Microevolutionary consequences of social structure in wild spotted hyenas

Kasha Strickland, Oliver Höner, Larissa Arantes, Joel Pick, Kenneth Aase, Loeske E. B. Kruuk, Eve Davidian

Social structure - arising from non-random associations and interactions among conspecifics - is a defining feature of most animal populations, yet evolutionary theory typically assumes genetic and social homogeneity. This disconnect limits our ability to predict how natural populations evolve. We combined nearly 30 years of behavioural, life-history, and genomic data from wild spotted hyenas (Crocuta crocuta) in Tanzania’s Ngorongoro Crater to test how social structure and male-biased dispersal shape genetic structure and the rate of adaptive evolution. Genome-wide analyses revealed subtle but consistent genetic differentiation among clans, reflecting cryptic population genetic structure. These differences were best explained by asymmetric dispersal between clans rather than geographic distance, indicating that social processes drive population stratification. Individuals with more immigrant ancestry had higher fitness, demonstrating adaptive benefits of gene flow and no evidence for selection against immigrants. Finally, additive genetic variance in fitness differed among clans, showing that evolutionary potential is unevenly distributed across the population. Together, these findings reveal how social structure and non-random dispersal generate hidden genetic structure and result in heterogenous rates of adaptive evolution. Our results underscore the need to integrate social structure in evolutionary models to better predict microevolutionary dynamics in the wild.