Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations

Abstract

Predicting the rate of adaptation to environmental change in wild populations is important for understanding evolutionary change. However, predictions may be unreliable if the two key variables affecting the rate of evolutionary change-heritability and selection-are both affected by the same environmental variable. To determine how general such an environmentally induced coupling of heritability and selection is, and how this may influence the rate of adaptation, we made use of freely accessible, open data on pedigreed wild populations to answer this question at the broadest possible scale. Using 16 populations from 10 vertebrate species, which provided data on 50 traits (relating to body mass, morphology, physiology, behaviour and life history), we found evidence for an environmentally induced relationship between heritability and selection in only 6 cases, with weak evidence that this resulted in an increase or decrease in the expected selection response. We conclude that such a coupling of heritability and selection is unlikely to strongly affect evolutionary change, even though both heritability and selection are commonly postulated to be dependent on the environment.

Figure 1. Heritability as a function of the standardized selection gradient.

Standard errors (SEs) are omitted when SE_h² > 0.5 and SE_β^′ > 1 for visual aid. Regression lines result from weighted least-squares regression models (weights: 1/[(SE_h²)²]), with bootstrapping to account for uncertainty in β′, shown only when the 95% CI did not include zero. Colours denote different trait classes (red: life history; green: body mass; blue: morphology; orange: miscellaneous), whereas shapes indicate selection based on survival (circles) or based on number of fledglings or recruits (triangles). Dotted horizontal lines denote the constant heritability as estimated from a standard animal model. Duplicate traits (from same population but different dataset) are not shown. Data sources by panel: (1,2,6,7) ref. ; (5,11,26) ref. ; (3,4,8,9,13,14,16,17,30,31) ref. ; (10) unpubl. data; (12) ref. ; (15,32) ref. ; (18,19,35,36,38) ref. ; (20,37) ref. ; (21) ref. ; (22–25,33,34) ref. ; (27,28,39,40) ref. ; (29) ref. ; (41–45) ref. ; (46) ref. ; (47–50) ref. .

Figure 2. Meta-analysis on the heritability–selection correlation coefficients.

Coefficients r were standardised using Fisher’s Z transformation prior to analysis. Estimates and bootstrapped 95% CIs are shown, predicted from a linear mixed-effects model and unconditioned on the random term ‘study area’. The summary statistic results from a model that included only the intercept as a fixed term. Estimates from an analysis excluding non-avian traits are shown for comparison.

Figure 3. No effect of a correlation between heritability and selection on differences in selection response.

Correlation coefficients (r ± standard errors) result from WLS regressions of heritability against standardised selection gradients; ΔR′ (± standard errors) is the mean, directional difference between expected responses to selection assuming varying vs. constant heritability. Each data point represents a single trait–species–population combination.