Parallel connectivity and genomic divergence but heterogeneous demographic history in sympatric Mediterranean clingfishes

Abstract

Understanding the extent to which marine connectivity can be predicted from shared oceanographic and biogeographic conditions remains a central challenge in marine ecology and evolution. Comparative analyses of sympatric species provide a powerful framework for testing whether common environmental contexts generate repeatable patterns of population structure and connectivity and if this also unfolds on a genomic level. Here, we investigated this question in the endemic Mediterranean clingfish genus Gouania, a group of cryptobenthic gravel-beach specialists with limited adult mobility and a short pelagic larval phase. We combined whole-genome resequencing of two sympatric eastern Mediterranean species (G. orientalis and G. hofrichteri) around Crete and Kythira with Lagrangian particle drift simulations, mitochondrial phylogeography across all five Gouania species and demographic reconstructions using MSMC2. Passive drift simulations predicted strong isolation of Kythira and restricted exchange between northern and southern Crete. These predictions closely matched genome-wide population structure in both species, revealing highly concordant patterns of connectivity despite independent evolutionary histories. Shared population contrasts were furthermore associated with a significant excess of parallel genomic divergence, with both genomic windows and candidate genes overlapping more frequently than expected by chance. Nevertheless, most differentiated genomic regions remained species-specific and functional enrichment analyses identified no dominant shared pathways, suggesting a largely polygenic basis of divergence. In contrast to the strong concordance observed for contemporary connectivity and genomic divergence, mitochondrial phylogeographic patterns and species-level demographic histories were considerably more heterogeneous across the genus. Together, our results demonstrate that the predictability of marine population structure is scale-dependent: shared seascapes can generate repeatable patterns of connectivity and partially parallel genomic divergence, whereas deeper phylogeographic and demographic histories remain strongly influenced by species-specific historical processes.