Human Nature

, Volume 2, Issue 4, pp 313–350 | Cite as

The evolution of premature reproductive senescence and menopause in human females

An evaluation of the “grandmother hypothesis”
  • Kim Hill
  • A. Magdalena Hurtado


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.

Key words

Menopause Senescence Kin selection Hunter-gatherers 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alexander, R. 1974 The Evolution of Social Behavior.Annual Review of Ecology and Systematics 5:325–383.CrossRefGoogle Scholar
  2. 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
  3. 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.CrossRefGoogle Scholar
  4. Block, E. 1952 Quantitative Morphological Investigations of the Follicular System in Women. Variations at Different Ages.Acta Anatomica 14:108–123.CrossRefGoogle Scholar
  5. 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 Unpublished manuscript.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
  6. Borgerhoff Mulder, M. 1989 Menarche, Menopause, and Reproduction in the Kipsigis of Kenya.Journal of Biosocial Sciences 21:179–192.Google Scholar
  7. Buikstra, J. E., and L. W. Konigsberg 1985 Paleodemography: Critiques and Controversies.American Anthropologist 87:316–333.CrossRefGoogle Scholar
  8. Charlesworth, B. 1980Evolution in Age-Structured Populations. Cambridge: Cambridge University Press.Google Scholar
  9. Charnov, E. L. 1991 Evolution of Life History Variation among Female Mammals.Proceedings of the Academy of Sciences 88:1134–1137.CrossRefGoogle Scholar
  10. Cheney, D. L., and R. M. Seyfarth 1990How Monkeys See the World. Chicago: University of Chicago Press.Google Scholar
  11. Clutton-Brock, T. H. 1991The Evolution of Parental Care. Princeton, New Jersey: Princeton University Press.Google Scholar
  12. Comfort, A. 1956The Biology of Senescence. New York: Rinehart.Google Scholar
  13. 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
  14. 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
  15. 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
  16. Early, J. D., and J. F. Peters 1990The Population Dynamics of the Mucajai Yanomama. New York: Academic Press.Google Scholar
  17. El-Faedy, M. A., and L. L. Bean 1987 Differential Paternity in Libya.Journal of Biosocial Science 19:395–403.Google Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. Fowler, C. W., and T. D. Smith, eds. 1981Dynamics of Large Mammal Populations. New York: John Wiley and Sons.Google Scholar
  21. Gaulin, S. J. 1980 Sexual Dimorphism in the Human Post-reproductive Lifespan: Possible Causes.Human Evolution 9:227–232.CrossRefGoogle Scholar
  22. 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
  23. Goldman, N., and M. Montgomery 1989 Fecundability and Husband’s Age.Social Biology 36:146–166.Google Scholar
  24. Goodall, J. 1986The Chimpanzees of Gombe. Cambridge, Massachusetts: Belknap Press.Google Scholar
  25. Gosden, R. G. 1987 Follicular Status at Menopause.Human Reproduction 2:617.Google Scholar
  26. Hamilton, W. D. 1964 The Genetical Evolution of Social Behavior.Journal of Theoretical Biology 7:1–52.CrossRefGoogle Scholar
  27. 1966 The Moulding of Senescence by Natural Selection.Journal of Theoretical Biology 12:12–45.CrossRefGoogle Scholar
  28. Harvey, P. H., and S. Nee 1991 How To Live Like a Mammal.Nature 350:23–24.CrossRefGoogle Scholar
  29. 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
  30. Hill, K., and A. M. Hurtado 1989 Hunter-Gatherers of the New World.American Scientist 77(5):436–443.Google Scholar
  31. 1991 Demographic/Life History of Ache Foragers. Hawthorne, New York: Aldine Press, in preparation.Google Scholar
  32. 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
  33. Howell, N. 1979Demography of the Dobe !Kung. New York: Academic Press.Google Scholar
  34. 1982 Village Composition Implied by a Paleodemographic Life Table: The Libben Site.American Journal of Physical Anthropology 59:263–269.CrossRefGoogle Scholar
  35. 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
  36. 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
  37. Kline, J., Z. Stein, and M. Susser 1989Conception to Birth: Epidemiology of Prenatal Development. New York: Oxford University Press.Google Scholar
  38. 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
  39. Llewellyn-Jones, D. 1974Human Reproduction and Society. New York: Pitman.Google Scholar
  40. 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
  41. 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
  42. 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.Google Scholar
  43. Millar, J. S., and R. M. Zammuto 1983 Life Histories of Mammals: An Analysis of Life Tables.Ecology 64:631–635.CrossRefGoogle Scholar
  44. 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
  45. 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
  46. 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
  47. 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
  48. 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.CrossRefGoogle Scholar
  49. SAS Institute Inc. 1986SUGI Supplemental Library Users Guide, Version 5 Edition. Cary, North Carolina: SAS Institute Inc.Google Scholar
  50. 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
  51. 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
  52. Smith, B. H. 1991 Dental Development and the Evolution of Life History in Hominidae.American Journal of Physical Anthropology, in press.Google Scholar
  53. 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
  54. 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
  55. Snowdon, D. A., et al. 1989 Is Early Menopause a Biological Marker of Health and Aging?American Journal of Public Health 79:709–714.CrossRefGoogle Scholar
  56. 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.Google Scholar
  57. 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
  58. 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
  59. Utian, W. H. 1980Menopause in Modern Perspective. London: Prentice Hall.Google Scholar
  60. van Wagenen, G. 1972 Vital Statistics from a Breeding Colony.Journal of Medical Primatology 1:3–28.Google Scholar
  61. van Wagenen, G., and M. E. Simpson 1973Postnatal Development of the Ovary in Homo sapiensand Macaca mulata. New Haven: Yale University Press.Google Scholar
  62. 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
  63. 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
  64. Washburn, S. L. 1981 Longevity in Primates. InAging, Biology and Behavior, J. March and J. McGaugh, eds. New York: Academic Press.Google Scholar
  65. 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
  66. Williams, G. C. 1957 Pleiotrophy, Natural Selection, and the Evolution of Senescence.Evolution 11:398–411.CrossRefGoogle Scholar
  67. Wilson, M. 1957Rituals of Kinship among the Nyakyusa. Oxford: Oxford University Press.Google Scholar
  68. Wood, J. W. 1990 Fertility in Anthropological Populations.Annual Review of Anthropology 19:211–242.Google Scholar

Copyright information

© Walter de Gruyter, Inc. 1991

Authors and Affiliations

  • Kim Hill
    • 1
    • 2
  • A. Magdalena Hurtado
    • 1
    • 2
  1. 1.Department of AnthropologyUniversity of MichiganAnn Arbor
  2. 2.Instituto Venezolano de Investigaciones CientificasVenezuela

Personalised recommendations