Indirect genetic effects: a key component of the genetic architecture of behaviour

Abstract

Behavioural ecology research increasingly focuses on why genetic behavioural variation can persist despite selection. Evolutionary theory predicts that directional selection leads to evolutionary change while depleting standing genetic variation. Nevertheless, evolutionary stasis may occur for traits involved in social interactions. This requires tight negative genetic correlations between direct genetic effects (DGEs) of an individual's genes on its own phenotype and the indirect genetic effects (IGEs) it has on conspecifics, as this could diminish the amount of genetic variation available to selection to act upon. We tested this prediction using a pedigreed laboratory population of Mediterranean field crickets (Gryllus bimaculatus), in which both exploratory tendency and aggression are heritable. We found that genotypes predisposed to be aggressive (due to DGEs) strongly decreased aggressiveness in opponents (due to IGEs). As a consequence, the variance in total breeding values was reduced to almost zero, implying that IGEs indeed greatly contribute to the occurrence of evolutionary stasis. IGEs were further associated with genetic variation in a non-social behaviour: explorative genotypes elicited most aggression in opponents. These key findings imply that IGEs indeed represent an important overlooked mechanism that can impact evolutionary dynamics of traits under selection.

Figure 1

Correlation structure of the five hypothesized multivariate model structures presented in Table 3 (detailed in the Methods). A is the correlation between DGEs and IGEs on aggressiveness; B is the correlation between DGEs on exploration and DGEs on aggressiveness; C is the correlation between DGEs on exploration and IGEs on aggressiveness. Estimated correlations with corresponding SEs derived from the full model (Model 5, presented in Table 2) are shown with each arrow; bolded arrows represent paths with statistical support from the LRT and AIC.