Linking social structure to fine-scale genetic structure 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 social relationships that influence dispersal, mating, and the spatial distribution of individuals. Theory predicts that social structure can affect gene flow and population genetic structure, as well as the distribution of genetic variance in fitness. However, these processes have never been examined together in natural populations. Using nearly 30 years of behavioural, life-history, and genomic data from spotted hyenas (Crocuta crocuta) in Tanzania’s Ngorongoro Crater, we investigated whether social structure, dispersal, genetic structure, and genetic variation in fitness covary in a spatially continuous population. Genome-wide analyses revealed modest genetic differentiation among social groups (called clans), despite genetic variation being distributed fairly continuously across the population. Genetic differentiation between clans decreased with increasing male dispersal, consistent with dispersal facilitating gene flow. Individuals with greater ancestry from outside the Crater had higher lifetime reproductive success and longer lifespans, suggesting that immigration introduced genetic variation associated with higher fitness. Finally, additive genetic variance in fitness differed among some clans, but not consistently across the population. Together, our findings suggest that social structure can shape fine-scale genetic structure and the genetic basis of fitness, although these patterns are evident in some social groups rather than others. More broadly, our study highlights the value of integrating social, behavioural, genomic, and quantitative genetic data to understand the interplay between social structure and microevolution in wild populations.