Skip to main content
SpringerLink
Log in

Post-Fertile Lifespan in Female Primates and Cetaceans

  • Chapter
  • First Online:
Primate Life Histories, Sex Roles, and Adaptability

Part of the book series: Developments in Primatology: Progress and Prospects ((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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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):13440–13445

    CAS  PubMed  Google Scholar 

  • Armstrong DT (2001) Effects of maternal age on oocyte developmental competence. Theriogeneology 55(6):1303–1322

    CAS  Google Scholar 

  • Arrigoni M, Manfredi P, Panigada S, Bramanti L, Santangelo G (2011) Life-history tables of the Mediterranean fin whale from stranding data. Mar Ecol 32:1–9

    Google Scholar 

  • Atsalis S, Margulis SW, Hof PR (2008) Primate reproductive aging: cross-taxon perspectives. Karger Press, Basel

    Google Scholar 

  • Bellino FL, Wise PM (2003) Nonhuman primate models of menopause workshop. Biol Reprod 68(1):10–18

    CAS  PubMed  Google Scholar 

  • Best PB, Canham PAS, Macleod N (1984) Patterns of reproduction in sperm whales, Physeter macrocephalus. Rep Int Whal Commn Spec 6:51–57

    Google Scholar 

  • 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 12:383–405

    Google Scholar 

  • 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 14:163–207

    Google Scholar 

  • 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):231–257

    Google Scholar 

  • 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):1325–1328

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cant MA, Johnstone RA (2008) Reproductive conflict and the separation of reproductive generations in humans. Proc Natl Acad Sci USA 105(14):5332–5336

    CAS  PubMed  Google Scholar 

  • 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 24–50

    Google Scholar 

  • 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):205–220

    Google Scholar 

  • Croft DP, Brent LJN, Franks DW, Cant MA (2015) The evolution of prolonged life after reproduction. Trends Ecol Evol 30(7):407–416

    PubMed  Google Scholar 

  • 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):298–304

    CAS  PubMed  Google Scholar 

  • Cutler RG (1975) Evolution of human longevity and the genetic complexity governing aging rate. Proc Natl Acad Sci 72(11):4664–4668

    CAS  PubMed  Google Scholar 

  • 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 488–498

    Google Scholar 

  • Foote AD (2008) Mortality rate acceleration and post-reproductive lifespan in matrilineal whale species. Biol Lett 4:189–191

    PubMed  PubMed Central  Google Scholar 

  • 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):1313

    CAS  PubMed  Google Scholar 

  • 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):906–909

    Google Scholar 

  • 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 56

    Google Scholar 

  • 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):335–340

    CAS  PubMed  Google Scholar 

  • Gosden RG (1985) Biology of menopause: the causes and consequences of ovarian ageing. Academic Press, London

    Google Scholar 

  • Gosden RG, Faddy MJ (1998) Biological bases of premature ovarian failure. Reprod Fertil Dev 10(1):73–78

    CAS  PubMed  Google Scholar 

  • Gosden R, Telfer E (1987) Numbers of follicles and oocytes in mammalian ovaries and their allometric relationships. J Zool 211(1):169–175

    Google Scholar 

  • Gould KG, Flint M, Graham CE (1981) Chimpanzee reproductive senescence: a possible model for evolution of the menopause. Maturitas 3(2):157–166

    CAS  PubMed  Google Scholar 

  • 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):581–598

    CAS  PubMed  Google Scholar 

  • Graham CE (1979) Reproductive function in aged female chimpanzees. Am J Phys Anthropol 50(3):291–300

    CAS  PubMed  Google Scholar 

  • 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 171:285–292

    Google Scholar 

  • Hawkes K (2003) Grandmothers and the evolution of human longevity. Am J Hum Biol 15(3):380–400

    PubMed  Google Scholar 

  • Hawkes K, Coxworth JE (2013) Grandmothers and the evolution of human longevity: a review of findings and future directions. Evol Anthropol 22(6):294–302

    PubMed  Google Scholar 

  • 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):313–350

    CAS  PubMed  Google Scholar 

  • Hill K, Hurtado AM (1996) Ache life history: the ecology and demography of a foraging people. Aldine de Gruyter, New York

    Google Scholar 

  • Johnstone RA, Cant MA (2010) The evolution of menopause in cetaceans and humans: the role of demography. Proc R Soc Lond B 277(1701):3765–3771

    Google Scholar 

  • 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):751–765

    Google Scholar 

  • 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 62–79

    Google Scholar 

  • 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):247–251

    CAS  PubMed  Google Scholar 

  • Kaplan H, Hill K, Lancaster J, Hurtado AM (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evol Anthropol 9(4):156–185

    Google Scholar 

  • 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 6:259–310

    Google Scholar 

  • Kasuya T, Izumisawa Y, Komyo Y, Ishino Y, Maejima Y (1997) Life history parameters of bottlenose dolphins off Japan. IBI Rep 7:71–107

    Google Scholar 

  • 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):215–235

    Google Scholar 

  • Lahdenpera M, Lummaa V, Helle S, Tremblay M, Russell AF (2004) Fitness benefits of prolonged post-reproductive lifespan in women. Nature 428(6979):178–181

    PubMed  Google Scholar 

  • 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):337–345

    PubMed  PubMed Central  Google Scholar 

  • Lahdenpera M, Gillespie DOS, Lummaa V, Russell AF (2012) Severe intergenerational reproductive conflict and the evolution of menopause. Ecol Lett 15(11):1283–1290

    PubMed  Google Scholar 

  • Levitis DA, Lackey LB (2011) A measure for describing and comparing postreproductive life span as a population trait. Methods Ecol Evol 2(5):446–453

    PubMed  PubMed Central  Google Scholar 

  • Levitis DA, Burger O, Lackey LB (2013) The human post-fertile lifespan in comparative evolutionary context. Evol Anth 22: 66–79.

    Google Scholar 

  • Lockyer C, Brown S (1979) A review of recent biological data for the fin whale population off Iceland. Rep Int Whal Comm Spec 29:185–190

    Google Scholar 

  • Marsh H, Kasuya T (1986) Evidence for reproductive senescence in female cetaceans. Rep Int Whal Comm Spec 8:57–74

    Google Scholar 

  • Martin AR, Rothery P (1993) Reproductive parameters of female long-finned pilot whales (Globicephala melas) around the Faroe Islands. Rep Int Whal Comm Spec 14:263–304

    Google Scholar 

  • Mizroch SA (1981) Analyses of some biological parameters in the Antarctic fin whale. Rep Int Whal Comm Spec 31:425–434

    Google Scholar 

  • 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–E28

    PubMed  Google Scholar 

  • 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):99–121

    Google Scholar 

  • 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):1250–1257

    CAS  PubMed  Google Scholar 

  • 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 12:209–243

    Google Scholar 

  • 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 21–37

    Google Scholar 

  • 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):105–124

    Google Scholar 

  • Pavelka MSM, Fedigan LM (1991) Menopause: a comparative life history perspective. Yearb Phys Anthropol 34:13–38

    Google Scholar 

  • Pavelka MSM, Fedigan LM (1999) Reproductive termination in female Japanese monkeys: a comparative life history perspective. Am J Phys Anthropol 109(4):455–464

    CAS  PubMed  Google Scholar 

  • 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 13–27

    Google Scholar 

  • Raichlen DA, Alexander GE (2014) Exercise, APOE genotype, and the evolution of the human lifespan. Trends Neurosci 37(5):247–255

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 177–233

    Google Scholar 

  • 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):511–521

    PubMed  Google Scholar 

  • Rogers AR (1993) Why menopause? Evol Ecol 7(4):406–420

    Google Scholar 

  • Rose MR (1991) Evolutionary biology of aging. Oxford University Press, Oxford

    Google Scholar 

  • Rose MR, Mueller LD (1998) Evolution of human lifespan: past, future, and present. Am J Hum Biol 10:409–420

    PubMed  Google Scholar 

  • Shanley DP, Sear R, Mace R, TBL K (2007) Testing evolutionary theories of menopause. Proc R Soc Lond B 274(1628):2943–2949

    Google Scholar 

  • Small MF (1982) Reproducive failure in macaques. Am J Primatol 2:137–147

    Google Scholar 

  • 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 249–259

    Google Scholar 

  • Sommer V, Srivastava A, Borries C (1992) Cycles, sexuality, and conception in free-ranging langurs (Presbytis entellus). Am J Primtol 28(1):1–27

    Google Scholar 

  • 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):630–649

    Google Scholar 

  • 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):199–211

    PubMed  PubMed Central  Google Scholar 

  • 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 19–33

    Google Scholar 

  • Strassmann BI, Garrard WM (2011) Alternatives to the grandmother hypothesis. Hum Nat 22:201

    PubMed  Google Scholar 

  • 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):169–180

    Google Scholar 

  • Tardif SD, Ziegler TE (1992) Features of female reproductive senescence in tamarins (Saguinus spp), a New World primate. J Reprod Fertil 94(2):411–421

    CAS  PubMed  Google Scholar 

  • 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 29–48

    Google Scholar 

  • 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):2150–2156

    CAS  PubMed Central  Google Scholar 

  • 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, 75vi

    Google Scholar 

  • Tuljapurkar SD, Puleston CO, Gurven MD (2007) Why men matter: mating patterns drive evolution of human lifespan. PLoS One 2(8):e785

    PubMed  PubMed Central  Google Scholar 

  • 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):291–299

    CAS  PubMed  Google Scholar 

  • 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 1213–1314

    Google Scholar 

  • Walker ML (1995) Menopause in female rhesus monkeys. Am J Primtol 35(1):59–71

    Google Scholar 

  • Walker ML, Herndon JG (2008) Menopause in nonhuman primates? Biol Reprod 79(3):398–406

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whitehead H (2003) Sperm whales: social evolution in the ocean. University of Chicago press, Chicago

    Google Scholar 

  • Whitehead H, Rendell L (2014) The cultural lives of whales and dolphins. University of Chicago Press, Chicago

    Google Scholar 

  • 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):385–398

    CAS  PubMed  Google Scholar 

  • Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11(4):398–411

    Google Scholar 

  • 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 483–490

    Google Scholar 

  • 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 105:41–56

    PubMed  PubMed Central  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Anthropology and Archaeology, University of Calgary, Calgary, AB, Canada

    Mary S. M. Pavelka & Linda M. Fedigan

  2. Department of Psychology, Washington Singer Laboratories, University of Exeter, Exeter, UK

    Lauren J. N. Brent & D. P. Croft

Authors
  1. Mary S. M. Pavelka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lauren J. N. Brent
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. P. Croft
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Linda M. Fedigan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mary S. M. Pavelka .

Editor information

Editors and Affiliations

  1. Department of Anthropology and McGill School of Environment, McGill University, Montreal, QC, Canada, Department of Anthropology and Archaeology, University of Calgary, Calgary, AB, Canada

    Urs Kalbitzer

  2. Department of Anthropology, Tulane University, New Orleans, LA, USA

    Katharine M. Jack

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Pavelka, M.S.M., Brent, L.J.N., Croft, D.P., Fedigan, L.M. (2018). Post-Fertile Lifespan in Female Primates and Cetaceans. In: Kalbitzer, U., Jack, K. (eds) Primate Life Histories, Sex Roles, and Adaptability. Developments in Primatology: Progress and Prospects. Springer, Cham. https://doi.org/10.1007/978-3-319-98285-4_3

Download citation

Publish with us

Policies and ethics

Search

Navigation