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.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Pomiankowski, A. & Møller, A. P. A resolution of the lek paradox. Proc. R. Soc. Lond. B 260, 21–29 (1995)
Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001)
Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics (Longman, 1996)
Promislow, D. E. L. Costs of sexual selection in natural populations of mammals. Proc. R. Soc. Lond. B 247, 203–210 (1992)
Bonduriansky, R. & Chenoweth, S. F. Intralocus sexual conflict. Trends Ecol. Evol. 24, 280–288 (2009)
Johnston, S. E. et al. Genome-wide association mapping identifies the genetic basis of discrete and quantitative variation in sexual weaponry in a wild sheep population. Mol. Ecol. 20, 2555–2566 (2011)
Rowe, L. & Houle, D. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. Lond. B 263, 1415–1421 (1996)
Tomkins, J. L., Radwan, J., Kotiaho, J. S. & Tregenza, T. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19, 323–328 (2004)
Chippindale, A. K., Gibson, J. R. & Rice, W. R. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl Acad. Sci. USA 98, 1671–1675 (2001)
Andersson, M. Sexual Selection (Princeton Univ. Press, 1994)
Kruuk, L. E. B., Slate, J. & Wilson, A. J. New answers for old questions: the evolutionary quantitative genetics of wild animal populations. Annu. Rev. Ecol. Evol. Syst. 39, 525–548 (2008)
Chenoweth, S. F. & McGuigan, K. The genetic basis of sexually selected variation. Annu. Rev. Ecol. Evol. Syst. 41, 81–101 (2010)
Stapley, J. et al. Adaptation genomics: the next generation. Trends Ecol. Evol. 25, 705–712 (2010)
Slate, J. et al. Genome mapping in intensively studied wild vertebrate populations. Trends Genet. 26, 275–284 (2010)
Ellegren, H. & Sheldon, B. C. Genetic basis of fitness differences in natural populations. Nature 452, 169–175 (2008)
Robinson, M. R., Pilkington, J. G., Clutton-Brock, T. H., Pemberton, J. M. & Kruuk, L. E. B. Live fast, die young: trade-offs between fitness components and sexually antagonistic selection on weaponry in Soay sheep. Evolution 60, 2168–2181 (2006)
Preston, B. T., Stevenson, I. R., Pemberton, J. M., Coltman, D. W. & Wilson, K. Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proc. R. Soc. Lond. B 270, 633–640 (2003)
Dominik, S., Henshall, J. M. & Hayes, B. J. A single nucleotide polymorphism on chromosome 10 is highly predictive for the polled phenotype in Australian Merino sheep. Anim. Genet. 43, 468–470 (2011)
Kijas, J. W. et al. Genome-wide analysis of the world’s sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biol. 10, e1001258 (2012)
Hedrick, P. Genetics of Populations (Jones and Bartlett, 2005)
Connallon, T. & Clark, A. G. A general population genetic framework for antagonistic selection that accounts for demography and recurrent mutation. Genetics 190, 1477–1489 (2012)
Allison, A. Protection afforded by sickle-cell trait against subtertian malarial infection. Br. Med. J. 1, 290–294 (1954)
Greaves, J. H., Redfern, R., Ayres, P. B. & Gill, J. E. Warfarin resistance: a balanced polymorphism in the Norway rat. Genet. Res. 30, 257–263 (1977)
Gemmell, N. J. & Slate, J. Heterozygote advantage for fecundity. PLoS ONE 1, e125 (2006)
Grubb, P. Island Survivors: the Ecology of the Soay Sheep of St Kilda, Ch. 8, 195–223 (Athlone Press, 1974)
Stevenson, I. R., Marrow, B., Preston, B. T., Pemberton, J. M. & Wilson, K. Soay Sheep: Dynamics and Selection in an Island Population, Ch. 9 243–275 (Cambridge Univ. Press, 2004)
Chessa, B. et al. Revealing the history of sheep domestication using retrovirus integrations. Science 324, 532–536 (2009)
Kijas, J. W. et al. A genome wide survey of SNP variation reveals the genetic structure of sheep breeds. PLoS ONE 4, e4668 (2009)
Hadfield, J. MCMC methods for multi-response Generalized Linear Mixed Models: The MCMCglmm R Package. J. Stat. Softw. 33, 1–22 (2010)
Gratten, J. et al. Selection and microevolution of coat pattern are cryptic in a wild population of sheep. Mol. Ecol. 21, 2977–2990 (2012)
Purcell, S. et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007)
Hadfield, J. D., Richardson, D. S. & Burke, T. Towards unbiased parentage assignment: combining genetic, behavioural and spatial data in a Bayesian framework. Mol. Ecol. 15, 3715–3730 (2006)
Hayward, A. D. et al. Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal. J. Evol. Biol. 24, 1664–1676 (2011)
Kenta, T. et al. Multiplex SNP-SCALE: a cost-effective medium-throughput single nucleotide polymorphism genotyping method. Mol. Ecol. Resour. 8, 1230–1238 (2008)
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.
The authors declare no competing financial interests.
About this article
Cite this article
Johnston, S., Gratten, J., Berenos, C. et al. Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature 502, 93–95 (2013). https://doi.org/10.1038/nature12489
Absence of reproduction-immunity trade-off in male Drosophila melanogaster evolving under differential sexual selection
BMC Evolutionary Biology (2020)
Consequences of Single-Locus and Tightly Linked Genomic Architectures for Evolutionary Responses to Environmental Change
Journal of Heredity (2020)
An 85K SNP Array Uncovers Inbreeding and Cryptic Relatedness in an Antarctic Fur Seal Breeding Colony
G3&#58; Genes|Genomes|Genetics (2020)
Conspicuous colours in a polymorphic orb-web spider: evidence of predator avoidance but not prey attraction
Animal Behaviour (2020)
Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon
PLOS Genetics (2020)