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.
Similar content being viewed by others
References
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.
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.
Andersson, M. (1994). Sexual Selection, Princeton University Press, Princeton, New Jersey.
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.
Bercovitch, F. B. (1991). Mate selection, consortship formation and reproductive tactics in adult female savanna baboons. Primates 32: 437–452.
Bercovitch, F. B. (1997). Reproductive strategies of rhesus macaques. Primates.38: 247–263.
Boinski, S. (1987). Mating patterns in squirrel monkeys Saimiri oesterdii: Implications for seasonal sexual dimorphism. Behav. Ecol. Sociobiol. 21: 13–21.
Brown, J. L. (1997). A theory of mate choice based on heterozygosity. Behav. Ecol. 8: 60–65.
Calkins, J. D., and Burley, N. T. (2003). Mate choice for multiple ornaments in the California quail, Callipepla californica. Anim. Behav. 65: 69–81.
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.
Cooper, V. J., and Hosey, G. R. (2003). Sexual dichromatism and female preference in Eulemur fulvus subspecies. Int. J. Primatol. 24: 1177–1188.
Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex, John Murray, London.
Dixson, A. F. (1998). Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings, Oxford University Press, Oxford.
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.
Fisher, R. A. (1930). The Genetical Theory of Natural Selection, Oxford University Press, Oxford.
Folstad, I., and Karter, A. J. (1992). Parasites, bright males and the immunocompetence handicap. Am. Nat. 139: 603–622.
Fox, E. A. (2002). Female tactics to reduce sexual harassment in the Sumatran orangutan Pongo pygmaeus abelii. Behav. Ecol. Sociobiol. 52: 93–101.
Galdikas, B. (1985). Subadult male orangutan sociality and reproductive behavior at Tanjung Putting. Am. J. Primatol. 8: 87–99.
Halliday, T. R. (1983). The study of mate choice. In Bateson, P. P. G. (ed.), Mate Choice, Cambridge University Press, Cambridge, pp. 3–32.
Hamilton, W. D., and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites. Science 218: 384–387.
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.
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.
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.
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.
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.
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.
Janson, C. (1984). Female choice and the mating system of the brown capuchin monkey, Cebus apella (Primates, Cebidae). Z. Tierpsychol. 65: 177–200.
Jawor, J. M., and Breitwisch, R. (2004). Multiple ornaments in male Northern cardinals, Cardinalis cardinalis, as indicators of condition. Ethology 110: 113–126.
Keddy, A. C. (1986). Female mate choice in female vervet monkeys Cercopithecus aethiops. Am. J. Primatol. 10: 125–143.
Luttbeg, B. (2003). Assessing the robustness and optimality of alternative decision rules with varying assumptions. Anim. Behav. 63: 805–814.
Manson, J. H. (1992). Measuring female mate choice in Cayo Santiago rhesus macaques. Anim. Behav. 44: 405–416.
Manson, J. H. (1995). Do female rhesus macaques choose novel males? Am. J. Primatol. 37: 285–296.
Martin, R. D., and Bateson, P. P. G. (1994). Measuring Behavior: An Introductory Guide, 2nd ed, Cambridge University Press, Cambridge.
Mitani, J. C. (1985). Sexual selection and adult male orangutan long calls. Anim. Behav. 33: 272–283.
Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Anim. Behav. 58: 299–246.
Owens, I. P. F., and Wilson, K. (1999). Immunocompetence: a neglected life history trait or conspicuous red herring? Nature 14: 170–172.
Paul, A. (2002). Sexual selection and mate choice. Int. J. Primatol. 23: 877–904.
Penn, D. J., and Potts, W. K. (1999). The evolution of mating preferences and major histocompatibility complex genes. Am. Nat. 153: 145–164.
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.
Petrie, M., Halliday, T., and Sanders, C. (1991). Peahens prefer peacocks with elaborate trains. Anim. Behav. 41: 323–331.
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.
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.
Setchell, J. M. (1999). Socio-sexual development in the male mandrill Mandrillus sphinx.
Setchell, J. M. (2003). Behavioral development in male mandrills Mandrillus sphinx: Puberty to adulthood. Behavior 140: 1053–1089.
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.
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.
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.
Setchell, J. M., and Dixson, A. F. (2002). Developmental variables and dominance rank in male mandrills Mandrillus sphinx. Am. J. Primatol. 56: 9–25.
Setchell, J. M., and Kappeler, P. M. (2003). Selection in relation to sex in primates. Adv. Study Behav. 33: 87–173.
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.
Siva-Jothy, M. T. (1995). “Immunocompetence”: conspicuous by its absence. Trends Ecol. Evol. 10: 205–206.
Small, M. F. (1989). Female mate choice in non human primates. Yrbk. Phys. Anthropol. 32: 103–127.
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.
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.
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.
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.
Trivers, R. L. (1972). Parental investment and sexual selection Campbell, B. (ed.), Sexual Selection and the Descent of Man, Aldine, Chicago, pp. 136–179.
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.
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.
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.
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.
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.
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.
Wickings, E. J. (1993). Hypervariable single and multi-locus DNA polymorphisms for genetic typing of non-human primates. Primates 34: 323–331.
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.
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.
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.
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.
Zahavi, A. (1975). Mate selection-a selection for handicap. J. Theor. Biol. 53: 205–214.
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.
Author information
Authors and Affiliations
Corresponding author
Rights 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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10764-005-5305-7