The Missing Response to Selection in the Wild

Abstract

Although there are many examples of contemporary directional selection, evidence for responses to selection that match predictions are often missing in quantitative genetic studies of wild populations. This is despite the presence of genetic variation and selection pressures - theoretical prerequisites for the response to selection. This conundrum can be explained by statistical issues with accurate parameter estimation, and by biological mechanisms that interfere with the response to selection. These biological mechanisms can accelerate or constrain this response. These mechanisms are generally studied independently but might act simultaneously. We therefore integrated these mechanisms to explore their potential combined effect. This has implications for explaining the apparent evolutionary stasis of wild populations and the conservation of wildlife.

Keywords: evolutionary potential; fitness-related traits; genetic variation; heritability; microevolutionary stasis.

Figure 1

Departure from Baseline Evolutionary Expectations: Widely Acknowledged Mechanisms. Quadrant plots illustrate the effect of widely acknowledged mechanisms on the response to selection (R) and the change in additive genetic variation (V_A) relative to baseline predictions. Mechanisms increasing the response to selection lie to the right of the y axis, and those decreasing it lie to the left. Mechanisms causing the maintenance of additive genetic variation lie above the x axis, those eroding it lie below. Where expectations are close to baseline predictions, the effect remains centered around the axis. These mechanisms are (A) phenotypic plasticity, (B) genetic correlations, (C) indirect genetic effects (maternal genetic effect), (D) age effects, where old age classes are often associated with increased additive genetic variation, and (E) fluctuating selection. Phenotypic plasticity (A) was split into (i) the effect of plasticity itself, (ii) the effect of the canalization of plastic trait variation that becomes constitutively expressed, as in the case of genetic assimilation, and (iii) genotype-by-environment interactions. Genetic correlations (B) were split into (i) the effect of genetic correlations aligned with the direction of selection, and (ii) the effect of genetic correlations that are antagonistic with the direction of selection. Fluctuating selection (E) was split into (i) the effect of a low-frequency fluctuation with sign changes, (ii) effect of fast frequency fluctuation with sign changes, (iii) low-amplitude fluctuation with sign changes, and (iv) low-amplitude fluctuation with consistent sign.

Figure 2

Departure from Baseline Evolutionary Expectations: New Mechanisms. In this figure we present in quadrant plots the effect of mechanisms that in our opinion should also be considered to affect the response to selection (R) and the change in additive genetic variation (V_A) relative to baseline predictions. Mechanisms increasing the response to selection lie to the right of the y axis, and those decreasing it lie to the left. Mechanisms causing the maintenance of additive genetic variation lie above the x axis, those eroding it lie below. Where expectations are close to baseline predictions, the effect remains centered around the axis. The mechanisms outlined here are (A) demography; we show here the effect of founding events, or long-term small population size associated with genetic drift, (B) coevolution, and (C) nongenetic inheritance.

Figure 3

An Integrative Framework for Predicting Microevolutionary Change. We show here how to integrate multiple mechanisms into our framework. The quadrant plots illustrate the effect of mechanisms that affect the response to selection (R) and the change in additive genetic variation (V_A) relative to baseline predictions. Mechanisms increasing the response to selection lie to the right of the y axis, and those decreasing it lie to the left. Mechanisms causing the maintenance of additive genetic variation lie above the x axis, those eroding it lie below. Where expectations are close to baseline predictions, the effect remains centered around the axis. Mechanisms are combined by superimposing the quadrant plots of their effects, which reveals a darkened area that corresponds to the most likely predictions about the response to selection and changes in genetic variation, relative to baseline expectations. Plot (A) illustrates how a sample of mechanisms known to characterize a particular population can be integrated. This illustrates predictions for an imaginary population, where founding effects, gene-by-environment interactions, and negative genetic correlations between traits under positive selection are combined to give predictions of reduced response to selection, accompanied by relatively negligible changes in genetic variation compared to the baseline expectation. Plot (B) illustrates the combined effect of all the mechanisms listed in the main text.