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Quantitative genetics of growth and cryptic evolution of body size in an island population

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Abstract

While evolution occurs when selection acts on a heritable trait, empirical studies of natural systems have frequently reported phenotypic stasis under these conditions. We performed quantitative genetic analyses of weight and hindleg length in a free-living population of Soay sheep (Ovis aries) to test whether genetic constraints can explain previously reported stasis in body size despite evidence for strong positive directional selection. Genetic, maternal and environmental covariance structures were estimated across ontogeny using random regression animal models. Heritability increased with age for weight and hindleg length, though both measures of size were highly heritable across ontogeny. Genetic correlations among ages were generally strong and uniformly positive, and the covariance structures were also highly integrated across ontogeny. Consequently, we found no constraint to the evolution of larger size itself. Rather we expect size at all ages to increase in response to positive selection acting at any age. Consistent with expectation, predicted breeding values for age-specific size traits have increased over a twenty-year period, while maternal performance for offspring size has declined. Re-examination of the phenotypic data confirmed that sheep are not getting larger, but also showed that there are significant negative trends in size at all ages. The genetic evolution is therefore cryptic, with the response to selection presumably being masked at the phenotypic level by a plastic response to changing environmental conditions. Density-dependence, coupled with systematically increasing population size, may contribute to declining body size but is insufficient to completely explain it. Our results demonstrate that an increased understanding of the genetic basis of quantitative traits, and of how plasticity and microevolution can occur simultaneously, is necessary for developing predictive models of phenotypic change in nature.

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Acknowledgements

We thank the National Trust for Scotland and Scottish Natural Heritage for permission to work on St. Kilda, the Royal Artillery Range (Hebrides) and QinetiQ and Eurest for logistic support. The long-term data collection on St. Kilda has been supported by the Natural Environment Research Council, the Wellcome Trust, the Biotechnology and Biological Sciences Research Council and the Royal Society, through grants to THCB, B.T. Grenfell, M.J. Crawley, T. Coulson, S. Albon, JMP and LEBK. The work described here was funded by a Leverhulme Trust research project grant to LEBK and D.W. Coltman. LEBK is supported by the Royal Society. We also thank the many previous members of the project (including many volunteers) who have collected field data or have contributed genotyping and paternity inference. T. Coulson and two anonymous referees provided useful comments on a previous version of this manuscript.

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Authors and Affiliations

  1. Institute of Evolutionary Biology, University of Edinburgh, West Mains Road, Edinburgh, EH9 3JT, UK

    A. J. Wilson, J. M. Pemberton, J. G. Pilkington & L. E. B. Kruuk

  2. Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK

    T. H. Clutton-Brock

  3. Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada, T6G2E9

    D. W. Coltman

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  1. A. J. Wilson
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  2. J. M. Pemberton
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  5. D. W. Coltman
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  6. L. E. B. Kruuk
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Correspondence to A. J. Wilson.

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Wilson, A.J., Pemberton, J.M., Pilkington, J.G. et al. Quantitative genetics of growth and cryptic evolution of body size in an island population. Evol Ecol 21, 337–356 (2007). https://doi.org/10.1007/s10682-006-9106-z

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  • DOI: https://doi.org/10.1007/s10682-006-9106-z

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