Abstract
Most animals reproduce until they die, but in humans, females can survive long after ceasing reproduction1,2. In theory, a prolonged post-reproductive lifespan will evolve when females can gain greater fitness by increasing the success of their offspring than by continuing to breed themselves3,4,5,6. Although reproductive success is known to decline in old age1,2,3,4,5,6, it is unknown whether women gain fitness by prolonging lifespan post-reproduction. Using complete multi-generational demographic records, we show that women with a prolonged post-reproductive lifespan have more grandchildren, and hence greater fitness, in pre-modern populations of both Finns and Canadians. This fitness benefit arises because post-reproductive mothers enhance the lifetime reproductive success of their offspring by allowing them to breed earlier, more frequently and more successfully. Finally, the fitness benefits of prolonged lifespan diminish as the reproductive output of offspring declines. This suggests that in female humans, selection for deferred ageing should wane when one's own offspring become post-reproductive and, correspondingly, we show that rates of female mortality accelerate as their offspring terminate reproduction.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Grandparental Support and Maternal Postpartum Mental Health
Human Nature Open Access 08 February 2023
-
Host age structure reshapes parasite symbiosis: collaboration begets pathogens, competition begets virulent mutualists
Biology Direct Open Access 12 November 2022
-
The interplay of grandparental investment according to the survival status of other grandparent types
Scientific Reports Open Access 23 August 2022
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout



References
Williams, G. C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411 (1957)
Hamilton, W. D. The moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45 (1966)
Hawkes, K., O'Connell, J. F., Blurton Jones, N. G., Alvarez, H. & Charnov, E. L. Grandmothering, menopause, and the evolution of human life histories. Proc. Natl Acad. Sci. USA 95, 1336–1339 (1998)
Hawkes, K., O'Connell, J. F. & Blurton Jones, N. G. Hadza women's time allocation, offspring provisioning, and the evolution of long postmenopausal lifespans. Curr. Anthropol. 38, 551–577 (1997)
Shanley, D. P. & Kirkwood, T. B. L. Evolution of the human menopause. Bioessays 23, 282–287 (2001)
Lee, R. D. Rethinking the evolutionary theory of aging: Transfers, not births, shape senescence in social species. Proc. Natl Acad. Sci. USA 100, 9637–9642 (2003)
Emlen, S. T. An evolutionary theory of the family. Proc. Natl Acad. Sci. USA 92, 8092–8099 (1995)
Russell, A. F., Brotherton, P. N. M., McIlrath, G. M., Sharpe, L. L. & Clutton-Brock, T. H. Breeding success in cooperative meerkats: effects of helper number and maternal state. Behav. Ecol. 14, 486–492 (2003)
Brown, J. L., Brown, E. R., Brown, S. D. & Dow, D. D. Helpers: effects of experimental removal on reproductive success. Science 215, 421–422 (1982)
Emlen, S. T. & Wrege, P. H. Breeding biology of white-fronted bee-eaters at Nakuru: the influence of helpers on breeder fitness. J. Anim. Ecol. 60, 309–326 (1991)
Clutton-Brock, T. H. et al. Effects of helpers on juvenile development and survival in meerkats. Science 293, 2446–2449 (2001)
Sear, R., Mace, R. & McGregor, I. A. The effects of kin on female fertility in rural Gambia. Evol. Hum. Behav. 24, 25–42 (2003)
Voland, E. & Beise, J. Opposite effects of maternal and paternal grandmothers on infant survival in historical Krummhörn. Behav. Ecol. Sociobiol. 52, 435–443 (2002)
Sear, R., Mace, R. & McGregor, I. A. Maternal grandmothers improve the nutritional status and survival of children in rural Gambia. Proc. R. Soc. Lond. B 267, 1641–1647 (2000)
Jamison, C. S., Cornell, L. L., Jamison, P. L. & Nakazato, H. Are all grandmothers equal? A review and a preliminary test of the grandmother hypothesis in Tokugawa Japan. Am. J. Phys. Anthropol. 119, 67–76 (2002)
Moring, B. Household and family in Finnish coastal societies 1635–1895. J. Fam. Hist. 18, 395–414 (1993)
Bouchard, G. Quelques Arpents d'Amérique. Histoire, Population et Famille au Saguenay, 1838–1971 (Boréal, Montréal, 1996)
McGraw, J. B. & Caswell, H. Estimation of individual fitness from life-history data. Am. Nat. 147, 47–64 (1996)
Lummaa, V., Haukioja, E., Lemmetyinen, R. & Pikkola, M. Natural selection on human twinning. Nature 394, 533–534 (1998)
Cockburn, A. Evolution of helping behavior in cooperatively breeding birds. Annu. Rev. Ecol. Syst. 29, 141–177 (1998)
Hawkes, K. Grandmothers and the evolution of human longevity. Am. J. Hum. Biol. 15, 380–400 (2003)
Luther, G. Suomen Tilastotoimen Historia vuoteen 1970 (WSOY, Helsinki, 1993)
Gille, H. The demographic history of the northern European countries in the eighteenth century. Popul. Stud. 3, 3–65 (1949)
Soininen, A. M. Old Traditional Agriculture in Finland in the 18th and 19th Centuries (Forssan Kirjapaino Oy, Forssa, 1974)
Karskela, S. Sukututkijan Tietokirja (Gummerus Kirjapaino Oy, Saarijärvi, 2001)
Bouchard, G., Roy, R., Casgrain, B. & Hubert, M. in From Information to Knowledge: Conceptual and Content Analyses by Computer (eds Nissan, E. & Schmidt, K.) 201–227 (Intellect, Oxford, 1995)
Lummaa, V. & Tremblay, M. Month of birth predicted reproductive success and fitness in pre-modern Canadian women. Proc. R. Soc. Lond. B 270, 2355–2361 (2003)
Schall, R. Estimation of generalized linear models with random effects. Biometrika 78, 719–727 (1991)
Littell, R. C., Milliken, G. A., Stroup, W. W. & Wolfinger, R. D. SAS System for Mixed Models (SAS Institute Inc, Cary, 1996)
Acknowledgements
We are grateful to T. Clutton-Brock, N. Davies, B. Hatchwell, E. Haukioja, J. Jokela and R. Kilner for comments, T. Coulson for help with calculating individual λ values, and K. Pokkinen, A. Siitonen and T. Verho for collecting the Finnish demographic data. We also thank the Royal Society, UK (V.L. and A.F.R.), Academy of Finland (V.L.), Wihuri Foundation (M.L.), Emil Aaltonen Foundation (S.H.) and Social Sciences and Humanities Research Council of Canada (M.T.) for funding.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing financial interests.
Rights and permissions
About this article
Cite this article
Lahdenperä, M., Lummaa, V., Helle, S. et al. Fitness benefits of prolonged post-reproductive lifespan in women. Nature 428, 178–181 (2004). https://doi.org/10.1038/nature02367
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature02367
This article is cited by
-
Grandparental Support and Maternal Postpartum Mental Health
Human Nature (2023)
-
Host age structure reshapes parasite symbiosis: collaboration begets pathogens, competition begets virulent mutualists
Biology Direct (2022)
-
The interplay of grandparental investment according to the survival status of other grandparent types
Scientific Reports (2022)
-
Human Females as a Dispersal-Egalitarian Species: A Hypothesis about Women and Status
Adaptive Human Behavior and Physiology (2022)
-
The Overloaded Mother
Archives of Sexual Behavior (2022)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.