Social structure shapes gene flow and genetic variance in fitness in spotted hyenas

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

Many animal populations are structured by stable social relationships which influence dispersal, mating, and the spatial distribution of individuals. Although theory predicts that social structure should affect microevolutionary processes such as gene flow, genetic structure, and the distribution of genetic variation underlying fitness, these links have rarely been quantified in natural populations. Using nearly 30 years of behavioural, life-history, and genomic data from a population of spotted hyenas (Crocuta crocuta), we examined how social structure is associated with patterns of genetic structure and additive genetic variation in fitness. Genome-wide analyses revealed fine-scale genetic structure among social groups within a spatially continuous population, associated primarily with socially mediated dispersal. Individuals with greater immigrant ancestry exhibited higher fitness, measured as lifetime reproductive success and lifespan, indicating that gene flow from outside the population is associated with variation in fitness. Finally, quantitative genetic analyses showed that additive genetic variance in fitness differed among social groups, indicating heterogeneity across social groups in the expected rate of contemporary adaptive evolution. Together, these results show that socially defined population substructure is associated with variation in genetic connectivity, fitness, and rates of adaptive evolution. Our findings highlight the importance of integrating social structure into empirical descriptions of microevolutionary processes occurring in wild populations.