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

Many evolutionary models remain limited in their ability to predict evolutionary change under realistic ecological conditions. A potential reason for this limitation could be that social structures are not yet well incorporated into most empirically parameterized evolutionary frameworks, despite being a defining feature of animal populations. This is of particular relevance because social structure determines who moves, mates, and interacts, all of which shape how genetic variation is distributed across space and time. Using nearly 30 years of behavioural, life-history, and genomic data from a natural population of spotted hyenas, we show that social structure shapes core microevolutionary processes. Genome-wide analyses reveal cryptic population genetic structure among social groups within a spatially continuous population that is driven primarily by asymmetric, socially mediated dispersal. Individuals with greater immigrant ancestry had higher fitness, measured as lifetime reproductive success and lifespan, demonstrating that social processes regulate both the flow and adaptive consequences of genetic variation. Finally, additive genetic variance in fitness differed among social groups, showing that evolutionary potential is unevenly distributed across the population. Together, our results show that social structure rearranges genetic variation across space and generates heterogeneity in adaptive potential across the population. Our study demonstrates that social structure can be a major, yet often overlooked, driver of microevolutionary dynamics in natural populations.