The social environment shapes fitness through indirect genetic effects in spotted hyenas

Kasha Strickland, Matthew Silk, Oliver P. Höner, Eve Davidian, Loeske E. B. Kruuk, Joel Pick

Additive genetic variance in fitness determines the rate of adaptive evolution. Yet, estimates from wild populations often exceed observed rates of contemporary evolution and realised population growth rates, suggesting that important sources of variation may remain unaccounted for. One important source of variation rarely fully accounted for is the social environment, because social interactions are known to influence survival and reproduction across taxa. Here, we combined social network analysis with quantitative genetic animal models in a wild population of spotted hyenas (Crocuta crocuta) inhabiting the Ngorongoro Crater, Tanzania, to explore how estimates of genetic variance in fitness are affected by the inclusion of social environment effects. In line with previous research, standard animal models recovered significant additive genetic variance in lifetime reproductive success. However, this variance substantially reduced to near zero when we accounted for shared social and spatial environments, indicating that previous estimates likely overestimated direct additive genetic variance. Instead, we found strong indirect genetic effects from social associations on fitness. Fine-scale spatial overlap also explained substantial variation in fitness whereas non-genetic indirect effects from social associations were comparatively small. Our results demonstrate that heritable variation in fitness may be expressed predominantly through social interactions rather than individuals' own genotypes in this population. More generally, our results suggest that incorporating realistic social environments into quantitative genetic models may be essential in understanding and predicting adaptive evolution in natural populations.