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Post-Fertile Lifespan in Female Primates and Cetaceans

  • Mary S. M. Pavelka
  • Lauren J. N. Brent
  • D. P. Croft
  • Linda M. Fedigan
Chapter
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Abstract

Popular and scientific interest in menopause in humans has led to an increased interest in the extent of post-fertile life in other animals, particularly in long-lived social species such as other primates and cetaceans. Information on maximum lifespan achieved and age at last birth are available from long-term observations of known individuals from 11 primate species in the wild. Comparable information from wild cetaceans are more difficult to obtain; however there are relevant fisheries data, as well as a small number of long-term individual-based studies. Using post-reproductive representation (PrR) as a population measure of post-fertile lifespan that allows comparisons across populations and species, this review confirms that among primates, only humans have a maximum lifespan significantly longer than 50 years, and only human female life history includes a significant post-fertile stage of life. We conclude that although a prolonged post-fertile stage of life is very rare in mammals, it does occur in some exceptionally long-lived taxa, such as humans and resident killer and short-finned pilot whales. Thus menopause evolved independently at least three times in mammals, and the reasons for its evolution may differ in different lineages.

Keywords

Evolution of menopause Whale menopause Post-fertile lifespan primates 

Notes

Acknowledgements

M.S.M. Pavelka’s research is supported by ongoing Discovery Grants from the Natural Sciences and Engineering Research Council of Canada (NSERC). L.J.N.Brent is supported by an Early Career Fellowship from the Leverhulme Trust. D.P. Croft acknowledges funding from the NERC (NE/K01286X/1). L.M. Fedigan’s research has been supported since 1983 by ongoing Discovery Grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and from 2002 to 2016 by the Canada Research Chairs Program. We are thankful to Dr. Katharine Jack and two anonymous reviewers for their helpful comments and suggestions on earlier versions of this manuscript.

References

  1. Alberts SC, Altmann J, Brockman DK, Cords M, Fedigan LM, Pusey A et al (2013) Reproductive aging patterns in primates reveal that humans are distinct. Proc Natl Acad Sci USA 110(33):13440–13445CrossRefGoogle Scholar
  2. Armstrong DT (2001) Effects of maternal age on oocyte developmental competence. Theriogeneology 55(6):1303–1322CrossRefGoogle Scholar
  3. Arrigoni M, Manfredi P, Panigada S, Bramanti L, Santangelo G (2011) Life-history tables of the Mediterranean fin whale from stranding data. Mar Ecol 32:1–9CrossRefGoogle Scholar
  4. Atsalis S, Margulis SW, Hof PR (2008) Primate reproductive aging: cross-taxon perspectives. Karger Press, BaselCrossRefGoogle Scholar
  5. Bellino FL, Wise PM (2003) Nonhuman primate models of menopause workshop. Biol Reprod 68(1):10–18CrossRefGoogle Scholar
  6. Best PB, Canham PAS, Macleod N (1984) Patterns of reproduction in sperm whales, Physeter macrocephalus. Rep Int Whal Commn Spec 6:51–57Google Scholar
  7. Bigg MA, Olesiuk PF, Ellis GM, Ford JKB, Balcomb KC (1990) Social organization and genealogy of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington state. Rep Int Whal Comm Spec 12:383–405Google Scholar
  8. Bloch D, Lockyer C, Zachariassen M (1993) Age and growth parameters of the long-finned pilot whale off the Faroe Islands. Rep Int Whal Comm Spec 14:163–207Google Scholar
  9. Borries C, Sommer V, Srivastave A (1991) Dominance, age, and reproductive success in free-ranging female Hanuman langurs (Presbytis entellus). Int J Primatol 12(3):231–257CrossRefGoogle Scholar
  10. Bronikowski AM, Altmann J, Brockman DK, Cords M, Fedigan LM, Pusey A et al (2011) Aging in the natural world: comparative data reveal similar mortality patterns across primates. Science 331(6022):1325–1328CrossRefPubMedCentralGoogle Scholar
  11. Cant MA, Johnstone RA (2008) Reproductive conflict and the separation of reproductive generations in humans. Proc Natl Acad Sci USA 105(14):5332–5336CrossRefPubMedCentralGoogle Scholar
  12. Cant MA, Johnstone RA, Russell AF (2009) Reproductive conflict and the evolution of menopause. In: Hager R, Jones CB (eds) Reproductive skew in vertebrates: proximate and ultimate causes. Cambridge Universtiy Press, Cambridge, pp 24–50CrossRefGoogle Scholar
  13. Caro TM, Sellen DW, Parish A, Frank R, Brown DM, Voland E, Borgerhoff Mulder M (1995) Termination of reproduction in nonhuman and human female primates. Int J Primatol 16(2):205–220CrossRefGoogle Scholar
  14. Croft DP, Brent LJN, Franks DW, Cant MA (2015) The evolution of prolonged life after reproduction. Trends Ecol Evol 30(7):407–416CrossRefGoogle Scholar
  15. Croft DP, Johnstone RA, Ellis S, Nattrass S, Franks DW, Brent LJ, Mazzi S, Balcomb KC, Ford JK, Cant MA (2017) Reproductive conflict and the evolution of menopause in killer whales. Curr Biol 27(2):298–304CrossRefPubMedCentralGoogle Scholar
  16. Cutler RG (1975) Evolution of human longevity and the genetic complexity governing aging rate. Proc Natl Acad Sci 72(11):4664–4668CrossRefGoogle Scholar
  17. Fedigan LM, Pavelka MSM (2011) Menopause: interspecific comparisons of reproductive termination in female primates. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (eds) Primates in perspective, 2nd edn. Oxford University Press, New York, pp 488–498Google Scholar
  18. Foote AD (2008) Mortality rate acceleration and post-reproductive lifespan in matrilineal whale species. Biol Lett 4:189–191CrossRefPubMedCentralGoogle Scholar
  19. Foster EA, Franks DW, Mazzi S, Darden SK, Balcomb KC, Ford JKB, Croft DP (2012) Adaptive prolonged postreproductive life span in killer whales. Science 337(6100):1313CrossRefPubMedCentralGoogle Scholar
  20. Franks DW, Nattrass S, Brent LJ, Whitehead H, Foote AD, Mazzi S, Ford JK, Balcomb KC, Cant MA, Croft DP (2016) The significance of postreproductive lifespans in killer whales: a comment on Robeck et al. J Mammal 97(3):906–909CrossRefGoogle Scholar
  21. George J, Follmann E, Zeh J, Sousa M, Tarpley R, Suydam R (2004) Inferences from bowhead whale ovarian and pregnancy data: age estimates, length at sexual maturity and ovulation rates. International Whaling Commission scientific paper 56Google Scholar
  22. Gilardi KG, Shideler SE, Valverde C, Roberts JA, Lasley BL (1997) Characterization of the onset of menopause in the rhesus macaque. Biol Reprod 57(2):335–340CrossRefPubMedCentralGoogle Scholar
  23. Gosden RG (1985) Biology of menopause: the causes and consequences of ovarian ageing. Academic Press, LondonGoogle Scholar
  24. Gosden RG, Faddy MJ (1998) Biological bases of premature ovarian failure. Reprod Fertil Dev 10(1):73–78CrossRefPubMedCentralGoogle Scholar
  25. Gosden R, Telfer E (1987) Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships. J Zool 211(1):169–175CrossRefGoogle Scholar
  26. Gould KG, Flint M, Graham CE (1981) Chimpanzee reproductive senescence: a possible model for evolution of the menopause. Maturitas 3(2):157–166CrossRefPubMedCentralGoogle Scholar
  27. Gould SJ, Lewontin RC (1979) The spandrels of san Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B 205(1161):581–598CrossRefPubMedCentralGoogle Scholar
  28. Graham CE (1979) Reproductive function in aged female chimpanzees. Am J Phys Anthropol 50(3):291–300CrossRefPubMedCentralGoogle Scholar
  29. Hamilton PK, Knowlton AR, Marx MK, Kraus SD (1998) Age structure and longevity in North Atlantic right whales Eubalaena glacialis and their relation to reproduction. Mar Ecol Prog Ser 171:285–292CrossRefGoogle Scholar
  30. Hawkes K (2003) Grandmothers and the evolution of human longevity. Am J Hum Biol 15(3):380–400CrossRefGoogle Scholar
  31. Hawkes K, Coxworth JE (2013) Grandmothers and the evolution of human longevity: a review of findings and future directions. Evol Anthropol 22(6):294–302CrossRefGoogle Scholar
  32. Hill K, Hurtado AM (1991) The evolution of premature reproductive senescence and menopause in human females: an evolution of the “grandmother hypothesis”. Hum Nat 2(4):313–350CrossRefGoogle Scholar
  33. Hill K, Hurtado AM (1996) Ache life history: the ecology and demography of a foraging people. Aldine de Gruyter, New YorkGoogle Scholar
  34. Johnstone RA, Cant MA (2010) The evolution of menopause in cetaceans and humans: the role of demography. Proc R Soc Lond B 277(1701):3765–3771CrossRefGoogle Scholar
  35. Johnson RL, Kapsalis E (1998) Menopause in free-ranging rhesus macaques: estimated incidence, relation to body condition, and adaptive significance. Int J Primatol 19(4):751–765CrossRefGoogle Scholar
  36. Johnson RL, Kapsalis E (2008) Heterogeneity of reproductive aging in free-ranging female rhesus macaques. In: Atsalis S, Margulis SW, Hof PR (eds) Primate reproductive aging: cross-taxon perspectives. Karger Press, Basel, pp 62–79CrossRefGoogle Scholar
  37. Jones K, Walker L, Anderson D, Lacreuse A, Robson SL, Hawkes K (2007) Depletion of ovarian follicles with age in chimpanzees: similarities to humans. Biol Reprod 77(2):247–251CrossRefGoogle Scholar
  38. Kaplan H, Hill K, Lancaster J, Hurtado AM (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9(4):156–185CrossRefGoogle Scholar
  39. Kasuya T, Marsh H (1984) Life history and reproductive biology of the short-finned pilot whale, Globicephala macrorhynchus, off the Pacific coast of Japan. Rep Int Whal Comm Spec 6:259–310Google Scholar
  40. Kasuya T, Izumisawa Y, Komyo Y, Ishino Y, Maejima Y (1997) Life history parameters of bottlenose dolphins off Japan. IBI Rep 7:71–107Google Scholar
  41. Koenig A, Borries C, Chalise MK, Winkler P (1997) Ecology, nutrition, and timing of reproductive events in an Asian primate, the Hanuman langur (Presbytis entellus). J Zool 243(2):215–235CrossRefGoogle Scholar
  42. Lahdenpera M, Lummaa V, Helle S, Tremblay M, Russell AF (2004) Fitness benefits of prolonged post-reproductive lifespan in women. Nature 428(6979):178–181CrossRefGoogle Scholar
  43. Lee PC, Fishlock V, Webber CE, Moss CJ (2016) The reproductive advantages of a long life: longevity and senescence in wild female African elephants. Behav Ecol Sociobiol 70(3):337–345CrossRefPubMedCentralGoogle Scholar
  44. Lahdenpera M, Gillespie DOS, Lummaa V, Russell AF (2012) Severe intergenerational reproductive conflict and the evolution of menopause. Ecol Lett 15(11):1283–1290CrossRefGoogle Scholar
  45. Levitis DA, Lackey LB (2011) A measure for describing and comparing postreproductive life span as a population trait. Methods Ecol Evol 2(5):446–453CrossRefPubMedCentralGoogle Scholar
  46. Levitis DA, Burger O, Lackey LB (2013) The human post-fertile lifespan in comparative evolutionary context. Evol Anth 22: 66–79.CrossRefGoogle Scholar
  47. Lockyer C, Brown S (1979) A review of recent biological data for the fin whale population off Iceland. Rep Int Whal Comm Spec 29:185–190Google Scholar
  48. Marsh H, Kasuya T (1986) Evidence for reproductive senescence in female cetaceans. Rep Int Whal Comm Spec 8:57–74Google Scholar
  49. Martin AR, Rothery P (1993) Reproductive parameters of female long-finned pilot whales (Globicephala melas) around the Faroe Islands. Rep Int Whal Comm Spec 14:263–304Google Scholar
  50. Mizroch SA (1981) Analyses of some biological parameters in the Antarctic fin whale. Rep Int Whal Comm Spec 31:425–434Google Scholar
  51. Morris W, Altmann J, Brockman D, Cords M, Fedigan L, Pusey A et al (2011) Low demographic variability in wild primate populations: fitness impacts of variation, covariation, and serial correlation in vital rates. Am Nat 177(1):E14–E28CrossRefGoogle Scholar
  52. Nishida T, Corp N, Hamai M, Hasegawa T, Hiraiwa-Hasegawa M, Hosaka K et al (2003) Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. Am J Primtol 59(3):99–121CrossRefGoogle Scholar
  53. Nozaki M, Mitsunaga F, Shimizu K (1995) Reproductive senescence in female Japanese monkeys (Macaca fuscata): age- and season-related changes in hypothalamic-pituitary-ovarian functions and fecundity rates. Biol Reprod 52(6):1250–1257CrossRefPubMedCentralGoogle Scholar
  54. Olesiuk PF, Bigg MA, Ellis GM (1990) Life history and population dynamics of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington state. Rep Int Whal Comm Spec 12:209–243Google Scholar
  55. Paul A (2005) Primate predispositions for human grandmaternal behavior. In: Voland E, Chasiotis A, Schiefenhovel W (eds) Grandmotherhood: the evolutionary significance of the second half of female life. Rutgers University Press, New Brunswick, pp 21–37Google Scholar
  56. Paul A, Kuester J, Podzuweit D (1993) Reproductive senescence and terminal investment in female barbary macaques (Macaca sylvanus) at Salem. Int J Primatol 14(1):105–124CrossRefGoogle Scholar
  57. Pavelka MSM, Fedigan LM (1991) Menopause: a comparative life history perspective. Yearb Phys Anthropol 34:13–38CrossRefGoogle Scholar
  58. Pavelka MSM, Fedigan LM (1999) Reproductive termination in female Japanese monkeys: a comparative life history perspective. Am J Phys Anthropol 109(4):455–464CrossRefPubMedCentralGoogle Scholar
  59. Pavelka MSM, Fedigan LM (2012) Costs and benefits of old age reproduction in the Arashiyama west female Japanese macaques. In: Leca JB, Huffman MA, Vasey PL (eds) The monkeys of Stormy Mountain: 60 years of primatological research on the Japanese macaques of Arashiyama. Cambridge University Press, Cambridge, pp 13–27Google Scholar
  60. Raichlen DA, Alexander GE (2014) Exercise, APOE genotype, and the evolution of the human lifespan. Trends Neurosci 37(5):247–255CrossRefPubMedCentralGoogle Scholar
  61. Rice DW (1989) Sperm whale Physeter macrocephalus Linnaeus, 1758. In: Ridgeway SH, Harrison R (eds) Handbook of marine mammals, vol 4. Academic Press, London, pp 177–233Google Scholar
  62. Robbins AM, Robbins MM, Gerald-Steklis N, Steklis HD (2006) Age-related patterns of reproductive success among female mountain gorillas. Am J Phys Anthropol 131(4):511–521CrossRefPubMedCentralGoogle Scholar
  63. Rogers AR (1993) Why menopause? Evol Ecol 7(4):406–420CrossRefGoogle Scholar
  64. Rose MR (1991) Evolutionary biology of aging. Oxford University Press, OxfordGoogle Scholar
  65. Rose MR, Mueller LD (1998) Evolution of human lifespan: past, future, and present. Am J Hum Biol 10:409–420CrossRefGoogle Scholar
  66. Shanley DP, Sear R, Mace R, TBL K (2007) Testing evolutionary theories of menopause. Proc R Soc Lond B 274(1628):2943–2949CrossRefGoogle Scholar
  67. Small MF (1982) Reproducive failure in macaques. Am J Primatol 2:137–147CrossRefGoogle Scholar
  68. Small MP (1984) Aging and reproductive success in female Macaca mulatta. In: Small MF (ed) Female primates: studies by women primatologists. Alan R Liss Inc., New York, pp 249–259Google Scholar
  69. Sommer V, Srivastava A, Borries C (1992) Cycles, sexuality, and conception in free-ranging langurs (Presbytis entellus). Am J Primtol 28(1):1–27CrossRefGoogle Scholar
  70. Stolen MK, Barlow J (2003) A model life table for bottlenose dolphins (Tursiops truncatus) from the Indian River lagoon system, Florida, USA. Mar Mamm Sci 19(4):630–649CrossRefGoogle Scholar
  71. Strier K, Altmann J, Brockman D, Bronikowski A, Cords M, Fedigan L et al (2010) The primate life history database: a unique shared ecological data resource. Methods Ecol Evol 1(2):199–211CrossRefPubMedCentralGoogle Scholar
  72. Strier K (2018, this volume). The temporal scale of behavioral and demographic flexibility: implications for comparative analyses and conservation. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability - essays in honour of Linda M. Fedigan. Developments in primatology: progress and prospects. Springer, New York, pp 19–33Google Scholar
  73. Strassmann BI, Garrard WM (2011) Alternatives to the grandmother hypothesis. Hum Nat 22:201CrossRefGoogle Scholar
  74. Takahata Y, Koyama N, Suzuki S (1995) Do old aged females experience a long post-reproductive life span?: the cases of Japanese macaques and chimpanzees. Primates 36(2):169–180CrossRefGoogle Scholar
  75. Tardif SD, Ziegler TE (1992) Features of female reproductive senescence in tamarins (Saguinus spp), a New World primate. J Reprod Fertil 94(2):411–421CrossRefGoogle Scholar
  76. Tardif SD, Araujo A, Arruda MF, French JA, Sousa MBC, Yamamoto ME (2008) Reproduction and aging in marmosets and tamarins. In: Atsalis S, Margulis SW, Hof PR (eds) Primate reproductive aging: cross-taxon perspectives. Karger Press, Basel, pp 29–48CrossRefGoogle Scholar
  77. Thompson ME, Jones JH, Pusey AE, Brewer-Marsden S, Goodall J, Marsden D et al (2007) Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause. Curr Biol 17(24):2150–2156CrossRefPubMedCentralGoogle Scholar
  78. Towers J, Ellis G, Ford J (2015) Photo-identification catalogue and status of the northern resident killer whale population in 2014. Canadian technical report of fisheries and aquatic sciences 3139, 75viGoogle Scholar
  79. Tuljapurkar SD, Puleston CO, Gurven MD (2007) Why men matter: mating patterns drive evolution of human lifespan. PLoS One 2(8):e785CrossRefPubMedCentralGoogle Scholar
  80. Videan EN, Fritz J, Heward CB, Murphy J (2006) The effects of aging on hormone and reproductive cycles in female chimpanzees (Pan troglodytes). Comp Med 56(4):291–299PubMedGoogle Scholar
  81. von Saal FS, Finch CE, Nelson JF (1994) Natural history and mechanisms of reproductive aging in humans, laboratory rodents, and other selected vertebrates. In: Knobil E, Neill J (eds) The physiology of reproduction. Raven Press, New York, pp 1213–1314Google Scholar
  82. Walker ML (1995) Menopause in female rhesus monkeys. Am J Primtol 35(1):59–71CrossRefGoogle Scholar
  83. Walker ML, Herndon JG (2008) Menopause in nonhuman primates? Biol Reprod 79(3):398–406CrossRefPubMedCentralGoogle Scholar
  84. Whitehead H (2003) Sperm whales: social evolution in the ocean. University of Chicago press, ChicagoGoogle Scholar
  85. Whitehead H, Rendell L (2014) The cultural lives of whales and dolphins. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  86. Wich SA, Utami-Atmoko SS, Mitra Setia T, Rijksen HD, Schurmann C, van Hooff JARAM, van Schaik CP (2004) Life history of wild Sumatran orangutans (Pongo abelii). J Hum Evol 47(6):385–398CrossRefPubMedCentralGoogle Scholar
  87. Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11(4):398–411CrossRefGoogle Scholar
  88. Wood JW, Holman DJ, O'Connor KA (2001) Did menopause evolve by antagonistic pleiotropy? In: Schultz M (ed) Homo: Unsere Herkunft und Zukunft. Cuvillier Verlag, Gottingen, pp 483–490Google Scholar
  89. Wood BM, Watts DP, Mitani JC (2017) Favorable ecological circumstances promote life expectancy in chimpanzees similar to that of human hunter-gatherers. J Hum Evol 105:41–56CrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Mary S. M. Pavelka
    • 1
  • Lauren J. N. Brent
    • 2
  • D. P. Croft
    • 2
  • Linda M. Fedigan
    • 1
  1. 1.Department of Anthropology and ArchaeologyUniversity of CalgaryCalgaryCanada
  2. 2.Department of Psychology, Washington Singer LaboratoriesUniversity of ExeterExeterUK

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