INTRODUCTION
Studies of local adaptation have long bridged the interface between
ecological and evolutionary questions by exploring how populations adapt
to differing environmental conditions. Traditionally, high degrees of
local adaptation were expected to be present only in fairly isolated
populations—those free from the homogenizing effects of high gene
flow—with a long history in those locations, providing the time
thought to be necessary for local adaptation to evolve (Lenormand,
2002). We now know that local adaptation occurs frequently even in
systems with high gene flow (Yeaman & Whitlock 2011; Tigano & Friesen,
2016) and often rapidly after colonization of a novel environment
(Prentis et al. , 2008). We continue to find evidence for rapid
local adaptation in systems as divergent as cane toads (Rollins et
al. , 2015), sticklebacks (Lescak et al. , 2015), honeybees
(Avalos et al., 2017), steelhead trout (Willoughby et al.,2018), deer mice (Pfeifer et al., 2018), and many more. These
studies show that many taxa can adapt rapidly to local conditions in
response to the new selection regimes they encounter as they expand
their range.
Invasive species that have recently expanded into new locations provide
tractable opportunities to investigate local adaptation as it originates
(Colautti & Lau, 2015). Invasions typically expand from the founding
population(s) following a predictable spatial and temporal pattern
(reviewed in Excoffier et al ., 2009). After successful
colonization of a new habitat, many invasive species show a demographic
boom that may be facilitated by their ecological release in the new
environment; ecological release is the concept that introduced species
are often released from top-down limitations to their population growth,
such as predators or pathogens in their native range (Riccardi et
al., 2013). Theory predicts that this rapid population growth will
plateau as the population approaches carrying capacity in a region, but
successful invasive species may continue to expand their range and thus
maintain a high rate of overall population growth.
When population density increases and demographic rates change,
introduced species may rapidly evolve traits that enable them to spread
(Szűcs et al. , 2017): for example, invasive cane toads in
Australia evolved a suite of morphological, physiological, and
behavioral traits that facilitated their expansion in only 80 years
(Rollins et al., 2015). Increased dispersal may evolve in concert
with the demographic boom, such that certain traits are selected for in
successful invasive species. Flexible dispersal strategies can result in
gene flow that counteracts inbreeding depression and increases adaptive
potential (Garant et al., 2007; Rius & Darling, 2014). If
particular traits enable individuals to disperse more easily to their
preferred habitat, gene flow may be directional and even adaptive
(Edelaar & Bolnick, 2012; Jacob et al., 2017). Invasions thus
allow us to observe interactions between demography and the early
processes of selection (Dlugosch et al., 2015) as populations
experience new environments. Importantly, these eco-evolutionary
interactions depend in part on the genetic variation in the established
population.
Recent work in invasion genetics aims to tease apart how selection and
demography might resolve a paradox of invasion (Estoup et al. ,
2016, Schrieber & Lachmuth, 2017): many invasive species experience
genetic bottlenecks as a result of an initial founder effect, but often
thrive and spread despite this loss of standing genetic diversity.
Theory predicts that introductions will typically result in an initial
contraction in population size and/or genetic diversity (Dlugosch &
Parker, 2008). However, bottlenecks of genetic variation clearly do not
limit the success of many invasive species (Schmid-Hempel et al.,2007; Dlugosch & Parker, 2008; Facon et al., 2011). Invaders
might adapt through soft sweeps that reduce genetic diversity while
selecting for adaptive variants from standing or novel genetic
variation, which is especially likely in the case of ecological
adaptation (Messer & Petrov, 2013). Furthermore, some invasions may
increase rather than reduce genetic diversity, as when multiple
invasions from different source populations introduce previously
isolated alleles and thereby facilitate admixture (Dlugosch & Parker,
2008). The new conditions can also select among standing variation,
where the presence of certain genetic variants in the native range
accelerates adaptation upon introduction (Tsutsui et al., 2000;
Schlaepfer et al., 2009; Hufbauer et al., 2011). In sum,
although genetic diversity in introduced populations is often viewed as
a pre-requisite to adaptation, changes in genetic diversity alone do not
explain invasiveness (Uller & Leimu, 2011). Regardless, chance may be
just as important as selection in an invasive species’ establishment and
spread (Gralka & Hallatschek, 2019).
The European starling (Sturnus vulgaris ) stands out as an
exceptionally successful avian colonist and invasive species. In North
America, an estimated 200 million starlings currently range from
northern Mexico to southern Alaska (Linz et al., 2007).
Introduced to New York City in 1890, starlings nearly covered the
continent within a few generations by expanding up to 91 km each year
(Bitton & Graham, 2014). The 1890 introduction is widely accepted as
the first successful establishment of starlings in North America, but
several populations were introduced in Cincinnati, OH (1872), Quebec,
Canada (1875), Allegheny, PA (1897), and Springfield, MA (1897), with
the second-most successful having been introduced to Portland, OR in
1889 (Forbush, 1915; Kalmbach & Gabrielson, 1921). Records indicate
that none of the earlier starling introductions survived more than a few
years after colonization, but it is possible that some populations in
the western U.S. persisted without record (Kessel, 1953).
During the starling expansion, ongoing migration and dispersal might
have also influenced patterns of genetic variation. In North America,
some—but not all—starling populations migrate (Dolbeer, 1982).
Previous studies indicate that there is considerable variation in
migratory distances within flyways (Burtt & Giltz, 1977). Models of
molt origin indicate that starlings in the western U.S. may disperse or
migrate shorter distances (Werner, Fischer, & Hobson, 2020). The models
used feathers from the same individuals sampled for this genetic survey,
and they initially hypothesized that starlings in the south may be less
likely to migrate long distances. Instead, they found that longitude
better explains the differences in molt origin among starling
populations: starling feathers collected west of -90° longitude were
more likely to have originated nearby. In other words, starlings that
migrate in eastern North America likely experience greater gene flow
among sampling locations (states, in our study), but overall starlings
tend to move only regionally and not continent-wide.
Early genetic work based on a small set of allozyme markers indicated
near-random mating at a continental scale in North American starlings,
with large demes (subpopulations) and high dispersal rates (Cabe, 1998;
Cabe, 1999). Here we use robust genomic markers to explore the genomic
and demographic patterns of range expansion in North American starlings
with three specific aims: (1) to characterize genome-wide levels of
diversity and differentiation among starlings; (2) to examine how
genetic variation changes across the contiguous United States; (3) to
test for a genetic bottleneck; and (4) to test for signatures of
selection associated with environmental gradients. We also interpret our
results in the context of range-wide data on starling migration and
dispersal (Werner, Fischer, & Hobson, 2020), as this movement certainly
influences population structure. Recent developments in
genotype-environment association methods can identify polygenic traits
which are locally adapted to overlapping environmental gradients
(Forester et al., 2018; Capblancq et al., 2018), whereas
traditional outlier-based methods may not recover evidence of local
adaptation in a species that likely has low overall levels of genetic
diversity. Especially with these more sensitive methods, the same low
genetic diversity resulting from a founder effect upon colonization
could improve our ability to discriminate signatures of selection from
low background divergence across the genome (Dlugosch et al.,2015). This work employs modern genomic and analytical tools to examine
the evolutionary history of this remarkably successful avian invasion.