Invasive species represent a significant threat to global biodiversity
(Early et al., 2016; Dueñas et al., 2021). They are an important driver
of species extinction (Bellard et al., 2017) and can have a strong
negative impact on native species abundance (Emery-Butcher et al.,
2020). The strength of the impact of invasive species on native
populations and communities depends on their abundance and trophic
level, with invasive predators typically having the most substantial
impact (Bradley et al., 2019). The extent of a biological invasion in a
geographic location will be determined by the limits of habitat
suitability in the area (Liu et al., 2020). Environmental gradients can
be important barriers restricting invasive species’ unchecked advance
(Mothes et al., 2019). For example, the range of the invasive Asian clam
in North America and Europe is currently limited by its inability to
tolerate minimum temperatures lower than -10°C and by altitudes higher
than 2000m (Crespo et al., 2015). Thus, impacted native species that can
tolerate a broader range of environmental parameters than the invaders
may have access to refuge habitats free from invaders (Chapman et al.,
2002; Reid et al., 2013). However, across large spatial scales or strong
environmental gradients, it is unclear whether this type of
’physiological refugia’ results from universally broad physiological
tolerance in native species or local adaptation of populations
experiencing distinct environmental conditions. Moreover, invasive
predators might impose additional divergent selection on native species
because local populations that overlap with the invader could experience
selection for anti-predator traits (Strauss et al., 2006; Brookes &
Rochette, 2007). Indeed, among natural and anthropogenic stressors,
invasive species are one of the strongest drivers of phenotypic change
in native populations (Sanderson et al., 2022).
Local adaptation could interact with demographic processes to facilitate
or hinder the co-existence of native species with an invasive predator
by providing demographic subsidies, genetic rescue, or by introducing
maladaptive alleles to recipient habitats. While some sites can have
environmental conditions more conducive to invasion and therefore suffer
stronger biotic selection from invasion, other sites can have
environmental conditions that exclude or reduce the density of invasive
predators, thereby acting as uninvaded refuges with lowered ecological
impacts from the invaders (Derry et al., 2013; Reid et al., 2013; Astorg
et al., 2021; Morissette et al., 2023). In this scenario, refuge
populations could also potentially serve as a demographic subsidy of
individuals for invaded populations experiencing population decline
(Foppen et al., 2000; With et al., 2006), and prevent their extinction
through demographic rescue (Hufbauer et al., 2015). Genetic rescue can
additionally occur when migrants prevent the extinction of declining
populations through increased genetic diversity that reduces inbreeding
depression (Carlson et al., 2014; Whiteley et al., 2015; Fitzpatrick et
al., 2016); if this genetic variation includes adaptive alleles, then
genetic rescue can also lead to an evolutionary rescue, i.e. the
avoidance of extinction via adaptation (G. Bell & Gonzalez, 2011;
Sexton et al., 2011; Hufbauer et al., 2015).
Conversely, gene flow could instead bring maladapted alleles into
invaded populations if populations have experienced strong divergent
selection across the environmental gradient (Bolnick & Nosil, 2007).
Migration from refuges could consequently pose some risks if recipient
and source populations are divergent due to local adaptation, which can
cause genetic incompatibilities in hybrids and lead to temporary
reductions in fitness (i.e., outbreeding depression, Fenster &
Galloway, 2000; Edmands, 2007; Frankham et al., 2011; D. A. Bell et al.,
2019). Thus, there could be a tension between demographic rescue
(immigrants from refuge populations providing individuals to bolster the
shrinking populations in invaded habitat) versus these immigrants
potentially being maladapted, thereby reducing the mean fitness of the
invaded populations. It is thus important to understand how these two
sources of adaptation (to the refuge vs. to the predator) can interact
with demographic processes to either facilitate or hinder the ability of
a native species to avoid population decline from an invasive predator.
Genomic methods are increasingly used to understand species and
populations’ responses to sudden environmental changes induced by
anthropogenic activities such as invasive species (Stern & Lee, 2020)
and are an important tool for informing conservation (Willi et al.,
2022; Bernatchez et al., 2023). They can enable the assessment of
population connectivity, investigate demographic and genetic changes,
and detect the potential for genetic adaptation (e.g., Marques et al.,
2019). Reconstructing demographic changes can help assess potential
population declines induced by invasive species. Additionally, inference
of gene flow can identify the source and recipient populations in a
metapopulation impacted by the invaders. Finally, assessing genetic
adaptation can determine if source and recipient populations are
divergent because of local adaptation (Cure et al., 2017), thus altering
the likelihood of genetic and/or evolutionary rescue from genetically
differentiated populations. Hence, knowledge of evolutionary forces,
which can be elucidated through genomic tools, is critical for
understanding the overall response of native species to the impact of
biological invasions.
Gastropods have been widely used to study adaptation in response to
predation (Brookes & Rochette, 2007; Hooks & Padilla, 2021), with
abiotic factors such as calcium concentration modulating this response
through changes in shell morphology and behavior (Rundle et al., 2004;
Bukowski & Auld, 2014). As such, they are a useful biological study
model for addressing evolutionary responses to biological invasions.Amnicola limosus is a small dominant freshwater gastropod species
with a wide geographical distribution in the USA and Canada
(www.gbif.org/species/5192461). This gastropod does not have a pelagic
larval phase: egg masses are deposited on the substrate, and juveniles
move from the substrate to the macro-algal substrate (Pinel-Alloul &
Magnin, 1973). Part of the range of A. limosus has been invaded
by the round goby (Neogobius melanostomus ), a molluscivorous
fish, from the lower Great Lakes and running downstream throughout the
Upper St. Lawrence River (Hickey & Fowlie, 2005). Amnicola
limosus is commonly found in the stomach contents of round gobies, and
following the goby invasion of Lake Saint-Louis, A. limosuspopulations experienced a 0.5-1 mm reduction in shell size (Kipp et al.,
2012). Because the mean gape size of the round goby is larger than the
maximum size of A. limosus , round gobies do not have to crush the
snail, which suggests that shell size reduction is likely to be due to
reduced predation pressure on smaller and less visible individuals
(round gobies are visual predators; Kipp et al., 2012). A considerable
reduction in small gastropod abundance (down to 2-5% of the original
population size, with A. limosus being the most abundant species)
and species richness in the Upper St. Lawrence River were also reported
since the invasion of round gobies in this ecosystem in 2005 (Kipp et
al., 2012). However, round gobies cannot tolerate low calcium
concentrations (Baldwin et al., 2012; Iacarella & Ricciardi, 2015), and
have not invaded the Ottawa River (Ca2+ concentrations
below 22 mg/L; Sanderson et al., 2021; Morissette et al., 2023) at its
junction with the Upper St. Lawrence River. On the contrary, this low
calcium concentration is not a physiological limit for A. limosusembryonic development (> 1.1 mg/L; Shaw & Mackie,
1990), and Pinel-Alloul & Magnin (1973) showed that A.
limosus was present in the Ottawa river before the invasion of gobies,
indicating that this species can tolerate the calcium concentration
found in the Ottawa river. These calcium-poor waters are thus acting as
a refuge from goby predation in this system (Astorg et al., 2021;
Morissette et al., 2023). Calcium-poor waters could potentially provide
demographic subsidies for the native populations at invaded sites (e.g.,
amphipods; Derry et al., 2013).
This study aims to investigate the potential adaptation of A.
limosus to the water calcium gradient and the presence of round goby
invasion in the Upper St. Lawrence River, as well as the demographic and
genetic consequences of the goby invasion on the native gastropod. We
tested for evidence of local adaptation via 1) genome scans for SNPs
associated with calcium concentration and round goby presence and 2) a
laboratory reciprocal transplant of wild A. limosus individuals
to measure survival and fecundity in factorially-crossed treatments of
water calcium concentration and round goby chemical cue. For the local
adaptation to the low calcium and high goby predation environmental
conditions, we expected to find outlier SNPs associated with one or both
of these covariables. In the transplant experiment, we also expected
populations to show a home versus transplant advantage in life-history
traits relative to the calcium concentration and presence of goby cues.
For demography, because of the large decrease in the population size of
gastropods observed in the Upper St. Lawrence River following round goby
invasion (Kipp et al., 2012), we hypothesized that A. limosuspopulations in invaded habitats could have undergone a similar decrease
in abundance, perhaps accompanied by a genetic bottleneck. If so,
uninvaded populations could potentially provide demographic, genetic,
and evolutionary rescue for invaded populations (Hufbauer et al., 2015;
Whiteley et al., 2015). However, this possibility would depend on the
level of gene flow between habitats and the extent of adaptive
differentiation. Because the life history of A. limosus does not
involve a pelagic larval phase (Pinel-Alloul & Magnin, 1973), we
expected to observe low gene flow in the absence of strong water
currents. Low gene flow impedes demographic and genetic rescue, and
strong adaptive differentiation will likely hinder evolutionary rescue.
As such, we hypothesized that local adaptation to the distinct habitat
types might have led to reduced gene flow (isolation by environment;
Wang & Bradburd, 2014). Our paper provides a rare empirical study to
address how spatial heterogeneity in both abiotic conditions and
invasive predator presence can interact with demographic processes to
shape the response of a native species to biological invasion.
Freshwater environments are deeply impacted by invasive species
(Gallardo et al., 2016). It is important to not only consider ecological
impacts of invasion but also the evolutionary and demographic responses
in native species that can help foster invasive-native species
coexistence in invaded freshwater ecosystems.