Local Adaptation With Gene Flow Has a Polygenic Basis in a Threatened Coastal Songbird.

Abstract

Species that span heterogenous environments often exhibit local adaptation despite gene flow among populations. In such cases, the maintenance of local adaptation is controlled by several factors, including the strength of selection, migration, assortative mating, and genomic architecture. The song sparrow (Melospiza melodia) is a widespread songbird with diverse subspecies, including the coastally adapted Atlantic song sparrow (M. m. atlantica). Despite extensive gene flow with a generalist subspecies, Atlantic song sparrow populations have been found to maintain their coastally adaptive phenotypes. We produced a new chromosome-level reference assembly for the species and whole-genome data to explore the genomic architecture of divergence with gene flow and the genetic basis of adaptation in this subspecies. Adaptation in the Atlantic song sparrow has a polygenic basis, with loci under divergent selection scattered throughout the genome rather than concentrated in low-recombination linkage blocks. Signatures of fine-scale population structure, limited genomic differentiation, and divergent selection on a small set of genes suggest a role for natural selection in maintaining this subspecies boundary. Our findings highlight the complex interplay among selection, gene flow, and recombination in shaping adaptation with gene flow and provide insights into the genomic architecture of ecological divergence within a widespread, morphologically diverse species.