Is a handful of genes responsible for the common starling invasion
success?
Invasive species have the ability to colonize new habitats across
distinct areas of the globe, rapidly adjusting to new biotic and abiotic
conditions, and often experiencing little impact from the decrease in
effective population size and genetic diversity. Still, as each invading
population represents a subsample of the original native distribution,
it is frequent to see variability in terms of the genetic makeup of
invading populations and consequently differences in invasion success
rates across their non-native range (Blackburn et al. 2017).
Invasion success results largely from a combination of the genetic
diversity in the native populations, the number of founders and founder
events that are effectively get established at the introduction sites,
the presence of particularly important genes or new interactions between
genes, and genotype x environment associations (GEAs) (Lee 2002;
Blackburn et al. 2017). From the genetic side of the process,
invasive populations undergo dramatic changes compared to their native
range due to a combination of genetic bottlenecks from the source
population with genetic drift at both the introduction site and at the
expansion front as the species invades new habitat (Dlugosch & Parker
2008). Most differences are observed at the neutral level, as quick
range expansions lead to an increase in frequency of random neutral
variants at the range expansion front, termed allele surfing (Excoffieret al. 2009). But allele surfing might also lead to an increase
in frequency of maladapted alleles, which might limit the expansion
success of invading populations (Peischl & Excoffier 2017).
The common starling (Sturnus vulgaris ) is an example of a
worldwide invasive species that has been introduced most successfully
from its Palearctic range into three other continents including North
America, Africa and Australia. Still, the success of the introductions
seems to vary between introduction sites. The biggest difference in
introduction success might be that found between North America and
Australia. Starling invasion of North America started with an
introduction of ~160 birds in the east coast in 1890s
that rapidly expanded across all of North America, establishing
populations in the west coast within 50 years (Bodt et al. 2020).
In Australia, while starlings were introduced at five locations about
sixteen times since the 19th century, only two
resulted in established populations (Bodt et al. 2020),
suggesting the existence of stronger barriers to expansion than in North
America. In a From the Cover article in this issue of Molecular Ecology,
Stuart and Cardilini et al. (2020) used Genotyping-by-Sequencing
to explore how landscape and environmental heterogeneity shaped the
genetic population structure and adaptation of the common starling
multiple invasions of Australia, and compare it to the patterns observed
in North America, examined in Hofmeister et al. (2019). Stuart
and Cardilini et al. (2020) determined that starlings in
Australia are distributed across three distinct environmental groups
characterized by temperature and precipitation in ‘arid’, ‘semi-arid’
and ‘non-arid’. However, neutral and adaptive population structure was
incongruent with the defined environmental subdivision, rather showing a
pattern of isolation-by-distance (IBD). This pattern was further
supported by the levels of genetic diversity and divergence across
populations. Genetic diversity decreased with distance from the
introduction sites in SE Australia, and genetic differentiation between
populations increased with geographic distance (Figure 1A and 1B). These
patterns contrast with those observed at other regions of the world
where starlings have been introduced (Hofmeister et al. 2019;
Bodt et al. 2020). The starling invasion of North America showed
a genetic pattern not consistent with IBD, but rather with
isolation-by-environment. In accordance to the rapid continent wide
expansion, Hofmeister et al. (2019) also found very low
differentiation between sampling localities, indicating not only high
dispersal ability but also a panmictic population across the entire
North America. Studies on invasion genetics clearly indicate that
multiple introductions lead to increased genetic diversity, which in
turn provide increased chances to expand into more diverse areas (more
genomic targets of selection) (Dlugosch & Parker 2008; Blackburnet al. 2017). However, despite multiple successful introductions
in Australia vs. a single introduction in North America, the extent of
the invasion is smaller in Australia and the levels of population
differentiation were found to be higher. The authors propose that
despite the higher genetic diversity, there could also be greater
constraints for gene flow, potentially attributed to environmental
(dis)similarities of the different introduction sites in Australia with
the native range. The North American climate is more similar to that of
the native range of the starling in the Palearctic, and thus it would be
expected that population structure would be more evident in Australia
where individuals would have to adapt to more extreme conditions than
they were adapted in the native range (Colautti & Lau 2017). To
understand the role of environmental variability on expansion, both
studies performed outlier-scans and GEAs to identify loci under
selection. Contrarily to initial expectations, outlier scans failed at
providing strong evidence of selection in association with population
structure or environmental variability. In the case of North American
starling, this could result from a low genetic diversity across
populations, approaching what would be expected in panmixia. In the case
in Australian starlings, even in the presence of population structure,
outlier detection might simply reflect stochastic patterns as a result
of allele surfing. Using redundancy analyses to detect GEAs, both
studies found evidence of adaptation to temperature and precipitation.
Stuart and Cardilini et al. (2020) found associations of the
populations found in ‘arid’ regions with environmental variables that
relate to higher and less variable temperatures, and with increased
variability in precipitation (Figure 1C and 1D). Associations with the
other environmental regimes (‘semi-arid’ and ‘non-arid’) were not as
clear, although subdivision of populations in the GEA analysis space
appeared to match neutral population structure for these populations.
Similarly, Hofmeister et al. (2019) also detected associations
between population structure and environmental variables, particularly
mean annual temperature.
One of the most interesting results that emerges from the combined
analysis of both studies is the identification of similar loci under
selection in both Australia and North America. Two genes were reported
as candidates for selection in both studies, and both are related to
cell structure regulation, suggesting a potential association with cell
viability in variable and extreme environments. As noted by many other
studies, successful invasions might only need to encompass a few genes
that then become important for adaptation to novel conditions (Lee 2002;
Nadeau & Urban 2019). Selection in just a few key loci can be easily
spread in species with high mobility, also benefiting from allele
surfing, leading to a rapid increase in frequency at the range expansion
front and potentially across the entire invasive range. This might
explain how such distinct invasion histories as those found across the
starling populations around the world led to contradicting expectations
in terms of invasiveness (Bodt et al. 2020). Still, the role of
other mechanisms such as plasticity, genomic rearrangements, epigenetic
variation, among others, still needs to be further examined to fully
explain the differences in starling invasion dynamics (Bock et
al. 2017). The results provided by Stuart and Cardilini et al.(2020) evidenced that particularly advantageous loci can be positively
selected multiple times, across multiple introduction events and through
very distinct geographic contexts, despite low effective population
sizes and various demographic scenarios. This manuscript suggests that
the common starling invasion success around the world has been greatly
impacted by a hand full of genes that allow adaptation to extreme
environmental conditions. But additional research in other less
successful introduction sites should provide further evidence into the
mechanisms involved in the invasion success and allow to build a more
comprehensive picture of the mechanisms involved.