Habitat association predicts population connectivity and persistence in flightless beetles: a population genomics approach within a dynamic archipelago

Habitat persistence has been proposed to affect evolutionary dynamics through its control on dispersal propensity, which is considered a key trait for lineage survival in geologically ephemeral habitats. The Habitat Constraint hypothesis proposes micro- and macroevolutionary expectations for stable vs. ephemeral habitat specialists, but the empirical evidence remains controversial and mostly derives from winged lineages. We here assess the effect of habitat persistence on the population dynamics of dispersal-limited lineages. We focus on two closely related insular lineages of the Eastern Mediterranean genus Eutagenia (Coleoptera: Tenebrionidae), which have equivalent dispersal limitations, but differ in soil-type preference: the psammophilous lineage is associated with ephemeral sandy coastal habitats, while the geophilous lineage is associated with comparatively stable inner-island habitats. Using genome-wide SNP data, we conduct comparative population genomic and demographic analyses between co-distributed psammophilous and geophilous demes across fourteen Aegean islands. Despite the absence of apparent dispersive traits in our focal organisms, our results support higher inter-island gene flow in the psammophilous lineage, presumably due to the physical properties of ephemeral sand dune habitats that promote passive dispersal. Furthermore, our analyses support frequent extinction and recolonisation events that act as an additional habitat-induced constraint in the ephemeral sand dunes. The inferred demographic processes are surprisingly uniform across islands for psammophilous demes, while they vary widely depending on island connectivity for geophilous demes, indicating more stringent constraints in the ephemeral habitat. This study provides new insights that support the Habitat Constraint hypothesis from a population genomics perspective.