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

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 gray 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 to historic large
fluctuations in habitat availability and connectivity resulting from
Quaternary glacial cycles. Here, we analyze fully sequenced genomes
sampled from 20 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 and highly supported clades among and within the
seas surrounding the Arabian Peninsula. Demographic modeling showed times
of divergence consistent with recent periods of geographic isolation and
low marine connectivity during glaciations, revealing 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 Arabian mangrove 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.