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

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 (ΦST=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.

Typical versions of learned swamp sparrow song types are more effective signals than are less typical versions

The learned songs of songbirds often cluster into population-wide types. Here, we test the hypothesis that male and female receivers respond differently to songs depending on how typical of those types they are. We used computational methods to cluster a large sample of swamp sparrow ( Melospiza georgiana ) songs into types and to estimate the degree to which individual song exemplars are typical of these types. We then played exemplars to male and female receivers. Territorial males responded more aggressively and captive females performed more sexual displays in response to songs that are highly typical than to songs that are less typical. Previous studies have demonstrated that songbirds distinguish song types that are typical for their species, or for their population, from those that are not. Our results show that swamp sparrows also discriminate typical from less typical exemplars within learned song-type categories. In addition, our results suggest that more typical versions of song types function better, at least in male–female communication. This finding is consistent with the hypothesis that syllable type typicality serves as a proxy for the assessment of song learning accuracy.