Advertisement

Sex differences in survival costs of reproduction in a promiscuous primate

  • Christy L. Hoffman
  • Angelina V. Ruiz-Lambides
  • Edgar Davila
  • Elizabeth Maldonado
  • Melissa S. Gerald
  • Dario Maestripieri
Original Paper

Abstract

In sexually promiscuous mammals, female reproductive effort is mainly expressed through gestation, lactation, and maternal care, whereas male reproductive effort is mainly manifested as mating effort. In this study, we investigated whether reproduction has significant survival costs for a seasonally breeding, sexually promiscuous species, the rhesus macaque, and whether these costs occur at different times of the year for females and males, namely in the birth and the mating season, respectively. The study was conducted with the rhesus macaque population on Cayo Santiago, Puerto Rico. Data on 7,402 births and 922 deaths over a 45-year period were analyzed. Births were concentrated between November and April, while conceptions occurred between May and October. As predicted, female mortality probability peaked in the birth season whereas male mortality probability peaked in the mating season. Furthermore, as the onset of the birth season gradually shifted over the years in relation to climatic changes, there was a concomitant shift in the seasonal peaks of male and female mortality. Taken together, our findings provide the first evidence of sex differences in the survival costs of reproduction in nonhuman primates and suggest that reproduction has significant fitness costs even in environments with abundant food and absence of predation.

Keywords

Survival costs of reproduction Sex differences Seasonal reproduction Climate change Rhesus macaques 

Notes

Acknowledgments

We thank all the staff of the Caribbean Primate Research Center and the researchers who, over the years, have contributed to the maintenance of the Cayo Santiago demographic and reproductive database. We also thank Brian J. Prendergast for earlier discussions of our results, Paul Rathouz for expert advice on statistical analyses, and Matt Kessler for helpful comments on the manuscript. This research was supported by National Institutes of Health (NIH) grant R21-AG029862 to D.M. and by intramural funds from the University of Chicago and the University of Puerto Rico, Medical Sciences Campus. This publication was made possible by grant number CM-5-P40RR003640 from the National Center for Research Resources (NCRR), a component of the NIH. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of NCRR or NIH.

References

  1. Ardito G (1976) Check-list of the data on the gestation length of primates. J Hum Evol 5:213–222CrossRefGoogle Scholar
  2. Bercovitch FB (1997) Reproductive strategies of rhesus macaques. Primates 38:247–263CrossRefGoogle Scholar
  3. Brockman DK, van Schaik CP (eds) (2005) Seasonality in primates: studies of living and extinct human and nonhuman primates. Cambridge University Press, CambridgeGoogle Scholar
  4. Carpenter CR (1942) Sexual behavior of free-ranging rhesus monkeys (Macaca mulatta). J Comp Psychol 33:113–162CrossRefGoogle Scholar
  5. Cheney DL, Seyfarth RM, Fischer J, Beehner J, Bergman T, Johnson SE, Kitchen DM, Palombit RA, Rendall D, Silk JB (2004) Factors affecting reproduction and mortality among baboons in the Okavango Delta, Botswana. Int J Primatol 25:401–428CrossRefGoogle Scholar
  6. Clinton WL, LeBoeuf BJ (1993) Sexual selection effects on male life history and the pattern of male mortality. Ecology 74:1884–1892CrossRefGoogle Scholar
  7. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. University of Chicago Press, ChicagoGoogle Scholar
  8. Cozzolino R, Cordischi C, Aureli F, Scucchi S (1992) Environmental temperature and reproductive seasonality in Japanese macaques. Primates 33:329–336CrossRefGoogle Scholar
  9. Herndon JG (1983) Seasonal breeding in rhesus monkeys: influence of the behavioral environment. Am J Primatol 5:197–204CrossRefGoogle Scholar
  10. Jewell PA (1997) Survival and behaviour of castrated Soay sheep (Ovis aries) in a feral island population on Hirta, St. Kilda, Scotland. J Zool 243:623–636CrossRefGoogle Scholar
  11. Kessler MJ, Berard JD, Rawlins RG, Bercovitch FB, Gerald MS, Laudenslager ML, Gonzalez JM (2006) Tetanus antibody titers and duration of immunity to clinical tetanus infections in free-ranging rhesus monkeys (Macaca mulatta). Am J Primatol 68:725–731PubMedCrossRefGoogle Scholar
  12. Koford CB (1965) Population dynamics of rhesus monkeys on Cayo Santiago. In: De Vore I (ed) Primate behavior: field studies of monkeys and apes. Holt, Rinehart & Winston, New York, pp 160–174Google Scholar
  13. McEwen BS, Biron CA, Brunson KW, Bulloch K, Chambers WH, Dhabhar FS, Goldfarb RH, Kitson RP, Miller AH, Spencer RL, Weiss JM (1997) The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions. Brain Res Rev 23:79–133PubMedCrossRefGoogle Scholar
  14. Michener GR (1998) Sexual differences in reproductive effort of Richardson’s ground squirrels. J Mammal 79:1–19CrossRefGoogle Scholar
  15. Michener GR, Locklear L (1990) Differential costs of reproductive effort for male and female Richardson’s ground squirrels. Ecology 71:855–868CrossRefGoogle Scholar
  16. Neuhaus P, Pelletier N (2001) Mortality in relation to season, age, sex, and reproduction in Columbian ground squirrels (Spermophilus columbianus). Can J Zool 79:465–470CrossRefGoogle Scholar
  17. Penn DJ, Smith KR (2007) Differential fitness costs of reproduction between the sexes. Proc Natl Acad Sci USA 104:553–558PubMedCrossRefGoogle Scholar
  18. Promislow DEL (1992) Costs of sexual selection in natural populations of mammals. Proc R Soc Lond B 247:203–210CrossRefGoogle Scholar
  19. Rawlins RG, Kessler MJ (1985) Climate and seasonal reproduction in the Cayo Santiago macaques. Am J Primatol 9:87–99CrossRefGoogle Scholar
  20. Rawlins RG, Kessler MJ (eds) (1986a) The Cayo Santiago macaques: history, behavior and biology. SUNY, AlbanyGoogle Scholar
  21. Rawlins RG, Kessler MJ (1986b) The history of the Cayo Santiago colony. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques: history, behavior and biology. SUNY, Albany, pp 13–45Google Scholar
  22. Rawlins RG, Kessler MJ (1986c) Demography of the free-ranging Cayo Santiago macaques (1976–1983). In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques: history, behavior and biology. SUNY, Albany, pp 47–72Google Scholar
  23. Riesen JW, Meyer RK, Wolf RC (1971) The effect of season on occurrence of ovulation in the rhesus monkey. Biol Reprod 5:111–114PubMedGoogle Scholar
  24. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239CrossRefGoogle Scholar
  25. Roff DA (2002) Life history evolution. Sinauer, SunderlandGoogle Scholar
  26. Sharma AK, Singh M, Kaumanns W, Krebs E, Singh M, Kumar MA, Kumara HN (2006) Birth patterns in wild and captive lion-tailed macaques (Macaca silenus). Int J Primatol 27:1429–1439CrossRefGoogle Scholar
  27. Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268CrossRefGoogle Scholar
  28. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  29. Vandenbergh JG (1969) Endocrine coordination in monkeys: male sexual responses to the female. Physiol Behav 4:261–264CrossRefGoogle Scholar
  30. Vandenbergh JG, Vessey S (1968) Seasonal breeding of free-ranging rhesus monkeys and related ecological factors. J Reprod Fert 15:71–79Google Scholar
  31. Van Horn RN (1980) Seasonal reproductive patterns in primates. Progr Reprod Biol 5:181–210Google Scholar
  32. Woodroffe R, MacDonald DW (1995) Costs of breeding status in the European badger, Meles meles. J Zool 235:237–245Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Christy L. Hoffman
    • 1
  • Angelina V. Ruiz-Lambides
    • 2
  • Edgar Davila
    • 3
  • Elizabeth Maldonado
    • 2
  • Melissa S. Gerald
    • 3
    • 4
  • Dario Maestripieri
    • 1
  1. 1.Department of Comparative Human DevelopmentThe University of ChicagoChicagoUSA
  2. 2.Caribbean Primate Research Center—Sabana SecaUniversity of Puerto Rico-Medical Sciences CampusSabana SecaUSA
  3. 3.Caribbean Primate Research Center—Cayo SantiagoUniversity of Puerto Rico-Medical Sciences CampusPunta SantiagoUSA
  4. 4.Laboratory for Primate Morphology and Genetics, Department of MedicineUniversity of Puerto Rico School of MedicineSan JuanUSA

Personalised recommendations