Evolution of quantitative traits in the wild: mind the ecology

Abstract

Recent advances in the quantitative genetics of traits in wild animal populations have created new interest in whether natural selection, and genetic response to it, can be detected within long-term ecological studies. However, such studies have re-emphasized the fact that ecological heterogeneity can confound our ability to infer selection on genetic variation and detect a population's response to selection by conventional quantitative genetics approaches. Here, I highlight three manifestations of this issue: counter gradient variation, environmentally induced covariance between traits and the correlated effects of a fluctuating environment. These effects are symptomatic of the oversimplifications and strong assumptions of the breeder's equation when it is applied to natural populations. In addition, methods to assay genetic change in quantitative traits have overestimated the precision with which change can be measured. In the future, a more conservative approach to inferring quantitative genetic response to selection, or genomic approaches allowing the estimation of selection intensity and responses to selection at known quantitative trait loci, will provide a more precise view of evolution in ecological time.

Figure 1.

Counter gradient variation in fledgling condition in collared flycatchers on Götland (Merilä et al. 2001). (a) Selection favours higher condition and became stronger over the time series. (b) The phenotypic values for condition declined over the study period. (c) The EBVs over the same period appear to increase, though see text for discussion of the use of EBVs to determine genetic trends.

Figure 2.

Environmentally induced covariance between antler weight and lifetime breeding success in red deer on Rum (Kruuk et al. 2002). (a) Selection favours heavy antlers, since there is a strong correlation between antler weight and lifetime breeding success (LBS) of stags. (b) The correlation is less apparent when comparing LBS and EBVs of antler weight but (c) more apparent when comparing LBS and the individual environmental components of antler weight. The observations in (b) were supported by a lack of genetic correlation between antler weight and LBS in a bivariate animal model (Kruuk et al. 2002). See text for discussion of the use of EBVs in such analyses.

Figure 3.

Inverse relationship between the strength of selection and heritability promoted by between-year variation in environmental conditions in Soay sheep birth weight on St Kilda (Wilson et al. 2006). Each year is represented by a data point. Total heritability refers to the combined heritability and maternal genetic effect. When conditions are good (left-hand side of plot) heritability is at its highest but selection is relatively weak. When conditions are poor (right-hand side of plot) selection is relatively strong but heritability is low.