Habitat Association Predicts Population Connectivity and Persistence in Flightless Beetles: A Population Genomics Approach Within a Dynamic Archipelago

Habitat association has been proposed to affect evolutionary dynamics through its control on dispersal propensity, which is considered a key trait for lineage survival in habitats of low durational stability. The Habitat Constraint hypothesis predicts different micro- and macroevolutionary patterns for stable versus dynamic habitat specialists, but the empirical evidence remains controversial and in insects mostly derives from winged lineages. We here use genome-wide SNP data to assess the effect of habitat association on the population dynamics of two closely related flightless lineages of the genus Eutagenia (Coleoptera: Tenebrionidae), which are co-distributed across the Cyclades islands in the Eastern Mediterranean but are associated with habitat types of different presumed stability: the psammophilous lineage is associated with dynamic sandy coastal habitats, while the geophilous lineage is associated with comparatively stable compact soil habitats. Our comparative population genomic and demographic analyses support higher inter-island gene flow in the psammophilous lineage, presumably due to the physical properties of dynamic sand-dune habitats that promote passive dispersal. We also find consistent bottlenecks in the psammophilous demes, suggesting that lineage evolution in the dynamic habitat is punctuated by local extinction and recolonisation events. The inferred demographic processes are surprisingly uniform among psammophilous demes, but vary considerably among geophilous demes depending on historical island connectivity, indicating more stringent constraints on the dynamic habitat lineage. This study extends the Habitat Constraint hypothesis by demonstrating that selection on dispersal traits is not the only mechanism that can drive consistent differences in evolutionary dynamics between stable versus dynamic habitat specialists.