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

Nature volume 502, pages 93–95 (2013)Cite this article

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Abstract

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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Figure 1: Horn morphology variation with RXFP2 genotype.
Figure 2: Annual fitness variation and RXFP2 genotype.

References

  1. Pomiankowski, A. & Møller, A. P. A resolution of the lek paradox. Proc. R. Soc. Lond. B 260, 21–29 (1995)

    Article  ADS  Google Scholar 

  2. Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001)

    Article  CAS  Google Scholar 

  3. Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics (Longman, 1996)

    Google Scholar 

  4. Promislow, D. E. L. Costs of sexual selection in natural populations of mammals. Proc. R. Soc. Lond. B 247, 203–210 (1992)

    Article  ADS  Google Scholar 

  5. Bonduriansky, R. & Chenoweth, S. F. Intralocus sexual conflict. Trends Ecol. Evol. 24, 280–288 (2009)

    Article  Google Scholar 

  6. 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)

    Article  Google Scholar 

  7. 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)

    Article  ADS  Google Scholar 

  8. Tomkins, J. L., Radwan, J., Kotiaho, J. S. & Tregenza, T. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19, 323–328 (2004)

    Article  Google Scholar 

  9. 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)

    Article  CAS  ADS  Google Scholar 

  10. Andersson, M. Sexual Selection (Princeton Univ. Press, 1994)

    Google Scholar 

  11. 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)

    Article  Google Scholar 

  12. Chenoweth, S. F. & McGuigan, K. The genetic basis of sexually selected variation. Annu. Rev. Ecol. Evol. Syst. 41, 81–101 (2010)

    Article  Google Scholar 

  13. Stapley, J. et al. Adaptation genomics: the next generation. Trends Ecol. Evol. 25, 705–712 (2010)

    Article  Google Scholar 

  14. Slate, J. et al. Genome mapping in intensively studied wild vertebrate populations. Trends Genet. 26, 275–284 (2010)

    Article  CAS  Google Scholar 

  15. Ellegren, H. & Sheldon, B. C. Genetic basis of fitness differences in natural populations. Nature 452, 169–175 (2008)

    Article  CAS  ADS  Google Scholar 

  16. 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)

    Article  Google Scholar 

  17. 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)

    Article  CAS  Google Scholar 

  18. 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)

    Article  Google Scholar 

  19. 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)

    Article  CAS  Google Scholar 

  20. Hedrick, P. Genetics of Populations (Jones and Bartlett, 2005)

    Google Scholar 

  21. 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)

    Article  Google Scholar 

  22. Allison, A. Protection afforded by sickle-cell trait against subtertian malarial infection. Br. Med. J. 1, 290–294 (1954)

    Article  CAS  Google Scholar 

  23. 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)

    Article  CAS  Google Scholar 

  24. Gemmell, N. J. & Slate, J. Heterozygote advantage for fecundity. PLoS ONE 1, e125 (2006)

    Article  ADS  Google Scholar 

  25. Grubb, P. Island Survivors: the Ecology of the Soay Sheep of St Kilda, Ch. 8, 195–223 (Athlone Press, 1974)

  26. 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)

    Google Scholar 

  27. Chessa, B. et al. Revealing the history of sheep domestication using retrovirus integrations. Science 324, 532–536 (2009)

    Article  CAS  ADS  Google Scholar 

  28. Kijas, J. W. et al. A genome wide survey of SNP variation reveals the genetic structure of sheep breeds. PLoS ONE 4, e4668 (2009)

    Article  ADS  Google Scholar 

  29. Hadfield, J. MCMC methods for multi-response Generalized Linear Mixed Models: The MCMCglmm R Package. J. Stat. Softw. 33, 1–22 (2010)

    Article  Google Scholar 

  30. Gratten, J. et al. Selection and microevolution of coat pattern are cryptic in a wild population of sheep. Mol. Ecol. 21, 2977–2990 (2012)

    Article  CAS  Google Scholar 

  31. 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)

    Article  CAS  Google Scholar 

  32. 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)

    Article  CAS  Google Scholar 

  33. 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)

    Article  CAS  Google Scholar 

  34. Kenta, T. et al. Multiplex SNP-SCALE: a cost-effective medium-throughput single nucleotide polymorphism genotyping method. Mol. Ecol. Resour. 8, 1230–1238 (2008)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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.

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Author notes

  1. Susan E. Johnston & Jacob Gratten

    Present address: 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.).,

Authors and 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

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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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Correspondence to Susan E. Johnston or Jon Slate.

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The authors declare no competing financial interests.

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Supplementary Information

This file contains Supplementary Figures 1-7, Supplementary Notes 1 – 3 and Supplementary Tables 1-10. This file was replaced on 7 August 2014. (PDF 1063 kb)

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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

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