Colonization of a novel environment by a small group of 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. Here, we use genome-wide SNP data to test the role of neutral and selective forces in driving the divergence of a unique urban population of the Oregon junco (Junco hyemalis oreganus), 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 sexual signaling and life-history traits relative to nearby montane populations. However, the geographic origin of the colonization and the factors involved in the onset of the differentiation process remained uncertain. Our genome-wide SNP dataset confirmed the marked genetic differentiation of the UCSD population, and phylogenomic analysis identified the coastal subspecies pinosus from central California as its sister group instead of the neighboring mountain population. Demographic inference based on site frequency spectra recovered a time of separation from pinosus as recent as 20 to 32 generations, and a strong bottleneck at the time of colonization, suggesting a relevant role of founder effects and drift in the genetic differentiation of the UCSD population. However, we also found significant associations between environmental parameters characterizing the urban habitat of UCSD and genome-wide variants linked to functional genes. Some of the identified gene functions, like heavy metal detoxification and high-pitched hearing, have been reported as potentially adaptive in birds inhabiting urban environments. These results suggest that the interplay between founder events and directional selection may result in rapid shifts in both neutral and adaptive loci across the genome, and reveal the UCSD population of juncos as an ongoing case of divergence following the colonization of an anthropic environment.

All methods and protocols are described in detail in the article.

All methods and protocols are described in detail in the article.