The genetic consequences of historic climate change on the contemporary population structure of a widespread temperate North American songbird

Studies of widely distributed species can inform our understanding of how past demographic events tied to historic glaciation and ongoing population genetic processes interact to shape contemporaneous patterns of biodiversity at a continental scale. In this study, we used whole-genome resequencing to investigate the current population structure and genetic signatures of past demographic events in the widespread migratory American goldfinch (Spinus tristis). Phylogenetic relationships inferred from whole mitochondrial genomes were poorly resolved. In contrast, a genome-wide panel of > 4.5 million single nucleotide polymorphisms (SNPs) strongly supported the existence of eastern and western populations separated by western mountain ranges and additional population structuring within the western clade. Demographic modeling estimated that the eastern and western populations diverged approximately one million years ago, and both populations experienced subsequent population bottlenecks during the last glacial period. Species distribution models showed a severe contraction of suitable habitat for the American goldfinch during this period, with predicted discontinuities that are consistent with multiple, isolated glacial refugia that coincide with present-day population structure. Low overall genetic differentiation between the eastern and western populations (F-ST similar to 0.01) suggests ongoing gene flow accompanied divergence, and individuals with admixed genomic signatures were sampled along a potential contact zone. Nevertheless, outlier SNPs were identified near genes associated with feather color, song, and migratory behavior and provide strong candidates for further study of the mechanisms underlying reproductive isolation and speciation in birds.