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Molecular responses to freshwater limitation in the mangrove tree Avicennia germinans (Acanthaceae)

Environmental variation along the geographical space can shape populations by natural selection. In the context of global warming, accompanied by substantial changes in precipitation regimes, it is crucial to understand the role of environmental heterogeneity in tropical trees adaptation, given their disproportional contribution to water and carbon biogeochemical cycles. Here we investigated how heterogeneity in freshwater availability along tropical wetlands has influenced molecular variations of the Black-Mangrove (Avicennia germinans). Fifty-seven trees were sampled in seven sites differing markedly on precipitation regime and riverine freshwater inputs. Using 2,297 genome-wide single nucleotide polymorphic markers, we found signatures of natural selection by the genotype association with the precipitation of the warmest quarter and the annual precipitation. We also found candidate loci for selection, based on statistical deviations from neutral expectations of interpopulation differentiation. Most candidate loci present within coding sequences were functionally associated with central aspects of drought-tolerance or plant response to drought. Complementarily, our results suggest the occurrence of rapid evolution of a population, likely in response to sudden and persistent limitation in plant access to soil water, following a road construction in 1974. Observations supporting rapid evolution included reduction in tree size and changes in allele frequencies and in transcripts expression levels associated with increased drought-tolerance, through accumulation of osmoprotectants and antioxidants, biosynthesis of plant cuticle, protection against stress-induced proteins degradation, stomatal closure, photorespiration and photosynthesis. We describe a major role of spatial heterogeneity in freshwater availability in the specialization of this typically tropical tree.