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8 - The evolution of post-reproductive life: adaptationist scenarios

Published online by Cambridge University Press:  16 May 2011

By
Lynnette Leidy Sievert
Edited by
C. G. Nicholas Mascie-Taylor  and
Lyliane Rosetta
Lynnette Leidy Sievert
Affiliation:
UMass Amherst, USA
C. G. Nicholas Mascie-Taylor
Affiliation:
University of Cambridge
Lyliane Rosetta
Affiliation:
Centre National de la Recherche Scientifique (CNRS), Paris
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Summary

Introduction

In adaptationist scenarios, traits are selected for if they are positively correlated with reproductive success (Fisher, 1930; Price, 1970). It seems counter-intuitive, then, that natural selection would select for a dampening, or complete cessation, of reproductive ability before the end of the somatic lifespan. If the production of offspring is a means by which favorable traits can be passed to future generations, then the continued production of offspring – even the costliest of offspring – would seem to be beneficial. Why was there a phylogenetic shift in female reproductive strategy away from continued egg production in fish, amphibians, and reptiles, to a finite number of eggs that slowly dwindles across the lifespan to the point, in some mammalian species, of follicular exhaustion and low levels of ovarian hormones prior to death? In other words, why is there a menopause?

This chapter reviews the evidence for two categories of adaptationist scenarios. In the first, menopause and post-reproductive life are the direct products of natural selection. In the second, menopause and post-reproductive life are the indirect by-products of natural selection for other traits. A similar differentiation between menopause as either adaptation or epiphenomenon has already been made (Peccei, 2001), but the argument presented here takes a slightly different tack by emphasizing the byproduct scenario as also adaptationist. In the byproduct scenarios presented here, mammalian patterns of early oogenesis (egg production) and lifelong atresia (ovarian follicle loss) are the reproductive strategies that underwent positive selection.

Type
Chapter
Information
Reproduction and Adaptation
Topics in Human Reproductive Ecology
 , pp. 149 - 170
Publisher: Cambridge University Press
Print publication year: 2011

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References

Adams, C. E. (1966). Ovarian control of early embryonic development within the uterus. In: Reproduction in the Female Mammal, ed. Lamming, G. E. and Amoroso, E. C., New York, NY: Plenum Press, pp. 532–548.Google Scholar
Alexander, R. D. (1974). The evolution of social behavior. Annual Review of Ecology and Systematics, 5, 325–383.CrossRefGoogle Scholar
Atsalis, S. & Margulis, S. W. (2006). Sexual and hormonal cycles in geriatric Gorilla gorilla gorilla. International Journal of Primatology, 27, 1663–1687.CrossRefGoogle Scholar
Baker, T. G. (1986). Gametogenesis. In: Comparative Primate Biology, Vol 3: Reproduction and Development, ed. Dukelow, W. R. and Erwin, J., New York, NY: Alan R. Liss, Inc, pp. 195–213.Google Scholar
Beyene, Y. (1986). Cultural significance and physiological manifestations of menopause: a biocultural analysis. Culture, Medicine and Psychiatry, 10, 47–71.CrossRefGoogle ScholarPubMed
Bribiescas, R. (1996). Testosterone levels among Ache hunter/gatherer men: a functional interpretation of population variation among adult males. Human Nature, 7, 163–188.CrossRefGoogle Scholar
Bribiescas, R. G. (2006). Men: Evolutionary and Life History. Harvard University Press.Google Scholar
Bromley, P. J., Ravier, C. & Witthames, P. R. (2000). The influence of feeding regime on sexual maturation, fecundity and atresia in first-time spawning turbot. Journal of Fish Biology, 56, 264–278.CrossRefGoogle Scholar
Byskov, A. G. (1979). Atresia. In: Ovarian Follicular Development and Function, ed. Rees, M. A. and Sadler, W. A., New York, NY: Raven, pp. 41–57.Google Scholar
Byskov, A. G. & Hoyer, P. E. (1988). Embryology of mammalian gonads. In: The Physiology of Reproduction, ed. Knobil, E. and Neill, J., New York, NY: Raven Press, pp. 265–302.Google Scholar
Cohen, A. A. (2004). Female post-reproductive lifespan: a general mammalian trait. Biological Reviews, 79, 733–750.CrossRefGoogle ScholarPubMed
Comfort, A. (1979). The Biology of Senescence, 3rd edn., New York, NY: Elsevier.Google Scholar
Crisp, T. M. (1992). Organization of the ovarian follicle and events in its biology: oogenesis, ovulation or atresia. Mutation Research, 296, 89–106.CrossRefGoogle ScholarPubMed
Croze, H., Hillman, A. K. K. & Lang, E. M. (1981). Elephants and their habitats: how do they tolerate each other? In: Dynamics of Large Mammal Populations, ed. Fowler, C. W.. New York, NY: John Wiley, pp. 297–316.Google Scholar
Dawkins, R. (1976). The Selfish Gene. New York, NY: Oxford University Press.Google Scholar
Bruin, J. P., Bovenhuis, H., Noord, P. A. H.et al. (2001). The role of genetic factors in age at natural menopause. Human Reproduction, 16, 2014–2018.CrossRefGoogle ScholarPubMed
DeLille Henderson, K., Bernstein, L., Henderson, B., Kolonel, L. & Pike, M. C. (2008). Predictors of the timing of natural menopause in the multiethnic cohort study. American Journal of Epidemiology, 167, 1287–1294.CrossRefGoogle Scholar
Deslypere, J. P. & Vermeulen, A. (1984). Leydig cell function in normal men: effect of age, lifestyle, residence, diet, and activity. Journal of Clinical and Endocrinology and Metabolism, 59, 955–962.CrossRefGoogle Scholar
Eaton, S. B & Eaton, S. B. (1999). Breast cancer in evolutionary context. In: Evolutionary Medicine, ed. Trevathan, W. R., Smith, E. O. and McKenna, J. J., New York, NY: Oxford University Press, pp. 429–442.Google Scholar
Ellison, P. T., Bribiescas, R. G., Bentley, G. R.et al. (2002). Population variation in age-related decline in male salivary testosterone. Human Reproduction, 17, 3251–3253.CrossRefGoogle ScholarPubMed
Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Oxford: Calarendon Press.CrossRefGoogle Scholar
Foote, A. D. (2008). Mortality rate acceleration and post-reproductive lifespan in matrilineal whale species. Biology Letters, 4, 189–191.CrossRefGoogle ScholarPubMed
Forbes, L. S. (1997). The evolutionary biology of spontaneous abortion in humans. Trends in Ecology and Evolution, 12, 446–50.CrossRefGoogle ScholarPubMed
Freeman, S. B., Yang, Q., Allran, K., Taft, L. F. & Sherman, S. L. (2000). Women with a reduced ovarian complement may have an increased risk for a child with Down syndrome. American Journal of Human Genetics, 66, 1680–1683.CrossRefGoogle ScholarPubMed
Gaulin, S. J. C. (1980). Sexual dimorphism in the human post-reproductive life-span: Possible causes. Journal of Human Evolution. 9, 227–232.CrossRefGoogle Scholar
Ghiselin, M. T. (1987). Evolutionary aspects of marine invertebrate reproduction. In: Reproduction of Marine Invertebrates, ed. Giese, A. C., Pearse, J. S. and Pearse, V. B., Palo Alto, CA: Blackwell Scientific, pp. 609–665.Google Scholar
Gosden, R. G. & Faddy, M. J. (1994). Ovarian aging, follicular depletion, and steroidogenesis. Experimental Gerontology, 29, 265–274.CrossRefGoogle ScholarPubMed
Gougeon, A., Ecochard, R. & Thalabard, J. C. (1994). Age-related changes of the population of human ovarian follicles: increase in the disappearance rate of nongrowing and early-growing follicles in aging women. Biology of Reproduction, 50, 653–663.CrossRefGoogle Scholar
Greenwald, G. S. & Terranova, P. F. (1988). Follicular selection and its control. In: The Physiology of Reproduction, ed. Knobil, E. and Neill, J., New York, NY: Raven Press, 387–445.Google Scholar
Guraya, S. S. (1985). Biology of Ovarian Follicles in Mammals. New York, NY: Springer–Verlag.CrossRefGoogle Scholar
Guraya, S. S. (1986). The Cell and Molecular Biology of Fish Oogenesis. Monographs in Developmental Biology, Vol 18. New York, NY: Karger.Google ScholarPubMed
Guraya, S. S. (1989). Ovarian Follicles in Reptiles and Birds. New York, NY: Springer–Verlag.CrossRefGoogle Scholar
Guraya, S. S. (1998). Cellular and Molecular Biology of Gonadal Development and Maturation in Mammals: Fundamentals and Biomedical Implications. New York, NY: Springer–Verlag.Google Scholar
Habibi, H. R. & Andreu-Vieyra, C. V. (2007). Hormonal regulation of follicular atresia in teleost fish. In: The Fish Oocyte: From Basic Studies to Biotechnological Applications, ed. Babin, P. J., Cerda, J. and Lubzens, E., Dordrecht: Springer, pp. 235–253.CrossRefGoogle Scholar
Hall, R. (2004). An energetics-based approach to understanding the menstrual cycle and menopause. Human Nature, 15, 83–99.CrossRefGoogle ScholarPubMed
Hamilton, W. D. (1966). The moulding of senescence by natural selection. Journal of Theoretical Biology, 12, 12–45.CrossRefGoogle ScholarPubMed
Hansen, K. R., Knowlton, N. S., Thyer, A. C.et al. (2008). A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Human Reproduction, 23, 699–708.CrossRefGoogle ScholarPubMed
Hardardottir, K., Kjesbu, O. S. & Marteinsdottir, G. (2003). Atresia in Icelandic cod (Gadus morhua L.) prior to and during spawning. Fisen og. Havet, 12, 51–55.Google Scholar
Hawkes, K. (2007). The evolutionary legacy of post-menopausal longevity & a grandmother hypothesis. Menopause, 14, 1074.Google Scholar
Hawkes, K., O'Connell, J. F. & Blurton Jones, N. G. (1997). Hadza women's time allocation, offspring provisioning and the evolution of post-menopausal lifespans. Current Anthropology, 38, 551–578.CrossRefGoogle Scholar
Hill, K. & 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.CrossRefGoogle Scholar
Hogarth, P. T. (1976). Viviparity, London: Edward Arnold.Google Scholar
Holman, D. J., Wood, J. W. & Campbell, K. L. (2000). Age-dependent decline of female fecundity is caused by early fetal loss. In: Female Reproductive Ageing, Studies in Profertility Series, ed. Velde, E. R., Broekmans, F. and Pearson, P., Camforth: Parthenon, pp. 123–136.Google Scholar
Hrdy, S. B. (1999). Mother Nature: a History of Mothers, Infants, and Natural Selection. New York, NY: Pantheon.Google Scholar
Hsueh, A. J. W., Billig, H. & Tsafriri, A. (1994). Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocrine Reviews, 15, 707–724.Google ScholarPubMed
Hunter, R. H. F. (2003). Physiology of the Graafian Follicle and Ovulation. New York, NY: Cambridge University Press.Google Scholar
Jamison, C. S., Cornell, L. L., Jamison, P. L. & Nakazato, H. (2002). Are all grandmothers equal? A review and a preliminary test of the “grandmother hypothesis” in Tokugawa Japan. American Journal of Physical Anthropology, 119, 67–76.CrossRefGoogle Scholar
Johnson, N. A. (2007). Darwinian Detectives: Revealing the Natural History of Genes and Genomes. New York, NY: Oxford University Press.CrossRefGoogle Scholar
Johnson, J., Canning, J., Kaneko, T., Pru, J. K. & Tilly, J. L. (2004). Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature, 428, 145–150.CrossRefGoogle ScholarPubMed
Jones, K. P., Walker, L. C., Anderson, D.et al. (2007). Depletion of ovarian follicles with age in chimpanzees: similarities to humans. Biology of Reproduction, 77, 247–251.CrossRefGoogle Scholar
Kaplan, H., Hill, K., Lancaster, J. & Hurtado, A. M. (2000). A theory of human life history evolution: diet, intelligence, and longevity. Evolutionary Anthropology, 9, 156–185.3.0.CO;2-7>CrossRefGoogle Scholar
Kelsey, J. L., Gammon, M. D. & John, E. M. (1993). Reproductive factors and breast cancer. Epidemiologic Reviews, 15, 36–47.CrossRefGoogle ScholarPubMed
Kline, J. & Levin, B. (1992). Trisomy and age at menopause: predicted associations given a link with rate of oocyte atresia. Paediatric and Perinatal Epidemiology, 6, 225–239.CrossRefGoogle Scholar
Kline, J., Kinney, A., Levin, B. & Warburton, D. (2000). Trisomic pregnancy and earlier age at menopause. American Journal of Human Genetics, 67, 395–404.CrossRefGoogle ScholarPubMed
Kohn, R. R. (1978). Principles of Mammalian Aging. Englewood Cliffs, NJ: Prentice–Hall.Google Scholar
Korenman, S. G., Morley, J. E., Morradian, A. D.et al. (1990). Secondary hypogonadism in older men: its relation to impotence. Journal of Clinical Endocrinology and Metabolism, 71, 963–969.CrossRefGoogle ScholarPubMed
Kuhle, B. X. (2007). An evolutionary perspective on the origin and ontogeny of menopause. Maturitas, 57, 329–337.CrossRefGoogle ScholarPubMed
Lahdenperä, M., Lummaa, V., Helle, S., Tremblay, M. & Russell, A. F. (2004). Fitness benefits of prolonged post-reproductive lifespan in women. Nature, 428, 178–181.CrossRefGoogle ScholarPubMed
Lancaster, J. B. & Lancaster, C. S. (1983). The parental investment: the hominid adaptation. In: How Humans Adapt: A Biocultural Odyssey, ed. Ortner, D. J., Washington, DC: Smithsonian Institution Press.Google Scholar
Langdon, J. H. (2005). The Human Strategy: An Evolutionary Perspective on Human Anatomy. New York, NY: Oxford University Press.Google Scholar
Leidy, L. E., Godfrey, L. R. & Sutherland, M. R. (1998). Is follicular atresia biphasic? Fertility and Sterility, 70, 851–859.CrossRefGoogle ScholarPubMed
Madrigal, L. & Meléndez-Obando, M. (2008). Grandmothers' longevity negatively affects daughters' fertility. American Journal of Physical Anthropology, 136, 223–229.CrossRefGoogle ScholarPubMed
Margulis, S. W., Atsalis, S., Bellem, A. & Wielebnowski, N. (2007). Assessment of reproductive behavior and hormonal cycles in geriatric western lowland gorillas. Zoo Biology, 26, 117–139.CrossRefGoogle ScholarPubMed
Martin, C. R. (1985). Endocrine Physiology. New York, NY: Oxford University Press.Google Scholar
Martin, R. (2008). Meiotic errors in human oogenesis and spermatogenesis. Reproductive BioMedicine Online, 16, 523–531.CrossRefGoogle ScholarPubMed
Marsh, H. & Kasuya, T. (1986). Evidence for reproductive senescence in female cetaceans. Report of the International Whaling Commission, 8, 57–74.Google Scholar
Merry, B. J. & Holehan, A. M. (1994). Aging of the male reproductive system. In: Physiological Basis of Aging and Geriatrics, ed. Timiras, P. S., 2nd edn, Ann Arbor, MI: CRC Press, pp. 171–178.Google Scholar
Mossman, H. W. & Duke, K. L. (1973). Comparative Morphology of the Mammalian Ovary. Madison, WI: The University of Wisconsin Press.Google Scholar
Murua, H., Kraus, G., Saborido-Rey, F.et al. (2003). Procedures to estimate fecundity of marine fish species in relation to their reproductive strategy. Journal of Northwest Atlantic Fishing Science, 33, 33–54.CrossRefGoogle Scholar
Murua, H. & Saborido-Rey, F. (2003). Female reproductive strategies of marine fish species of the North Atlantic. Journal of Northwest Atlantic Fishing Science, 33, 23–31.CrossRefGoogle Scholar
Nishida, T., Corp, N., Hamai, M.et al. (2003). Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. American Journal of Primatology, 59, 99–121.CrossRefGoogle ScholarPubMed
Novak, E. R. (1970). Ovulation after fifty. Obstetric Gynecology, 36, 903–910.Google ScholarPubMed
O'Connell, J. F., Hawkes, K. & Blurton Jones, N. G. (1999). Grandmothering and the evolution of Homo erectus. Journal of Human Evolution, 36, 461–485.CrossRefGoogle ScholarPubMed
Olesiuk, P. F., Bigg, M. A. & Ellis, G. M. (1990). Life history and population dynamics of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State. Report to the International Whaling Commission 12, 209–243.Google Scholar
O'Rourke, M. T. & Ellison, P. T. (1993). Menopause and ovarian senescence in human females. American Journal of Physical Anthropology, Suppl. 16, 154.Google Scholar
Packer, C., Tatar, M. & Collins, A. (1998). Reproductive cessation in female mammals. Nature, 392, 807–811.CrossRefGoogle ScholarPubMed
Parker, K. L. & Schimmer, B. P. (2006). Embryology and genetics of the mammalian gonads and ducts. In: Knobil and Neill's Physiology of Reproduction, ed. Neill, J. D., 3rd edn, Boston, MA: Elsevier, pp. 313–336.CrossRefGoogle Scholar
Pavard, S., Metcalf, C. J. E. & Heyer, E. (2008). Senescence of reproduction may explain adaptive menopause in humans: a test of the “mother” hypothesis. American Journal of Physical Anthropology, 136, 194–203.CrossRefGoogle ScholarPubMed
Pavelka, M. S. M. & Fedigan, L. M. (1999). Reproductive termination in female Japanese monkeys: a comparative life history perspective. American Journal of Physical Anthropology, 109, 455–464.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Peccei, J. S. (1995). A hypothesis for the origin and evolution of menopause. Maturitas, 21, 83–89.CrossRefGoogle ScholarPubMed
Peccei, J. S. (1999). First estimates of heritability in the age of menopause. Current Anthropology, 40, 553–558.CrossRefGoogle Scholar
Peccei, J. S. (2001). Menopause: adaptation or epiphenomenon? Evolutionary Anthropology, 10, 43–57.CrossRefGoogle Scholar
Peters, H. & McNatty, K. P. (1980). The Ovary: A Correlation of Structure and Function in Mammals. New York, NY: Granada.Google Scholar
Pollard, I. (1994). A Guide to Reproduction: Social Issues and Human Concerns. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Price, G. R. (1970). Selection and covariance. Nature, 227, 520–521.CrossRefGoogle ScholarPubMed
Rajkovic, A., Pangas, S. A. & Matzuk, M. M. (2006). Follicular development: mouse, sheep and human models. In: Knobil and Neill's Physiology of Reproduction, ed. Neill, J. D., 3rd edn, Boston, MA: Elsevier, pp. 383–423.CrossRefGoogle Scholar
Reynolds, R. F. & Obermeyer, C. M. (2005). Age at natural menopause in Spain and the United States: Results from the DAMES project. American Journal of Human Biology, 17, 331–340.CrossRefGoogle ScholarPubMed
Richardson, S. J, Senikas, V. & Nelson, J. F. (1987). Follicular depletion during the menopausal transition: evidence for accelerated loss and ultimate exhaustion. Journal of Clinical Endocrinology and Metabolism, 65, 1231–1237.CrossRefGoogle ScholarPubMed
Ricklefs, R. E. (2008). The evolution of senescence from a comparative perspective. Functional Ecology, 22, 379–392.CrossRefGoogle Scholar
Ricklefs, R. E., Scheuerlein, A. & Cohen, A. (2003). Age-related patterns of fertility in captive populations of birds and mammals. Experimental Gerontology, 38, 741–745.CrossRefGoogle ScholarPubMed
Rolaki, A., Drakakis, P., Millingos, S., Loutradis, D. & Makrigiannakis, A. (2005). Novel trends in follicular development, atresia and corpus luteum regression: a role for apoptosis. Reproductive BioMedicine Online, 11, 93–103.CrossRefGoogle ScholarPubMed
Rothchild, I. (2003). The yolkless egg and the evolution of eutherian viviparity. Biology of Reproduction, 68, 337–357.CrossRefGoogle ScholarPubMed
Ryan, R. J. (1981). Follicular atresia: some speculations of biochemical markers and mechanisms. Dynamics of Ovarian Function, ed. Schwartz, N. B. and Hunzicker-Dunn, M., New York, NY: Raven Press, pp. 1–11.Google Scholar
Sadleir, R. (1973). The Reproduction of Vertebrates. New York, NY: Academic Press.Google Scholar
Sear, R., Mace, R. & McGregor, I. A. (2000). Maternal grandmothers improve nutritional status and survival of children in rural Gambia. Proceedings of the Royal Society B, 267, 1641–1647.CrossRefGoogle ScholarPubMed
Sear, R., Steele, F., McGregor, A. A. & Mace, R. (2002). The effects of kin on child mortality in rural Gambia. Demography, 39, 43–63.CrossRefGoogle Scholar
Shanley, D. P., Sear, R., Mace, R. & Kirkwood, T. B. L. (2007). Testing evolutionary theories of menopause. Proceedings of the Royal Society B, 274, 2943–2949.CrossRefGoogle ScholarPubMed
Sievert, L. L. (2001). Aging and reproductive senescence. In: Reproductive Ecology and Human Evolution, ed. Ellison, P., Hawthorne, NY: Aldine de Gruyter, pp. 267–292.Google Scholar
Sievert, L. L. (2006). Menopause: A Biocultural Approach. Rutgers University Press.Google Scholar
Sievert, L. L. & Hautaniemi, S. I. (2003). Age at menopause in Puebla, Mexico. Human Biology, 75, 205–226.CrossRefGoogle ScholarPubMed
Snieder, H., MacGregor, A. J. & Spector, T. D. (1998). Genes control the cessation of a woman's reproductive life: a twin study of hysterectomy and age at menopause. Journal of Clinical Endocrinology and Metabolism, 83, 1875–1880.Google ScholarPubMed
Strassman, B. I. (1996). The evolution of endometrial cycles and menstruation. Quarterly Review of Biology, 71, 181–220.CrossRefGoogle Scholar
Tapanainen, J. S. & Vasikivuo, T. (2002). Apoptosis in the human ovary. Reproductive Medicine Online, 6, 24–35.Google Scholar
Thomas, F., Renaud, F., Benefice, E., Meeus, T. & Guegan, J-F. (2001). International variability of ages at menarche and menopause: patterns and main determinants. Human Biology, 73, 271–290.CrossRefGoogle ScholarPubMed
Thorsen, A., Marshall, C. T. & Kjesbu, O.S. (2006). Comparison of various potential fecundity models for north-east Arctic cod Gadus morhua, L. using oocyte diameter as a standardizing factor. Journal of Fish Biology, 69, 1709–1730.CrossRefGoogle Scholar
Treloar, S. A., Do, K.-A. & Martin, N. G. (1998). Genetic influences on the age at menopause. Lancet, 352, 1084–1085.CrossRefGoogle ScholarPubMed
Uchida, A. R., Bribiescas, R. G., Kanamori, M.et al. (2002). Salivary testosterone levels in healthy 90-year-old Japanese males: implications for endocrine senescence. Paper presented at International Society for Human Ethology, Montreal.
Vihko, R. & Apter, D. (1981). Endocrine maturation in the course of female puberty. In: Hormones and Breast Cancer, Banbury Report #8, ed. Pike, M. C., Siiteri, P. K. and Welsch, C. W., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, pp.57–69.Google ScholarPubMed
Voland, E. & Beise, J. (2002). Opposite effects of maternal and paternal grandmothers on infant survival in historical Krummhörn. Behavioral Ecology and Sociobiology, 52, 435–443.CrossRefGoogle Scholar
Voland, E. & Beise, J. (2005). “The husband's mother is the devil in house” Data on the impact of the mother-in-law on stillbirth mortality in historical Kummhorn (1750–1874) and some thoughts on the evolution of postgenerative female life. In: Grandmotherhood: The Evolutionary Significance of the Second Half of Female Life, ed. Voland, E., Chasiotis, A., Schiefenhovel, W., New Brunswick, New Jersey:Rutgers University Press, pp. 239–55.Google Scholar
Voland, E., Chasiotis, A. & Schiefenhovel, W. (2005). Grandmotherhood: The Evolutionary Significance of the Second Half of Female Life. New Brunswick, NJ:Rutgers University Press.Google Scholar
Wasser, S. K. & Place, N. J. (2001). Reproductive filtering and the social environment. In: Reproductive Ecology and Human Evolution, ed. Ellison, P. T., Hawthorne, NY: Aldine de Gruyter, pp.137–157.Google Scholar
,World Health Organization (WHO). (1996). Research on the Menopause in the 1990s. WHO Technical Report Series No. 866, Geneva: WHO.Google Scholar
Williams, G. C. (1957). Pleiotropy, natural selection, and the evolution of senescence. Evolution, 11, 398–411.CrossRefGoogle Scholar
Wood, J. W. (1994). Dynamics of Human Reproduction: Biology, Biometry, Demography. New York, NY: Aldine de Gruyter.Google Scholar
Wood, J. W., Holman, D. J. & O'Connor, K. A. (2001). Did menopause evolve by antagonistic pleiotropy? In: Homo unsere Herkunft und Zukunft. Proceedings 4. Kongress der Gesellschaft für Anthropologie (GfA). Göttingen: Cuvillier Verlag, pp. 483–490.Google Scholar

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