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Measuring selection for genes that promote long life in a historical human population

Nature Ecology & Evolution volume 1, pages 1773–1781 (2017)Cite this article

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Abstract

The unusually long lifespans of humans and the persistence of post-reproductive lifespans in women represent evolutionary puzzles because natural selection cannot directly favour continued living in post-menopausal women or elderly men. Suggested sources of indirect selection require genetic correlations between fitness and survival or reproduction at younger ages, reproduction in the opposite sex, or late-life contributions to offspring or grandoffspring fitness. Here we apply quantitative genetic analyses to data from a historical human population to explicitly test these evolutionary genetic hypotheses. Total genetic selection increased the male post-50 lifespans by 0.138 years per generation; 94% of this arose from indirect selection acting to favour early-life fitness in both sexes. These results argue strongly against life-history models of ageing that depend on trade-offs between reproduction and late-life survival. No source of indirect selection for female post-50 lifespan was detected, deepening the mystery of why female post-reproductive survival persists. This result is probably due to recent changes in the genetic architecture of female lifespan, and it highlights the need for similar quantitative genetic analyses of human populations at other points along demographic transitions.

Natural selection favours increased lifespans whenever continued living is expected to yield future reproductive dividends, and this expectation declines with advancing age in humans of both sexes1. In males, the prevailing assumption is that late-life reproduction selects for late-life survival2, but this hypothesis remains untested and males often succeed in living long beyond the last ages of male reproduction3. In females, the late-life attenuation of phenotypic selection is more extreme, as menopause reduces this selective force to zero in middle age. Nevertheless, even women in primitive hunter–gatherer and horticultural populations can live many decades post-menopause4,5,6 in apparent violation of simple evolutionary predictions that late-acting deleterious mutations should accumulate unchecked7 (or even aided8) by natural selection. While there is controversy regarding the precise mechanisms for the genesis of post-reproductive lifespans9,10,11, evolutionary theory requires that its continued persistence must be explained by selection for traits with which it is genetically correlated (indirect selection).

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Fig. 1: Causal diagram of hypothesized pathways by which selection for sex-specific lifespan beyond female post-reproductive age Y could act.

References

  1. Hamilton, W. D. Moulding of senescence by natural selection. J. Theor. Biol. 12, 12–45 (1966).

    Article  CAS  PubMed  Google Scholar 

  2. Tuljapurkar, S., Puleston, C. O. & Gurven, M. D. Why men matter: mating patterns drive evolution of human lifespan. PLoS ONE 2, e785 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Vinicius, L., Mace, R. & Migliano, A. Variation in male reproductive longevity across traditional societies. PLoS ONE 9, e112236 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hawkes, K., O’Connell, J. F. & Jones, N. G. B. Hadza women’s time allocation, offspring provisioning, and the evolution of long postmenopausal life spans. Curr. Anthropol. 38, 551–577 (1997).

    Article  Google Scholar 

  5. Hawkes, K., O’Connell, J. F., Jones, N. G. B., Alvarez, H. & Charnov, E. L. Grandmothering, menopause, and the evolution of human life histories. Proc. Natl Acad. Sci. USA 95, 1336–1339 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lancaster, J. B. & King, B. J. in In Her Prime (eds. Kerns, V. & Brown, J. K.) 264 (Univ. Illinois Press, Urbana and Chicago, IL, 1992).

    Google Scholar 

  7. Medawar, P. B. An Unsolved Problem of Biology (H. K. Lewis & Co, London, 1952).

  8. Williams, G. C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398–411 (1957).

    Article  Google Scholar 

  9. Croft, D. P., Brent, L. J. N., Franks, D. W. & Cant, M. A. The evolution of prolonged life after reproduction. Trends Ecol. Evol. 30, 407–416 (2015).

    Article  PubMed  Google Scholar 

  10. Hawkes, K. & Coxworth, J. E. Grandmothers and the evolution of human longevity: a review of findings and future directions. Evol. Anthr. 22, 294–302 (2013).

    Article  Google Scholar 

  11. Levitis, D. A., Burger, O. & Lackey, L. B. The human post-fertile lifespan in comparative evolutionary context. Evol. Anthr. 22, 66–79 (2013).

    Article  Google Scholar 

  12. Charlesworth, B. Patterns of age-specific means and genetic variances of mortality rates predicted by the mutation-accumulation theory of ageing. J. Theor. Biol. 210, 47–65 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Marlowe, F. W. The patriarch hypothesis—an alternative explanation of menopause. Hum. Nat. 11, 27–42 (2000).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  15. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wolf, J. B., Brodie, E. D., Cheverud, J. M., Moore, A. J. & Wade, M. J. Evolutionary consequences of indirect genetic effects. Trends Ecol. Evol. 13, 64–69 (1998).

    Article  CAS  PubMed  Google Scholar 

  17. Lahdenpera, M., Lummaa, V., Helle, S., Tremblay, M. & Russell, A. F. Fitness benefits of prolonged post-reproductive lifespan in women. Nature 428, 178–181 (2004).

    Article  CAS  PubMed  Google Scholar 

  18. Lynch, M. & Walsh, J. B. Genetics and Analysis of Quantitative Traits (Sinauer Associates, Sunderland, MA, 1998).

    Google Scholar 

  19. Milot, E. et al. Evidence for evolution in response to natural selection in a contemporary human population. Proc. Natl Acad. Sci. USA 108, 17040–17045 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Pettay, J. E., Kruuk, L. E. B., Jokela, J. & Lummaa, V. Heritability and genetic constraints of life-history trait evolution in preindustrial humans. Proc. Natl Acad. Sci. USA 102, 2838–2843 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Lande, R. Quantitative genetic-analysis of multivariate evolution, applied to brain–body size allometry. Evolution 33, 402–416 (1979).

    Article  PubMed  Google Scholar 

  22. Gosden, R. G. Biology of Menopause: the Causes and Consequences of Ovarian Ageing (Academic Press, London, 1985).

    Google Scholar 

  23. Bean, L. L., Mineau, G. & Anderton, D. Fertility Change on the American Frontier (Univ. California Press, Berkeley, CA, 1990).

    Google Scholar 

  24. Moorad, J. A. A demographic transition altered the strength of selection for fitness and age-specific survival and fertility in a 19th century American population. Evolution 67, 1622–1634 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Merila, J. & Sheldon, B. C. Lifetime reproductive success and heritability in nature. Am. Nat. 155, 301–310 (2000).

    Article  CAS  PubMed  Google Scholar 

  26. Foerster, K. et al. Sexually antagonistic genetic variation for fitness in red deer. Nature 447, 1107–1110 (2007).

    Article  CAS  PubMed  Google Scholar 

  27. Morrissey, M. B. et al. The prediction of adaptive evolution: empirical application of the secondary theorem of selection and comparison to the Breeder’s Equation. Evolution 66, 2399–2410 (2012).

    Article  PubMed  Google Scholar 

  28. McCleery, R. H. et al. Components of variance underlying fitness in a natural population of the great tit Parus major. Am. Nat. 164, E62–E72 (2004).

    Article  CAS  PubMed  Google Scholar 

  29. Herskind, A. M. et al. The heritability of human longevity: a population-based study of 2872 Danish twin pairs born 1870–1900. Hum. Genet. 97, 319–323 (1996).

    Article  CAS  PubMed  Google Scholar 

  30. McGue, M., Vaupel, J. W., Holm, N. & Harvald, B. Longevity is moderately heritable in a sample of Danish twins born 1870–1880. J. Gerontol. 48, B237–B244 (1993).

    Article  CAS  PubMed  Google Scholar 

  31. Hamilton, W. D. Genetical evolution of social behaviour I. J. Theor. Biol. 7, 1–16 (1964).

    Article  CAS  PubMed  Google Scholar 

  32. Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. Evolution 37, 1210–1226 (1983).

    Article  PubMed  Google Scholar 

  33. Hill, K. & Hurtado, A. M. Aché Life History: the Ecology and Demography of a Foraging People (Aldine de Gruyter, New York, 1996).

    Google Scholar 

  34. Hill, K., Hurtado, A. M. & Walker, R. S. High adult mortality among Hiwi hunter–gatherers: implications for human evolution. J. Hum. Evol. 52, 443–454 (2007).

    Article  PubMed  Google Scholar 

  35. Marlowe, F. W. Hadza: Hunter–Gatherers of Tanzania (Univ. California Press, Berkeley, CA, 2010).

    Google Scholar 

  36. Bean, L. L., Smith, K. R., Mineau, G. P. & Fraser, A. Infant deaths in Utah, 1850–1939. Utah Hist. Q. 70, 158–173 (2002).

    Google Scholar 

  37. Sgro, C. M. & Hoffmann, A. A. Genetic correlations, tradeoffs and environmental variation. Heredity 93, 241–248 (2004).

    Article  CAS  PubMed  Google Scholar 

  38. Reznick, D., Nunney, L. & Tessier, A. Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol. Evol. 15, 421–425 (2000).

    Article  CAS  PubMed  Google Scholar 

  39. Moorad, J. Review of Sociality, Hierarchy, Health: Comparative Biodemography: A Collection of Papers, edited by M. Weinstein and M. A. Lane. Evol. Med. Public Health 2016, 67–68 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Bronikowski, A. M. et al. Aging in the natural world: comparative data reveal similar mortality patterns across primates. Science 331, 1325–1328 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Charnov, E. L. & Berrigan, D. Why do primates have such long life spans and so few babies? Evol. Anthropol. 1, 191–194 (1993).

    Article  Google Scholar 

  42. Jones, O. R. et al. Diversity of ageing across the tree of life. Nature 505, 169–173 (2014).

    Article  CAS  PubMed  Google Scholar 

  43. Kirkwood, T. B. Evolution of ageing. Nature 270, 301–304 (1977).

    Article  CAS  PubMed  Google Scholar 

  44. Kirkwood, T. B. L. Evolution of ageing. Mech. Ageing Dev. 123, 737–745 (2002).

    Article  PubMed  Google Scholar 

  45. Rose, M. R. & Charlesworth, B. Genetics of life-history in Drosophila melanogaster. I. Sib analysis of adult females. Genetics 97, 172–186 (1981).

    Google Scholar 

  46. Charlesworth, B. Evolution in Age-structured Populations. (Cambridge Univ. Press, Cambridge, UK, 1994).

    Book  Google Scholar 

  47. Vaupel, J. W. et al. Biodemographic trajectories of longevity. Science 280, 855–860 (1998).

    Article  CAS  PubMed  Google Scholar 

  48. Chen, H. Y. & Maklakov, A. A. Longer life span evolves under high rates of condition-dependent mortality. Curr. Biol. 22, 2140–2143 (2012).

    Article  CAS  PubMed  Google Scholar 

  49. Kimber, C. M. & Chippindale, A. K. Mutation, condition, and the maintenance of extended lifespan in Drosophila. Curr. Biol. 23, 2283–2287 (2013).

    Article  CAS  PubMed  Google Scholar 

  50. Reynolds, R. M. et al. Age specificity of inbreeding load in Drosophila melanogaster and implications for the evolution of late-life mortality plateaus. Genetics 177, 587–595 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Moorad, J. A., Promislow, D. E. L., Smith, K. R. & Wade, M. J. Mating system change reduces the strength of sexual selection in an American frontier population of the 19th century. Evol. Hum. Behav. 32, 147–155 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Smith, K. R., Garibotti, G., Fraser, A. & Mineau, G. P. Adult mortality and geographical proximity of parents in Utah in the 19th and 20th centuries. In Symp. Kinship Demographic Behavior (International Union for the Scientific Study of Population, Paris, France, 2005). 

  53. Mineau, G. P. & Anderton, D. L. Household formation systems and the role of proximate kin. In 52nd Annual Meeting of the Population Association of America (Population Association of America, Chicago, IL, 1987).

  54. Moorad, J. A. Individual fitness and phenotypic selection in age-structured populations with constant growth rates. Ecology 95, 1087–1095 (2014).

    Article  PubMed  Google Scholar 

  55. Moorad, J. A. & Wade, M. J. Selection gradients, the opportunity for selection, and the coefficient of determination. Am. Nat. 181, 291–300 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Moorad, J. A. Multi-level sexual selection: individual and family-level selection for mating success in a historical human population. Evolution 67, 1635–1648 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Sorensen, T. I. A., Nielsen, G. G., Andersen, P. K. & Teasdale, T. W. Genetic and environmental-influences on premature death in adult adoptees. N. Engl. J. Med. 318, 727–732 (1988).

    Article  CAS  PubMed  Google Scholar 

  58. Kerber, R. A., O’Brien, E., Smith, K. R. & Cawthon, R. M. Familial excess longevity in Utah genealogies. J. Gerontol. A Biol. Sci. Med. Sci. 56, B130–B139 (2001).

    Article  CAS  PubMed  Google Scholar 

  59. Perls, T. T., Bubrick, E., Wager, C. G., Vijg, J. & Kruglyak, L. Siblings of centenarians live longer. Lancet 351, 1560 (1998).

    Article  CAS  PubMed  Google Scholar 

  60. Schoenmaker, M. et al. Evidence of genetic enrichment for exceptional survival using a family approach: the Leiden Longevity Study. Eur. J. Hum. Genet. 14, 79–84 (2006).

    Article  PubMed  Google Scholar 

  61. Kruuk, L. E. B. Estimating genetic parameters in natural populations using the ‘animal model’. Phil. Trans. R. Soc. B 359, 873–890 (2004).

    Article  Google Scholar 

  62. Gogel, B. J., Gilmour, A. R., Welham, S. J., Cullis, B. R. & Thompson, R. ASReml (VSN International, Hemel Hempstead, 2015).

    Google Scholar 

  63. Lerner, I. M. The Genetic Basis of Selection (Wiley, New York, 1958).

    Google Scholar 

  64. Lush, J. L. Animal Breeding Plans (Iowa State Press, Ames, IA, 1937).

    Google Scholar 

  65. Price, G. R. Selection and covariance. Nature 227, 520–521 (1970).

    Article  CAS  PubMed  Google Scholar 

  66. Robertson, A. A mathematical model of culling process in dairy cattle. Animal Production 8, 95–108 (1966).

    Google Scholar 

  67. Rausher, M. D. The measurement of selection on quantitative traits—biases due to environmental covariances between traits and fitness. Evolution 46, 616–626 (1992).

    Article  PubMed  Google Scholar 

  68. Morrissey, M. B., Kruuk, L. E. B. & Wilson, A. J. The danger of applying the breeder’s equation in observational studies of natural populations. J. Evol. Biol. 23, 2277–2288 (2010).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the Pedigree and Population Resource of the Huntsman Cancer Institute, University of Utah (funded in part by the Huntsman Cancer Foundation) for its role in the ongoing compilation, maintenance and support of the Utah Population Database. We also thank K. Smith for providing the data used in this study. C.A.W. was funded by a Natural Environment Research Council postdoctoral fellowship (NE/I020245/1) and a University of Edinburgh Chancellor’s fellowship. We thank A. Gilmour, J. Hadfield and A. Wilson for helpful technical advice. Comments from J. Pemberton, L. Kruuk, D. Nussey, P. Smiseth and B. Whittaker greatly improved the paper.

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  1. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EH9 3FL, UK

    Jacob A. Moorad & Craig A. Walling

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J.A.M. conceived the study. J.A.M. and C.A.W. contributed to its design, analysis and wrote the paper.

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Correspondence to Jacob A. Moorad.

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Moorad, J.A., Walling, C.A. Measuring selection for genes that promote long life in a historical human population. Nat Ecol Evol 1, 1773–1781 (2017). https://doi.org/10.1038/s41559-017-0329-x

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