Life history trade-offs at a single locus maintain sexually selected genetic variation

Journal name:
Nature
Volume:
502,
Pages:
93–95
Date published:
DOI:
doi:10.1038/nature12489
Received
Accepted
Published online

Sexual selection, through intra-male competition or female choice, is assumed to be a source of strong and sustained directional selection in the wild1, 2. In the presence of such strong directional selection, alleles enhancing a particular trait are predicted to become fixed within a population, leading to a decrease in the underlying genetic variation3. However, there is often considerable genetic variation underlying sexually selected traits in wild populations, and consequently, this phenomenon has become a long-discussed issue in the field of evolutionary biology1, 4, 5. In wild Soay sheep, large horns confer an advantage in strong intra-sexual competition, yet males show an inherited polymorphism for horn type and have substantial genetic variation in their horn size6. Here we show that most genetic variation in this trait is maintained by a trade-off between natural and sexual selection at a single gene, relaxin-like receptor 2 (RXFP2). We found that an allele conferring larger horns, Ho+, is associated with higher reproductive success, whereas a smaller horn allele, HoP, confers increased survival, resulting in a net effect of overdominance (that is, heterozygote advantage) for fitness at RXFP2. The nature of this trade-off is simple relative to commonly proposed explanations for the maintenance of sexually selected traits, such as genic capture7, 8 (‘good genes’) and sexually antagonistic selection5, 9. Our results demonstrate that by identifying the genetic architecture of trait variation, we can determine the principal mechanisms maintaining genetic variation in traits under strong selection and explain apparently counter-evolutionary observations.

At a glance

Figures

  1. Horn morphology variation with RXFP2 genotype.
    Figure 1: Horn morphology variation with RXFP2 genotype.

    Examples of adult male horn morphology with their corresponding RXFP2 genotypes. a, Four-year-old normal-horned Ho+Ho+. b, Five-year-old normal-horned Ho+HoP. c, Five-year-old normal-horned HoPHoP. d, Three-year-old scurred HoPHoP.

  2. Annual fitness variation and RXFP2 genotype.
    Figure 2: Annual fitness variation and RXFP2 genotype.

    a, Reproductive success in adult males (n = 640). b, Survival in all males (n = 1,243). c, Overall fitness in all males (n = 1,204). Effect sizes were estimated from the posterior mode of a MCMC generalized linear mixed model and are given relative to the model intercept at Ho+Ho+. Vertical bars indicate the 95% credible interval. The single asterisk and double asterisk indicate a significant difference from the intercept at Ho+Ho+ at PMCMC = 0.05 and 0.01, respectively; single and double daggers indicate the same for the model intercept at Ho+HoP.

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Author information

Affiliations

  1. Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK

    • Susan E. Johnston,
    • Jacob Gratten &
    • Jon Slate
  2. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK

    • Susan E. Johnston,
    • Camillo Berenos,
    • Jill G. Pilkington &
    • Josephine M. Pemberton
  3. Queensland Brain Institute, University of Queensland, Brisbane 4072, Australia

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

    • Tim H. Clutton-Brock
  5. Present addresses: Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK (S.E.J.); Queensland Brain Institute, University of Queensland, Brisbane 4072, Australia (J.G.).

    • Susan E. Johnston &
    • Jacob Gratten

Contributions

J.G.P., T.H.C.-B. and J.M.P. organized the long-term collection of phenotypic data and DNA samples. S.E.J. and J.S. designed the study. S.E.J., C.B. and J.G. performed laboratory work and C.B. constructed the pedigree. S.E.J. and J.G. analysed the data. S.E.J. and J.S. wrote the paper and all authors contributed to revisions.

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The authors declare no competing financial interests.

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