Climate change vulnerability of Arctic char across Scandinavia.

Climate change is anticipated to cause species to shift their ranges upward and poleward, yet space for tracking suitable habitat conditions may be limited for range-restricted species at the highest elevations and latitudes of the globe. Consequently, range-restricted species inhabiting Arctic freshwater ecosystems, where global warming is most pronounced, face the challenge of coping with changing abiotic and biotic conditions or risk extinction. Here, we use an extensive fish community and environmental dataset for 1762 lakes sampled across Scandinavia (mid-1990s) to evaluate the climate vulnerability of Arctic char (Salvelinus alpinus), the world's most cold-adapted and northernly distributed freshwater fish. Machine learning models show that abiotic and biotic factors strongly predict the occurrence of Arctic char across the region with an overall accuracy of 89 percent. Arctic char is less likely to occur in lakes with warm summer temperatures, high dissolved organic carbon levels (i.e., browning), and presence of northern pike (Esox lucius). Importantly, climate warming impacts are moderated by habitat (i.e., lake area) and amplified by the presence of competitors and/or predators (i.e., northern pike). Climate warming projections under the RCP8.5 emission scenario indicate that 81% of extant populations are at high risk of extirpation by 2080. Highly vulnerable populations occur across their range, particularly near the southern range limit and at lower elevations, with potential refugia found in some mountainous and coastal regions. Our findings highlight that range shifts may give way to range contractions for this cold-water specialist, indicating the need for pro-active conservation and mitigation efforts to avoid the loss of Arctic freshwater biodiversity.

Species invasion progressively disrupts the trophic structure of native food webs.

Species invasions can have substantial impacts on native species and ecosystems, with important consequences for biodiversity. How these disturbances drive changes in the trophic structure of native food webs through time is poorly understood. Here, we quantify trophic disruption in freshwater food webs to invasion by an apex fish predator, lake trout, using an extensive stable isotope dataset across a natural gradient of uninvaded and invaded lakes in the northern Rocky Mountains, USA. Lake trout invasion increased fish diet variability (trophic dispersion), displaced native fishes from their reference diets (trophic displacement), and reorganized macroinvertebrate communities, indicating strong food web disruption. Trophic dispersion was greatest 25 to 50 y after colonization and dissipated as food webs stabilized in later stages of invasion (>50 y). For the native apex predator, bull trout, trophic dispersion preceded trophic displacement, leading to their functional loss in late-invasion food webs. Our results demonstrate how invasive species progressively disrupt native food webs via trophic dispersion and displacement, ultimately yielding biological communities strongly divergent from those in uninvaded ecosystems.

Specialized meltwater biodiversity persists despite widespread deglaciation.

Glaciers are important drivers of environmental heterogeneity and biological diversity across mountain landscapes. Worldwide, glaciers are receding rapidly due to climate change, with important consequences for biodiversity in mountain ecosystems. However, the effects of glacier loss on biodiversity have never been quantified across a mountainous region, primarily due to a lack of adequate data at large spatial and temporal scales. Here, we combine high-resolution biological and glacier change (ca. 1850-2015) datasets for Glacier National Park, USA, to test the prediction that glacier retreat reduces biodiversity in mountain ecosystems through the loss of uniquely adapted meltwater stream species. We identified a specialized cold-water invertebrate community restricted to the highest elevation streams primarily below glaciers, but also snowfields and groundwater springs. We show that this community and endemic species have unexpectedly persisted in cold, high-elevation sites, even in catchments that have not been glaciated in ∼170 y. Future projections suggest substantial declines in suitable habitat, but not necessarily loss of this community with the complete disappearance of glaciers. Our findings demonstrate that high-elevation streams fed by snow and other cold-water sources continue to serve as critical climate refugia for mountain biodiversity even after glaciers disappear.

High dispersal rates in hybrids drive expansion of maladaptive hybridization.

Hybridization between native and invasive species, a major cause of biodiversity loss, can spread rapidly even when hybrids have reduced fitness. This paradox suggests that hybrids have greater dispersal rates than non-hybridized individuals, yet this mechanism has not been empirically tested in animal populations. Here, we test if non-native genetic introgression increases reproductive dispersal using a human-mediated hybrid zone between native cutthroat trout (<i>Oncorhynchus clarkii</i>) and invasive rainbow trout (<i>Oncorhynchus mykiss</i>) in a large and connected river system. We quantified the propensity for individuals to migrate from natal rearing habitats (migrate), reproduce in non-natal habitats (stray), and the joint probability of dispersal as a function of genetic ancestry. Hybrid trout with predominantly non-native rainbow trout ancestry were more likely to migrate as juveniles and to stray as adults. Overall, hybrids with greater than 50% rainbow trout ancestry were 5.7 times more likely to disperse than native or hybrid trout with small amounts of rainbow trout ancestry. Our results show a genetic basis for increased dispersal in hybrids that is likely contributing to the rapid expansion of invasive hybridization between these species. Management actions that decrease the probability of hybrid dispersal may mitigate the harmful effects of invasive hybridization on native biodiversity.

Microbial assemblages reflect environmental heterogeneity in alpine streams.

Alpine streams are dynamic habitats harboring substantial biodiversity across small spatial extents. The diversity of alpine stream biota is largely reflective of environmental heterogeneity stemming from varying hydrological sources. Globally, alpine stream diversity is under threat as meltwater sources recede and stream conditions become increasingly homogeneous. Much attention has been devoted to macroinvertebrate diversity in alpine headwaters, yet to fully understand the breadth of climate change threats, a more thorough accounting of microbial diversity is needed. We characterized microbial diversity (specifically Bacteria and Archaea) of 13 streams in two disjunct Rocky Mountain subranges through 16S rRNA gene sequencing. Our study encompassed the spectrum of alpine stream sources (glaciers, snowfields, subterranean ice, and groundwater) and three microhabitats (ice, biofilms, and streamwater). We observed no difference in regional (γ) diversity between subranges but substantial differences in diversity among (ß) stream types and microhabitats. Within-stream (α) diversity was highest in groundwater-fed springs, lowest in glacier-fed streams, and positively correlated with water temperature for both streamwater and biofilm assemblages. We identified an underappreciated alpine stream type-the icy seep-that are fed by subterranean ice, exhibit cold temperatures (summer mean <2°C), moderate bed stability, and relatively high conductivity. Icy seeps will likely be important for combatting biodiversity losses as they contain similar microbial assemblages to streams fed by surface ice yet may be buffered against climate change by insulating debris cover. Our results show that the patterns of microbial diversity support an ominous trend for alpine stream biodiversity; as meltwater sources decline, stream communities will become more diverse locally, but regional diversity will be lost. Icy seeps, however, represent a source of optimism for the future of biodiversity in these imperiled ecosystems.

Climate-induced glacier and snow loss imperils alpine stream insects.

Climate warming is causing rapid loss of glaciers and snowpack in mountainous regions worldwide. These changes are predicted to negatively impact the habitats of many range-restricted species, particularly endemic, mountaintop species dependent on the unique thermal and hydrologic conditions found only in glacier-fed and snow melt-driven alpine streams. Although progress has been made, existing understanding of the status, distribution, and ecology of alpine aquatic species, particularly in North America, is lacking, thereby hindering conservation and management programs. Two aquatic insects - the meltwater stonefly (Lednia tumana) and the glacier stonefly (Zapada glacier) - were recently proposed for listing under the U.S. Endangered Species Act due to climate-change-induced habitat loss. Using a large dataset (272 streams, 482 total sites) with high-resolution climate and habitat information, we describe the distribution, status, and key environmental features that limit L. tumana and Z. glacier across the northern Rocky Mountains. Lednia tumana was detected in 113 streams (175 sites) within Glacier National Park (GNP) and surrounding areas. The probability of L. tumana occurrence increased with cold stream temperatures and close proximity to glaciers and permanent snowfields. Similarly, densities of L. tumana declined with increasing distance from stream source. Zapada glacier was only detected in 10 streams (24 sites), six in GNP and four in mountain ranges up to ~600 km southwest. Our results show that both L. tumana and Z. glacier inhabit an extremely narrow distribution, restricted to short sections of cold, alpine streams often below glaciers predicted to disappear over the next two decades. Climate warming-induced glacier and snow loss clearly imperils the persistence of L. tumana and Z. glacier throughout their ranges, highlighting the role of mountaintop aquatic invertebrates as sentinels of climate change in mid-latitude regions.

Legacy introductions and climatic variation explain spatiotemporal patterns of invasive hybridization in a native trout.

Hybridization between invasive and native species, a significant threat to worldwide biodiversity, is predicted to increase due to climate-induced expansions of invasive species. Long-term research and monitoring are crucial for understanding the ecological and evolutionary processes that modulate the effects of invasive species. Using a large, multidecade genetics dataset (N = 582 sites, 12,878 individuals) with high-resolution climate predictions and extensive stocking records, we evaluate the spatiotemporal dynamics of hybridization between native cutthroat trout and invasive rainbow trout, the world's most widely introduced invasive fish, across the Northern Rocky Mountains of the United States. Historical effects of stocking and contemporary patterns of climatic variation were strongly related to the spread of hybridization across space and time. The probability of occurrence, extent of, and temporal changes in hybridization increased at sites in close proximity to historical stocking locations with greater rainbow trout propagule pressure, warmer water temperatures, and lower spring precipitation. Although locations with warmer water temperatures were more prone to hybridization, cold sites were not protected from invasion; 58% of hybridized sites had cold mean summer water temperatures (<11°C). Despite cessation of stocking over 40 years ago, hybridization increased over time at half (50%) of the locations with long-term data, the vast majority of which (74%) were initially nonhybridized, emphasizing the chronic, negative impacts of human-mediated hybridization. These results show that effects of climate change on biodiversity must be analyzed in the context of historical human impacts that set ecological and evolutionary trajectories.

Accounting for adaptive capacity and uncertainty in assessments of species' climate-change vulnerability.

Climate-change vulnerability assessments (CCVAs) are valuable tools for assessing species' vulnerability to climatic changes, yet failure to include measures of adaptive capacity and to account for sources of uncertainty may limit their effectiveness. We took a more comprehensive approach that incorporates exposure, sensitivity, and capacity to adapt to climate change. We applied our approach to anadromous steelhead trout (Oncorhynchus mykiss) and nonanadromous bull trout (Salvelinus confluentus), threatened salmonids within the Columbia River Basin (U.S.A.). We quantified exposure on the basis of scenarios of future stream temperature and flow, and we represented sensitivity and capacity to adapt to climate change with metrics of habitat quality, demographic condition, and genetic diversity. Both species were found to be highly vulnerable to climate change at low elevations and in their southernmost habitats. However, vulnerability rankings varied widely depending on the factors (climate, habitat, demographic, and genetic) included in the CCVA and often differed for the 2 species at locations where they were sympatric. Our findings illustrate that CCVA results are highly sensitive to data inputs and that spatial differences can complicate multispecies conservation. Based on our results, we suggest that CCVAs be considered within a broader conceptual and computational framework and be used to refine hypotheses, guide research, and compare plausible scenarios of species' vulnerability to climate change.

Vive la résistance: genome-wide selection against introduced alleles in invasive hybrid zones.

Evolutionary and ecological consequences of hybridization between native and invasive species are notoriously complicated because patterns of selection acting on non-native alleles can vary throughout the genome and across environments. Rapid advances in genomics now make it feasible to assess locus-specific and genome-wide patterns of natural selection acting on invasive introgression within and among natural populations occupying diverse environments. We quantified genome-wide patterns of admixture across multiple independent hybrid zones of native westslope cutthroat trout and invasive rainbow trout, the world's most widely introduced fish, by genotyping 339 individuals from 21 populations using 9380 species-diagnostic loci. A significantly greater proportion of the genome appeared to be under selection favouring native cutthroat trout (rather than rainbow trout), and this pattern was pervasive across the genome (detected on most chromosomes). Furthermore, selection against invasive alleles was consistent across populations and environments, even in those where rainbow trout were predicted to have a selective advantage (warm environments). These data corroborate field studies showing that hybrids between these species have lower fitness than the native taxa, and show that these fitness differences are due to selection favouring many native genes distributed widely throughout the genome.

Climate variables explain neutral and adaptive variation within salmonid metapopulations: the importance of replication in landscape genetics.

Understanding how environmental variation influences population genetic structure is important for conservation management because it can reveal how human stressors influence population connectivity, genetic diversity and persistence. We used riverscape genetics modelling to assess whether climatic and habitat variables were related to neutral and adaptive patterns of genetic differentiation (population-specific and pairwise FST ) within five metapopulations (79 populations, 4583 individuals) of steelhead trout (Oncorhynchus mykiss) in the Columbia River Basin, USA. Using 151 putatively neutral and 29 candidate adaptive SNP loci, we found that climate-related variables (winter precipitation, summer maximum temperature, winter highest 5% flow events and summer mean flow) best explained neutral and adaptive patterns of genetic differentiation within metapopulations, suggesting that climatic variation likely influences both demography (neutral variation) and local adaptation (adaptive variation). However, we did not observe consistent relationships between climate variables and FST across all metapopulations, underscoring the need for replication when extrapolating results from one scale to another (e.g. basin-wide to the metapopulation scale). Sensitivity analysis (leave-one-population-out) revealed consistent relationships between climate variables and FST within three metapopulations; however, these patterns were not consistent in two metapopulations likely due to small sample sizes (N = 10). These results provide correlative evidence that climatic variation has shaped the genetic structure of steelhead populations and highlight the need for replication and sensitivity analyses in land and riverscape genetics.

Dispersal and selection mediate hybridization between a native and invasive species.

Hybridization between native and non-native species has serious biological consequences, but our understanding of how dispersal and selection interact to influence invasive hybridization is limited. Here, we document the spread of genetic introgression between a native (Oncorhynchus clarkii) and invasive (Oncorhynchus mykiss) trout, and identify the mechanisms influencing genetic admixture. In two populations inhabiting contrasting environments, non-native admixture increased rapidly from 1984 to 2007 and was driven by surprisingly consistent processes. Individual admixture was related to two phenotypic traits associated with fitness: size at spawning and age of juvenile emigration. Fish with higher non-native admixture were larger and tended to emigrate at a younger age--relationships that are expected to confer fitness advantages to hybrid individuals. However, strong selection against non-native admixture was evident across streams and cohorts (mean selection coefficient against genotypes with non-native alleles (s) = 0.60; s.e. = 0.10). Nevertheless, hybridization was promoted in both streams by the continuous immigration of individuals with high levels of non-native admixture from other hybrid source populations. Thus, antagonistic relationships between dispersal and selection are mediating invasive hybridization between these fish, emphasizing that data on dispersal and natural selection are needed to fully understand the dynamics of introgression between native and non-native species.

Genetic diversity is related to climatic variation and vulnerability in threatened bull trout.

Understanding how climatic variation influences ecological and evolutionary processes is crucial for informed conservation decision-making. Nevertheless, few studies have measured how climatic variation influences genetic diversity within populations or how genetic diversity is distributed across space relative to future climatic stress. Here, we tested whether patterns of genetic diversity (allelic richness) were related to climatic variation and habitat features in 130 bull trout (Salvelinus confluentus) populations from 24 watersheds (i.e., ~4-7th order river subbasins) across the Columbia River Basin, USA. We then determined whether bull trout genetic diversity was related to climate vulnerability at the watershed scale, which we quantified on the basis of exposure to future climatic conditions (projected scenarios for the 2040s) and existing habitat complexity. We found a strong gradient in genetic diversity in bull trout populations across the Columbia River Basin, where populations located in the most upstream headwater areas had the greatest genetic diversity. After accounting for spatial patterns with linear mixed models, allelic richness in bull trout populations was positively related to habitat patch size and complexity, and negatively related to maximum summer temperature and the frequency of winter flooding. These relationships strongly suggest that climatic variation influences evolutionary processes in this threatened species and that genetic diversity will likely decrease due to future climate change. Vulnerability at a watershed scale was negatively correlated with average genetic diversity (r = -0.77; P < 0.001); watersheds containing populations with lower average genetic diversity generally had the lowest habitat complexity, warmest stream temperatures, and greatest frequency of winter flooding. Together, these findings have important conservation implications for bull trout and other imperiled species. Genetic diversity is already depressed where climatic vulnerability is highest; it will likely erode further in the very places where diversity may be most needed for future persistence.

Local environments, not invasive hybridization, influence cardiac performance of native trout under acute thermal stress.

Climate-induced expansion of invasive hybridization (breeding between invasive and native species) poses a significant threat to the persistence of many native species worldwide. In the northern U.S. Rocky Mountains, hybridization between native cutthroat trout and non-native rainbow trout has increased in recent decades due, in part, to climate-driven increases in water temperature. It has been postulated that invasive hybridization may enhance physiological tolerance to climate-induced thermal stress because laboratory studies indicate that rainbow trout have a higher thermal tolerance than cutthroat trout. Here, we assessed whether invasive hybridization improves cardiac performance response to acute water temperature stress of native wild trout populations. We collected trout from four streams with a wide range of non-native admixture among individuals and with different temperature and streamflow regimes in the upper Flathead River drainage, USA. We measured individual cardiac performance (maximum heart rate, "MaxHR", and temperature at arrhythmia, "ArrTemp") during laboratory trials with increasing water temperatures (10-28°C). Across the study populations, we observed substantial variation in cardiac performance of individual trout when exposed to thermal stress. Notably, we found significant differences in the cardiac response to thermal regimes among native cutthroat trout populations, suggesting the importance of genotype-by-environment interactions in shaping the physiological performance of native cutthroat trout. However, rainbow trout admixture had no significant effect on cardiac performance (MaxHR and ArrTemp) within any of the three populations. Our results indicate that invasive hybridization with a warmer-adapted species does not enhance the cardiac performance of native trout under warming conditions. Maintaining numerous populations across thermally and hydrologically diverse stream environments will be crucial for native trout to adapt and persist in a warming climate.

Genomic patterns of introgression in rainbow and westslope cutthroat trout illuminated by overlapping paired-end RAD sequencing.

Rapid and inexpensive methods for genomewide single nucleotide polymorphism (SNP) discovery and genotyping are urgently needed for population management and conservation. In hybridized populations, genomic techniques that can identify and genotype thousands of species-diagnostic markers would allow precise estimates of population- and individual-level admixture as well as identification of 'super invasive' alleles, which show elevated rates of introgression above the genomewide background (likely due to natural selection). Techniques like restriction-site-associated DNA (RAD) sequencing can discover and genotype large numbers of SNPs, but they have been limited by the length of continuous sequence data they produce with Illumina short-read sequencing. We present a novel approach, overlapping paired-end RAD sequencing, to generate RAD contigs of >300-400 bp. These contigs provide sufficient flanking sequence for design of high-throughput SNP genotyping arrays and strict filtering to identify duplicate paralogous loci. We applied this approach in five populations of native westslope cutthroat trout that previously showed varying (low) levels of admixture from introduced rainbow trout (RBT). We produced 77 141 RAD contigs and used these data to filter and genotype 3180 previously identified species-diagnostic SNP loci. Our population-level and individual-level estimates of admixture were generally consistent with previous microsatellite-based estimates from the same individuals. However, we observed slightly lower admixture estimates from genomewide markers, which might result from natural selection against certain genome regions, different genomic locations for microsatellites vs. RAD-derived SNPs and/or sampling error from the small number of microsatellite loci (n = 7). We also identified candidate adaptive super invasive alleles from RBT that had excessively high admixture proportions in hybridized cutthroat trout populations.

Socioeconomic resilience to climatic extremes in a freshwater fishery.

Heterogeneity is a central feature of ecosystem resilience, but how this translates to socioeconomic resilience depends on people's ability to track shifting resources in space and time. Here, we quantify how climatic extremes have influenced how people (fishers) track economically valuable ecosystem services (fishing opportunities) across a range of spatial scales in rivers of the northern Rocky Mountains, USA, over the past three decades. Fishers opportunistically shifted from drought-sensitive to drought-resistant rivers during periods of low streamflows and warm temperatures. This adaptive behavior stabilized fishing pressure and expenditures by a factor of 2.6 at the scale of the regional fishery (i.e., portfolio effect). However, future warming is predicted to homogenize habitat options that enable adaptive behavior by fishers, putting ~30% of current spending at risk across the region. Maintaining a diverse portfolio of fishing opportunities that enable people to exploit shifting resources provides an important resilience mechanism for mitigating the socioeconomic impacts of climate change on fisheries.

Hybridization alters growth and migratory life-history expression of native trout.

Human-mediated hybridization threatens many native species, but the effects of introgressive hybridization on life-history expression are rarely quantified, especially in vertebrates. We quantified the effects of non-native rainbow trout admixture on important life-history traits including growth and partial migration behavior in three populations of westslope cutthroat trout over five years. Rainbow trout admixture was associated with increased summer growth rates in all populations and decreased spring growth rates in two populations with cooler spring temperatures. These results indicate that non-native admixture may increase growth under warmer conditions, but cutthroat trout have higher growth rates during cooler periods. Non-native admixture consistently increased expression of migratory behavior, suggesting that there is a genomic basis for life-history differences between these species. Our results show that effects of interspecific hybridization on fitness traits can be the product of genotype-by-environment interactions even when there are minor differences in environmental optima between hybridizing species. These results also indicate that while environmentally mediated traits like growth may play a role in population-level consequences of admixture, strong genetic influences on migratory life-history differences between these species likely explains the continued spread of non-native hybridization at the landscape-level, despite selection against hybrids at the population-level.

Detecting population declines via monitoring the effective number of breeders (Nb ).

Estimating the effective population size and effective number of breeders per year (Nb ) can facilitate early detection of population declines. We used computer simulations to quantify bias and precision of the one-sample LDNe estimator of Nb in age-structured populations using a range of published species life history types, sample sizes, and DNA markers. Nb estimates were biased by ~5%-10% when using SNPs or microsatellites in species ranging from fishes to mosquitoes, frogs, and seaweed. The bias (high or low) was similar for different life history types within a species suggesting that life history variation in populations will not influence Nb estimation. Precision was higher for 100 SNPs (H ≈ 0.30) than for 15 microsatellites (H ≈ 0.70). Confidence intervals (CIs) were occasionally too narrow, and biased high when Nb was small (Nb  < 50); however, the magnitude of bias would unlikely influence management decisions. The CIs (from LDNe) were sufficiently narrow to achieve high statistical power (≥0.80) to reject the null hypothesis that Nb  = 50 when the true Nb  = 30 and when sampling 50 individuals and 200 SNPs. Similarly, CIs were sufficiently narrow to reject Nb  = 500 when the true Nb  = 400 and when sampling 200 individuals and 5,000 loci. Finally, we present a linear regression method that provides high power to detect a decline in Nb when sampling at least five consecutive cohorts. This study provides guidelines and tools to simulate and estimate Nb for age structured populations (https://github.com/popgengui/agestrucnb/), which should help biologists develop sensitive monitoring programmes for early detection of changes in Nb and population declines.

Climate change and expanding invasive species drive widespread declines of native trout in the northern Rocky Mountains, USA.

Climate change and invasive species are major threats to native biodiversity, but few empirical studies have examined their combined effects at large spatial and temporal scales. Using 21,917 surveys collected over 30 years, we quantified the impacts of climate change on the past and future distributions of five interacting native and invasive trout species throughout the northern Rocky Mountains, USA. We found that the occupancy of native bull trout and cutthroat trout declined by 18 and 6%, respectively (1993­2018), and was predicted to decrease by an additional 39 and 16% by 2080. However, reasons for these occupancy reductions markedly differed among species: Climate-driven increases in water temperature and decreases in summer flow likely caused declines of bull trout, while climate-induced expansion of invasive species largely drove declines of cutthroat trout. Our results demonstrate that climate change can affect ecologically similar, co-occurring native species through distinct pathways, necessitating species-specific management actions.