhesus macaques.Anim. Behav., 48: 473–475.CrossRefGoogle Scholar
  48. Manson, J. H. 1997. Primate consortships: a critical review.Cur. Anthropol., 38: 353–374.CrossRefGoogle Scholar
  49. Mori, A.;Yamaguchi, N.;Watanabe, K.;Shimizu, K. 1997. Sexual maturation of female Japanese macaques under poor nutritional conditions and food-enhanced perineal swelling in the Koshima troop.Int. J. Primatol., 18: 553–579.CrossRefGoogle Scholar
  50. Nunn, C. L. 1996. Male harassment and the evolution of prominent estrous advertisement in primates. Paper presented at the International Primatological Society, American Society of Primatologists Joint Congress, Madison, Wisconsin.Google Scholar
  51. O'Connell, S. M.;Cowlishaw, G. 1994. Infanticide avoidance, sperm competition and mate choice: the function of copulation calls in female baboons.Anim. Behav., 48: 687–694.CrossRefGoogle Scholar
  52. Oi, T. 1987. Sexual behavior of the wild pig-tailed macaques in west Sumatra: Kyoto Univ. Overseas Res. Rep. Studies on Asian Non-human Primates, No. 6. Primate Res. Instit., Kyoto Univ., Inuyama, Japan.Google Scholar
  53. Oi, T. 1996. Sexual behaviour and mating system of the wild pig-tailed macaque in West Sumatra. In:Evolution and Ecology of Macaque Societies,Fa,J. E.;Lindburg,D. G. (eds.), Cambridge Univ. Press, Cambridge, pp. 342–368.Google Scholar
  54. Olsson, M.;Madsen, T.;Shine, R. 1997. Is sperm really so cheap?: costs of reproduction in male adders,Vipera berus.Proc. R. Soc. Lond. B, 264: 455–459.CrossRefGoogle Scholar
  55. Olsson, M.;Shine, R.;Madsen, T.;Gullberg, A.;Tegelstrom, H. 1996. Sperm selection by females.Nature, 383: 585.CrossRefGoogle Scholar
  56. Owens, I. P. F.;Thompson, D. B. A. 1994. Sex differences, sex ratios and sex roles.Proc. R. Soc. Lond. B, 258: 93–99.CrossRefGoogle Scholar
  57. Pagel, M. 1994. The evolution of conspicuous oestrous advertisement in Old World monkeys.Anim. Behav., 47: 1333–1341.CrossRefGoogle Scholar
  58. Paul, A. 1989. Determinants of male mating success in a large group of barbary macaques (Macaca sylvanus) at Affenberg Salem.Primates, 30: 461–476.CrossRefGoogle Scholar
  59. Perrigo, G.;Bryant, W. C.;vom Saal, F. S. 1990. A unique neural timing system prevents male mice from harming their own offspring.Anim. Behav., 39: 535–539.CrossRefGoogle Scholar
  60. Petrie, M. 1994. Improved growth and survival of offspring of peacocks with more elaborate trains.Nature, 371: 598–599.CrossRefGoogle Scholar
  61. Promislow, D. E. L.;Smith, E. A.;Pearse, L. 1998. Adult fitness consequences of sexual selection inDrosophila melanogaster.Proc. Natl. Acad. Sci. USA, 95: 10687–10692.PubMedCrossRefGoogle Scholar
  62. Pusey, A.;Williams, J.;Goodall, J. 1997. The influence of dominance rank on the reproductive success of female chimpanzees.Science, 277: 828–831.PubMedCrossRefGoogle Scholar
  63. Qvarnström, A.;Forsgren, E. 1998. Should females prefer dominant males?Trends Ecol. Evol., 13: 498–501.CrossRefGoogle Scholar
  64. Reynolds, J. D.;Gross, M. R. 1992. Female mate preference enhances offspring growth and reproduction in a fish,Poecilia reticulata.Proc. R. Soc. Lond. B, 250: 57–62.CrossRefGoogle Scholar
  65. Roldan, E. R. S.;Cassinello, J.;Abaigar, T.;Gomendio, M. 1998. Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate.Proc. R. Soc. Lond. B, 265: 243–248.CrossRefGoogle Scholar
  66. Roldan, E. R. S.;Gomendio, M. 1995. Sperm length and sperm competition in primates: a rebuttal of criticism.Folia Primatol., 64: 225–230.PubMedCrossRefGoogle Scholar
  67. Ryan, M. J.;Wagner, W. E. 1987. Asymmetries in mating preferences between species: female swordtails prefer heterospecific males.Science, 236: 595–597.CrossRefPubMedGoogle Scholar
  68. Ryan, M. J.;Fox, J. H.;Wilczynski, W.;Rand, A. S. 1990. Sexual selection for sensory exploitation in the frogPhysalaemus pustulosus.Nature, 343: 66–67.PubMedCrossRefGoogle Scholar
  69. Schwagmeyer, P. L.;Parker, G. A. 1990. Male mate choice as predicted by sperm competition in thirteenlined ground squirrels.Nature, 348: 62–64.CrossRefGoogle Scholar
  70. Sillen-Tullberg, B.;Møller, A. P. 1993. The relationship between concealed ovulation and mating systems in anthropoid primates: a phylogenetic analysis.Amer. Naturalist, 141: 1–25.CrossRefGoogle Scholar
  71. Small, M. F. 1989. Female choice in nonhuman primates.Yrbk. Phys. Anthropol., 32: 103–127.CrossRefGoogle Scholar
  72. Smuts, B. B. 1985.Sex and Friendship in Baboons, Aldine, Chicago.Google Scholar
  73. Smuts, B. B. 1987a. Sexual competition and mate choice. In:Primate Societies,Smuts,B. B.;Cheney,D. L.;Seyfarth,R. M.;Wrangham,R. W.;Struhsaker,T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 385–399.Google Scholar
  74. Smuts, B. B. 1987b. Gender, aggression, and influence. In:Primate Societies,Smuts,B. B.;Cheney,D. L.;Seyfarth,R. M.;Wrangham,R. W.;Struhsaker,T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 400–412.Google Scholar
  75. Thierry, B.; Aujard, F.; Hodges, J. K. 1996a. Correlations between behavioral, hormonal and morphological variations in the menstrual cycle of female Tonkean macaques. Paper presented at the International Primatological Society, American Society of Primatologists Joint Congress, Madison, Wisconsin.Google Scholar
  76. Thierry, B.;Heistermann, M.;Aujard, F.;Hodges, J. K. 1996b. Long-term data on basic reproductive parameters and evaluation of endocrine, morphological, and behavioral measures for monitoring reproductive status in a group of semifree-ranging Tonkean macaques (Macaca tonkeana).Amer. J. Primatol., 39: 47–62.CrossRefGoogle Scholar
  77. van Schaik, C. P. 1983. Why are diurnal primates living in groups?Behaviour, 87: 120–144.Google Scholar
  78. van Voorhies, W. A. 1992. Production of sperm reduces nematode lifespan.Nature, 360: 456–458.PubMedCrossRefGoogle Scholar
  79. Watson, P. J. 1990. Female-enhanced male competition determines the first mate and principle sire in the spiderLinyphia litigiosa (Lyniphiidae).Behav. Ecol. Sociobiol., 26: 77–90.CrossRefGoogle Scholar
  80. Watson, P. J. 1998. Multi-male mating and female choice increases offspring growth in the spiderNeriene litigiosa (Linyphidae).Anim. Behav., 55: 387–403.PubMedCrossRefGoogle Scholar
  81. Whitten, P. L.;Russell, E. 1996. Information content of sexual swellings and fecal steroids in sooty mangabeys (Cercocebus torquatus atys).Amer. J. Primatol., 40: 67–82.CrossRefGoogle Scholar
  82. Wickler, W. 1967. Socio-sexual signals and their intra-specific imitation among primates. In:Primate Ethology,Morris,D. (ed.), Doubleday, New York, pp. 89–189.Google Scholar
  83. Wildt, D. E.;Doyle, L. L.;Stone, S. C.;Harrison, R. M. 1977. Correlation of perineal swelling with serum ovarian hormone levels, vaginal cytology, and ovarian follicular development during the baboon reproductive cycle.Primates, 18: 261–270.CrossRefGoogle Scholar
  84. Wilson, N.;Tubman, S. C.;Eady, P. E.;Robertson, G. W. 1997. Female genotype affects male success in sperm competition.Proc. R. Soc. Lond. B, 264: 1491–1495.CrossRefGoogle Scholar
  85. Woodroffe, R.;Vincent, A. 1994. Mother's little helpers: patterns of male care in mammals.Trends Ecol. Evol., 9: 294–297.CrossRefGoogle Scholar
  86. Wrangham, R. W. 1993. The evolution of sexuality in chimpanzees and bonobos.Human Nature, 4: 47–79.Google Scholar
  87. Yasui, Y. 1997. A “good-sperm” model can explain the evolution of costly multiple matings by females.Amer. Naturalist., 149: 573–584.CrossRefGoogle Scholar
  88. Zahavi, A. 1975. Mate selection: a selection for a handicap.J. Theor. Biol., 53: 205–214.PubMedCrossRefGoogle Scholar
  89. Zeh, J. A. 1997. Polyandry and enhanced reproductive success in the harlequin-beetle-riding pseudoscorpion.Behav. Ecol. Sociobiol., 40: 111–118.CrossRefGoogle Scholar
  90. Zumpe, D.;Michael, R. P. 1987. Relation between the dominance rank of female rhesus monkeys and their access to males.Amer. J. Primatol., 13: 155–169.CrossRefGoogle Scholar
  91. Zumpe, D.;Michael, R. P. 1989. Female dominance rank and behavior during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta).Amer. J. Primatol., 17: 287–304.CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre 1999

Authors and Affiliations

  • Robert R. Stallmann
    • 1
  • Jeffery W. Froehlich
    • 2
  1. 1.Department of AnthropologyUniversity of CaliforniaDavisU.S.A.
  2. 2.Department of AnthropologyUniversity of New MexicoAlbuquerqueU.S.A.

Personalised recommendations