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

University of Cambridge, Cambridge, England, United Kingdom
Evolutionary Ecology (Impact Factor: 2.52). 06/2007; 21(3):337-356. DOI: 10.1007/s10682-006-9106-z


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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Available from: Alastair J Wilson
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    • "Offspring size effects are known to diminish over time, such that early estimates of effects may result in overestimates of the subsequent optimal size (Heath et al. 1999; Lindholm et al. 2006). One mechanism for this diminished effect is compensatory growth, whereby initial differences among offspring are reduced due to increases in the relative growth rate of smaller offspring (Wilson et al. 2007; Dias and Marshall 2010). Other sources of variation in early development include maternal and paternal effects that can cause cohort differences in various fitness components (Lindstrom 1999). "
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    • "To separate genetic and environmental effects, " common garden " type experiments or reciprocal transplants of target populations must be used. These can be very difficult to conduct for large, wild mammals (see Pelletier et al. 2007; Wilson et al. 2007 for studies of the genetic basis of the body size of wild sheep populations). Therefore, intraspecific studies of body size variation in mammals have focused on identifying an empirical relationship between the body size and environmental factors (Gay & Best 1996; Wigginton & Dobson 1999; Smith et al. 2002; Wolverton et al. 2009; Gür 2010). "
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    ABSTRACT: This review addresses the question “Are interspecific and macroevolutionary trends observed in ruminant morphology found among populations of a single species?” Several case studies of the Japanese sika deer, Cervus nippon, are discussed. The Japanese sika deer is a suitable species for this purpose because it inhabits various environments from the northern subarctic forests to the southern subtropical forests. It shows conspicuous variations in feeding habits, body size, and other morphological and behavioral traits. It can be concluded that selective pressures governing interspecific variations among ruminants, e.g., tooth wear due to grazing or mountainous habitat, promote morphological adaptation of local sika deer populations. However, in some cases, genetic differentiation among local populations is relatively small, resulting in a small degree of change compared to that observed between species. Intraspecific comparison of an ecologically diverse species like the Japanese sika deer is useful for elucidating the evolutionary patterns within ruminants and the possible causes for those patterns.
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    • "In contrast, selection on size (tarsus length or body mass) in great tits (Parus major) over 29 years was mostly positive (or non significant, depending on the population), and there was no evidence for a temporal change in selection during the study period (Husby et al. 2011). Similarly, in Soay sheep (Ovis aries), selection for body mass was positive (Wilson et al. 2007; Gratten et al. 2010) but selection explained only a small fraction of body mass variation over the last 20 years (Ozgul et al. 2009). The lack of significant selection for smaller size in these systems is sufficient to exclude the possibility that the size decrease is adaptive. "
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