Low genomic divergence and high gene flow between locally adapted populations of the swamp sparrow

Abstract

Populations that have recently diverged across sharp environmental gradients provide an opportunity to study the mechanisms by which natural selection drives adaptive divergence. Inland and coastal populations of the North American swamp sparrow have become an emerging model system for studies of natural selection because they are morphologically and behaviourally distinct despite a very recent divergence time (<15,000 years), yet common garden experiments have demonstrated a genetic basis for their phenotypic differences. We characterized genomic patterns of variation within and between inland and coastal swamp sparrows via reduced representation sequencing in order to reconstruct the contributions of demography, gene flow and selection to this case of recent adaptive divergence. Compared to inland swamp sparrows, coastal swamp sparrows exhibited fewer polymorphic sites and reduced nucleotide diversity at those sites, indicating that a bottleneck and/or recent selective sweeps occurred in that population during coastal colonization and local adaptation. Estimates of genome-wide differentiation (FST=0.02) and sequence divergence ({Phi}ST=0.05) between inland and coastal populations were very low, consistent with postglacial divergence. A small number of SNPs were strongly differentiated (max FST=0.8) suggesting selection at linked sites. Swamp sparrows sampled from breeding sites at the habitat transition between freshwater and brackish marshes exhibited high levels of genetic admixture. Such evidence of active contemporary gene flow makes the evolution and maintenance of local adaptation in these two populations even more notable. We summarize several features of the swamp sparrow system that may facilitate the maintenance of adaptive diversity despite gene flow, including the presence of a magic trait.