Rapid evolutionary divergence of a songbird population following recent colonization of an urban area

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.