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.

Increased developmental density decreases the magnitude of indirect genetic effects expressed during agonistic interactions in an insect

“…; Santostefano et al. ). As we failed to detect significant covariance between DGEs and IGEs (COV Ad,Ai ) in the two density treatments, the evolutionary response of aggression in the group of unrelated individuals will be greater in the high‐density environment due to large DGEs (assuming that similar selection acts between density environments).…”

“…Our recent research has demonstrated that IGEs significantly contribute to variance in aggression in this species (Santostefano et al. ). In addition, developmental density influences maturation time, survival, and body mass in this species (Iba et al.…”

“…; Santostefano et al. ). Insight into the roles of IGEs in the genetic architecture of phenotypic traits under density‐dependent selection is therefore required to properly predict their evolution.…”

“…), Drosophila melanogaster (Saltz ), and southern field crickets ( Gryllus bimaculatus ) (Santostefano et al. ). Moreover, positive versus negative genetic correlations between DGEs and IGEs elicit (Wilson et al.…”

“…) versus depress (Santostefano et al. ) conspecific aggression, respectively, implying that IGEs exist because individuals modify their aggression as a function of the level of aggression expressed in interaction partners. Importantly, IGEs in aggression are expected to vary as a function of environmental factors, such as conspecific density experienced during development.…”