Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Sexually antagonistic genetic variation for fitness in red deer

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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.

References

  1. Merila, J., Sheldon, B. C. & Kruuk, L. E. B. Explaining stasis: microevolutionary studies in natural populations. Genetica 112, 199–222 (2001)

    Article  Google Scholar 

  2. Barton, N. H. & Keightley, P. D. Understanding quantitative genetic variation. Nature Rev. Genet. 3, 11–21 (2002)

    CAS  Article  Google Scholar 

  3. Turelli, M. & Barton, N. H. Polygenic variation maintained by balancing selection: Pleiotropy, sex-dependent allelic effects and G × E interactions. Genetics 166, 1053–1079 (2004)

    Article  Google Scholar 

  4. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer, Sunderland, Massachusetts, 1998)

    Google Scholar 

  5. Hedrick, P. W. Antagonistic pleiotropy and genetic polymorphism: a perspective. Heredity 82, 126–133 (1999)

    Article  Google Scholar 

  6. Rice, W. R. & Chippindale, A. K. Intersexual ontogenetic conflict. J. Evol. Biol. 14, 685–693 (2001)

    Article  Google Scholar 

  7. Rice, W. R. Sex chromosomes and the evolution of sexual dimorphism. Evolution Int. J. Org. Evolution 38, 735–742 (1984)

    Article  Google Scholar 

  8. 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)

    ADS  CAS  Article  Google Scholar 

  9. Fedorka, K. M. & Mousseau, T. A. Female mating bias results in conflicting sex-specific offspring fitness. Nature 429, 65–67 (2004)

    ADS  CAS  Article  Google Scholar 

  10. Rice, W. R. Sexually antagonistic genes: experimental evidence. Science 256, 1436–1439 (1992)

    ADS  CAS  Article  Google Scholar 

  11. Gibson, J. R., Chippindale, A. K. & Rice, W. R. The X chromosome is a hot spot for sexually antagonistic fitness variation. Proc. R. Soc. Lond. B 269, 499–505 (2002)

    Article  Google Scholar 

  12. Meagher, T. R. The quantitative genetics of sexual dimorphism in Silene latifolia (Caryophyllaceae). 1. Genetic variation. Evolution Int. J. Org. Evolution 46, 445–457 (1992)

    Article  Google Scholar 

  13. Forsman, A. Opposing fitness consequences of colour pattern in male and female snakes. J. Evol. Biol. 8, 53–70 (1995)

    Article  Google Scholar 

  14. Calsbeek, R. & Sinervo, B. Within-clutch variation in offspring sex determined by differences in sire body size: cryptic mate choice in the wild. J. Evol. Biol. 17, 464–470 (2004)

    Article  Google Scholar 

  15. 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 Int. J. Org. Evolution 60, 2168–2181 (2006)

    Article  Google Scholar 

  16. Rice, W. R. Dangerous liaisons. Proc. Natl Acad. Sci. USA 97, 12953–12955 (2000)

    ADS  CAS  Article  Google Scholar 

  17. Coulson, T. et al. Estimating individual contributions to population growth: evolutionary fitness in ecological time. Proc. R. Soc. Lond. B 273, 547–555 (2006)

    CAS  Google Scholar 

  18. Sokal, R. R. & Rohlf, F. J. Biometry 3rd edn (Freeman, New York, 1995)

    MATH  Google Scholar 

  19. Kruuk, L. E. B. Estimating genetic parameters in natural populations using the ‘animal model’. Phil. Trans. R. Soc. Lond. B 359, 873–890 (2004)

    Article  Google Scholar 

  20. Kruuk, L. E. B. et al. Heritability of fitness in a wild mammal population. Proc. Natl Acad. Sci. USA 97, 698–703 (2000)

    ADS  CAS  Article  Google Scholar 

  21. Houle, D. Comparing evolvability and variability of quantitative traits. Genetics 130, 195–204 (1992)

    CAS  Article  Google Scholar 

  22. Kruuk, L. E. B. et al. Antler size in red deer: heritability and selection but no evolution. Evolution Int. J. Org. Evolution 56, 1683–1695 (2002)

    CAS  Article  Google Scholar 

  23. Kokko, H. Fisherian and ‘good genes’ benefits of mate choice: how (not) to distinguish between them. Ecol. Lett. 4, 322–326 (2001)

    Article  Google Scholar 

  24. Pischedda, A. & Chippindale, A. K. Intralocus sexual conflict diminishes the benefits of sexual selection. PLoS Biol. 4, e356 (2006)

    Article  Google Scholar 

  25. Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. Red Deer: Behavior and Ecology of Two Sexes (Univ. of Chicago Press, Chicago, 1982)

    Google Scholar 

  26. Kruuk, L. E. B., Clutton-Brock, T. H., Rose, K. E. & Guinness, F. E. Early determinants of lifetime reproductive success differ between the sexes in red deer. Proc. R. Soc. Lond. B 266, 1655–1661 (1999)

    CAS  Article  Google Scholar 

  27. Coulson, T., Albon, S., Guinness, F., Pemberton, J. & Clutton-Brock, T. Population substructure, local density, and calf winter survival in red deer (Cervus elaphus). Ecology 78, 852–863 (1997)

    Article  Google Scholar 

  28. Marshall, T. C. et al. Estimating the prevalence of inbreeding from incomplete pedigrees. Proc. R. Soc. Lond. B 269, 1533–1539 (2002)

    CAS  Article  Google Scholar 

  29. Gilmour, A. R., Gogel, B. J., Cullis, B. R., Welham, S. J. & Thompson, R. ASReml User Guide 1.0. (VSN International, Hemel Hempstead, 2002)

    Google Scholar 

  30. Metcalf, C. J. E. & Pavard, S. Why evolutionary biologists should be demographers. Trends Ecol. Evol. 22, 205–212 (2007)

    Article  Google Scholar 

  31. Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. The costs of reproduction to red deer hinds. J. Anim. Ecol. 52, 367–383 (1983)

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Katharina Foerster or Loeske E. B. Kruuk.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

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)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature05912

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing