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.
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References
Ardito G (1976) Check-list of the data on the gestation length of primates. J Hum Evol 5:213–222
Bercovitch FB (1997) Reproductive strategies of rhesus macaques. Primates 38:247–263
Brockman DK, van Schaik CP (eds) (2005) Seasonality in primates: studies of living and extinct human and nonhuman primates. Cambridge University Press, Cambridge
Carpenter CR (1942) Sexual behavior of free-ranging rhesus monkeys (Macaca mulatta). J Comp Psychol 33:113–162
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 25:401–428
Clinton WL, LeBoeuf BJ (1993) Sexual selection effects on male life history and the pattern of male mortality. Ecology 74:1884–1892
Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. University of Chicago Press, Chicago
Cozzolino R, Cordischi C, Aureli F, Scucchi S (1992) Environmental temperature and reproductive seasonality in Japanese macaques. Primates 33:329–336
Herndon JG (1983) Seasonal breeding in rhesus monkeys: influence of the behavioral environment. Am J Primatol 5:197–204
Jewell PA (1997) Survival and behaviour of castrated Soay sheep (Ovis aries) in a feral island population on Hirta, St. Kilda, Scotland. J Zool 243:623–636
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 68:725–731
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 160–174
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 23:79–133
Michener GR (1998) Sexual differences in reproductive effort of Richardson’s ground squirrels. J Mammal 79:1–19
Michener GR, Locklear L (1990) Differential costs of reproductive effort for male and female Richardson’s ground squirrels. Ecology 71:855–868
Neuhaus P, Pelletier N (2001) Mortality in relation to season, age, sex, and reproduction in Columbian ground squirrels (Spermophilus columbianus). Can J Zool 79:465–470
Penn DJ, Smith KR (2007) Differential fitness costs of reproduction between the sexes. Proc Natl Acad Sci USA 104:553–558
Promislow DEL (1992) Costs of sexual selection in natural populations of mammals. Proc R Soc Lond B 247:203–210
Rawlins RG, Kessler MJ (1985) Climate and seasonal reproduction in the Cayo Santiago macaques. Am J Primatol 9:87–99
Rawlins RG, Kessler MJ (eds) (1986a) The Cayo Santiago macaques: history, behavior and biology. SUNY, Albany
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 13–45
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 47–72
Riesen JW, Meyer RK, Wolf RC (1971) The effect of season on occurrence of ovulation in the rhesus monkey. Biol Reprod 5:111–114
Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239
Roff DA (2002) Life history evolution. Sinauer, Sunderland
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 27:1429–1439
Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Vandenbergh JG (1969) Endocrine coordination in monkeys: male sexual responses to the female. Physiol Behav 4:261–264
Vandenbergh JG, Vessey S (1968) Seasonal breeding of free-ranging rhesus monkeys and related ecological factors. J Reprod Fert 15:71–79
Van Horn RN (1980) Seasonal reproductive patterns in primates. Progr Reprod Biol 5:181–210
Woodroffe R, MacDonald DW (1995) Costs of breeding status in the European badger, Meles meles. J Zool 235:237–245
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.
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Hoffman, C.L., Ruiz-Lambides, A.V., Davila, E. et al. Sex differences in survival costs of reproduction in a promiscuous primate. Behav Ecol Sociobiol 62, 1711–1718 (2008). https://doi.org/10.1007/s00265-008-0599-z
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DOI: https://doi.org/10.1007/s00265-008-0599-z