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.
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We thank the numerous Soay sheep project members and volunteers for collection of data and samples; M. Robinson, J. Hadfield, D. Childs and D. Nussey for statistical advice and discussions; J. McEwan, N. Pickering and J. Kijas for SNP information; D. Beraldi, E. Brown and P. Ellis for laboratory assistance; L. Evenden, J. Gibson and L. Murphy at the Wellcome Trust Clinical Research Facility Genetics Core for genome-wide SNP genotypes; I. Stevenson for database development; G. Prior and A. Ozgul for images; National Trust for Scotland and Scottish Natural Heritage for permission to work on St Kilda; and QinetiQ and Eurest for logistical support. The Soay sheep project is funded by the Natural Environment Research Council (NERC). SNP genotyping was funded by NERC and the European Research Council (ERC). S.E.J. was funded by a Biotechnology and Biological Sciences Research Council CASE studentship.
This zipped file contains the source data for Supplementary Figures 2 - 7.
About this article
Nature Reviews Genetics (2019)