Revealing the abiotic and biotic drivers of past and future local adaptation in a coastal dogwhelk

Abstract

Predicting whether populations can persist under rapid environmental change requires identifying the ecological drivers of local adaptation, uncovering their genetic bases, and understanding how adaptive variation will respond to future selection. Here, we combine landscape genomics, environmental data, and evolutionary simulations to identify the selective forces shaping adaptation across 1,500 km of the west coast of North America in the low-dispersing coastal dogwhelk Nucella canaliculata, determine their genomic bases, and forecast future evolutionary responses. We found strong associations of genome-wide variation with both abiotic (i.e., mean pH) and biotic variation (i.e., cross-sectional shell thickness of the mussel prey species, Mytilus californianus). These patterns are underlain by two large-effect loci, including a biomineralization gene associated with pH tolerance and a locus near a thiamine transporter associated with prey shell thickness. Genomic offset analyses and population genetic simulations further predict that ongoing ocean acidification will disrupt existing adaptive patterns and generate maladaptation in high latitude populations, with evolutionary outcomes strongly influenced by gene flow, which determines the rate at which adaptive alleles spread across the species range. Together, these findings reveal how biotic and abiotic selective pressures shape adaptive genomic variation and provide a framework for forecasting evolutionary responses to future global change.