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The evolution of premature reproductive senescence and menopause in human females

An evaluation of the “grandmother hypothesis”

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Abstract

Reproductive senescence in human females takes place long before other body functions senesce. This fact presents an evolutionary dilemma since continued reproduction should generally be favored by natural selection. Two commonly proposed hypotheses to account for human menopause are (a) a recent increase in the human lifespan and (b) a switch to investment in close kin rather than direct reproduction. No support is found for the proposition that human lifespans have only recently increased. Data from Ache hunter-gatherers are used to test the kin selection hypothesis. Ache data do not support the proposition that females can gain greater fitness benefits in old age by helping kin rather than continuing to reproduce. Nevertheless, one crucial parameter in the model, when adjusted to the highest value within the measured 95% confidence interval, would lead to the evolution of reproductive senescence at about 53 years of age. Further investigation is necessary to determine whether the kin selection hypothesis of menopause can account for its current maintenance in most populations.

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References

  • Alexander, R. 1974 The Evolution of Social Behavior.Annual Review of Ecology and Systematics 5:325–383.

    Article  Google Scholar 

  • Bell, G., and V. Koufopanou 1986 The Cost of Reproduction. InOxford Surveys of Evolutionary Biology, R. Dawkins, ed. Pp. 83–131. Oxford: Oxford University Press.

    Google Scholar 

  • Biggers, J. D., C. A. Finn, and A. McLaren 1962 Long-Term Reproductive Performance of Female Mice, I: Variation of Litter Size with Parity.Journal of Reproductive Fertility 3:303–312.

    Article  Google Scholar 

  • Block, E. 1952 Quantitative Morphological Investigations of the Follicular System in Women. Variations at Different Ages.Acta Anatomica 14:108–123.

    Article  Google Scholar 

  • Blurton Jones, N., K. Hawkes, and J. O’Connell 1991 Demography of the Hadza. Unpublished manuscript. Los Angeles: Department of Anthropology, University of California.

    Google Scholar 

  • Borgerhoff Mulder, M. 1989 Menarche, Menopause, and Reproduction in the Kipsigis of Kenya.Journal of Biosocial Sciences 21:179–192.

    Google Scholar 

  • Buikstra, J. E., and L. W. Konigsberg 1985 Paleodemography: Critiques and Controversies.American Anthropologist 87:316–333.

    Article  Google Scholar 

  • Charlesworth, B. 1980Evolution in Age-Structured Populations. Cambridge: Cambridge University Press.

    Google Scholar 

  • Charnov, E. L. 1991 Evolution of Life History Variation among Female Mammals.Proceedings of the Academy of Sciences 88:1134–1137.

    Article  Google Scholar 

  • Cheney, D. L., and R. M. Seyfarth 1990How Monkeys See the World. Chicago: University of Chicago Press.

    Google Scholar 

  • Clutton-Brock, T. H. 1991The Evolution of Parental Care. Princeton, New Jersey: Princeton University Press.

    Google Scholar 

  • Comfort, A. 1956The Biology of Senescence. New York: Rinehart.

    Google Scholar 

  • Croze, H., A. K. Hillman, and E. M. Lang 1981 Elephants and Their Habitats: How Do They Tolerate Each Other? InDynamics of Large Mammal Populations, C. W. Fowler and T. D. Smith, eds. New York: John Wiley and Sons.

    Google Scholar 

  • Deslypere, J. P., and A. Vermeulen 1984 Leydig Cell Function in Normal Men: Effect of Age, Lifestyle, Residence, Diet, and Activity.Journal of Clinical Endocrinology and Metabolism 59:955–962.

    Google Scholar 

  • Dunbar, R. I. M. 1987 Demography and Reproduction. InPrimate Societies, B. Smuts, D. Cheney, R. Seyfarth, R. Wrangham, and T. Struhsaker, eds. Pp. 240–249. Chicago: University of Chicago Press.

    Google Scholar 

  • Early, J. D., and J. F. Peters 1990The Population Dynamics of the Mucajai Yanomama. New York: Academic Press.

    Google Scholar 

  • El-Faedy, M. A., and L. L. Bean 1987 Differential Paternity in Libya.Journal of Biosocial Science 19:395–403.

    Google Scholar 

  • Fairbanks, L. A., and M. T. McGuire 1986 Age, Reproductive Value, and Dominance-Related Behavior in Vervet Monkey Females: Cross-Generational Social Influences on Social Relationships and Reproduction.Animal Behavior 34:1718–1721.

    Article  Google Scholar 

  • Festing, M. F. W., and D. K. Blackmore 1971 Life Span of Specified Pathogen-free (MRC Category 4) Mice and Rats.Laboratory Animal Bulletin 5:179–192.

    Article  Google Scholar 

  • Fowler, C. W., and T. D. Smith, eds. 1981Dynamics of Large Mammal Populations. New York: John Wiley and Sons.

    Google Scholar 

  • Gaulin, S. J. 1980 Sexual Dimorphism in the Human Post-reproductive Lifespan: Possible Causes.Human Evolution 9:227–232.

    Article  Google Scholar 

  • George Washington University Medical Center 1975 Population Reports, Series J, No. 8: Family Planning Programs. Washington, D.C.: Department of Medical and Public Affairs, George Washington University Medical Center.

    Google Scholar 

  • Goldman, N., and M. Montgomery 1989 Fecundability and Husband’s Age.Social Biology 36:146–166.

    Google Scholar 

  • Goodall, J. 1986The Chimpanzees of Gombe. Cambridge, Massachusetts: Belknap Press.

    Google Scholar 

  • Gosden, R. G. 1987 Follicular Status at Menopause.Human Reproduction 2:617.

    Google Scholar 

  • Hamilton, W. D. 1964 The Genetical Evolution of Social Behavior.Journal of Theoretical Biology 7:1–52.

    Article  Google Scholar 

  • 1966 The Moulding of Senescence by Natural Selection.Journal of Theoretical Biology 12:12–45.

    Article  Google Scholar 

  • Harvey, P. H., and S. Nee 1991 How To Live Like a Mammal.Nature 350:23–24.

    Article  Google Scholar 

  • Hawkes, K., J. F. O’Connell, and N. G. Blurton Jones 1989 Hardworking Hadza Grandmothers. InComparative Socioecology: The Behavioural Ecology of Humans and Other Mammals, V. Standen and R. A. Foley, eds. Oxford: Blackwell Scientific Publications.

    Google Scholar 

  • Hill, K., and A. M. Hurtado 1989 Hunter-Gatherers of the New World.American Scientist 77(5):436–443.

    Google Scholar 

  • 1991 Demographic/Life History of Ache Foragers. Hawthorne, New York: Aldine Press, in preparation.

    Google Scholar 

  • Hurtado, A. M., and K. Hill 1990 Seasonality in a Foraging Society: Variation in Diet, Work Effort, Fertility, and the Sexual Division of Labor among the Hiwi of Venezuela.Journal of Anthropological Research 46:293–346.

    Google Scholar 

  • Howell, N. 1979Demography of the Dobe !Kung. New York: Academic Press.

    Google Scholar 

  • 1982 Village Composition Implied by a Paleodemographic Life Table: The Libben Site.American Journal of Physical Anthropology 59:263–269.

    Article  Google Scholar 

  • Irons, W. 1979 Cultural and Biological Success. InEvolutionary Biology and Human Social Behavior: An Anthropological Perspective, N. A. Chagnon and W. Irons, eds. North Scituate, Massachusetts: Duxbury Press.

    Google Scholar 

  • Jones, E. C. 1975 The Post-reproductive Phase in Mammals. InFrontiers of Hormone Research, Vol. 3, P. van Keep and C. Lauritzen, eds. Pp. 1–20. Basel: Karger.

    Google Scholar 

  • Kline, J., Z. Stein, and M. Susser 1989Conception to Birth: Epidemiology of Prenatal Development. New York: Oxford University Press.

    Google Scholar 

  • Lancaster, J. B., and B. J. King 1985 An Evolutionary Perspective on Menopause. InIn Her Prime: A New View of Middle Aged Women, J. K. Brown and J. K. Brown and V. Kerns, eds. Pp. 13–20. Massachusetts: Bergin and Garvey.

    Google Scholar 

  • Llewellyn-Jones, D. 1974Human Reproduction and Society. New York: Pitman.

    Google Scholar 

  • Marsh, H., and T. Kasuya 1986 Evidence for Reproductive Senescence in Female Cetaceans.Report of the International Whaling Commission, Special Issue 8:57–74.

    Google Scholar 

  • Melacon, T. 1982Marriage and Reproduction among the Yanomamo Indians of Venezuela. Ph.D. dissertation, Pennsylvania State University. Ann Arbor, Michigan: University Microfilms International.

    Google Scholar 

  • Mildvan, A. S., and B. L. Strehler 1960 A Critique of Theories of Mortality. InThe Biology of Aging, B. L. Strehler, ed. American Institute of Biological Sciences.

  • Millar, J. S., and R. M. Zammuto 1983 Life Histories of Mammals: An Analysis of Life Tables.Ecology 64:631–635.

    Article  Google Scholar 

  • Mizrooh, S. A. 1981 Analysis of Some Biological Parameters in the Antarctic Fin Whale.Report of the International Whaling Commission 31:425–434.

    Google Scholar 

  • Nishida, T., H. Takasaki, and Y. Takahata 1990 Demography and Reproductive Profiles. InThe Chimpanzees of Mahale Mountains, T. Nishida, ed. Tokyo: University of Tokyo Press.

    Google Scholar 

  • Promislow, D. E. L., and P. H. Harvey 1990 Living Fast and Dying Young: A Comparative Analysis of Life-History Variation among Mammals.Journal of Zoology 220:417–437.

    Google Scholar 

  • Ravenholt, R. T., and J. Chao 1974 World Fertility Trends. Population Reports, Series J, No. 2. Washington, D.C.: Department of Medical and Public Affairs, George Washington University Medical Center.

    Google Scholar 

  • Richardson, S. J., V. Senikas, and J. F. Nelson 1987 Follicular Depletion during the Menopausal Transition: Evidence for Accelerated Loss and Ultimate Exhaustion.Journal of Clinical Endocrinology and Metabolism 65:1231–1237.

    Article  Google Scholar 

  • SAS Institute Inc. 1986SUGI Supplemental Library Users Guide, Version 5 Edition. Cary, North Carolina: SAS Institute Inc.

    Google Scholar 

  • Sacher, G. A. 1975 Maturation and Longevity in Relation to Cranial Capacity in Hominid Evolution. InPrimate Functional Morphology and Evolution, R. H. Tuttle, ed. Pp. 417–441. The Hague: Mouton.

    Google Scholar 

  • Sade, D. S., K. Cushing, P. Cushing, J. Dunaif, A. Figueroa, J. R. Kaplan, C. Laver, D. Rhodes, and J. Schneider 1976 Population Dynamics in Relation to Social Structure on Cayo Santiago.Yearbook of Physical Anthropology 20:253–262.

    Google Scholar 

  • Smith, B. H. 1991 Dental Development and the Evolution of Life History in Hominidae.American Journal of Physical Anthropology, in press.

  • Smith, T., and T. Polacheck 1981 Reexamination of the Life Table for Northern Fur Seals with Implications about Population Regulatory Mechanisms. InDynamics of Large Mammal Populations, C. W. Fowler and T. D. Smith, eds. New York: John Wiley and Sons.

    Google Scholar 

  • Smuts, G. L. 1977 Reproduction and Population Characteristics of Elephants in the Kruger National Park.Journal of the African Wildlife Management Association 5(1):1–10.

    Google Scholar 

  • Snowdon, D. A., et al. 1989 Is Early Menopause a Biological Marker of Health and Aging?American Journal of Public Health 79:709–714.

    Article  Google Scholar 

  • Tracer, D. P. 1991 Fertility-related Changes in Maternal Body Composition among the Av of Papua New Guinea.American Journal of Physical Anthropology, in press.

  • Trivers, R. 1972 Parental Investment and Sexual Selection. InSexual Selection and the Descent of Man, B. Campbell, ed. Pp. 136–179. Chicago: Aldine.

    Google Scholar 

  • Turke, P. 1988 Helpers at the Nest: Childcare Networks on Ifaluk. InHuman Reproductive Behavior: A Darwinian Perspective, L. Betzig, M. Borgerhoff Mulder, and P. Turke, eds. Cambridge: Cambridge University Press.

    Google Scholar 

  • Utian, W. H. 1980Menopause in Modern Perspective. London: Prentice Hall.

    Google Scholar 

  • van Wagenen, G. 1972 Vital Statistics from a Breeding Colony.Journal of Medical Primatology 1:3–28.

    Google Scholar 

  • van Wagenen, G., and M. E. Simpson 1973Postnatal Development of the Ovary in Homo sapiensand Macaca mulata. New Haven: Yale University Press.

    Google Scholar 

  • vom Saal, F. S., and C. E. Finch 1988 Reproductive Senescence: Phenomena and Mechanisms in Mammals and Selected Vertebrates. InThe Physiology of Reproduction, E. Knobil, J. D. Neill, L. L. Ewing, G. S. Greenwald, C. L. Markert, and D. W. Pfaff, eds. Pp. 2351–2413. New York: Raven Press.

    Google Scholar 

  • Wallinga, J. H., and H. Baker 1978 Effects of Long Term Selection for Litter Size in Mice on Lifetime Reproduction.Journal of Animal Science 46:1563–1571.

    Google Scholar 

  • Washburn, S. L. 1981 Longevity in Primates. InAging, Biology and Behavior, J. March and J. McGaugh, eds. New York: Academic Press.

    Google Scholar 

  • Weiss, K. M. 1981 Evolutionary Perspectives on Human Aging. InOther Ways of Growing Old, P. Amoss and S. Harrell, eds. Stanford, California: Stanford University Press.

    Google Scholar 

  • Williams, G. C. 1957 Pleiotrophy, Natural Selection, and the Evolution of Senescence.Evolution 11:398–411.

    Article  Google Scholar 

  • Wilson, M. 1957Rituals of Kinship among the Nyakyusa. Oxford: Oxford University Press.

    Google Scholar 

  • Wood, J. W. 1990 Fertility in Anthropological Populations.Annual Review of Anthropology 19:211–242.

    Google Scholar 

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Authors and Affiliations

  1. Department of Anthropology, University of Michigan, 1054 LSA, 48109-1382, Ann Arbor, MI

    Kim Hill & A. Magdalena Hurtado

  2. Instituto Venezolano de Investigaciones Cientificas, Venezuela

    Kim Hill & A. Magdalena Hurtado

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  1. Kim Hill
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  2. A. Magdalena Hurtado
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Discussions with Peter Ellison, Kristen Hawkes, and Alan Rogers were especially valuable throughout. This research was supported by NSF grant BNS8613186 and grants from the Rackham Graduate School and the L. S. B. Leakey Foundation.

Kim Hill and A. Magdalena Hurtado collaborate in research on the evolutionary ecology of numan reproductive strategies, sexual division of labor, life history, and resource acquisition strategies. They have worked among Ache of Paraguay and Hiwi of Venezuela, as well as Machiguenga and Yora natives of Peru.

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Hill, K., Hurtado, A.M. The evolution of premature reproductive senescence and menopause in human females. Human Nature 2, 313–350 (1991). https://doi.org/10.1007/BF02692196

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