Abstract
Evolutionary biologists often argue that menopause evolved in the human female as the result of selection for a postreproductive phase of life, during which increased maternal investment in existing progeny could lead to enhanced survivorship of descendents. Adaptive theories relating menopause to enhanced maternal investment are known as the mother (first-generation) and grandmother (second-generation-offspring) hypotheses. Although menopause—universal midlife termination of reproduction—has not been documented in primates other than humans, some researchers have argued that postreproductive alloprimates also have a positive impact on the survivorship of first and second generation progeny. We tested the maternal investment hypotheses in Japanese macaques by comparing the survivorship of offspring, final infants, and great-offspring of females that terminated reproduction before death with females that continued to reproduce until death. SURVIVAL analyses revealed no significant difference in the survivorship of descendents of postreproductive and reproductive females, though final infants of postreproductive females were 13% more likely to survive than final infants of females that reproduced until death were. We also explored possible differences between these two groups of females, other than survivorship of progeny. We found no difference in dominance rank, matrilineal affiliation, body weight, infant sex ratio, age at first birth, fecundity rate or lifetime reproductive success. However, postreproductive females are significantly longer-lived than reproductive females and as a result experienced more years of reproduction and produced more infants in total. Apart from final infants, offspring survival is marginally lower in postreproductive females. Since offspring survival is not significantly enhanced in postreproductive females, the greater number of infants produced did not translate into greater lifetime reproductive success. Our findings fail to support the maternal investment hypotheses and instead suggest that reproductive termination in this population of Japanese macaques is most closely associated with enhanced longevity and its repercussions.
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REFERENCES
Alexander, R. D. (1974). The evolution of social behavior. Ann. Rev. Ecol. Syst. 5: 325–383.
Austad, S. N. (1997). Postreproductive survival. In Wachter, K. W., and Finch, C. E. (eds.) Between Zeus and the Salmon: the Biodemography of Longevity, National Academy Press, Washington, D.C., pp. 161–174.
Borries, C. (1988). Patterns of grandmaternal behavior in free-ranging Hanuman langurs (Presbytis entellus). Hum. Evol. 3: 239–260.
Brambilla, D. J., and McKinlay, S. M. (1989). A prospective study of factors affecting age at menopause. J. Clin. Epidemiol. 42: 1031–1039.
Brown, D. (1988). Components of lifetime reproductive success. In Clutton-Brock, C. (ed.) Reproductive Success. Studies of Individual Variation in Contrasting Breeding Systems. University of Chicago Press, Chicago, pp. 439–471.
Caro, T. M., Sellen, D. W., Parish, A., Frank, R., Brown, D. M., Voland, E., and Borgerhoff Mulder, M. (1995). Termination of reproduction in nonhuman and human female primates. Int. J. Primatol. 16: 205–220.
Clutton-Brock, C. (1988). Reproductive success. In Clutton-Brock, C. (ed.) Reproductive Success. Studies of IndividualVariation in Contrasting Breeding Systems. University of Chicago Press, Chicago, pp. 472–485.
Fedigan, L. M. (1991). History of the Arashiyama West macaques in Texas. In Fedigan, L. M. and Asquith, P. J. (eds.) The Monkeys of Arashiyama: Thirty-Five Years of Research in Japan and the West, State University of New York, Albany, pp. 54–73.
Fedigan, L. M., Fedigan, L. Gouzoules, S. Gouzoules, H., and Koyama, N. (1986). Lifetime reproductive success in female Japanese macaques. Folia primatol. 47: 143–157.
Fedigan, L. M., and Zohar, S. (1997). Sex differences in mortality of Japanese macaques: twentyone years of data from the Arashiyama West population. Am. J. Phys. Anth. 102: 161–175.
Gaulin, S. J. C. (1980). Sexual dimorphism in the human post-reproductive life-span: possible causes. J. Hum. Evol. 9: 227–232.
Hamilton, W. D. (1966). The moulding of senescence by natural selection. J. Theor. Biol. 12: 12–45.
Hawkes, K., O'Connell, J. F., and Blurton Jones, N. G. (1989). Hardworking Hadza grandmothers. In Standen, V. and Foley, R. (eds.), Comparative Socioecology of Mammals and Man, London: Blackwell, pp. 341–366.
Hawkes, K., O'Connell, J. F., and Blurton Jones, N. G. (1997). Hadza women's time allocation, offspring provisioning, and the evolution of long postmenopausal life spans. Curr. Anth. 38: 551–577.
Hawkes, K., O'Connell, J. F., Blurton Jones, N. G., Alvarez, H., and Charnov, E. L. (1998). Grandmothering, menopause, and the evolution of human life histories. Proc. Natl. Acad. Sci, USA 95: 1136–1139.
Hill, K., and Hurtado, A. M. (1991). The evolution of premature reproductive senescence and menopause in human females. An evaluation of the grandmother hypothesis. Human Nature 2: 313–350.
Hill, K., and Hurtado, A. M. (1996). Ache Life History. The Ecology and Demography of a Foraging People, Aldine de Gruyter, New York.
Hrdy, S. B. (1981). “Nepotists” and “altruists”: the behavior of old females among macaques and langur monkeys. In Amoss, P. T., and Harrell, S. (eds.) Other Ways of Growing Old: Anthropological Perspectives, Stanford University Press, Stanford, pp. 59–96.
Jaszmann, L., Van Lith, N. D., and Zaat, J. C. A. (1969). The age at menopause in the Netherlands: the statistical analysis of a survey. Int. J. Fertil. 14: 106–117.
Johnson, R. L., and Kapsalis, E. (1995). Ageing, infecundity and reproductive senescence in free-ranging female rhesus monkeys. J. Reprod. Fert. 105: 271–278.
Johnson, R. L., and Kapsalis, E. (1998). Menopause in free-ranging rhesus macaques: estimated incidence, relation to body condition, and adaptive significance. Int. J. Primatol. 19: 751–765.
Kaplan, H. (1997). The evolution of the human life course. In Wachter, K. W., and Finch, C. E. (eds.), Between Zeus and the Salmon: The Biodemography of Longevity, National Academy Press, Washington, D.C., pp. 175–211.
Lancaster, J. B., and King, B. J. (1985). An evolutionary perspective on menopause. In Borwn, J. K., and Kerns, V. (eds.), In Her Prime: A New View of Middle-Aged Women, Bergin and Garvey Press, South Hadley, Mass., pp. 13–20.
Lancaster, J. B., and Lancaster, C. S. (1983). Parental investment: the hominid adaptation. In: Ortner, D. (ed.), How Parents Adapt: A Biocultural Odyssey, Smithsonian Institution, Washington, D.C., pp. 33–65.
Nishida, T., Takasaki, H., and Takahata, Y. (1990). Demography and reproductive profiles. In Nishida, T. (ed.), The Chimpanzees of the Mahale Mountains: Sexual and Life History Strategies, University of Tokyo Press, Tokyo, pp. 63–97.
Norusis, M. J. (1993). SPSS for Windows. Advanced Statistics Release 6.0. Chicago: SPSS, Inc.
O'Connell, J.F., Hawkes, K., and Blurton Jones, N. G. (1999). Grandmothering and the evolution of Homo erectus. J. Hum. Evol. 36: 461–485.
Packer, C. Tatar, M., and Collins, A. (1998). Reproductive cessation in female mammals. Nature 392: 807–811.
Paul, A. Kuester, J., and Podzuweit, D. (1993). Reproductive senescence and terminal investment in female Barbary macaques (Macaca sylvanus) at Salem. Int. J. Primatol. 14: 105–124.
Pavelka, M. S. M. (1993). Monkeys of the Mesquite. The Social Life of the South Texas Snow Monkey, Kendall-Hunt Publ. Co., Dubuque, Iowa.
Pavelka, M. S. M., and Fedigan, L. M. (1991). Menopause: A comparative life history perspective. Yearbook of Phys. Anth. 34: 13–38.
Pavelka, M. S. M., and Fedigan, L. M. (1999). Reproductive termination in female Japanese monkeys: a comparative life history perspective. Am. J. Phys Anth. 109: 455–464.
Pavelka, M. S. M., Gillespie, M. W., and Griffin, L. (1991). Interacting effect of age and rank on the sociability of adult female Japanese monkeys. In Fedigan, L. M. and Asquith, P. J. (eds.), The Monkeys of Arashiyama. Thirty-Five Years of Research in Japan and the West, SUNY Press, Albany, N.Y., pp. 194–204.
Peccei, J. S. (1995a). A hypothesis for the origin and evolution of menopause. Maturitas 21: 83–89.
Peccei, J. S. (1995b). The origin and evolution of menopause: The altriciality-lifespan hypothesis. Ethol. and Sociobiol. 16: 425–450.
Rogers, A. (1993). Why menopause? Evol. Ecol. 7: 406–420.
Rogers, A. (1994). Evolution of time preference by natural selection. Am. Eco. Rev. 84: 460–481.
Sommer, V., Srivastava, A., and Borries, C. (1992). Cycles, sexuality and conception in free-ranging langurs (Presbytis entellus). Am. J. Primatol. 28: 1–27.
Takahata, Y. Koyama, N., and Suzuki, S. (1995). Do the old aged females experience a long post-reproductive life span? The cases of Japanese macaques and chimpanzees. Primates 36: 169–180.
Washburn, S. L. (1981). Longevity in primates. In McGaugh, J. L., and Keisler, S. B. (eds.), Aging. Biology and Behavior, Academic Press, New York, pp. 11–29.
Weiss, K. (1981). Evolutionary perspectives on human aging. In Amoss, P. T. and Harrell, S. (eds.), Other Ways of Growing Old: Anthropological Perspectives, Stanford University Press, Stanford, pp. 25–58.
Williams, G. C. (1957). Pleiotropy, natural selection and the evolution of senescence. Evol. 11: 398–411.
Wood, J. W. (1994). Dynamics of human reproduction: biology, biometry, and demography. New York: Aldine de Gruyter.
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Fedigan, L.M., Pavelka, M.S.M. Is There Adaptive Value to Reproductive Termination in Japanese Macaques? A Test of Maternal Investment Hypotheses. International Journal of Primatology 22, 109–125 (2001). https://doi.org/10.1023/A:1005618312088
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DOI: https://doi.org/10.1023/A:1005618312088