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Sexually antagonistic genetic variation for fitness in red deer

Nature volume 447, pages 1107–1110 (2007)Cite this article

Abstract

Evolutionary theory predicts the depletion of genetic variation in natural populations as a result of the effects of selection, but genetic variation is nevertheless abundant for many traits that are under directional or stabilizing selection1. Evolutionary geneticists commonly try to explain this paradox with mechanisms that lead to a balance between mutation and selection2. However, theoretical predictions of equilibrium genetic variance under mutation–selection balance are usually lower than the observed values, and the reason for this is unknown3. The potential role of sexually antagonistic selection in maintaining genetic variation has received little attention in this debate, surprisingly given its potential ubiquity in dioecious organisms. At fitness-related loci, a given genotype may be selected in opposite directions in the two sexes. Such sexually antagonistic selection will reduce the otherwise-expected positive genetic correlation between male and female fitness4. Both theory5,6,7 and experimental data8,9,10,11,12 suggest that males and females of the same species may have divergent genetic optima, but supporting data from wild populations are still scarce13,14,15. Here we present evidence for sexually antagonistic fitness variation in a natural population, using data from a long-term study of red deer (Cervus elaphus). We show that male red deer with relatively high fitness fathered, on average, daughters with relatively low fitness. This was due to a negative genetic correlation between estimates of fitness in males and females. In particular, we show that selection favours males that carry low breeding values for female fitness. Our results demonstrate that sexually antagonistic selection can lead to a trade-off between the optimal genotypes for males and females; this mechanism will have profound effects on the operation of selection and the maintenance of genetic variation in natural populations.

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Figure 1: Sex-specific parent–offspring regressions of observed fitness in red deer.
Figure 2: Selection on opposite-sex breeding values of annual fitness in males and females.

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Acknowledgements

We thank F. Guinness, A. Donald, S. Morris and many other project field workers; K. Connaghan, K. Byrne, S. Lewis, D. Nussey and J. Slate for genotyping work; and D. Nussey and A. Wilson for comments on earlier drafts of the manuscript. We thank Scottish Natural Heritage for permission to work on the Isle of Rum and their local staff for help and support. This work was funded by the Natural Environment Research Council, the Royal Society, and a Marie Curie European Fellowship.

Author Contributions The idea for this study originated from discussions between L.E.B.K., B.C.S. and K.F. The data used stem from a long-term study run by T.H.B.C., with involvement from L.E.B.K. and J.M.P.; J.M.P. was also responsible for the molecular paternity analysis. K.F. conducted all data analyses and drafted the manuscript. L.K. helped with the quantitative genetics analyses, and T.C. helped in applying the de-lifing approach. All authors discussed the results and commented on the manuscript.

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Authors and Affiliations

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

    Katharina Foerster, Josephine M. Pemberton & Loeske E. B. Kruuk

  2. Division of Biology and Centre for Population Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7PY, UK,

    Tim Coulson

  3. Department of Zoology, Edward Grey Institute, University of Oxford, Oxford OX1 3PS, UK,

    Ben C. Sheldon

  4. Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK,

    Tim H. Clutton-Brock

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  1. Katharina Foerster
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  2. Tim Coulson
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  5. Tim H. Clutton-Brock
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Correspondence to Katharina Foerster or Loeske E. B. Kruuk.

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Supplementary information

Supplementary Information 1

This file contains Supplementary Notes with the analysis of lifetime reproductive success (LRS), a more traditional fitness measure. The Supplementary Table S1 presents variance components, heritability, coefficients of additive genetic variation, and the inter-sexual genetic correlation of LRS. These results are compared with those obtained for the de-lifing measure pt(i). (PDF 98 kb)

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Foerster, K., Coulson, T., Sheldon, B. et al. Sexually antagonistic genetic variation for fitness in red deer. Nature 447, 1107–1110 (2007). https://doi.org/10.1038/nature05912

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