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.