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

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.

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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.

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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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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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