Indirect genetic effects increase the heritable variation available to selection and are largest for behaviours: a meta-analysis

Abstract The evolutionary potential of traits is governed by the amount of heritable variation available to selection. While this is typically quantified based on genetic variation in a focal individual for its own traits (direct genetic effects, DGEs), when social interactions occur, genetic variation in interacting partners can influence a focal individual’s traits (indirect genetic effects, IGEs). Theory and studies on domesticated species have suggested IGEs can greatly impact evolutionary trajectories, but whether this is true more broadly remains unclear. Here we perform a systematic review and meta-analysis to quantify the amount of trait variance explained by IGEs and the contribution of IGEs to predictions of adaptive potential. We identified 180 effect sizes from 47 studies across 21 species and found that, on average, IGEs of a single social partner account for a small but statistically significant amount of phenotypic variation (0.03). As IGEs affect the trait values of each interacting group member and due to a typically positive – although statistically nonsignificant – correlation with DGEs ( r DGE-IGE = 0.26), IGEs ultimately increase trait heritability substantially from 0.27 (narrow-sense heritability) to 0.45 (total heritable variance). This 66% average increase in heritability suggests IGEs can increase the amount of genetic variation available to selection. Furthermore, whilst showing considerable variation across studies, IGEs were most prominent for behaviours, and to a lesser extent for reproduction and survival, in contrast to morphological, metabolic, physiological, and development traits. Our meta-analysis therefore shows that IGEs tend to enhance the evolutionary potential of traits, especially for those tightly related to interactions with other individuals such as behaviour and reproduction. Lay Summary Predicting evolutionary change is important for breeding better livestock and crops, for understanding how biodiversity arises and how populations respond to environmental change. Normally, these predictions are based on how the genetic variants in an organism influence its own traits (characteristics). However, when organisms socially interact, for instance by fighting or cooperating, then the genes in one individual can influence the traits of others, therefore affecting the potential for evolutionary change. We compared 47 studies across 21 animal species and found that the effect of the genes of a single social partner is small but statistically significant, while the total contribution of social genetic effects to evolutionary potential is large. These effects are particularly important for the evolution of animals’ behaviours and reproductive traits, but less so for other traits such as body size and physiology. We also found that, because an individual can interact with many others and influence them all, social interactions can substantially increase the potential for a population to evolve from generation to generation. Our results show how social interactions can potentially alter the evolution of those traits known to respond to social interactions in comparison to standard expectations.

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