Skip to main content
Log in

Sexual selection and reproductive careers in mandrills (Mandrillus sphinx)

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

In sexually dimorphic, polygynous species, where males provide little parental care and competition between males for access to fertile females is high, sexual selection theory predicts sex differences in age-specific reproductive output and mortality profiles, and greater variance in lifetime reproductive success in males than in females. We examined age-specific reproductive output, mortality patterns and the extent and causes of variation in reproductive success for a semi-free-ranging colony of mandrills (Mandrillus sphinx, Cercopithecidae) in Franceville, Gabon, using long-term (20 year) demographic records and microsatellite parentage analysis. Although differences in the demography and feeding ecology of this closed, provisioned colony, in comparison with wild mandrills, limit interpretation of our results, sex differences in reproductive output and mortality showed the patterns predicted by sexual selection theory. Mortality was higher in males than in females after sexual maturity, and lifespan was significantly shorter in males (mean 14 year) than in females (>22 year). Age at first reproduction was significantly earlier in females (mean 4.2 year) than in males (11.6 year), and male reproductive output declined earlier. All females of breeding age produced offspring; while only 17 of 53 sexually mature males (32%) sired. Males sired a maximum of 41 offspring, versus 17 in females, and variance in male reproductive output was significantly greater than in females at all ages. The most important influence on variation in lifetime reproductive output in both sexes was joint variation between length of the breeding period and reproductive rate, due to lower reproductive rates in younger animals. Finally, social rank significantly influenced reproductive output in both sexes: high-ranking females began their reproductive careers earlier and had a higher subsequent reproductive rate than low-ranking females, while males that achieved top rank during their career sired far more offspring than males that did not.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abernethy KA, White LJT, Wickings EJ (2002) Hordes of mandrills (Mandrillus sphinx): Extreme group size and seasonal male presence. J Zool 258:131–137

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Alberts SC, Altmann J (2003) Matrix models for primate life history analysis. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. Chicago University Press, Chicago and London, pp 66–102

    Google Scholar 

  • Alberts SC, Altmann J, Wilson ML (1996) Mate guarding constrains foraging activity of male baboons. Anim Behav 51:1269–1277

    Article  Google Scholar 

  • Alberts SC, Watts H, Altmann J (2003) Queuing and queue jumping: Long-term patterns of dominance rank and mating success in male savannah baboons. Anim Behav 65:821–840

    Article  Google Scholar 

  • Altmann J, Alberts SC, Haines SA, Dubach J, Muruthi P, Coote T, Geffen E, Cheesman DJ, Mututua RS, Saiyalel SN, Wayne RK, Lacy RC, Bruford MW (1996) Behavior predicts genetic structure in a wild primate group. Proc Natl Acad Sci USA 93:5797–5801

    Article  CAS  PubMed  Google Scholar 

  • Altmann J, Hausfater G, Altmann SA (1988) Determinants of reproductive success in savannah baboons, Papio cynocephalus. In: Clutton-Brock TH (ed) Reproductive success: Studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 403–418

    Google Scholar 

  • Asquith PJ (1989) Provisioning and the study of free-ranging primates: History, effects, and prospects. Yearbook Phys Anthropol 32:129–158

    Google Scholar 

  • Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Google Scholar 

  • Bercovitch FB (1983) Time budgets and consortships in olive baboons (Papio anubis). Folia Primatolog 41:180–190

    Google Scholar 

  • Bercovitch FB (1993) Dominance rank and reproductive maturation in male rhesus macaques (Macaca mulatta). J Reprod Fertil 99:113–120

    CAS  PubMed  Google Scholar 

  • Bercovitch FB, Berard JD (1993) Life-history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behav Ecol Sociobiol 32:103–109

    Article  Google Scholar 

  • Bercovitch FB, Goy RW (1990) The socioendocrinology of reproductive development and reproductive success in macaques. In: Ziegler TE, Bercovitch FB (eds) Sociendocrinology of primate reproduction. Wiley-Liss, New York, pp 59–93

    Google Scholar 

  • Bercovitch FB, Nürnberg P (1996) Socioendocrine and morphological correlates of paternity in rhesus macaques (Macaca mulatta). J Reprod Fertil 107:59–68

    CAS  PubMed  Google Scholar 

  • Bercovitch FB, Widdig A, Trefilov A, Kessler MJ, Berard JD, Schmidtke J, Nürnberg P, Krawczak M (2003) A longitudinal study of age-specific reproductive output and body condition among male rhesus macaques, Macaca mulatta. Naturwissenschaften 271:819–826

    Google Scholar 

  • Bobek B, Perzanowski K, Weiner J (1990) Energy expenditure for reproduction in male red deer. J Mammal 71:230–232

    Google Scholar 

  • Brown D (1988) Components of lifetime reproductive success. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 439–453

    Google Scholar 

  • Cercueil A, Bellemain E, Manel S (2002) Parente: A software package for parentage analysis. J Hered 93:458–459

    Article  CAS  PubMed  Google Scholar 

  • Charpentier M, Peignot P, Hossaert-McKey M, Gimenez O, Setchell JM, Wickings EJ (2005) Constraints on control: Factors influencing reproductive success in male mandrills (Mandrillus sphinx). Behav Ecol (in press)

    Google Scholar 

  • Cheney DL, Seyfarth RM, Andelman SJ, Lee PC (1988) Reproductive success in vervet monkeys. In: Clutton-Brock TH (ed) Reproductive success: Studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 384–402

    Google Scholar 

  • Clinton WL, le Boeuf BJ (1993) Sexual selection’s effects on male life history and the pattern of male mortality. Ecology 74:1884–1892

    Google Scholar 

  • Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123:212–229

    Article  Google Scholar 

  • Clutton-Brock TH (1988) Reproductive Success. In: Clutton-Brock TH (ed) Reproductive success: Studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 472–485

    Google Scholar 

  • Clutton-Brock TH, Albon SD, Guinness FE (1988) Reproductive success in male and female red deer. In: Clutton-Brock TH (ed) Reproductive Success. University of Chicago Press, Chicago, pp 325–343

    Google Scholar 

  • Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: Behavior and ecology of two sexes. University of Chicago Press, Chicago

    Google Scholar 

  • Clutton-Brock TH, Vincent ACJ (1991) Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60

    Article  CAS  PubMed  Google Scholar 

  • Coltman DW, Smith JA, Bancroft DR, Pilkington J, MacColl ADC, Clutton-Brock TH, Pemberton JM (1999) Density-dependent variation in lifetime breeding success and natural and sexual selection in Soay rams. Am Nat 154:730–746

    Article  PubMed  Google Scholar 

  • Darwin C (1871) The descent of man and selection in relation to sex. John Murray, London

    Google Scholar 

  • Dittus WPJ (1977) The social regulation of population density and age–sex distributution in the toque monkey. Behaviour 63:281–322

    Google Scholar 

  • Drews C (1996) Contexts and patterns of injuries in free-ranging male baboons (Papio cynocephalus). Behaviour 133:443–474

    Google Scholar 

  • Drickamer LC (1974) Social rank, observability and sexual behaviour of rhesus monkeys. J Reprod Fertil 37:117–120

    CAS  PubMed  Google Scholar 

  • Dunbar RIM (1988) Primate social systems. Comstock Press, Ithaca, NY

    Google Scholar 

  • Eberhard WG (1996) Female control: Sexual selection by cryptic female choice. Princeton University Press, New Jersey

    Google Scholar 

  • Fedigan LM, Fedigan l, Gouzoules S, Gouzoules H, Koyama N (1986) Lifetime reproductive success in female Japanese macaques. Folia Primatolog 47:143–157

    CAS  Google Scholar 

  • Fedigan LM, Zohar S (1997) Sex differences in mortality of Japanese macaques: Twenty-one years of data from the Arashiyama West population. Am J Phys Anthropol 102:161–17

    Article  CAS  PubMed  Google Scholar 

  • Goodman D (1960) On the exact variance of products. J Am Stat Assoc 55:708–713

    Google Scholar 

  • Harcourt AH (1987) Dominance and fertility among female primates. J Zool 213:417–487

    Google Scholar 

  • Harrison MJS (1988) The mandrills in Gabon’s rain forest: Ecology, distribution and status. Oryx 22:218–228

    Google Scholar 

  • Hausfater G (1975) Dominance and reproduction in Baboons Papio cynocephalus. Karger, Basel

    Google Scholar 

  • Hill WCO (1970) Primates, comparative anatomy and taxonomy, Vol. 8. Cynopithecinae, Papio, Mandrillus, Theropithecus. Edinburgh University Press

    Google Scholar 

  • Hrdy SB (1987) Sex-biased parental investment among primates and other mammals: A critical review of the Trivers–Willard hypothesis. In: Gelles RJ, Lancaster JB (eds) Child abuse and neglect: Biosocial dimensions. Aldine, New York, pp 97–147

    Google Scholar 

  • Hrdy SB, Williams GC (1983) Behavioural biology and the double standard. In: Wasser SK (ed) Social behaviour of female vertebrates. Academic Press, New York, pp 3–17

    Google Scholar 

  • Isbell LA Young TP (2002) Ecological models of female social relationships in primates: Similarities, disparities, and some directions for future clairity. Behaviour 139:177–202

    Article  Google Scholar 

  • Kokko H (1997) Evolutionary stable strategies of age-dependent sexual advertisement. Behav Ecol Sociobiol 41:99–107

    Article  Google Scholar 

  • Komers PE, Pelabon C, Stenstrom D (1997) Age at first reproduction in male fallow deer: Age-specific versus dominance-specific behaviors. Behav Ecol 8:456–462

    Google Scholar 

  • Kruuk LEB, Clutton-Brock TH, Rose KE, Guinness FE (1999) Early determinants of lifetime reproductive success differ between the sexes in red deer. Proc R Soc Lond B—Biologic Sci 266:1655–1661

    Google Scholar 

  • Kuester J, Paul A, Arnemann J (1995) Age-related and individual differences of reproductive success in male and female barbary macaques (Macaca sylvanus). Primates 36:461–476

    Google Scholar 

  • le Boeuf BJ, Reiter J (1988) Lifetime reproductive success in northern elephant seals. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 344–362

    Google Scholar 

  • Lee PC, Bowman JE (1995) Influence of ecology and energetics on primate mothers and infants. In: Pryce CR, Martin RD, Skuse D (eds) Motherhood in human and nonhuman primates. Karger, Basel, pp 47–58

    Google Scholar 

  • Leigh S, Setchell JM, Buchanan LS (2005) Ontogenetic basis of canine dimorphism in Anthropoid primates. Am J Phys Anthropol (in press)

  • Loison A, Festa-Bianchet M, Gaillard J-M, Jorgenson JT, Jullien J-M (1999) Age-specific survival in five populations of ungulates: Evidence for senescence. Ecology 80:2539–2554

    Google Scholar 

  • Maher CR, Byers JA (1987) Age-related changes in reproductive effort of male bison. Behav Ecol 21:91–96

    Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  CAS  PubMed  Google Scholar 

  • McElligott AG (2000) Lifetime mating success, sexual selection and life history of fallow bucks (Dama dama). Behav Ecol 48:203–210

    Article  Google Scholar 

  • McElligott AG, Mattiangeli V, Mattiello S, Verga M, Reynolds CA, Hayden TJ (1998) Fighting tactics of fallow bucks (Dama dama, Cervidae): Reducing the risks of serious conflict. Ethology 104:789–803

    Google Scholar 

  • McNamara JM, Houston AI (1992) State-dependent life histories. Nature 380:215–221

    Article  Google Scholar 

  • Meikle DB, Tilford BL, Vessey SH (1984) Dominance rank, secondary sex ratio and reproduction of offspring in polygynous primates. Am Nat 124:173–188

    Article  Google Scholar 

  • Owen-Smith N (1993) Comparative mortality rates of male and female kudus: The costs of sexual dimorphism. Anim Ecol 62:428–440

    Google Scholar 

  • Packer C (1979) Male dominance and reproductive activity in Papio anubis. Anim Behav 27:37–45

    Article  PubMed  Google Scholar 

  • Packer C, Herbst L, Pusey AE, Bygott JD, Hanby JP, Cairns SJ, Borgerhoff Mulder M (1988) Reproductive success of lions. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 363–383

    Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biologic Rev Cam Philos Soc 45:525–567

    Google Scholar 

  • Partridge L, Harvey PH (1985) Costs of reproduction. Nature 316:20

    Article  Google Scholar 

  • Paul A, Kuester J (1996) Differential reproduction in male and female Barbary macaques. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaque societies. Cambridge University Press, Cambridge, pp 293–317

    Google Scholar 

  • Paul A, Kuester J, Arnemann J (1992) Maternal rank affects reproductive success of male Barbary macaques (Macaca sylvanus): Evidence from DNA fingerprinting. Behav Ecol Sociobiol 30:337–341

    Google Scholar 

  • Paul A, Kuester J, Podzuweit D (1993) Reproductive senescence and terminal investment in female Barbary macaques (Macaca sylvanus) at Salem. Int J Primatol 14:105–124

    Google Scholar 

  • Pavelka MSM, Fedigan LM (1999) Reproductive termination in female Japanese monkeys: A comparative life history perspective. Am J Phys Anthropol 109:455–464

    CAS  PubMed  Google Scholar 

  • Promislow DEL (1992) Costs of sexual selection in natural populations of mammals. Proc R Soc Lond B—Biologic Sci 247:203–210

    Google Scholar 

  • Ralls K, Brownwell RL, Ballou J (1980) Differential mortality by sex and age in mammals with specific reference to the sperm whale. Rep Int Whaling Commission, Special Issue 2:223–243

    Google Scholar 

  • Rhine RJ, Norton GW, Wasser SK (2000) Lifetime reproductive success, longevity, and reproductive life history of female yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania. Am J Primatol 51:229–241

    Article  CAS  PubMed  Google Scholar 

  • Ron T, Henzi SP, Motro U (1996) Do female chacma baboons compete for a safe spatial position in a southern woodland habitat? Behaviour 133:475–490

    Google Scholar 

  • Setchell JM (1999) Socio-sexual development in the male mandrill (Mandrillus sphinx). PhD Thesis. University of Cambridge, UK

    Google Scholar 

  • Setchell JM (2005) Do female mandrills (Mandrillus sphinx) prefer brightly coloured males? Int J Primatol (in press)

  • Setchell JM (2003) Behavioural development in male mandrills (Mandrillus sphinx): Puberty to adulthood. Behaviour 140:1053–1089

    Article  Google Scholar 

  • Setchell JM, Dixson AF (2001) Arrested development of secondary sexual adornments in subordinate adult male mandrills (Mandrillus sphinx). Am J Phys Anthropol 115:245–252

    Article  CAS  PubMed  Google Scholar 

  • Setchell JM, Dixson AF (2002) Developmental variables and dominance rank in male mandrills (Mandrillus sphinx). Am J Primatol 56:9–25

    Article  CAS  PubMed  Google Scholar 

  • Setchell JM, Kappeler PM (2003) Selection in relation to sex in primates. Adv Study Behav 33:87–173

    Article  Google Scholar 

  • Setchell JM, Lee PC, Wickings EJ, Dixson AF (2001) Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx). Am J Phys Anthropol 115:349–360

    Article  CAS  PubMed  Google Scholar 

  • Setchell JM, Lee PC, Wickings EJ, Dixson AF (2002) Reproductive parameters and maternal investment in mandrills (Mandrillus sphinx). Int J Primatol 23:51–68

    Article  Google Scholar 

  • Setchell JM, Wickings EJ (2004) Social and seasonal influences on the reproductive cycle in female mandrills (Mandrillus sphinx). Am J Phys Anthropol 1:73–84

    Article  Google Scholar 

  • Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41: 291–309

    Article  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179

    Google Scholar 

  • van Noordwijk MA, van Schaik CP (1987) Competition among female long-tailed macaques, Macaca fascicularis. Anim Behav 35:577–589

    Google Scholar 

  • van Noordwijk MA, van Schaik CP (1999) The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40:105–130

    Google Scholar 

  • van Schaik CP (1989) The ecology of social relationships among female primates. In: Standen V, Foley RA (eds) Comparative socioecology: The behavioural ecology of humans and other mammals. Blackwell Scientific Publishing, Oxford, pp 195–218

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wickings EJ, Bossi T, Dixson AF (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 

  • Wickings EJ, Dixson AF (1992a) Development from birth to sexual maturity in a semi-free-ranging colony of mandrills (Mandrillus sphinx) in Gabon. J Reprod Fertil 95:129–138

    CAS  PubMed  Google Scholar 

  • Wickings EJ, Dixson AF (1992b) Testicular function, secondary sexual development, and social status in male mandrills (Mandrillus sphinx). Physiol Behav 52:909–916

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Centre International de Recherches Médicales and past and present staff of the Primate Centre for making this study possible. Colony conditions comply with the current laws of the Republic of Gabon. The CIRMF is financed by the Gabonese government, Total Gabon and the Ministère Français des Affaires Etrangères. Mandrill paternity analyses were funded by a National Institutes of Health USA grant to Dr. Preston A. Marx, Tulane University, USA. JMS was supported during a part of the data collection by a research studentship from the Medical Research Council, UK and a CIRMF internship, and during writing of the manuscript by a Leverhulme Trust project grant award to Dr. Leslie A. Knapp, Department of Biological Anthropology, University of Cambridge. MC was supported by the Ministère Français des Affaires Etrangères while conducting paternity analyses. We are grateful to three anonymous reviewers for suggesting improvements to the manuscript

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joanna M. Setchell.

Additional information

Communicated by A. Widdig

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Setchell, J.M., Charpentier, M. & Wickings, E.J. Sexual selection and reproductive careers in mandrills (Mandrillus sphinx). Behav Ecol Sociobiol 58, 474–485 (2005). https://doi.org/10.1007/s00265-005-0946-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-005-0946-2

Keywords

Navigation