Rapid lineage diversification of gray mangroves (Avicennia marina) driven by isolation in cryptic glacial refugia and extreme environmental conditions in the Arabian Peninsula

Abstract

Plant 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. Here, we analyzed fully sequenced genomes to study diversification mechanisms in the gray mangroves [Avicennia marina (Forssk.) Vierh.] of Arabia, where they occur at the edge of the species’ range and are subject to variable, often extreme, environmental conditions. We conducted population structure, phylogenomic and demographic analyses to reconstruct the evolutionary history of the species across Arabia. We also applied genotype-environment association methods to study adaptive mechanisms of lineage diversification. Our analyses revealed marked genetic structure and highly supported clades among and within the seas surrounding the Arabian Peninsula. Inferred divergence times were consistent with recent periods of low marine connectivity during glacial periods, revealing the presence of (cryptic) glacial refugia in the Red Sea and the Persian/Arabian Gulf. Genetic-environment association analyses revealed high levels of adaptive differentiation, 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.