Contrasting genetic diversity and structure between endemic and widespread damselfishes are related to differing adaptive strategies

Aim Several marine biogeographical provinces meet at the Arabian Peninsula. Where and how these junctions affect species is poorly understood. We herein aimed to identify the barriers to dispersal and how these shape fish populations, leading to differing biogeographies despite shared habitat and co-ancestry. Taxon Dascyllus marginatus (endemic) and Dascyllus abudafur (widespread). Location Coral reefs from the Red Sea (RS), Djibouti, Yemen, Oman, and Madagascar. Methods We tested potential barriers to gene flow using RADseq-derived SNPs and identified whether population genetic differences on each side of these barriers were neutral or selective to relate this to the biogeography of the species. Seven locations (ranging over 5100 km) were sampled for the endemic and six (ranging over 7400 km) for the widespread species, taking 20 individuals per location, with two exceptions. Results Dascyllus marginatus populations (comprising 5648 SNPs) had an order of magnitude higher genetic differentiation compared to D. abudafur (comprising 10,667 SNPs), as well as several outlier loci that were absent in D. abudafur despite equal sampling locations. In both species, the RS and Djibouti specimens formed one genetic cluster separated from all other locations. Although ranging from the RS to Madagascar, D. abudafur was absent in Yemen and Oman. Main Conclusions Stronger genetic structure at smaller geographical scales and outlier loci in the endemic species seem associated with faster adaptation to environmental differences and selective pressure. Genetic differentiation in the widespread species is neutral and only occurs at large geographical distances. Restrictive transitions (between the Gulf of Aqaba and the RS or the RS and the Gulf of Aden) do not hinder gene flow in either species, and the environmental shift within the RS (at 22°N/20°N) only affected the endemic species. The genetic break in the Gulf of Aden likely reflects historical colonization processes and not contemporary environmental regimes.