Environmental Gradients Decouple Demographic and Adaptive Connectivity in a Highly Mobile Coastal Marine Species

Understanding how eco-evolutionary processes shape genetic variation and persistence in marine species with highly variable recruitment dynamics and dispersal potential remains a fundamental challenge, particularly when considering the interplay between gene flow and local adaptation. Here, we employed a seascape genomics approach to investigate population connectivity and local adaptation in Australasian snapper (Chrysophrys auratus, Sparidae) along 1500 km of the environmentally heterogeneous southern Australian coastline. Using genome-wide SNPs, we identified distinct eastern and western regional populations aligned with known biogeographical regions. Genotype-environment association analyses revealed 855 candidate adaptive loci associated with environmental variation, including temperature, salinity and primary productivity. Connectivity analyses using neutral markers indicated high gene flow within both eastern and western regions, while candidate adaptive loci revealed substantially reduced connectivity, especially for Northern Spencer Gulf and West Coast populations. This contrast implies a decoupling of demographic and adaptive connectivity, in which strong environmental gradients appear to reduce the effective exchange of adaptive variation despite high overall connectivity. Our results support contingent migration as a potential mechanism modulating the balance between local adaptation and gene flow in this economically and ecologically important marine species. These findings might also have implications for regional management of other coastal fisheries that are experiencing substantial declines. As climate change alters coastal marine environments around the world, the dynamics of local recruitment, site fidelity and local adaptation are expected to change. This highlights the importance of integrating knowledge about eco-evolutionary processes into marine resource management, fisheries stock assessment, and restocking and stock enhancement activities.