Association with dynamic habitats disrupts speciation and reduces the efficacy of purifying selection in flightless beetles

Abstract Association with temporally dynamic habitats has been proposed as a strong predictor of effective population size (Ne) and speciation rates, and thus also potentially of molecular evolution rates, but empirical insights remain limited. We use a genomic dataset of over 2,000 single-copy orthologs to evaluate how habitat association shapes molecular evolution in closely related flightless beetle lineages (Coleoptera: Tenebrionidae: Eutagenia), co-distributed across Eastern Mediterranean islands. The focal taxa occupy either dynamic coastal sand dunes or stable compact-soil habitats but share uniform life-history traits and morphology. Species delimitation analyses identified a single widespread coastal dune species, whereas the stable-habitat clade has diversified into nine allopatric species across the same geographic space and timeframe. Despite its wide distribution, the dynamic-habitat lineage exhibits the lowest long-term Ne and accordingly the highest median nonsynonymous-to-synonymous substitution rate ratio (dN/dS), yet its total substitution rate is not significantly higher. We propose that recurrent local population extinction in dynamic habitats hinders the completion of speciation and reduces the efficacy of purifying selection, thus elevating the dN/dS ratio. More broadly, these findings indicate that diversification and molecular evolution rates may become decoupled under recurrent population turnover, a hypothesis that requires further empirical and theoretical investigation.