Discussion
The redistribution of species globally has ignited interest in and
urgency for understanding eco-evolutionary dynamics of range shifts.
Foundational theoretical work has provided a basis for understanding the
interplay between stochastic and deterministic forces in facilitating or
hindering range expansion. In many cases, range expansions are expected
to lead to higher divergence and lower genetic diversity at the
expanding edge compared to the core due to small population sizes,
serial bottlenecks, reduced gene flow, and selection pressures . This
mixture of neutral and adaptive processes across the expansion axis
often leads to spatial structuring and patterns of isolation by distance
. Termed a “pulled wave”, the founders at the range edge pull the
expansion forward through increased dispersal and reproduction that
stratifies demes . However, the opposite pattern of maintained/increased
genetic variance at expansion fronts has also been reported in several
empirical studies . Conceptual frameworks term these cases “pushed
waves,” where genetic variation is maintained at the range edge due to
gene flow from the range core and potentially positive density
dependence, novel interspecific competition or environmental stress that
result in less genetic sorting at the edge . These varying outcomes
suggest that the interplay between neutral and selective evolutionary
processes create variation in range expansion outcomes giving rise to
more nuanced approaches to eco-evolutionary dynamics. . In the
well-documented contemporary range expansion in C. anna ,
we show patterns largely consistent with expectations of a “pushed
wave” expansion; gene flow is high throughout the entire range and we
find no strong divergence in allele frequencies between the core of the
range and expansion fronts. We do find reduced genetic diversity at
expansion fronts, which are characteristic of pulled waves, but the
magnitude of the reduction in genetic diversity is small. Together our
evidence highlights both the complexity of rapid range shifts in natural
populations and potential limitations of genomic data in investigating
eco-evolutionary phenomena.
Evidenced by low species-wide genetic divergence and a lack of spatial
structuring or signals of selection at the expansion edges or
species-wide, we show that C. anna has few, if any, limits
to gene flow. These results support a previous genetic study in C.
anna that found no genetic structure among three California populations
using mitochondrial DNA . The preservation of genetic diversity across
the expanded ranges is consistent with recent, rapid range expansions
characterized by a short time frame, growing population sizes, and
multiple independent expansion fronts. Our results align with the
well-documented rapid range expansion in C. anna over the past 80
years . While movement details remain enigmatic, C. anna has a
broad diet, relatively large territories, and some seasonal migration
that was documented based on abundance data , all of which could
contribute to high gene flow in this system. Regardless of the
mechanism, we observe no population structure and little evidence for
increased differentiation at the expansion fronts. Long-distance
dispersal, especially from the core, has been shown to preserve genetic
diversity in other taxa . This result is often seen in highly mobile
species and recent invasions. Examples of high gene flow within species
in newly colonized territories include the following: invasive
Indo-Pacific lionfish (Pterois volitans ) in the Caribbean
, European starlings (Sturnus vulgaris ) in South Africa
and North America , Pyrenean rocket (Sisymbriumaustriacum ) in the Meuse River Basin , and round gobies
(Neogobius melanostomus ) in the Great Lake tributaries .
The similarities with colonizing species expansions (e.g., propagule and
dispersal pressure, novel biotic and abiotic interactions) underscore
the emerging work viewing range shifts and expansions of native species,
especially those caused by climate change, through the lens of invasion
biology . By incorporating theory from invasion biology including
assessing the potential impacts, positive and negative, of colonizing
species on novel environments, we can gain a more holistic understanding
of range expansion.
Range expansions often expose species to novel environments containing
new combinations of biotic and abiotic interactions that can coincide
with niche shifts, expansions, or unfilling . Previous modeling showed
that the expanded regions fell within C. anna’s fundamental
climatic niche prior to the range expansion, suggesting that previous
range limits were defined by the presence of resources . Although it is
possible that selection was overlooked due to the limitations of genome
scans (see below), the lack of selective signatures between the core and
expanded ranges identified here aligns with the previous hypothesis that
the range expansion in C. anna could be the result of an
ecological release facilitated by human-mediated landscapes. This
hypothesis states that introduced plants and supplemental feeding have
allowed C. anna to fill out its existing climate niche even in
the expanded regions. While other ecological factors induced by
urbanization and climate change could also be aiding the expansion, a
similar pattern of spatial expansion and ecological release associated
with supplemental feeding has been documented in Eurasian Blackcap
warbler . Together, these studies provide evidence for the role of local
anthropogenic alterations of the landscape shaping broadscale shifts in
species’ ranges.
High gene flow can be maladaptive at the expansion edge and inhibited
selection during pushed wave expansions often slows and/or prevents
further range expansion , such as the southeastern invasion edge of cane
toads in Australia that is thought to be limited by cold temperatures .
Despite this paradigm, C. anna expansions do not appear to be
hindered by gene flow from the range core or lack of selection at the
expanding edge, adding to the growing literature that gene flow does not
limit species ranges or their range expansions (Kottler, Dickman,
Sexton, Emery, & Franks, 2021). This again supports the hypothesis that
the C. anna range was potentially limited by resource
availability and thus adaptation may not be required for expansion.
Recently, a growing breeding population of C. anna has been found
in Idaho , an area predicted to be suitable for C. anna .
Southeast Washington state and sections of Utah are also predicted to
have suitable habitat for C. anna , potentially suggesting that
the expansion will continue in the coming decades.
Despite high gene flow and lack of genomic signatures of selection, we
do find very subtle evidence of classic core-edge patterns of genetic
diversity. While we did not detect structure in the PCA or admixture
analysis, we observed lower nucleotide diversity at both expansion
fronts. This result could indicate that mating is not completely random
across the entire range despite high gene flow . Increased relatedness
among individuals due to small populations sizes could drive the
decrease, however this does not appear to be the cause in C.
anna . Alternatively, lower genetic diversity could be a result of
decreased observed individual heterozygosity, which is what we observed.
The loss of heterozygosity at the expansion front could be caused by
genetic drift, specifically in response to population bottlenecks or
allele surfing or by selective sweeps in the expanded ranges, although
we were not able to detect any with our genome scans. Relatedly, many of
the northern expansion front samples were collected in earlier years
(2000 vs late 2010s) which may represent a time point closer to a
founding bottleneck before more birds dispersed from the core, a pattern
previously suggested in the invasive Indo-Pacific lionfish . However,
this decreased heterozygosity does not appear to be strong and
consistent enough to result in signatures of divergence and selection
between the range core and expansion fronts.
The seemingly contradicting observations of decreased genetic diversity
in the absence of signals of selection or structure could have several
biological or technical explanations. One possibility is that the
expansion is too recent for the detection of significant divergence in
range edge populations and more differentiation may develop over time.
Further, our low-coverage approach and moderate sample size may not have
the power to detect multiple small shifts in allele frequencies across
loci that could lead to adaptive evolution, a common issue with
genome-wide scans for polygenic traits (Kemper, Saxton, Bolormaa, Hayes,
& Goddard, 2014; Pritchard, Pickrell, & Coop, 2010). Reduced diversity
in the expanded regions could therefore reflect this weak genome-wide
selection that was not detected at any single SNP. Alternatively,
environment-mediated trait differences may be plastic - perhaps looking
at gene expression or plasticity would provide a more
timeframe-appropriate picture of how these birds are responding to the
novel environments at the expansion edges. For example, there is
widespread use of torpor in Trochilidae and C. anna is no
exception. In fact, C. anna were found to increase their use of
torpor in cold temperatures . Plastic behavioral changes at the
expansion edges, such as increased use of torpor, could account for how
these birds are surviving colder northern temperatures without seeing
genetic changes, and warrant further study. Finally, our samples
represent a single snapshot in time thus cannot rule out that selection
is happening at the range edges, but not enough time has passed to shift
allele frequencies that would be detected in the current study,
especially in the face of high gene flow.
Anthropogenic influences are changing the genetic landscape through
shifting species ranges. Much of the recent focus has been on the role
of climate change in facilitating range shifts and the likely
eco-evolutionary dynamics of these phenomena. However, this study
demonstrates that not all expanding species respond in predicted ways,
in fact, not all human-induced range expansions show obvious signatures
of evolution. Further work is needed to confirm these results and test
the stability of our conclusions over time. For example, using museum
specimens to understand the genetic landscape in C. anna before
the expansions could confirm past gene flow or illuminate if increased
urbanization is decreasing genetic diversity, increasing homogenization,
or favoring certain alleles. Additionally, while we focused on the
northern and eastern expansions, sampling individuals from what might be
the “trailing edge” in Mexico would further our understanding of
whether climate or resources are defining species range limits inC. anna . This study contributes to the growing literature on the
consequences of human-mediated range expansions by adding empirical
evidence that eco-evolutionary dynamics are not one-size fits all.