Rapid diversification of grey mangroves (Avicennia marina) driven by geographic isolation and extreme environmental conditions in the Arabian Peninsula.

ABSTRACT

Biological systems occurring in ecologically heterogeneous and spatially discontinuous habitats provide an ideal opportunity to investigate the relative roles of neutral and selective factors in driving lineage diversification. The grey mangroves (Avicennia marina) of Arabia occur at the northern edge of the species' range and are subject to variable, often extreme, environmental conditions, as well as historic large fluctuations in habitat availability and connectivity resulting from Quaternary glacial cycles. Here, we analyse fully sequenced genomes sampled from 19 locations across the Red Sea, the Arabian Sea and the Persian/Arabian Gulf (PAG) to reconstruct the evolutionary history of the species in the region and to identify adaptive mechanisms of lineage diversification. Population structure and phylogenetic analyses revealed marked genetic structure correlating with geographic distance and highly supported clades among and within the seas surrounding the Arabian Peninsula. Demographic modelling showed times of divergence consistent with recent periods of geographic isolation and low marine connectivity during glaciations, suggesting the presence of (cryptic) glacial refugia in the Red Sea and the PAG. Significant migration was detected within the Red Sea and the PAG, and across the Strait of Hormuz to the Arabian Sea, suggesting gene flow upon secondary contact among populations. Genetic-environment association analyses revealed high levels of adaptive divergence and detected signs of multi-loci local adaptation driven by temperature extremes and hypersalinity. These results support a process of rapid diversification resulting from the combined effects of historical factors and ecological selection and reveal mangrove peripheral environments as relevant drivers of lineage diversity.