Introduction
Colonization of newly available habitats has led to some of the most
conspicuous cases of biological diversification known in natural systems
(e.g. Carson & Kaneshiro 1976; Lerner et al. 2011; Sato et
al. 2001), raising questions about the relative roles of random founder
effects and selection in population divergence (Carson 1975; Mayr 1963;
Price et al. 2010; Templeton 1980). Population divergence
following colonization can occur due to both local adaptation to novel
selective pressures (Rundle & Nosil 2005; Schluter 2000), and to
stochastic effects derived from rapid changes in effective population
size (Charlesworth 2009; Lande 1980; Simpson 1953). Founder effects and
directional selection may result in rapid shifts in allele frequencies
and accelerated rates of trait evolution, as shown by instances of rapid
evolution following colonization events at time scales of thousands to a
few million years (e.g. Lerner et al. 2011; Millien 2006; Satoet al. 2001; Seehausen 2006; Wessel et al. 2013), to
scales as short as a few decades (e.g. Chen et al. 2018; Jensenet al. 2017; Mathys & Lockwood 2011; Sendell-Price et al.2020). In the context of global environmental change, contemporary
colonization of modified habitats provides the opportunity to study
evolution in progress (Colautti & Lau 2015; Huey et al. 2000;
Johnson & Munshi-South 2017; Perrier et al. 2020; Reznick &
Ghalambor 2001; Salmón et al. 2021), and to understand the
relative contributions of directional selection, phenotypic plasticity,
gene flow and demography in driving rapid divergence in newly
established populations (Campbell-Staton et al. 2020; Szulkinet al. 2020b).
A potential case of contemporary colonization is provided by a suburban
population of the Oregon junco (Junco [hyemalis ]oreganus ), a small passerine that typically inhabits
mixed-coniferous forests of western North America (Miller 1941; Nolanet al. 2002). In the early 1980s, a group of Oregon juncos became
naturally established on the campus of the University of California at
San Diego (UCSD) (McCaskie 1986; Rasner et al. 2004; Yeh 2004),
on the coast of the Pacific Ocean. More recently, other Oregon junco
populations have been identified in suburban areas of southern
California, where they inhabit a mixed landscape of buildings and park
areas. The early colonists from UCSD continued breeding and formed a
resident population of about 70 pairs that has remained stable (Atwellet al. 2014; Yeh & Price 2004). Mark-recapture studies have
shown that they are year-round residents at UCSD, but between September
and May they are joined by small flocks of wintering Oregon juncos
coming from other populations (Fudickar et al. 2017; Unitt 1984;
Yeh 2004).
The Oregon junco is composed of various geographic forms that originated
recently as part of the postglacial radiation of the dark‐eyed junco
(Junco hyemalis ), following the northward recolonization of the
North American continent as ice sheets receded after the Last Glacial
Maximum (LGM), ca. 18,000 years ago (Friis et al. 2016; Miláet al. 2007). The Oregon junco has been traditionally divided
into at least seven geographically structured forms showing considerable
phenotypic and habitat variation (Dwight 1918; Friis et al. 2018;
Miller 1941; Nolan et al. 2002). These forms include, from south
to north: townsendi from the San Pedro Martir mountains in
northern Baja California, Mexico; pontilis from the Sierra Juarez
mountains, also in Baja California; thurberi from the mountains
of southern to northern California; pinosus from the coastal
region of central California; montanus from the interior regions
of Oregon, Washington and British Columbia; shufeldti from
coastal regions of Oregon and Washington; and oreganus from
coastal British Columbia and southern Alaska (Miller 1941; Nolanet al. 2002) (Fig. 1).
Previous studies on the ecology and evolution of the UCSD junco
population have generally assumed that it originated from the nearest
breeding population of Oregon juncos, located in the Laguna Mountains,
70 km east of UCSD (Fig. 1), based on the appearance of birds sampled
during the non-breeding season. This population belongs to the
subspecies thurberi and inhabits elevations above 1,500 m, a
montane habitat with a more extreme temperature regime than the milder
Mediterranean climate of the UCSD campus (Unitt 1984; Yeh & Price
2004). Studies published to date have focused on the evolution of social
signaling traits during colonization of a novel environment (Priceet al. 2008; Reichard et al. 2020; Yeh 2004); the role of
plasticity in population persistence during the early stages of
colonization (Price et al. 2008; Yeh & Price 2004); patterns of
morphological and genetic variation in comparison with other California
populations, using both microsatellites (Rasner et al. 2004) and
MHC loci (Whittaker et al. 2012) and hormonal changes underlying
shifts in phenotypic and life-history traits during adjustments to urban
environments (Atwell et al. 2012; Atwell et al. 2014;
Fudickar et al. 2017). Based on phenotypes of over-wintering
non-resident birds and proximity to potential sources, Yeh (2004)
proposed that the population of UCSD juncos had likely originated from
the thurberi population in the nearby mountains as a result of
overwintering birds remaining to breed. Simulation-based analyses using
microsatellite data reported in Rasner et al. (2004) were congruent with
the hypothesis that the UCSD population experienced a founder event,
with the Ne of the founding population ranging from 7 to
70 birds. Fudickar et al. (2017) used genome-wide SNP data to
distinguish between year-round residents and wintering visitors at UCSD,
and revealed marked differentiation of UCSD residents with respect to
other Oregon junco populations. Divergence levels were in fact
comparable to those found among dark-eyed junco lineages originated
during the post-glacial radiation of the complex (Friis et al.2016; Friis et al. 2018; Friis & Milá 2020), suggesting that
high-throughput SNP data may provide a level of phylogenetic resolution
not afforded by the more limited genetic sampling of previous studies.
Here we use genome-wide SNP data and extensive geographic sampling of
Oregon junco forms across the region to reconstruct the evolutionary and
demographic history of the UCSD junco population. First, we use
phylogenetic and co-ancestry analyses to identify the source junco
population from which the UCSD population originated. We then apply
demographic modelling to test whether the UCSD population is more likely
to have resulted from a founder event ca. 30 generations ago, as
previously assumed based on the date of appearance at UCSD, or instead
diverged elsewhere for a longer period before colonizing the campus. We
also use feather isotope ratios to determine whether birds that appear
to be winter visitors at UCSD based on genetic data have indeed bred at
a different latitude as opposed to being recent recruits into the
resident breeding population. Finally, to infer potential selective
pressures involved in rapid genetic divergence, we implement a
genotype-environment association (GEA) analysis, and take advantage of a
newly annotated version of the Junco hyemalis reference genome
(Feng et al. 2020; Friis et al. 2018) to identify
candidate loci under divergent selection.