Oceanography and population genomics unravel low natural connectivity, ship-mediated long dispersal, and local adaptation in two Mediterranean sympatric topshell species

Contemporary climate change is reshaping marine ecosystems worldwide. Thus, understanding how population connectivity and local adaptation interact with contemporary climate change is critical for predicting ecosystem resilience and recovery. Here, we investigated the genomic signatures of two sympatric intertidal gastropods with low-dispersive early life-history stages, Phorcus articulatus and Phorcus turbinatus, across a contemporary climate change hotspot, the Mediterranean Sea. We generated genotyping-by-sequencing data from 336 Mediterranean specimens to unravel connectivity patterns across the Mediterranean and to identify environmentally associated genomic variation. Lagrangian particle-tracking simulations revealed strong short-term larval retention and basin-scale isolation. Accordingly, our genomic data showed a pronounced east-west population structure, with P. articulatus showing stronger population differentiation than P. turbinatus. However, we found unexpected genetic affinities among several distant localities, indicating recent human-mediated connectivity, most likely via maritime transport. We also found contrasting genomic architectures and different adaptive responses. Specifically, genotype-environment association analyses identified ∼600 high-quality SNPs potentially under selection. These loci showed limited overlap between species, suggesting divergent evolutionary strategies to overcome similar environmental pressures: P. articulatus showed evidence of local adaptation driven only by temperature, whereas P. turbinatus displayed adaptive associations involving temperature and salinity. Our results suggest that P. turbinatus will be more resilient to future climatic conditions than P. articulatus, given its higher population connectivity and capacity to adapt to multiple stressors. These findings highlight the importance of conducting studies that include both comparative population genomics and oceanographic modelling to understand how evolutionary dynamics are shaped by contemporary climate change across species ranges.