Batrachochytrium dendrobatidis strain affects transcriptomic response in liver but not skin in latitudinal populations of the common toad (Bufo bufo).

Batrachochytrium dendrobatidis (Bd) is a fungal pathogen that has decimated amphibian populations worldwide for several decades. We examined the changes in gene expression in response to Bd infection in two populations of the common toad, Bufo bufo, in a laboratory experiment. We collected B. bufo eggs in southern and northern Sweden, and infected the laboratory-raised metamorphs with two strains of the global panzoonotic lineage Bd-GPL. Differential expression analysis showed significant differences between infected and control individuals in both liver and skin. The skin samples showed no discernible differences in gene expression between the two strains used, while liver samples were differentiated by strain, with one of the strains eliciting no immune response from infected toads. Immune system genes were overexpressed in skin samples from surviving infected individuals, while in liver samples the pattern was more diffuse. Splitting samples by population revealed a stronger immune response in northern individuals. Differences in transcriptional regulation between populations are particularly relevant to study in Swedish amphibians, which may have experienced varying exposure to Bd. Earlier exposure to this pathogen and subsequent adaptation or selection pressure may contribute to the survival of some populations over others, while standing genetic diversity in different populations may also affect the infection outcome.

Body size mediates latitudinal population differences in the response to chytrid fungus infection in two amphibians.

Factors behind intraspecific variation in sensitivity to pathogens remain poorly understood. We investigated how geographical origin in two North European amphibians affects tolerance to infection by the chytrid fungus Batrachochytrium dendrobatidis (Bd), a generalist pathogen which has caused amphibian population declines worldwide. We exposed newly metamorphosed individuals of moor frog Rana arvalis and common toad Bufo bufo from two latitudinal regions to two different BdGPL strains. We measured survival and growth as infections may cause sub-lethal effects in fitness components even in the absence of mortality. Infection loads were higher in B. bufo than in R. arvalis, and smaller individuals had generally higher infection loads. B. bufo had high mortality in response to Bd infection, whereas there was little mortality in R. arvalis. Bd-mediated mortality was size-dependent and high-latitude individuals were smaller leading to high mortality in the northern B. bufo. Bd exposure led to sub-lethal effects in terms of reduced growth suggesting that individuals surviving the infection may have reduced fitness mediated by smaller body size. In both host species, the Swedish Bd strain caused stronger sublethal effects than the British strain. We suggest that high-latitude populations can be more vulnerable to chytrids than those from lower latitudes and discuss the possible mechanisms how body size and host geographical origin contribute to the present results.

Short-term responses of Rana arvalis tadpoles to pH and predator stress: adaptive divergence in behavioural and physiological plasticity?

Environmental stress is a major driver of ecological and evolutionary processes in nature. To cope with stress, organisms can adjust through phenotypic plasticity and/or adapt through genetic change. Here, we compared short-term behavioural (activity) and physiological (corticosterone levels, CORT) responses of Rana arvalis tadpoles from two divergent populations (acid origin, AOP, versus neutral origin, NOP) to acid and predator stress. Tadpoles were initially reared in benign conditions at pH 7 and then exposed to a combination of two pH (acid versus neutral) and two predator cue (predator cue versus no predator cue) treatments. We assessed behavioural activity within the first 15 min, and tissue CORT within 8 and 24 h of stress exposure. Both AOP and NOP tadpoles reduced their activity in acidic pH, but the response to the predator cue differed between the populations: AOP tadpoles increased whereas NOP tadpoles decreased their activity. The AOP and NOP tadpoles differed also in their CORT responses, with AOP being more responsive (CORT levels of NOP tadpoles did not differ statistically across treatments). After 8 h exposure, AOP tadpoles had elevated CORT levels in the acid-predator cue treatment and after 24 h exposure they had elevated CORT levels in all three stress treatments (relative to the benign neutral-no-cue treatment). These results suggest that adaptation to environmental acidification in R. arvalis is mediated, in part, via behavioural and hormonal plasticity.

Context dependent variation in corticosterone and phenotypic divergence of Rana arvalis populations along an acidification gradient.

BACKGROUND: Physiological processes, as immediate responses to the environment, are important mechanisms of phenotypic plasticity and can influence evolution at ecological time scales. In stressful environments, physiological stress responses of individuals are initiated and integrated via the release of hormones, such as corticosterone (CORT). In vertebrates, CORT influences energy metabolism and resource allocation to multiple fitness traits (e.g. growth and morphology) and can be an important mediator of rapid adaptation to environmental stress, such as acidification. The moor frog, Rana arvalis, shows adaptive divergence in larval life-histories and predator defense traits along an acidification gradient in Sweden. Here we take a first step to understanding the role of CORT in this adaptive divergence. We conducted a fully factorial laboratory experiment and reared tadpoles from three populations (one acidic, one neutral and one intermediate pH origin) in two pH treatments (Acid versus Neutral pH) from hatching to metamorphosis. We tested how the populations differ in tadpole CORT profiles and how CORT is associated with tadpole life-history and morphological traits. RESULTS: We found clear differences among the populations in CORT profiles across different developmental stages, but only weak effects of pH treatment on CORT. Tadpoles from the acid origin population had, on average, lower CORT levels than tadpoles from the neutral origin population, and the intermediate pH origin population had intermediate CORT levels. Overall, tadpoles with higher CORT levels developed faster and had shorter and shallower tails, as well as shallower tail muscles. CONCLUSIONS: Our common garden results indicate among population divergence in CORT levels, likely reflecting acidification mediated divergent selection on tadpole physiology, concomitant to selection on larval life-histories and morphology. However, CORT levels were highly environmental context dependent. Jointly these results indicate a potential role for CORT as a mediator of multi-trait divergence along environmental stress gradients in natural populations. At the same time, the population level differences and high context dependency in CORT levels suggest that snapshot assessment of CORT in nature may not be reliable bioindicators of stress.

The effects of drift and selection on latitudinal genetic variation in Scandinavian common toads (Bufo bufo) following postglacial recolonisation.

Clinal variation is paramount for understanding the factors shaping genetic diversity in space and time. During the last glacial maximum, northern Europe was covered by glacial ice that rendered the region uninhabitable for most taxa. Different evolutionary processes during and after the recolonisation of this area from different glacial refugia have affected the genetic landscape of the present day European flora and fauna. In this study, we focus on the common toad (Bufo bufo) in Sweden and present evidence suggesting that these processes have resulted in two separate lineages of common toad, which colonised Sweden from two directions. Using ddRAD sequencing data for demographic modelling, structure analyses, and analysis of molecular variance (AMOVA), we provide evidence of a contact zone located between Uppland and Västerbotten in central Sweden. Genetic diversity was significantly higher in southern Sweden compared to the north, in accordance with a pattern of decreased genetic diversity with increasing distance from glacial refugia. Candidate genes under putative selection are identified through outlier detection and gene-environment association methods. We provide evidence of divergent selection related to stress response and developmental processes in these candidate genes. The colonisation of Sweden by two separate lineages may have implications for how future conservation efforts should be directed by identifying management units and putative local adaptations.

Small-scale population divergence is driven by local larval environment in a temperate amphibian.

Genomic variation within and among populations is shaped by the interplay between natural selection and the effects of genetic drift and gene flow. Adaptive divergence can be found in small-scale natural systems even when population sizes are small, and the potential for gene flow is high, suggesting that local environments exert selection pressures strong enough to counteract the opposing effects of drift and gene flow. Here, we investigated genomic differentiation in nine moor frog (Rana arvalis) populations in a small-scale network of local wetlands using 16,707 ddRAD-seq SNPs, relating levels of differentiation with local environments, as well as with properties of the surrounding landscape. We characterized population structure and differentiation, and partitioned the effects of geographic distance, local larval environment, and landscape features on total genomic variation. We also conducted gene-environment association studies using univariate and multivariate approaches. We found small-scale population structure corresponding to 6-8 clusters. Local larval environment was the most influential component explaining 2.3% of the total genetic variation followed by landscape features (1.8%) and geographic distance (0.8%), indicative of isolation-by-environment, -by-landscape, and -by-distance, respectively. We identified 1000 potential candidate SNPs putatively under divergent selection mediated by the local larval environment. The candidate SNPs were involved in, among other biological functions, immune system function and development. Our results suggest that small-scale environmental differences can exert selection pressures strong enough to counteract homogenizing effects of gene flow and drift in this small-scale system, leading to observable population differentiation.

Occurrence of Batrachochytrium dendrobatidis in Sweden: higher infection prevalence in southern species.

The chytrid fungus Batrachochytrium dendrobatidis (Bd) has caused worldwide declines in amphibian populations. While Bd is widespread in southern and central Europe, its occurrence and distribution in northernmost Europe is mostly unknown. We surveyed for Bd in breeding anurans in Sweden by sampling 1917 amphibians from 101 localities and 3 regions in Sweden (southern, northern and central). We found that Bd was widespread in southern and central Sweden, occurring in all 9 investigated species and in 45.5% of the 101 localities with an overall prevalence of 13.8%. No infected individuals were found in the 4 northern sites sampled. The records from central Sweden represent the northernmost records of Bd in Europe. While the proportion of sites positive for Bd was similar between the southern and central regions, prevalence was much higher in the southern region. This was because southern species with a distribution mainly restricted to southernmost Sweden had a higher prevalence than widespread generalist species. The nationally red-listed green toad Bufotes variabilis and the fire-bellied toad Bombina bombina had the highest prevalence (61.4 and 48.9%, respectively). Across species, Bd prevalence was strongly positively, correlated with water temperature at the start of egg laying. However, no individuals showing visual signs of chytridiomycosis were found in the field. These results indicate that Bd is widespread and common in southern and central Sweden with southern species, breeding in higher temperatures and with longer breeding periods, having higher prevalence. However, the impact of Bd on amphibian populations in northernmost Europe remains unknown.

Parental effects influence life history traits and covary with an environmental cline in common frog populations.

Across latitudinal clines, the juvenile developmental rates of ectotherms often covary with the length of the growing season, due to life-history trade-offs imposed by the time-constrained environments. However, as the start of the growing season often varies substantially across years, adaptive parental effects on juvenile developmental rates may mediate the costs of a delayed season. By employing a meta-analysis, we tested whether larval developmental rates across a latitudinal cline of the common frog (Rana temporaria) are affected by fluctuating onsets of breeding, across years. We predicted that larval developmental rate will be inversely related to the onset of breeding, and that northern populations will be more prone to shorten their developmental rate in response to late breeding, as the costs of delayed metamorphosis should be highest in areas with a shorter growing season. We found that the larval period of both northern and southern populations responded to parental environmental conditions to a similar degree in absolute terms, but in different directions. In northern populations, a late season start correlated with decreased development time, suggesting that the evolution of parental effects aids population persistence in time-constrained environments. In southern populations, late season start correlated with increased development time, which could potentially be explained as a predator avoidance strategy. Our findings suggest that local ecological variables can induce adaptive parental effects, but responses are complex, and likely trade-off with other ecological factors.

Antimicrobial peptide and sequence variation along a latitudinal gradient in two anurans.

BACKGROUND: While there is evidence of both purifying and balancing selection in immune defense genes, large-scale genetic diversity in antimicrobial peptides (AMPs), an important part of the innate immune system released from dermal glands in the skin, has remained uninvestigated. Here we describe genetic diversity at three AMP loci (Temporin, Brevinin and Palustrin) in two ranid frogs (Rana arvalis and R. temporaria) along a 2000 km latitudinal gradient. We amplified and sequenced part of the Acidic Propiece domain and the hypervariable Mature Peptide domain (~ 150-200 bp) in the three genes using Illumina Miseq and expected to find decreased AMP genetic variation towards the northern distribution limit of the species similarly to studies on MHC genetic patterns. RESULTS: We found multiple loci for each AMP and relatively high gene diversity, but no clear pattern of geographic genetic structure along the latitudinal gradient. We found evidence of trans-specific polymorphism in the two species, indicating a common evolutionary origin of the alleles. Temporin and Brevinin did not form monophyletic clades suggesting that they belong to the same gene family. By implementing codon evolution models we found evidence of strong positive selection acting on the Mature Peptide. We also found evidence of diversifying selection as indicated by divergent allele frequencies among populations and high Theta k values. CONCLUSION: Our results suggest that AMPs are an important source of adaptive diversity, minimizing the chance of microorganisms developing resistance to individual peptides.

Gene Flow Limits Adaptation along Steep Environmental Gradients.

When environmental variation is spatially continuous, dispersing individuals move among nearby sites with similar habitat conditions. But as an environmental gradient becomes steeper, gene flow may connect more divergent habitats, and this is predicted to reduce the slope of the adaptive cline that evolves. We compared quantitative genetic divergence of Rana temporaria frog populations along a 2,000-m elevational gradient in eastern Switzerland (new experimental results) with divergence along a 1,550-km latitudinal gradient in Fennoscandia (previously published results). Both studies found significant countergradient variation in larval development rate (i.e., animals from cold climates developed more rapidly). The cline was weaker with elevation than with latitude. Animals collected on both gradients were genotyped at ∼2,000 single-nucleotide polymorphism markers, revealing that dispersal distance was 30% farther on the latitudinal gradient but 3.9 times greater with respect to environmental conditions on the elevational gradient. A meta-analysis of 19 experimental studies of anuran populations spanning temperature gradients revealed that countergradient variation in larval development, while significant overall, was weaker when measured on steeper gradients. These findings support the prediction that adaptive population divergence is less pronounced, and maladaptation more pervasive, on steep environmental gradients.

Genetic basis of amphibian larval development along a latitudinal gradient: Gene diversity, selection and links with phenotypic variation in transcription factor C/EBP-1.

Ectotherm development rates often show adaptive divergence along climatic gradients, but the genetic basis for this variation is rarely studied. Here, we investigated the genetic basis for phenotypic variation in larval development in the moor frog Rana arvalis from five regions along a latitudinal gradient from Germany to northern Sweden. We focused on the C/EBP-1 gene, a transcription factor associated with larval development time. Allele frequencies at C/EBP-1 varied strongly among geographical regions. Overall, the distribution of alleles along the gradient was in concordance with the dual post-glacial colonization routes into Scandinavia, with a large number of alleles exclusively present along the southern colonization route. Only three of 38 alleles were shared between the routes. Analysis of contemporary selection on C/EBP-1 showed divergent selection among the regions, probably reflecting adaptation to the local environmental conditions, although this was especially strong between southern and northern regions coinciding also with lineages from different colonization routes. Overall, the C/EBP-1 gene has historically been under purifying selection, but two specific amino acid positions showed significant signals of positive selection. These positions showed divergence between southern and northern regions, and we suggest that they are functionally involved in the climatic adaptation of larval development. Using phenotypic data from a common garden experiment, we found evidence for specific C/EBP-1 alleles being correlated with larval development time, suggesting a functional role in adaptation of larval development to large-scale climatic variation.

Latitudinal divergence in a widespread amphibian: Contrasting patterns of neutral and adaptive genomic variation.

Stochastic effects from demographic processes and selection are expected to shape the distribution of genetic variation in spatially heterogeneous environments. As the amount of genetic variation is central for long-term persistence of populations, understanding how these processes affect variation over large-scale geographical gradients is pivotal. We investigated the distribution of neutral and putatively adaptive genetic variation, and reconstructed demographic history in the moor frog (Rana arvalis) using 136 individuals from 15 populations along a 1,700-km latitudinal gradient from northern Germany to northern Sweden. Using double digest restriction-site associated DNA sequencing we obtained 27,590 single nucleotide polymorphisms (SNPs), and identified differentiation outliers and SNPs associated with growing season length. The populations grouped into a southern and a northern cluster, representing two phylogeographical lineages from different post-glacial colonization routes. Hybrid index estimation and demographic model selection showed strong support for a southern and northern lineage and evidence of gene flow between regions located on each side of a contact zone. However, patterns of past gene flow over the contact zone differed between neutral and putatively adaptive SNPs. While neutral nucleotide diversity was higher along the southern than the northern part of the gradient, nucleotide diversity in differentiation outliers showed the opposite pattern, suggesting differences in the relative strength of selection and drift along the gradient. Variation associated with growing season length decreased with latitude along the southern part of the gradient, but not along the northern part where variation was lower, suggesting stronger climate-mediated selection in the north. Outlier SNPs included loci involved in immunity and developmental processes.

Post-glacial colonization routes coincide with a life-history breakpoint along a latitudinal gradient.

Although adaptive divergence along environmental gradients has repeatedly been demonstrated, the role of post-glacial colonization routes in determining phenotypic variation along gradients has received little attention. Here, we used a hierarchical QST -FST approach to separate the roles of adaptive and neutral processes in shaping phenotypic variation in moor frog (Rana arvalis) larval life histories along a 1,700 km latitudinal gradient across northern Europe. This species has colonized Scandinavia via two routes with a contact zone in northern Sweden. By using neutral SNP and common garden phenotypic data from 13 populations at two temperatures, we showed that most of the variation along the gradient occurred between the two colonizing lineages. We found little phenotypic divergence within the lineages; however, all phenotypic traits were strongly diverged between the southern and northern colonization routes, with higher growth and development rates and larger body size in the north. The QST estimates between the colonization routes were four times higher than FST , indicating a prominent role for natural selection. QST within the colonization routes did not generally differ from FST , but we found temperature-dependent adaptive divergence close to the contact zone. These results indicate that lineage-specific variation can account for much of the adaptive divergence along a latitudinal gradient.

Urban environment and reservoir host species are associated with Batrachochytrium dendrobatidis infection prevalence in the common toad.

Human-induced changes of the environment, including landscape alteration and habitat loss, may affect wildlife disease dynamics and have important ramifications for wildlife conservation. Amphibians are among the vertebrate taxa most threatened by anthropogenic habitat change. The emerging fungal pathogen Batrachochytrium dendrobatidis (Bd) has caused extinctions and population declines in hundreds of anuran species globally. We studied how the urban landscape is associated with the prevalence of Bd infections by sampling 655 anurans of 3 species (mainly the common toad Bufo bufo) in 42 ponds surrounded by different amounts of urban habitat (defined as towns, cities or villages). We also examined the association between Bd infections and a potential reservoir host species (the moor frog Rana arvalis). We found that 38% of the sites were positive for Bd with an infection prevalence of 4.4%. The extent of urban landscape was negatively correlated with Bd infection prevalence. However, the positive association of Bd with the presence of the possible reservoir species was substantially stronger than the urban effects. The body condition index of B. bufo was negatively associated with Bd infection. This Bd effect was stronger than the negative effect of urban landscape on body condition. Our results suggest that urban environments in Sweden have a negative impact on Bd infections, while the presence of the reservoir species has a positive impact on Bd prevalence. Our study also highlights the potential importance of Bd infection on host fitness, especially in rural landscapes.

Effects of host species and environmental factors on the prevalence of Batrachochytrium dendrobatidis in northern Europe.

The fungal pathogen Batrachochytrium dendrobatidis (Bd) poses a major threat to amphibian populations. To assist efforts to address such threats, we examined differences in Bd host infection prevalence among amphibian species and its relations to both local environmental factors in breeding habitats and landscape variables measured at three scales (500, 2000 and 5000 m radii) around breeding sites in southernmost Sweden. We sampled 947 anurans of six species in 31 ponds and assessed their infection status. We then examined correlations of infection prevalence with canopy cover, pond perimeter and pH (treated as local-scale pond characteristics), and the number of ponds, area of arable land, area of mature forest, number of resident people and presence of sea within the three radii (treated as landscape variables). The Bd infection prevalence was very low, 0.5-1.0%, in two of the six anuran species (Bufo bufo and Rana temporaria), and substantially higher (13-64%) in the other four (Bombina bombina, Bufotes variabilis, Epidalea calamita, Rana arvalis). In the latter four species Bd infection prevalence was positively associated with ponds' pH (site range: 5.3-8.1), and negatively associated with areas of mature forest and/or wetlands in the surroundings. Our results show that the infection dynamics of Bd are complex and associated with host species, local pond characteristics and several landscape variables at larger spatial scales. Knowledge of environmental factors associated with Bd infections and differences in species' susceptibility may help to counter further spread of the disease and guide conservation action plans, especially for the most threatened species.

Development and worldwide use of non-lethal, and minimal population-level impact, protocols for the isolation of amphibian chytrid fungi.

Parasitic chytrid fungi have emerged as a significant threat to amphibian species worldwide, necessitating the development of techniques to isolate these pathogens into culture for research purposes. However, early methods of isolating chytrids from their hosts relied on killing amphibians. We modified a pre-existing protocol for isolating chytrids from infected animals to use toe clips and biopsies from toe webbing rather than euthanizing hosts, and distributed the protocol to researchers as part of the BiodivERsA project RACE; here called the RML protocol. In tandem, we developed a lethal procedure for isolating chytrids from tadpole mouthparts. Reviewing a database of use a decade after their inception, we find that these methods have been applied across 5 continents, 23 countries and in 62 amphibian species. Isolation of chytrids by the non-lethal RML protocol occured in 18% of attempts with 207 fungal isolates and three species of chytrid being recovered. Isolation of chytrids from tadpoles occured in 43% of attempts with 334 fungal isolates of one species (Batrachochytrium dendrobatidis) being recovered. Together, these methods have resulted in a significant reduction and refinement of our use of threatened amphibian species and have improved our ability to work with this group of emerging pathogens.

Interacting effects of predation risk and resource level on escape speed of amphibian larvae along a latitudinal gradient.

Fast-growing genotypes living in time-constrained environments are often more prone to predation, suggesting that growth-predation risk trade-offs are important factors maintaining variation in growth along climatic gradients. However, the mechanisms underlying how fast growth increases predation-mediated mortality are not well understood. Here, we investigated if slow-growing, low-latitude individuals have faster escape swimming speed than fast-growing high-latitude individuals using common frog (Rana temporaria) tadpoles from eight populations collected along a 1500 km latitudinal gradient. We measured escape speed in terms of burst and endurance speeds in tadpoles raised in the laboratory at two food levels and in the presence and absence of a predator (Aeshna dragonfly larvae). We did not find any latitudinal trend in escape speed performance. In low food treatments, burst speed was higher in tadpoles reared with predators but did not differ between high-food treatments. Endurance speed, on the contrary, was lower in high-food tadpoles reared with predators and did not differ between treatments at low food levels. Tadpoles reared with predators showed inducible morphology (increased relative body size and tail depth), which had positive effects on speed endurance at low but not at high food levels. Burst speed was positively affected by tail length and tail muscle size in the absence of predators. Our results suggest that escape speed does not trade-off with fast growth along the latitudinal gradient in R. temporaria tadpoles. Instead, escape speed is a plastic trait and strongly influenced by the interaction between resource level and predation risk.

Recent Asian origin of chytrid fungi causing global amphibian declines.

Globalized infectious diseases are causing species declines worldwide, but their source often remains elusive. We used whole-genome sequencing to solve the spatiotemporal origins of the most devastating panzootic to date, caused by the fungus Batrachochytrium dendrobatidis, a proximate driver of global amphibian declines. We traced the source of B. dendrobatidis to the Korean peninsula, where one lineage, BdASIA-1, exhibits the genetic hallmarks of an ancestral population that seeded the panzootic. We date the emergence of this pathogen to the early 20th century, coinciding with the global expansion of commercial trade in amphibians, and we show that intercontinental transmission is ongoing. Our findings point to East Asia as a geographic hotspot for B. dendrobatidis biodiversity and the original source of these lineages that now parasitize amphibians worldwide.

Can heat waves change the trophic role of the world's most invasive crayfish? Diet shifts in Procambarus clarkii.

In the Mediterranean basin, the globally increasing temperatures are expected to be accompanied by longer heat waves. Commonly assumed to benefit cold-limited invasive alien species, these climatic changes may also change their feeding preferences, especially in the case of omnivorous ectotherms. We investigated heat wave effects on diet choice, growth and energy reserves in the invasive red swamp crayfish, Procambarus clarkii. In laboratory experiments, we fed juvenile and adult crayfish on animal, plant or mixed diets and exposed them to a short or a long heat wave. We then measured crayfish survival, growth, body reserves and Fulton's condition index. Diet choices of the crayfish maintained on the mixed diet were estimated using stable isotopes (13C and 15N). The results suggest a decreased efficiency of carnivorous diets at higher temperatures, as juveniles fed on the animal diet were unable to maintain high growth rates in the long heat wave; and a decreased efficiency of herbivorous diets at lower temperatures, as juveniles in the cold accumulated less body reserves when fed on the plant diet. Heat wave treatments increased the assimilation of plant material, especially in juveniles, allowing them to sustain high growth rates in the long heat wave. Contrary to our expectations, crayfish performance decreased in the long heat wave, suggesting that Mediterranean summer heat waves may have negative effects on P. clarkii and that they are unlikely to boost its populations in this region. Although uncertain, it is possible that the greater assimilation of the plant diet resulted from changes in crayfish feeding preferences, raising the hypotheses that i) heat waves may change the predominant impacts of this keystone species and ii) that by altering species' trophic niches, climate change may alter the main impacts of invasive alien species.