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.