Introduction
The study of species’ geographic limits encompasses some of the most fundamental processes in ecology and evolution including dispersal, gene flow, and adaptation. Species’ ranges can be limited by abiotic factors such as precipitation, day length, and soil chemistry as well as by biotic factors such as population density, interspecific interactions, and predator-prey relationships. Anthropogenic-induced changes in these factors can therefore result in rapid shifts in species abundance and distribution . For example, a staggering decline in North American bird abundance since 1970 has been documented and is potentially attributed to increased agriculture, urbanization, habitat loss, and climate change . However, not all environmental shifts result in population decline — some species have also been able to adapt to these changes or track optimal conditions, especially moving poleward and to higher elevation . In fact, a number of North American birds appear to be shifting their ranges northward due in part to warmer temperatures and land use changes . Contemporary shifts in species’ ranges provide an opportunity to examine the factors defining range limits in real time.
While the ecological causes of range expansions are often well documented, a complex combination of evolutionary processes also contribute to the push and pull of species distributions. A suite of evolutionary processes can promote range expansion including spatial sorting, natural selection, and genetic drift. Spatial sorting followed by assortative mating among successful colonizers can shift phenotypic traits associated with expansion, such as dispersal abilities, which in turn can lead to further colonization . Selection on life history traits that increase the reproductive rate can also promote range expansion, as can adaptation to novel environments . Large-effect mutations may increase expansion potential , but limits to genetic variance also affect the capacity for expansion . In contrast, evolutionary processes can also slow or inhibit range expansion. Small population sizes and serial bottlenecks at the range edge lead to strong genetic drift, which decrease genetic variation and expansion potential . Density-dependent dynamics such as the Allee effect limit population growth and therefore expansion .
In combination, the theoretical and empirical literature show us that the same evolutionary processes can have conflicting effects on range expansion outcomes depending on the context . For example, allele surfing, the fixation of alleles along an expansion front, can lead to greater expansion potential if the fixed alleles are neutral or beneficial, but the fixation of deleterious alleles can reduce fitness at the edge — a phenomenon known as expansion load — reducing the expansion potential . Broadly, reduced gene flow from the species’ core to the range edge can decrease genetic diversity and thus adaptive potential. However, high gene flow can lead to either increased genetic diversity and higher evolutionary potential or a propagation of maladaptive alleles from the species core that can limit local adaptation at the edges . Understanding and predicting the dynamics of range expansions therefore requires an understanding of gene flow, genetic diversity, and adaptive divergence across the species range paired with a knowledge of the ecological context in which the range expansion is occurring.
A recent and dramatic range expansion in Anna’s hummingbird (Calypte anna) provides an ideal system to examine the evolutionary processes associated with rapid range expansion . The historical range of C. anna is central and southern California, USA and northwestern Mexico. By leveraging community science (Project FeederWatch, Christmas Bird Count) and museum data, previous studies showed a northern and eastern expansion starting around 1940 . Currently, C. anna can be found as far north as British Colombia, Canada and southern Alaska, USA and as far east as western Texas, USA. Human habitation and climate change appear to be the drivers of the expansion. In the expanded ranges C. anna individuals were more likely to colonize areas with higher housing density and were more likely to visit bird feeders compared to those in the historical range . However, like many North American migratory birds, they may also experience mortality associated with urban settings such as window collisions and encounters with domesticated animals . Increases in minimum winter temperatures were also shown to facilitate the expansion . However, Battey (2019) suggested that the range expansion was largely driven by an ‘ecological release’ facilitated by introduced plants and supplemental feeding, and that C. anna ’s climate niche had previously existed in the expanded ranges.
Little is known about genetic variation and population structure inC. anna beyond one study that showed low divergence between three California populations and sparse anecdotes of long-distance dispersal in C. anna . Further, the genetic makeup of populations in the expanded regions and whether they are adapting to the novel environments has not yet been explored. Here we present the first species-wide genomics study of C. anna , testing evolutionary hypotheses regarding their distribution. If range expansion is the result of spatial expansion of the historical fundamental niche linked to an increase in the presence of feeders and ornamental plants (Battey 2019), adaptation may not be necessary to facilitate expansion at the leading edge. However, many abiotic and biotic conditions vary across the range so although adaptation might not be required for expansion, it may still occur as the result of moving into a new environment. The degree to which adaptation occurs and can be detected in our data will depend on a number of factors, including gene flow across the range, the strength of selection, and the genetic architecture of traits under selection. The two leading edges (northern and eastern) allow us to compare these pseudo-replicate expansions, rare in most studies, to answer questions specifically about adaptation, gene flow, and genetic diversity across the native and expanded range, and broadly add to our understanding of eco-evolutionary dynamics in natural populations.