Reproductive cessation in female mammals (original) (raw)

Nature volume 392, pages 807–811 (1998)Cite this article

Abstract

In female mammals, fertility declines abruptly at an advanced age. The human menopause is one example, but reproductive cessation has also been documented in non-human primates, rodents, whales, dogs, rabbits, elephants and domestic livestock1,2,3. The human menopause has been considered an evolutionary adaptation4,5,6,7 assuming that elderly women avoid the increasing complications of continued childbirth to better nurture their current children and grandchildren. But an abrupt reproductive decline might be only a non-adaptive by-product of life-history patterns. Because so many individuals die from starvation, disease and predation, detrimental genetic traits can persist (or even be favoured) as long as their deleterious effects are delayed until an advanced age is reached, and, for a given pattern of mortality, there should be an age by which selection would be too weak to prevent the onset of reproductive senescence4,5,8. We provide a systematic test of these alternatives using field data from two species in which grandmothers frequently engage in kin-directed behaviour. Both species show abrupt age-specific changes in reproductive performance that are characteristic of menopause. But elderly females do not suffer increased mortality costs of reproduction, nor do post-reproductive females enhance the fitness of grandchildren or older children. Instead, reproductive cessation appears to result from senescence.

This is a preview of subscription content, access via your institution

Access options

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Additional access options:

Similar content being viewed by others

References

  1. vom Saal, F. S., Finch, C. E. & Nelson, J. F. in The Physiology of Reproduction 2nd edn (eds Knobil, E. & Neill, J. D.) 1213–1314 (Raven, New York, 1994).
    Google Scholar
  2. Finch, C. E. Longevity, Senescence and the Genome (Univ. Chicago Press, 1990).
    Google Scholar
  3. Laws, R. M., Parker, I. S. C. & Johnstone, R. C. B. Elephants and their Habitats (Clarendon, Oxford, 1975).
    Google Scholar
  4. Williams, G. C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411 (1957).
    Article Google Scholar
  5. Hamilton, W. D. The moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45 (1966).
    Article CAS PubMed Google Scholar
  6. Hawkes, K., O'Connell, J. F. & Blurton-Jones, N. Hadza women's time allocation, offspring provisioning, and the evolution of long postmenopausal life spans. Curr. Anthropol. 38, 551–565 (1997).
    Article Google Scholar
  7. Rogers, A. R. Why menopause? Evol. Ecol. 7, 406–420 (1993).
    Article Google Scholar
  8. Charlesworth, B. Evolution in Age-structured Populations (Cambridge Univ. Press, Cambridge, 1980).
    MATH Google Scholar
  9. van Noord, P. A. H., Dubas, J. S., Dorland, M., Boersma, H. & te Velde, E. Age at natural menopause in a population-based screening cohort: the role of menarche, fecundity, and lifestyle factors. Fertil. Steril. 68, 95–102 (1997).
    Article CAS PubMed Google Scholar
  10. Gouzoules, S. & Gouzoules, H. in Primate Societies (eds Smuts, B. B. et al.) 299–305 (Univ. Chicago Press, 1987).
    Google Scholar
  11. Packer, C., Scheel, D. & Pusey, A. E. Why lions form groups: food is not enough. Am. Nat. 136, 1–19 (1990).
    Article Google Scholar
  12. McComb, K., Packer, C. & Pusey, A. E. Roaring and numerical assessment in contests between groups of female lions, Panthera leo. Anim. Behav. 47, 379–387.
  13. Heinsohn, R. & Packer, C. Complex cooperative strategies in group-territorial African lions. Science 269, 1260–1262 (1995).
    Article ADS CAS PubMed Google Scholar
  14. Pusey, A. E. & Packer, C. Non-offspring nursing in social carnivores: minimizing the costs. Behav. Ecol. 5, 362–374 (1994).
    Article Google Scholar
  15. Reznick, D. Costs of reproduction: an evaluation of the empirical evidence. Oikos 44, 257–267 (1985).
    Article Google Scholar
  16. Vaupel, J. W. & Iashin, A. I. Heterogeneity's ruses: some surprising effects of selection on population dynamics. Am. Stat. 39, 177–185 (1985).
    MathSciNet Google Scholar
  17. Medawar, P. B. The Uniqueness of the Individual (Dover, New York, 1952).
    Google Scholar
  18. Caswell, H. Matrix Population Models (Sinauer, Sunderland, MA, 1989).
    Google Scholar
  19. Wise, P. M., Krajnak, K. M. & Kashon, M. L. Menopause: The aging of multiple pacemakers. Science 273, 67–70 (1996).
    Article ADS CAS PubMed Google Scholar
  20. Stolwijk, A. M., Zielhuis, G. A., Sauer, M. V., Hamilton, C. J. C. M. & Paulson, R. J. The impact of the woman's age on the success of standard and donor in vitro fertilization. Fertil. Steril. 67, 702–710 (1997).
    Article CAS PubMed Google Scholar
  21. Hill, K. & Hurtado, A. M. The evolution of premature reproductive senescence and menopause in human females: an evaluation of the “Grandmother Hypothesis.” Hum. Nature 2, 313–350 (1991).
    Article CAS Google Scholar
  22. Packer, C. et al. Reproductive constraints on aggressive competition in female baboons. Nature 373, 60–63 (1995).
    Article ADS CAS PubMed Google Scholar
  23. Packer, C. & Pusey, A. E. The Lack clutch in a communal breeder: lion litter size is a mixed evolutionarily stable strategy. Am. Nat. 145, 833–841 (1995).
    Article Google Scholar
  24. Altmann, S. A. The pregnancy sign in savannah baboons. Lab. Anim. Digest 6, 7–10 (1970).
    Google Scholar
  25. Lee, E. T. Statistical Methods for Survival Data Analysis,2nd edn (J. Wiley, New York, 1992).
    Google Scholar

Download references

Acknowledgements

We thank E. C. Birney, M. Borgerhoff Mulder, E. L. Charnov, C. E. Finch, K. Hawkes, P. A. Hunt, M. McClintock, D. Promislow, A. R. Rogers, F. S. vom Saal and P. M. Wise for comments and discussion. Fieldwork on the baboons was supported by the Jane Goodall Institute and grants from the Physical Anthropology program at NSF; the lion study was supported by the LTREB program at NSF.

Author information

Authors and Affiliations

  1. Department of Ecology, Evolution and Behavior, University of Minnesota, 1987 Upper Buford Circle, St Paul, 55108, Minnesota, USA
    Craig Packer
  2. Department of Ecology and Evolutionary Biology, Brown University, Providence, 02912, Rhode Island, USA
    Marc Tatar
  3. Gombe Stream Research Centre, Box 185, Kigoma, Tanzania
    Anthony Collins

Authors

  1. Craig Packer
    You can also search for this author inPubMed Google Scholar
  2. Marc Tatar
    You can also search for this author inPubMed Google Scholar
  3. Anthony Collins
    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toCraig Packer.

Rights and permissions

About this article

Cite this article

Packer, C., Tatar, M. & Collins, A. Reproductive cessation in female mammals.Nature 392, 807–811 (1998). https://doi.org/10.1038/33910

Download citation

This article is cited by

Associated content