Rapid evolutionary divergence of a songbird population following recent colonization of an anthropogenic habitat

Abstract

Colonization of a novel environment by a few individuals can lead to rapid evolutionary change, yet evidence of the relative contributions of neutral and selective factors in promoting divergence during the early stages of colonization remain scarce. We explore the role of neutral and selective forces in the divergence of a unique urban population of the dark-eyed junco (Junco hyemalis), which became established on the campus of the University of California at San Diego (UCSD) in the early 1980s. Previous studies based on microsatellite loci documented significant genetic differentiation of the urban population as well as divergence in phenotypic traits relative to nearby montane populations, yet the geographic origin of the colonization and the factors involved remained uncertain. Our genome-wide SNP dataset confirmed the marked genetic differentiation of the UCSD population, and we identified the coastal subspecies pinosus from central California as its sister group instead of the neighboring mountain population. Demographic inference recovered a separation from pinosus as recent as 20 to 32 generations ago after a strong bottleneck, suggesting a role for drift in genetic differentiation. However, we also found significant associations between habitat variables and genome-wide variants linked to functional genes, some of which have been reported as potentially adaptive in birds inhabiting modified environments. These results suggest that the interplay between founder events and selection may result in rapid shifts in neutral and adaptive loci across the genome, and reveal the UCSD junco population as a case of contemporary evolutionary divergence in an anthropogenic environment.