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Vol. 56, No. 1, 2010
Issue release date: January 2010
Section title: Viewpoint
Free Access
Gerontology 2010;56:73–79
(DOI:10.1159/000236045)

The Grandmother Effect: Implications for Studies on Aging and Cognition

Herndon J.G.
Yerkes National Primate Research Center, Emory University, Atlanta, Ga., USA
email Corresponding Author

Abstract

Background: Women experience more years of vigorous life after ovulation has ceased than do females of other primate species. Is this an epiphenomenon of the greater life expectancy humans have enjoyed in the past century or so, or is long post-menopausal survival the result of an evolutionary selection process? Recent research implies the latter: Long post-menopausal survival came about through natural selection. One prominent line of thought explaining this selection process is the grandmother hypothesis. Objective: To evaluate the implications of the hypothesis for non-human primate studies of aging and cognition. Method: The author presents a synopsis of the hypothesis, evaluates the uniqueness of the ‘grandmother effect’ to humans, and discusses its implications for non-human primate models of cognitive aging. Results: The hypothesis contends that, in past epochs, women who remained vigorous beyond their fertile years may have enhanced their reproductive success by providing care for their grandchildren. This care would have enabled their daughters to resume reproduction sooner, endowing them with greater lifetime fertility. Genes of grandmothers possessing such old-age vigor would be more likely to persist in subsequent generations. Is midlife menopause a uniquely human phenomenon, or does the chimpanzee, our closest primate relative, also display this trait? If so, we might expect a grandmother effect in this species as well. However, female chimpanzees continue to cycle until near the end of their maximum life span of about 60 years. Conclusion: Long survival beyond fertility and a long life expectancy are distinctive human adaptations. The robustness of ancestral human grandmothers necessarily included resistance to cognitive decline through preservation of functions present in many primates but also development of processes of social cognition unique to our species. Cognitive traits such as language and social cognitive functions may function in our species in particular as mechanisms to compensate for age-related decline. This has significant implications for research in which non-human primates are considered as models of human cognitive aging; it also means that some processes can be studied only in humans.

© 2009 S. Karger AG, Basel


  

Key Words

  • Grandmother hypothesis
  • Evolution
  • Aging and cognition
  • Non-human primates

References

  1. O’Connell J, Hawkes K, Blurton Jones NG: Grandmothering and the evolution of Homo erectus. J Hum Evol 1999;36:461–485.
  2. Charnov EL: Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology. Oxford, Oxford University Press, 1993.
  3. Kirkwood TBL, Rose MR: Evolution of senescence: late survival sacrificed for reproduction. Philos Trans Biol Sci 1991;332:15–24.
  4. Williams GC: Pleiotropy, natural selection, and the evolution of senescence. Evolution 1957;11:398–411.

    External Resources

  5. Hawkes K: Grandmothers and the evolution of human longevity. Am J Hum Biol 2003;15:380–400.
  6. Hawkes K: Life history and human evolution: a chronicle of ideas and findings; in Hawkes K, Paine RR (eds): The Evolution of Human Life History. Santa Fe, School of American Research Press, 2006, pp 45–94.
  7. Hawkes K: Slow life histories and human evolution; in Hawkes K, Paine RR (eds): The Evolution of Human Life History. Santa Fe, School of American Research Press, 2006, pp 95–126.
  8. Hawkes K, O’Connell JF, Blurton Jones NG: Human life histories: primate tradeoffs, grandmothering socioecology, and the fossil record; in Kappeler P, Pereira M (eds): Primate Life Histories and Socioecology. Chicago, University of Chicago Press, 2003, pp 204–227.
  9. Hawkes K, O’Connell JF, Blurton Jones NG: Hadza women’s time allocation, offspring provisioning, and the evolution of long postmenopausal life spans. Curr Anthropol 1997;38:551–577.
  10. Sear R, Mace R, McGregor IA: Maternal grandmothers improve nutritional status and survival of children in rural Gambia. Proc Biol Sci 2000;267:1641–1647.
  11. Jamison CS, Cornell LL, Jamison PL, Nakazato H: Are all grandmothers equal? A review and a preliminary test of the ‘grandmother hypothesis’ in Tokugawa, Japan. Am J Phys Anthropol 2002;119:67–76.
  12. Voland E, Beise J: Opposite effects of maternal and paternal grandmothers on infant survival in historical Krummhörn. Behav Ecol Sociobiol 2002;52:435–443.
  13. Sear R, Mace R: Who keeps children alive? A review of the effects of kin on child survival. Evol Hum Behav 2008;29:1–18.

    External Resources

  14. Lahdenperä M, Lummaa V, Helle S, Tremblay M, Russell AF: Fitness benefits of prolonged post-reproductive lifespan in women. Nature 2004;428:178–181.
  15. Walker ML, Herndon JG: Menopause in nonhuman primates? Biol Reprod 2008;79:398–406.
  16. Tigges J, Gordon TP, McClure HM, Hall EC, Peters A: Survival rate and life span of rhesus monkeys at the Yerkes Regional Primate Research Center. Am J Primatol 1988;15:263–273.
  17. Rosen RD: Lie of the Jungle: The Truth about Cheeta the Chimpanzee. Washington Post, Washington, DC, December 14, 2008.
  18. Herndon JG, Tigges J, Anderson DC, Klumpp SA, McClure HM: Brain weight throughout the life span of the chimpanzee. J Comp Neurol 1999;409:567–572.
  19. Bellino FL, Wise PM: Nonhuman primate models of menopause workshop. Biol Reprod 2003;68:10–18.
  20. Graham CE: Reproductive function in aged female chimpanzees. Am J Phys Anthropol 1979;50:291–300.
  21. Gould KG, Flint M, Graham CE: Chimpanzee reproductive senescence: a possible model for the evolution of menopause. Maturitas 1981;3:157–166.
  22. Videan EN, Fritz J, Heward CB, Murphy J: The effects of aging on hormone and reproductive cycles in female chimpanzees (Pan troglodytes). Comp Med 2006;56:291–299.
  23. Emery Thompson M, Jones JH, Pusey AE, Brewer-Marsden S, Goodall J, Marsden D, Matsuzawa T, Nishida T, Reynolds V, Sugiyama Y, Wrangham RW: Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause. Curr Biol 2007;17:2150–2156.
  24. Burger HG: The endocrinology of the menopause. J Steroid Biochem Mol Biol 1999;69:31–35.
  25. Deschner T, Heistermann M, Hodges K, Boesch C: Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Horm Behav 2004;46:204–215.
  26. Graham CE, Collins DC, Robinson H, Preedy JR: Urinary levels of estrogens and pregnanediol and plasma levels of progesterone during the menstrual cycle of the chimpanzee; relationship to the sexual swelling. Endocrinology 1972;91:13–24.
  27. Dahl J, Nadler RD, Collins DC: Monitoring the ovarian cycles of Pan troglodytes and P. paniscus: a comparative approach. Am J Primatol 1991;24:195–209.
  28. Nadler RD, Graham CE, Gosselin R, Collins DC: Serum levels of gonadotropins and gonadal steroids, including testosterone, during the menstrual cycle of the chimpanzee (Pan troglodytes). Am J Primatol 1985;9:273–284.
  29. McArthur JW, Beitens IZ, Gorman A, Collins DC, Preedy JRK, Graham CE: The interrelationships between sex skin swelling and the urinary excretion of LH, estrone, and pregnanediol by the cycling female chimpanzee. Am J Primatol 1981;1:265–270.

    External Resources

  30. Emery Thompson M: Reproductive endocrinology of wild female chimpanzees (Pan troglodytes schweinfurthii): methodological considerations and the role of hormones in sex and conception. Am J Primatol 2005;67:137–158.
  31. Lacreuse A, Chennareddi L, Gould KG, Hawkes K, Wijayawardana SR, Chen J, Easley KA, Herndon JG: Menstrual cycles continue into advanced old age in the common chimpanzee (Pan troglodytes). Biol Reprod 2008;79:407–412.
  32. Puschmann W, Federer E: Ein neuer Fertilitätsnachweis bei einer hoch betagten Schimpansin und Anmerkungen zum Höchstalter von Pan troglodytes. Zool Gart 2008;77:182–185.

    External Resources

  33. Vaupel JW, Carey JR, Christensen K, Johnson TE, Yashin AI, Holm NV, Iachine IA, Kannisto V, Khazaeli AA, Liedo P, Longo VD, Zeng Y, Manton KG, Curtsinger JW: Biodemographic trajectories of longevity. Science 1998;280:855–860.
  34. Peccei JS: Menopause: adaptation or epiphenomenon? Evol Anthrop 2001;10:43–57.

    External Resources

  35. Finch CE, Sapolsky RM: The evolution of Alzheimer disease, the reproductive schedule, and apoeE isoforms. Neurobiol Aging 1999;20:407–428.
  36. Allen JS, Bruss J, Damasio H: The aging brain: the cognitive reserve hypothesis and hominid evolution. Am J Hum Biol 2005;17:673–689.
  37. Stern Y: What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 2002;8:448–460.
  38. Dunbar R: The social brain hypothesis. Evol Anthrop 1998;6:179–190.

    External Resources

  39. Carstensen LL, Lockenhoff CE: Aging, emotion, and evolution: The bigger picture. Ann NY Acad Sci 2003;1000:152–179.
  40. Herndon JG, Moss MB, Rosene DL, Killiany RJ: Patterns of cognitive decline in aged rhesus monkeys. Behav Brain Res 1997;87:25–34.
  41. Moss MB, Moore TL, Schettler SP, Killiany RJ, Rosene DL: Successful versus unsuccessful aging in the rhesus monkey; in Riddle DR (ed): Brain Aging: Models, Methods, and Mechanisms. Boca Raton, CRC Press, 2007, pp 21–38.
  42. Herndon JG, Tigges J, Klumpp SA, Anderson DC: Brain weight does not decrease with age in adult rhesus monkeys. Neurobiol Aging 1998;19:267–272.
  43. Hartmann P, Ramseier A, Gudat F, Mihatsch MJ, Polasek W: Das Normgewicht des Gehirns beim Erwachsenen in Abhängigkeit von Alter, Geschlecht, Körpergrösse und Gewicht. Pathologe 1994;15:165–170.
  44. Rapp PR, Amaral DG: Evidence for task-dependent memory dysfunction in the aged monkey. J Neurosci 1989;9:3568–3576.
  45. Riopelle AJ, Rogers CM: Age changes in chimpanzees; in Schrier AM, Stolnitz F (eds): Behavior of Nonhuman Primates: Modern Research Trends. New York, Academic Press, 1965, pp 449–462.
  46. Judge DS, Carey JR: Postreproductive life predicted by primate patterns. J Gerontol A Biol Sci Med Sci 2000;55:B201–B209.
  47. Jones KP, Walker LC, Anderson D, Lacreuse A, Robson SL, Hawkes K: Depletion of ovarian follicles with age in chimpanzees: similarities to humans. Biol Reprod 2007;77:247–251.
  48. Hawkes K, Smith K, Robson S: Mortality and fertility rates in humans and chimpanzees: how within-species variation complicates cross-species comparisons. Am J Hum Biol 2009;21:578–586.
  49. Oeppen J, Vaupel JW: Demography. Broken limits to life expectancy. Science 2002;296:1029–1031.
  50. Database HM: University of California, Berkeley (USA), and Max Planck Institute for Demographic Research (Germany). Available at www.mortality.org or www. humanmortality.de (data downloaded on January 5, 2009).

  

Author Contacts

James G. Herndon, PhD
Yerkes National Primate Research Center, Emory University
954 Gatewood Rd. NE, Atlanta, GA 30329 (USA)
Tel. +1 404 727 7752, Fax +1 404 727 3278
E-Mail james.herndon@emory.edu

  

Article Information

Received: January 22, 2009
Accepted after revision: June 10, 2009
Published online: September 3, 2009
Number of Print Pages : 7
Number of Figures : 1, Number of Tables : 0, Number of References : 50

  

Publication Details

Gerontology (International Journal of Experimental, Clinical, Behavioural and Technological Gerontology)

Vol. 56, No. 1, Year 2010 (Cover Date: January 2010)

Journal Editor: Wick G. (Innsbruck)
ISSN: 0304-324X (Print), eISSN: 1423-0003 (Online)

For additional information: http://www.karger.com/GER


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References

  1. O’Connell J, Hawkes K, Blurton Jones NG: Grandmothering and the evolution of Homo erectus. J Hum Evol 1999;36:461–485.
  2. Charnov EL: Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology. Oxford, Oxford University Press, 1993.
  3. Kirkwood TBL, Rose MR: Evolution of senescence: late survival sacrificed for reproduction. Philos Trans Biol Sci 1991;332:15–24.
  4. Williams GC: Pleiotropy, natural selection, and the evolution of senescence. Evolution 1957;11:398–411.

    External Resources

  5. Hawkes K: Grandmothers and the evolution of human longevity. Am J Hum Biol 2003;15:380–400.
  6. Hawkes K: Life history and human evolution: a chronicle of ideas and findings; in Hawkes K, Paine RR (eds): The Evolution of Human Life History. Santa Fe, School of American Research Press, 2006, pp 45–94.
  7. Hawkes K: Slow life histories and human evolution; in Hawkes K, Paine RR (eds): The Evolution of Human Life History. Santa Fe, School of American Research Press, 2006, pp 95–126.
  8. Hawkes K, O’Connell JF, Blurton Jones NG: Human life histories: primate tradeoffs, grandmothering socioecology, and the fossil record; in Kappeler P, Pereira M (eds): Primate Life Histories and Socioecology. Chicago, University of Chicago Press, 2003, pp 204–227.
  9. Hawkes K, O’Connell JF, Blurton Jones NG: Hadza women’s time allocation, offspring provisioning, and the evolution of long postmenopausal life spans. Curr Anthropol 1997;38:551–577.
  10. Sear R, Mace R, McGregor IA: Maternal grandmothers improve nutritional status and survival of children in rural Gambia. Proc Biol Sci 2000;267:1641–1647.
  11. Jamison CS, Cornell LL, Jamison PL, Nakazato H: Are all grandmothers equal? A review and a preliminary test of the ‘grandmother hypothesis’ in Tokugawa, Japan. Am J Phys Anthropol 2002;119:67–76.
  12. Voland E, Beise J: Opposite effects of maternal and paternal grandmothers on infant survival in historical Krummhörn. Behav Ecol Sociobiol 2002;52:435–443.
  13. Sear R, Mace R: Who keeps children alive? A review of the effects of kin on child survival. Evol Hum Behav 2008;29:1–18.

    External Resources

  14. Lahdenperä M, Lummaa V, Helle S, Tremblay M, Russell AF: Fitness benefits of prolonged post-reproductive lifespan in women. Nature 2004;428:178–181.
  15. Walker ML, Herndon JG: Menopause in nonhuman primates? Biol Reprod 2008;79:398–406.
  16. Tigges J, Gordon TP, McClure HM, Hall EC, Peters A: Survival rate and life span of rhesus monkeys at the Yerkes Regional Primate Research Center. Am J Primatol 1988;15:263–273.
  17. Rosen RD: Lie of the Jungle: The Truth about Cheeta the Chimpanzee. Washington Post, Washington, DC, December 14, 2008.
  18. Herndon JG, Tigges J, Anderson DC, Klumpp SA, McClure HM: Brain weight throughout the life span of the chimpanzee. J Comp Neurol 1999;409:567–572.
  19. Bellino FL, Wise PM: Nonhuman primate models of menopause workshop. Biol Reprod 2003;68:10–18.
  20. Graham CE: Reproductive function in aged female chimpanzees. Am J Phys Anthropol 1979;50:291–300.
  21. Gould KG, Flint M, Graham CE: Chimpanzee reproductive senescence: a possible model for the evolution of menopause. Maturitas 1981;3:157–166.
  22. Videan EN, Fritz J, Heward CB, Murphy J: The effects of aging on hormone and reproductive cycles in female chimpanzees (Pan troglodytes). Comp Med 2006;56:291–299.
  23. Emery Thompson M, Jones JH, Pusey AE, Brewer-Marsden S, Goodall J, Marsden D, Matsuzawa T, Nishida T, Reynolds V, Sugiyama Y, Wrangham RW: Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause. Curr Biol 2007;17:2150–2156.
  24. Burger HG: The endocrinology of the menopause. J Steroid Biochem Mol Biol 1999;69:31–35.
  25. Deschner T, Heistermann M, Hodges K, Boesch C: Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Horm Behav 2004;46:204–215.
  26. Graham CE, Collins DC, Robinson H, Preedy JR: Urinary levels of estrogens and pregnanediol and plasma levels of progesterone during the menstrual cycle of the chimpanzee; relationship to the sexual swelling. Endocrinology 1972;91:13–24.
  27. Dahl J, Nadler RD, Collins DC: Monitoring the ovarian cycles of Pan troglodytes and P. paniscus: a comparative approach. Am J Primatol 1991;24:195–209.
  28. Nadler RD, Graham CE, Gosselin R, Collins DC: Serum levels of gonadotropins and gonadal steroids, including testosterone, during the menstrual cycle of the chimpanzee (Pan troglodytes). Am J Primatol 1985;9:273–284.
  29. McArthur JW, Beitens IZ, Gorman A, Collins DC, Preedy JRK, Graham CE: The interrelationships between sex skin swelling and the urinary excretion of LH, estrone, and pregnanediol by the cycling female chimpanzee. Am J Primatol 1981;1:265–270.

    External Resources

  30. Emery Thompson M: Reproductive endocrinology of wild female chimpanzees (Pan troglodytes schweinfurthii): methodological considerations and the role of hormones in sex and conception. Am J Primatol 2005;67:137–158.
  31. Lacreuse A, Chennareddi L, Gould KG, Hawkes K, Wijayawardana SR, Chen J, Easley KA, Herndon JG: Menstrual cycles continue into advanced old age in the common chimpanzee (Pan troglodytes). Biol Reprod 2008;79:407–412.
  32. Puschmann W, Federer E: Ein neuer Fertilitätsnachweis bei einer hoch betagten Schimpansin und Anmerkungen zum Höchstalter von Pan troglodytes. Zool Gart 2008;77:182–185.

    External Resources

  33. Vaupel JW, Carey JR, Christensen K, Johnson TE, Yashin AI, Holm NV, Iachine IA, Kannisto V, Khazaeli AA, Liedo P, Longo VD, Zeng Y, Manton KG, Curtsinger JW: Biodemographic trajectories of longevity. Science 1998;280:855–860.
  34. Peccei JS: Menopause: adaptation or epiphenomenon? Evol Anthrop 2001;10:43–57.

    External Resources

  35. Finch CE, Sapolsky RM: The evolution of Alzheimer disease, the reproductive schedule, and apoeE isoforms. Neurobiol Aging 1999;20:407–428.
  36. Allen JS, Bruss J, Damasio H: The aging brain: the cognitive reserve hypothesis and hominid evolution. Am J Hum Biol 2005;17:673–689.
  37. Stern Y: What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc 2002;8:448–460.
  38. Dunbar R: The social brain hypothesis. Evol Anthrop 1998;6:179–190.

    External Resources

  39. Carstensen LL, Lockenhoff CE: Aging, emotion, and evolution: The bigger picture. Ann NY Acad Sci 2003;1000:152–179.
  40. Herndon JG, Moss MB, Rosene DL, Killiany RJ: Patterns of cognitive decline in aged rhesus monkeys. Behav Brain Res 1997;87:25–34.
  41. Moss MB, Moore TL, Schettler SP, Killiany RJ, Rosene DL: Successful versus unsuccessful aging in the rhesus monkey; in Riddle DR (ed): Brain Aging: Models, Methods, and Mechanisms. Boca Raton, CRC Press, 2007, pp 21–38.
  42. Herndon JG, Tigges J, Klumpp SA, Anderson DC: Brain weight does not decrease with age in adult rhesus monkeys. Neurobiol Aging 1998;19:267–272.
  43. Hartmann P, Ramseier A, Gudat F, Mihatsch MJ, Polasek W: Das Normgewicht des Gehirns beim Erwachsenen in Abhängigkeit von Alter, Geschlecht, Körpergrösse und Gewicht. Pathologe 1994;15:165–170.
  44. Rapp PR, Amaral DG: Evidence for task-dependent memory dysfunction in the aged monkey. J Neurosci 1989;9:3568–3576.
  45. Riopelle AJ, Rogers CM: Age changes in chimpanzees; in Schrier AM, Stolnitz F (eds): Behavior of Nonhuman Primates: Modern Research Trends. New York, Academic Press, 1965, pp 449–462.
  46. Judge DS, Carey JR: Postreproductive life predicted by primate patterns. J Gerontol A Biol Sci Med Sci 2000;55:B201–B209.
  47. Jones KP, Walker LC, Anderson D, Lacreuse A, Robson SL, Hawkes K: Depletion of ovarian follicles with age in chimpanzees: similarities to humans. Biol Reprod 2007;77:247–251.
  48. Hawkes K, Smith K, Robson S: Mortality and fertility rates in humans and chimpanzees: how within-species variation complicates cross-species comparisons. Am J Hum Biol 2009;21:578–586.
  49. Oeppen J, Vaupel JW: Demography. Broken limits to life expectancy. Science 2002;296:1029–1031.
  50. Database HM: University of California, Berkeley (USA), and Max Planck Institute for Demographic Research (Germany). Available at www.mortality.org or www. humanmortality.de (data downloaded on January 5, 2009).