Robinson, Matthew RichardISTA ; Wilson, Alastair J.; Pilkington, Jill G.; Clutton-Brock, Tim H.; Pemberton, Josephine M.; Kruuk, Loeske E. B.
This work demonstrates that environmental conditions experienced by individuals can shape their development and affect the stability of genetic associations. The implication of this observation is that the environmental response may influence the evolution of traits in the wild. Here, we examined how the genetic architecture of a suite of sexually dimorphic traits changed as a function of environmental conditions in an unmanaged population of Soay sheep (Ovis aries) on the island of Hirta, St. Kilda, northwest Scotland. We examined the stability of phenotypic, genetic, and environmental (residual) covariance in males during the first year of life between horn length, body weight, and parasite load in environments of different quality. We then examined the same covariance structures across environments within and between the adult sexes. We found significant genotype-by-environment interactions for lamb male body weight and parasite load, leading to a change in the genetic correlation among environments. Horn length was genetically correlated with body weight in males but not females and the genetic correlation among traits within and between the sexes was dependent upon the environmental conditions experienced during adulthood. Genetic correlations were smaller in more favorable environmental conditions, suggesting that in good environments, loci are expressed that have sex-specific effects. The reduction in genetic correlation between the sexes may allow independent evolutionary trajectories for each sex. This study demonstrates that the genetic architecture of traits is not stable under temporally varying environments and highlights the fact that evolutionary processes may depend largely upon ecological conditions. ENVIRONMENTAL heterogeneity has long been recognized as an important factor influencing the evolution of fitness-related traits in the wild (Roff 2002). The evolution of a trait depends upon the selection upon it, underlying genetic variation, and to a large degree the genetic relationships with other traits (Lynch and Walsh 1998). There is evidence that selection can vary considerably from year to year (Price et al. 1984; Robinson et al. 2008) and genetic variability in quantitative traits can change in response to environmental conditions (Hoffmann and Merilä 1999; Charmantier and Garant 2005). However, we know surprisingly little about the influence of environmental conditions on genetic correlations between traits in wild populations. Laboratory evidence suggests that the environment may influence genetic relationships between traits (Sgrò and Hoffmann 2004), but estimates obtained in a controlled or in an arbitrary range of conditions show a lack of concordance with those obtained in wild habitats (Conner et al. 2003). As a result, laboratory and environment-specific estimates of genetic correlations can make predictions for a trait's evolution, but these are valid only for the environment in which they were measured. Therefore, at present, it is difficult to generalize about the evolution of a trait that is expressed in populations that experience variable environmental conditions (Steppan et al. 2002). The influence of changing environmental conditions on the G matrix (the matrix of additive genetic variance and covariances corresponding to a set of traits) has been the focus of theoretical quantitative genetic studies (e.g., Jones et al. 2003). There is evidence of genotype-by-environment interaction for many traits expressed in wild populations (Charmantier and Garant 2005) and thus we may also expect that associations between traits may depend upon the environmental conditions encountered by an individual. Genetic correlations among traits may arise from pleiotropy, where a given locus affects more than one trait (Cheverud 1988; Lynch and Walsh 1998), which may limit the potential for those traits to evolve independently. There has recently been much interest in assessing genetic correlations between the sexes (Rice and Chippindale 2001; Foerster et al. 2007; Poissant et al. 2008), but all of these predictions have also been made in average environmental conditions. For sexually dimorphic traits, expectations of between-sex genetic correlations are unclear (Lande 1980; Badyaev 2002). We might expect that the genetic determination of a trait and the patterns of genetic covariance between traits may differ both within and between the sexes, producing the differences in trait growth that are commonly observed (Lande 1980; Badyaev 2002; Roff 2002), but so far evidence suggests that genetic expression in both sexes is influenced by the same developmental pathway (Roff 2002; Jensen et al. 2003; Parker and Garant 2005). However, to our knowledge, no study has yet determined whether genetic correlations, both within and between the sexes, vary across gradients of the environmental conditions encountered by individuals in the wild (Garant et al. 2008). This study aims to assess the stability of phenotypic, genetic, and environmental (residual) associations between traits, within and between the sexes, across a range of environmental conditions experienced by a wild population. We focus on the traits of horn length, body weight, and parasite load in a feral population of Soay sheep (Ovis aries) from the island of Hirta, St. Kilda, United Kingdom. Weather conditions, population density, and consequently resource availability fluctuate from year to year, providing substantial differences between individuals in the environments they experience and thus their survival rates (Clutton-Brock and Pemberton 2004). These varying conditions, combined with a large pedigree and extensive repeated morphological measures, provide an excellent opportunity to assess the potential effects of environmental heterogeneity on genetic architecture of traits. Previous studies on this population have shown additive genetic variance for many morphological traits (Milner et al. 2000; Coltman et al. 2001; Wilson et al. 2005), genetic correlations between traits (Coltman et al. 2001), and genotype-by-environment interactions for birth weight (Wilson et al. 2006). Here we apply a random regression animal model approach to assess the extent to which quantitative genetic parameters of a range of morphological traits measured during life vary as a function of environmental conditions. We then extend this methodology to the multivariate case, testing whether the phenotypic covariance structure, and the underlying G matrix, depends on the environmental conditions experienced. Since the traits considered here are known to be sexually dimorphic and there are differences in trait growth and survival across ages, we look at sex-specific traits in lambs and then across all ages.
Robinson MR, Wilson AJ, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB. The impact of environmental heterogeneity on genetic architecture in a wild population of soay sheep. Genetics. 2009;181(4):1639-1648. doi:10.1534/genetics.108.086801
Robinson, M. R., Wilson, A. J., Pilkington, J. G., Clutton-Brock, T. H., Pemberton, J. M., & Kruuk, L. E. B. (2009). The impact of environmental heterogeneity on genetic architecture in a wild population of soay sheep. Genetics. Genetics Society of America. https://doi.org/10.1534/genetics.108.086801
Robinson, Matthew Richard, Alastair J. Wilson, Jill G. Pilkington, Tim H. Clutton-Brock, Josephine M. Pemberton, and Loeske E. B. Kruuk. “The Impact of Environmental Heterogeneity on Genetic Architecture in a Wild Population of Soay Sheep.” Genetics. Genetics Society of America, 2009. https://doi.org/10.1534/genetics.108.086801.
M. R. Robinson, A. J. Wilson, J. G. Pilkington, T. H. Clutton-Brock, J. M. Pemberton, and L. E. B. Kruuk, “The impact of environmental heterogeneity on genetic architecture in a wild population of soay sheep,” Genetics, vol. 181, no. 4. Genetics Society of America, pp. 1639–1648, 2009.
Robinson MR, Wilson AJ, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB. 2009. The impact of environmental heterogeneity on genetic architecture in a wild population of soay sheep. Genetics. 181(4), 1639–1648.
Robinson, Matthew Richard, et al. “The Impact of Environmental Heterogeneity on Genetic Architecture in a Wild Population of Soay Sheep.” Genetics, vol. 181, no. 4, Genetics Society of America, 2009, pp. 1639–48, doi:10.1534/genetics.108.086801.