Genotypic covariance between the performance of a resident species and community assembly in the field

Genetic variation in resident species can influence the assembly and dynamics of communities, but the potential for these genetic effects to persist across generations is largely unresolved. In principle, persistent, directional changes in communities are only predicted when community properties covary genetically with the fitness of resident species. Estimates of genetic covariance between the fitness of a resident species and its community are therefore necessary to “close the eco‐evolutionary loop” in studies of community genetics, but such estimates are rare. Emulating community genetics experiments in plants, we used clonal replicates of 21 genotypes of a resident species (the encrusting bryozoan, Hippopodina) to investigate the magnitude of genotypic variance contributing to assembly of a marine benthic community. Genotypes explained up to 35% of variation in community assembly. Critically, the performance of Hippopodina genotypes covaried both with the evenness of communities and with the abundances of some individual species, representing an indirect genetic effect that creates the potential for multigenerational interactions between Hippopodina and co‐existing species. Our results suggest that different genotypes will associate with different community members consistently across generations, and such non‐random associations can give rise to specialization. Further interactions between species other than Hippopodina itself may also be altered by effects of genetic variation in the focal species. Furthermore, species in the community other than Hippopodina itself will interact more commonly in the presence of some genotypes over others. Our results support the potential for genetic variation in one species to have deterministic effects on the dynamics of ecological communities. A plain language summary is available for this article.