Gene Flow and Recent Lineage Colonization Constrain Genetic Differentiation Despite Local Adaptation

Abstract

Demographic processes such as colonization to new environments and gene flow fundamentally shape the genomic landscape, either facilitating or constraining the efficiency of selection by altering the balance between genetic diversity and adaptive responses. Although theoretical predictions suggest that the efficacy of selection is dictated by a species' demographic history, empirical studies often overlook these constraints, yielding misleading observations. In this study, we present the first functional genome annotation for the wood frog (Lithobates sylvaticus), providing a critical genomic resource for understanding the adaptive capacity of the species. Based on the annotation, we examined the potential for selection to drive genomic and phenotypic divergence among populations distributed across vernal ponds in Northeastern Connecticut, USA. A genotypexenvironment association analysis revealed that the frequency of an outlier loci (Rab28) spikes in response to one wetland that is notable for having relatively low canopy cover and large area. We also found that selection has driven a strong disparity in embryonic development among populations of wood frog at a rate exceeding that of neutral genetic drift. This genomic signature of selection together with a remarkable phenotypic differentiation suggests that natural selection overcomes the power of genetic drift, even in a landscape characterized by relatively recent colonization and substantial evidence of connectivity among breeding wetlands. These findings improve our understanding of the wood frog's variation at a microgeographic scale.