Whole genome scan reveals the multigenic basis of recent tidal marsh adaptation in a sparrow

Natural selection acts on functional molecular variation to create local adaptation, the good fit we observe between an organism's phenotype and its environment. Genomic comparisons of lineages in the earliest stages of adaptive divergence have high power to reveal genes under natural selection because molecular signatures of selection on functional loci are maximally detectable when overall genomic divergence is low. We conducted a scan for local adaptation genes in the North American swamp sparrow (Melospiza georgiana), a species that includes geographically connected populations that are differentially adapted to freshwater vs. brackish tidal marshes. The brackish tidal marsh form has rapidly evolved tolerance for salinity, a deeper bill, and darker plumage since colonizing coastal habitats within the last 15,000 years. Despite their phenotypic differences, background genomic divergence between these populations is very low, rendering signatures of natural selection associated with this recent coastal adaptation highly detectable. We recovered a multigenic snapshot of ecological selection via a whole genome scan that revealed robust signatures of selection at 31 genes with functional connections to bill shape, plumage melanism and salt tolerance. As in Darwin's finches, BMP signaling appears responsible for changes in bill depth, a putative magic trait for ecological speciation. A signal of selection at BNC2, a melanocyte transcription factor responsible for human skin color saturation, implicates a shared genetic mechanism for sparrow plumage color and human skin tone. Genes for salinity tolerance constituted the majority of adaptive candidates identified in this genome scan (23/31) and included vasoconstriction hormones that can flexibly modify osmotic balance in tune with the tidal cycle by influencing both drinking behavior and kidney physiology. Other salt tolerance genes had potential pleiotropic effects on bill depth and melanism (6/31), offering a mechanistic explanation for why these traits have evolved together in coastal swamp sparrows, and in other organisms that have converged on the same salt marsh syndrome. As a set, these candidates capture the suite of physiological changes that coastal swamp sparrows have evolved in response to selection pressures exerted by a novel and challenging habitat.