Skip to main content

Do Female Mandrills Prefer Brightly Colored Males?

Abstract

Although secondary sexual adornments are widespread in male primates, few studies have examined female choice for these characters. Mandrills (Mandrillus sphinx) present an extreme example of sexual dimorphism, with males exhibiting an array of striking adornments. The most dominant adult male in a group exhibits the brightest and most extensive red coloration, while the other males are less brightly colored. I examined whether female mandrills prefer brightly colored males using data on periovulatory sexual behavior during the 1996 mating season for all males 8 years old (n = 5) and all parous females (n = 9) in a semifree-ranging colony at CIRMF, Gabon. Brightness of male coloration is significantly positively correlated with time spent within 2 m of females, female responsibility for proximity, number of sexual presentations received, % approaches accepted by females, and % inspections with which females cooperated. Females also groomed only the brightest male. Behaviors indicating female preference are not correlated significantly with male dominance rank, and partial correlations confirm that the influence of male color on female behavior is stronger than that of male rank. With the influence of male dominance rank controlled, correlation coefficients between female behaviors and male mating success are high and positive. In further support of the hypothesis that females show mate choice for brightly colored males, independent of dominance rank, I report an unusual case wherein the alpha male fell in rank without loss of coloration. He experienced no significant change in female responsibility for proximity, sexual presentations received, or female reaction to approaches or inspections, though he was no longer observed to mate. Accordingly, female mandrills attend to differences in male secondary sexual characters and favor brightly colored males. As brightly colored males are also dominant this reinforces the influence of male-male competition on male reproductive success and may explain the very high reproductive skew in mandrill males and their extraordinary appearance.

This is a preview of subscription content, access via your institution.

References

  1. Abernethy, K. A., White, L. J. T., and Wickings, E. J. (2002). Hordes of mandrills Mandrillus sphinx: extreme group size and seasonal male presence. J. Zool. 258: 131–137.

    Article  Google Scholar 

  2. Alberts, S. C., and Altmann, J. (1995). Preparation and activation: Determinants of age at reproductive maturity in male baboons. Behav. Ecol. Sociobiol. 36: 397–406.

    Article  Google Scholar 

  3. Andersson, M. (1994). Sexual Selection, Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  4. Andersson, S., Pryke, S. R., Ornborg, J., Lawes, M. J., and Andersson, M. (2002). Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird. Am. Nat. 160: 683–691.

    Article  Google Scholar 

  5. Bercovitch, F. B. (1991). Mate selection, consortship formation and reproductive tactics in adult female savanna baboons. Primates 32: 437–452.

    Google Scholar 

  6. Bercovitch, F. B. (1997). Reproductive strategies of rhesus macaques. Primates.38: 247–263.

    Google Scholar 

  7. Boinski, S. (1987). Mating patterns in squirrel monkeys Saimiri oesterdii: Implications for seasonal sexual dimorphism. Behav. Ecol. Sociobiol. 21: 13–21.

    Article  Google Scholar 

  8. Brown, J. L. (1997). A theory of mate choice based on heterozygosity. Behav. Ecol. 8: 60–65.

    Google Scholar 

  9. Calkins, J. D., and Burley, N. T. (2003). Mate choice for multiple ornaments in the California quail, Callipepla californica. Anim. Behav. 65: 69–81.

    Article  Google Scholar 

  10. Charpentier, M., Peignot, P., Hossaert-McKey, M., Gimenez, O., Setchell, J. M., and Wickings, E. J. (2005). Constraints on control: Factors influencing reproductive success in male mandrills (Mandrillus sphinx). Behav. Ecol. 16: 614–623.

    Article  Google Scholar 

  11. Cooper, V. J., and Hosey, G. R. (2003). Sexual dichromatism and female preference in Eulemur fulvus subspecies. Int. J. Primatol. 24: 1177–1188.

    Article  Google Scholar 

  12. Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex, John Murray, London.

    Google Scholar 

  13. Dixson, A. F. (1998). Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings, Oxford University Press, Oxford.

    Google Scholar 

  14. Dixson, A. F., Bossi, T., and Wickings, E. J. (1993). Male dominance and genetically determined reproductive success in the mandrill Mandrillus sphinx. Primates 34: 525–532.

    Google Scholar 

  15. Fisher, R. A. (1930). The Genetical Theory of Natural Selection, Oxford University Press, Oxford.

    Google Scholar 

  16. Folstad, I., and Karter, A. J. (1992). Parasites, bright males and the immunocompetence handicap. Am. Nat. 139: 603–622.

    Article  Google Scholar 

  17. Fox, E. A. (2002). Female tactics to reduce sexual harassment in the Sumatran orangutan Pongo pygmaeus abelii. Behav. Ecol. Sociobiol. 52: 93–101.

    Google Scholar 

  18. Galdikas, B. (1985). Subadult male orangutan sociality and reproductive behavior at Tanjung Putting. Am. J. Primatol. 8: 87–99.

    Article  Google Scholar 

  19. Halliday, T. R. (1983). The study of mate choice. In Bateson, P. P. G. (ed.), Mate Choice, Cambridge University Press, Cambridge, pp. 3–32.

    Google Scholar 

  20. Hamilton, W. D., and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites. Science 218: 384–387.

    PubMed  Google Scholar 

  21. Heisler, L., Andersson, M. B., Arnold, S. J., Boake, C. R., Borgia, G., Hausfater, G., Kirkpatrick, M., Lande, R., Maynard Smith, J., O’Donald, P., Thornhill, R., and Weissing, F. J. (1987). The evolution of mating preferences and sexually selected traits. In Bradbury, J. W. and Andersson, M. B. (eds.), Sexual Selection: Testing the Alternatives, Wiley, New York, pp. 97–118.

    Google Scholar 

  22. Hendrickx, A. G., and Kraemer, D. C. (1969). Observations on the menstrual cycle, optimal mating time and pre-implantation embryos of the baboon, Papio anubis and Papio cynocephalus. J. Reprod. Fertil. 6: 119–128.

    Google Scholar 

  23. Hews, D. K., and Moore, M. C. (1997). Hormones and sex-specific traits: critical questions Beckage, N. E. (ed.), Parasites and Pathogens: Effects on Host Hormones and Behavior, Chapman and Hall, New York, pp. 277–292.

    Google Scholar 

  24. Hinde, R. A., and Atkinson, S. (1970). Assessing the roles of social partners in maintaining mutual proximity as exemplified by mother-infant relations in rhesus monkeys. Anim. Behav. 18: 169–176.

    Article  Google Scholar 

  25. Hrdy, S. B. (2000). The optimal number of fathers: Evolution, demography, and history in the shaping of female mate preferences LeCroy, D. and Moller, P. (eds.), Evolutionary Perspectives on Human Reproductive Behavior, New York Academy of Sciences, New York, pp. 75–96.

    Google Scholar 

  26. Hrdy, S. B., and Whitten, P. L. (1987). Patterning of sexual activity Smuts, B., Cheney, D., Seyfarth, R., Wrangham, R. and Struhsaker, T. (eds.), Primate Societies, University of Chicago Press, pp. 370–384.

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

    Google Scholar 

  28. Jawor, J. M., and Breitwisch, R. (2004). Multiple ornaments in male Northern cardinals, Cardinalis cardinalis, as indicators of condition. Ethology 110: 113–126.

    Article  Google Scholar 

  29. Keddy, A. C. (1986). Female mate choice in female vervet monkeys Cercopithecus aethiops. Am. J. Primatol. 10: 125–143.

    Article  Google Scholar 

  30. Luttbeg, B. (2003). Assessing the robustness and optimality of alternative decision rules with varying assumptions. Anim. Behav. 63: 805–814.

    Article  Google Scholar 

  31. Manson, J. H. (1992). Measuring female mate choice in Cayo Santiago rhesus macaques. Anim. Behav. 44: 405–416.

    Article  Google Scholar 

  32. Manson, J. H. (1995). Do female rhesus macaques choose novel males? Am. J. Primatol. 37: 285–296.

    Article  Google Scholar 

  33. Martin, R. D., and Bateson, P. P. G. (1994). Measuring Behavior: An Introductory Guide, 2nd ed, Cambridge University Press, Cambridge.

    Google Scholar 

  34. Mitani, J. C. (1985). Sexual selection and adult male orangutan long calls. Anim. Behav. 33: 272–283.

    Google Scholar 

  35. Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Anim. Behav. 58: 299–246.

    Article  Google Scholar 

  36. Owens, I. P. F., and Wilson, K. (1999). Immunocompetence: a neglected life history trait or conspicuous red herring? Nature 14: 170–172.

    Google Scholar 

  37. Paul, A. (2002). Sexual selection and mate choice. Int. J. Primatol. 23: 877–904.

    Article  Google Scholar 

  38. Penn, D. J., and Potts, W. K. (1999). The evolution of mating preferences and major histocompatibility complex genes. Am. Nat. 153: 145–164.

    Article  Google Scholar 

  39. Pereira, M. E., and Weiss, M. L. (1991). Female mate choice, male migration and the threat of infanticide in ringtailed lemurs. Behav. Ecol. Sociobiol. 18: 141–152.

    Google Scholar 

  40. Petrie, M., Halliday, T., and Sanders, C. (1991). Peahens prefer peacocks with elaborate trains. Anim. Behav. 41: 323–331.

    Google Scholar 

  41. Sauermann, U., NËurnberg, P., Bercovitch, F. B., Berard, J. D., Trefilov, A., Widdig, A., Kessler, M., Schmidtke, J., and Krawczak, M. (2001). Increased reproductive success of MHC class II heterozygous males among free-ranging rhesus macaques. Hum. Genet. 108: 249–254.

    Article  PubMed  Google Scholar 

  42. SchËurmann, C. L. (1982). Mating behavior of wild orangutans de Boer, L. (ed.), The Orang-Utan: Its Biology and Conservation, Junk Publishers, The Hague, pp. 271–286.

    Google Scholar 

  43. Setchell, J. M. (1999). Socio-sexual development in the male mandrill Mandrillus sphinx.

  44. Setchell, J. M. (2003). Behavioral development in male mandrills Mandrillus sphinx: Puberty to adulthood. Behavior 140: 1053–1089.

    Article  Google Scholar 

  45. Setchell, J. M., Charpentier, M., and Wickings, E. J. (2005). Mate-guarding and paternity in mandrills (Mandrillus sphinx): Factors influencing monopolisation of females by the alpha male. Anim. Behav. in press.

  46. Setchell, J. M., and Dixson, A. F. (2001a). Arrested development of secondary sexual adornments in subordinate adult male mandrills Mandrillus sphinx. Am. J. Phys. Anthropol. 115: 245–252.

    Article  Google Scholar 

  47. Setchell, J. M., and Dixson, A. F. (2001b). Changes in the secondary sexual adornments of male mandrills Mandrillus sphinx are associated with gain and loss of alpha status. Horm. Behav. 39: 177–184.

    Article  Google Scholar 

  48. Setchell, J. M., and Dixson, A. F. (2002). Developmental variables and dominance rank in male mandrills Mandrillus sphinx. Am. J. Primatol. 56: 9–25.

    Article  PubMed  Google Scholar 

  49. Setchell, J. M., and Kappeler, P. M. (2003). Selection in relation to sex in primates. Adv. Study Behav. 33: 87–173.

    Google Scholar 

  50. Shaikh, A. A., Celaya, C. L., Gomez, I., and Schaik, S. A. (1982). Temporal relationship of hormonal peaks to ovulation and sex skin deturgescence in the baboon. Primates 23: 444–452.

    Google Scholar 

  51. Siva-Jothy, M. T. (1995). “Immunocompetence”: conspicuous by its absence. Trends Ecol. Evol. 10: 205–206.

    Article  Google Scholar 

  52. Small, M. F. (1989). Female mate choice in non human primates. Yrbk. Phys. Anthropol. 32: 103–127.

    Article  Google Scholar 

  53. Smuts, B., and Smuts, R. W. (1993). Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv. Study Behav. 22: 1–63.

    Google Scholar 

  54. Snowdon, C. T. (2004). Sexual selection and communication Kappeler, P. K. and van Schaik, C. P. (eds.), Sexual Selection in Primates: New and Comparative Perspectives, Cambridge University Press, Cambridge, pp. 57–70.

    Google Scholar 

  55. Soltis, J., Mitsunaga, F., Shimizu, K., Nozaki, M., Yanagihara, Y., DomingoRoura, X., and 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 

  56. Soltis, J., Thomsen, R., and Takenaka, O. (2001). The interaction of male and female reproductive strategies and paternity in wild Japanese macaques, Macaca fuscata. Anim. Behav. 62: 485–494.

    Article  Google Scholar 

  57. Trivers, R. L. (1972). Parental investment and sexual selection Campbell, B. (ed.), Sexual Selection and the Descent of Man, Aldine, Chicago, pp. 136–179.

    Google Scholar 

  58. van Schaik, C. P. (2000). Infanticide by male primates: the sexual selection hypothesis revisited van Schaik, C. P. and Janson, C. H. (eds.), Infanticide by Males and its Implications, Cambridge University Press, Cambridge, pp. 27–60.

    Google Scholar 

  59. van Schaik, C. P., Pradhan, G. R., and van Noordwijk, M. A. (2004). Mating conflict in primates: Infanticide, sexual harassment and female sexuality Kappeler, P. M. and van Schaik, C. P. (eds.), Sexual Selection in Primates: New and Comparative Perspectives, Cambridge University Press, Cambridge, pp. 131–150.

    Google Scholar 

  60. van Schaik, C. P., and van Hooff, J. A. R. A. M. (1996). Towards an understanding of the orangutan’s social system McGrew, W. C., Marchant, L. F. and Nishida, T. (eds.), Great Ape Societies, University of Chicago Press, Chicago, pp. 3–15.

    Google Scholar 

  61. Verhulst, S., Dieleman, S. J., and Parmentier, H. K. (1999). A tradeoff between immunocompetence and sexual ornamentation in domestic fowl. Proc. Natl. Acad. Sci. USA. 96: 4478–4481.

    Article  PubMed  Google Scholar 

  62. Waitt, C., Little, A. C., Wolfensohn, S., Honess, P., Brown, A. P., Buchanan-Smith, H. M., and Perret, D. I. (2003). Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proc. R. Soc. Lond. Ser. B-Biol. Sci. (Suppl.). 270: S144–S146.

    Google Scholar 

  63. Welker, C., Hohmann, H., and Schafer–Witt, C. (1990). Signifiance of kin relations and individual preferences in the social behavior of Cebus apella. Folia Primatol. 54: 166–170.

    PubMed  Google Scholar 

  64. Wickings, E. J. (1993). Hypervariable single and multi-locus DNA polymorphisms for genetic typing of non-human primates. Primates 34: 323–331.

    Google Scholar 

  65. Wickings, E. J. (1995). Genetic self-management in a captive colony of mandrills Mandrillus sphinx as revealed by DNA minisatellite fingerprints. Electrophoresis 16: 1678–1683.

    Article  PubMed  Google Scholar 

  66. Wickings, E. J., Bossi, T., and Dixson, A. F. (1993). Reproductive success in the mandrill, Mandrillus sphinx: correlations of male dominance and mating success with paternity, as determined by DNA fingerprinting. J. Zool. 231: 563–574.

    Google Scholar 

  67. Wickings, E. J., and Dixson, A. F. (1992). Testicular function, secondary sexual development, and social status in male mandrills Mandrillus sphinx. Physiol. Behav. 52: 909–916.

    Article  PubMed  Google Scholar 

  68. Wildt, D. E., Doyle, U., Stone, S. C., and 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.

    Google Scholar 

  69. Zahavi, A. (1975). Mate selection-a selection for handicap. J. Theor. Biol. 53: 205–214.

    Article  PubMed  Google Scholar 

  70. Zeh, J. A., and Zeh, D. W. (1997). The evolution of polyandry. II. Post-copulatory defences against genetic incompatibility. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 264: 69–75.

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Joanna M. Setchell.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Setchell, J.M. Do Female Mandrills Prefer Brightly Colored Males?. Int J Primatol 26, 715–735 (2005). https://doi.org/10.1007/s10764-005-5305-7

Download citation

Keywords

  • sexual selection
  • female choice
  • proceptivity
  • receptivity
  • coloration