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As climate change continues, species pushed outside their physiological tolerance limits must adapt or face extinction. When change is rapid, adaptation will largely harness ancestral variation, making the availability and characteristics of that variation of critical importance. Here, we used whole-genome sequencing and genetic-environment association analyses to identify adaptive variation and its significance in the context of future climates in a small Palearctic mammal, the bank vole ( Clethrionomys glareolus ). We found that peripheral populations of bank vole in Britain are already at the extreme bounds of potential genetic adaptation and may require an influx of adaptive variation in order to respond. Analyses of adaptive loci suggest regional differences in climate variables select for variants that influence patterns of population adaptive resilience, including genes associated with antioxidant defense, and support a pattern of thermal/hypoxic cross-adaptation. Our findings indicate that understanding potential shifts in genomic composition in response to climate change may be key to predicting species’ fate under future climates. A species’ response to anthropogenic climate change may depend on its adaptations to past climate changes. Here, the authors use whole-genome resequencing and genetic-environment association to identify genes important for local adaptation and project adaptation under future climate scenarios across bank vole populations in Britain.

Bank voles (Myodes glareolus syn. Clethrionomys glareolus) are frequently used as an animal model in ecological and biomedical studies and are an important reservoir of viral and bacterial zoonotic pathogens, e.g., Puumala hantavirus (PUUV). Here we describe an accidental PUUV outbreak in a large bank vole laboratory colony caused by an accidental introduction of infected wild-trapped bank voles, and the successful eradication of the virus. The eradication plan was based on results of previous studies showing that maternal antibodies (MatAb) protect the young from infection for up to 40 days after weaning, four weeks longer than the estimated duration of PUUV infectivity in the environment. After ensuring that most animals were infected, 620 pairs were mated on the same day. Only females that showed PUUV-specific antibodies and produced offspring within 26 days after mating were retained. All individuals of the parental generation were euthanized before the last weaning. The weaned offspring were moved to individually ventilated cages (IVC) and repeatedly tested for the presence of PUUV-specific antibodies and RNA. A few infected or suspect animals were euthanized. The animals were then mated (in IVC) and, after producing grand-offspring generation, euthanized and tested for PUUV RNA in the lungs. No PUUV RNA was detected, and no animals showed PUUV-specific antibodies in subsequent generations. The successful clearance confirmed the protective efficiency of PUUV-specific MatAb. The procedure for PUUV clearance in the bank vole colony may represent a blueprint for similar approaches in valuable colonies of other rodents infected by similar pathogens.

Current species distributions at high latitudes are the product of expansion from glacial refugia into previously uninhabitable areas at the end of the last glaciation. The traditional view of postglacial colonization is that southern populations expanded their ranges into unoccupied northern territories. Recent findings on mitochondrial DNA (mtDNA) of British small mammals have challenged this simple colonization scenario by demonstrating a more complex genetic turnover in Britain during the Pleistocene–Holocene transition where one mtDNA clade of each species was replaced by another mtDNA clade of the same species. Here, we provide evidence from one of those small mammals, the bank vole (Clethrionomys glareolus), that the replacement was genome-wide. Using more than 10 000 autosomal SNPs we found that similar to mtDNA, bank vole genomes in Britain form two (north and south) clusters which admix. Therefore, the genome of the original postglacial colonists (the northern cluster) was probably replaced by another wave of migration from a different continental European population (the southern cluster), and we gained support for this by modelling with approximate Bayesian computation. This finding emphasizes the importance of analysis of genome-wide diversity within species under changing climate in creating opportunities for sophisticated testing of population history scenarios.

Understanding pest evolution in agricultural systems is crucial for developing effective and innovative pest control strategies. Types of cultivation, such as crop monocultures versus polycultures or crop rotation, may act as a selective pressure on pests’ capability to exploit the host’s resources. In this study, we examined the herbivorous mite Aceria tosichella (commonly known as wheat curl mite), a widespread wheat pest, to understand how fluctuating versus stable environments influence its niche breadth and ability to utilize different host plant species. We subjected a wheat‐bred mite population to replicated experimental evolution in a single‐host environment (either wheat or barley), or in an alternation between these two plant species every three mite generations. Next, we tested the fitness of these evolving populations on wheat, barley, and on two other plant species not encountered during experimental evolution, namely rye and smooth brome. Our results revealed that the niche breadth of A. tosichella evolved in response to the level of environmental variability. The fluctuating environment expanded the niche breadth by increasing the mite’s ability to utilize different plant species, including novel ones. Such an environment may thus promote flexible host‐use generalist phenotypes. However, the niche expansion resulted in some costs expressed as reduced performances on both wheat and barley as compared to specialists. Stable host environments led to specialized phenotypes. The population that evolved in a constant environment consisting of barley increased its fitness on barley without the cost of utilizing wheat. However, the population evolving on wheat did not significantly increase its fitness on wheat, but decreased its performance on barley. Altogether, our results indicated that, depending on the degree of environmental heterogeneity, agricultural systems create different conditions that influence pests’ niche breadth evolution, which may in turn affect the ability of pests to persist in such systems.

Abstract Host–parasite co-evolution drives the diversification of host immune genes involved in the recognition of pathogen antigens and molecular patterns. In contrast, the immune genes involved in self-recognition and inhibition of immune responses against self-cells (missing-self immunity) may be evolutionarily constrained by the need to interact with self-components. However, many pathogens, such as the Lyme disease agent Borrelia, hijack these genes to evade the immune system and may therefore select for their diversification. How these contrasting but concurrent selective forces shape the evolution of missing-self regulators is not clearly understood. To fill this gap, we investigated polymorphism and molecular signatures of selection acting on a missing-self regulator, the complement factor H (CFH), in bank vole populations, which are an important wild reservoir for Borrelia. We then compared the geographic structuring in the CFH domain interacting with Borrelia (CCP 20) against a genomic background represented by RAD-seq markers. We found signals of positive and diversifying selection at CCP 20, suggesting that CFH evolved in response to pressures from pathogens. Additionally, we found other innate immunity genes within the alternative complement pathway, which is regulated by CFH, under diversifying selection, highlighting its involvement in host–parasite coevolution. This study demonstrates that an innate missing-self sensor in a wild vertebrate is under diversifying selection, likely driven by pathogens.

Previous studies indicated that in some species phylogeographic patterns obtained in the analysis of nuclear and mitochondrial DNA (mtDNA) markers can be different. Such mitonuclear discordance can have important evolutionary and ecological consequences. In the present study, we aimed to check whether there was any discordance between mtDNA and nuclear DNA in the bank vole population in the contact zone of its two mtDNA lineages. We analysed the population genetic structure of bank voles using genome-wide genetic data (SNPs) and diversity of sequenced heart transcriptomes obtained from selected individuals from three populations inhabiting areas outside the contact zone. The SNP genetic structure of the populations confirmed the presence of at least two genetic clusters, and such division was concordant with the patterns obtained in the analysis of other genetic markers and functional genes. However, genome-wide SNP analyses revealed the more detailed structure of the studied population, consistent with more than two bank vole recolonisation waves, as recognised previously in the study area. We did not find any significant differences between individuals representing two separate mtDNA lineages of the species in functional genes coding for protein-forming complexes, which are involved in the process of cell respiration in mitochondria. We concluded that the contemporary genetic structure of the populations and the width of the contact zone were shaped by climatic and environmental factors rather than by genetic barriers. The studied populations were likely isolated in separate Last Glacial Maximum refugia for insufficient amount of time to develop significant genetic differentiation.

The information about the magnitude of differences in thermal plasticity both between and within populations, as well as identification of the underlying molecular mechanisms are key to understanding the evolution of thermal plasticity. In particular, genes underlying variation in the physiological response to temperature can provide raw material for selection acting on plastic traits. Using RNAseq, we investigate the transcriptional response to temperature in males and females from bulb mite populations selected for the increased frequency of one of two discrete male morphs (fighter- and scrambler-selected populations) that differ in relative fitness depending on temperature. We show that different mechanisms underlie the divergence in thermal response between fighter- and scrambler-selected populations at decreased vs. increased temperature. Temperature decrease to 18 °C was associated with higher transcriptomic plasticity of males with more elaborate armaments, as indicated by a significant selection-by-temperature interaction effect on the expression of 40 genes, 38 of which were upregulated in fighter-selected populations in response to temperature decrease. In response to 28 °C, no selection-by-temperature interaction in gene expression was detected. Hence, differences in phenotypic response to temperature increase likely depended on genes associated with their distinct morph-specific thermal tolerance. Selection of males also drove gene expression patterns in females. These patterns could be associated with temperature-dependent fitness differences between females from fighter- vs. scrambler-selected populations reported in previous studies. Our study shows that selection for divergent male sexually selected morphologies and behaviors has a potential to drive divergence in metabolic pathways underlying plastic response to temperature in both sexes.

The evolution of costly traits such as deer antlers and peacock trains, which drove the formation of Darwinian sexual selection theory, has been suggested to both reflect and affect patterns of genetic variance across the genome, but direct tests are missing. Here, we used an evolve and resequence approach to reveal patterns of genome-wide diversity associated with the expression of a sexually selected weapon that is dimorphic among males of the bulb mite, Rhizoglyphus robini . Populations selected for the weapon showed reduced genome-wide diversity compared to populations selected against the weapon, particularly in terms of the number of segregating non-synonymous positions, indicating enhanced purifying selection. This increased purifying selection reduced inbreeding depression, but outbred female fitness did not improve, possibly because any benefits were offset by increased sexual antagonism. Most single nucleotide polymorphisms (SNPs) that consistently diverged in response to selection were initially rare and overrepresented in exons, and enriched in regions under balancing or relaxed selection, suggesting they are probably moderately deleterious variants. These diverged SNPs were scattered across the genome, further demonstrating that selection for or against the weapon and the associated changes to the mating system can both capture and influence genome-wide variation. Populations of a bulb mite that were experimentally selected for a male weapon showed reduced diversity across the genome, indicating that strong sexual selection increases the strength of purifying selection.

If genetic architectures of various quantitative traits are similar, as studies on model organisms suggest, comparable selection pressures should produce similar molecular patterns for various traits. To test this prediction, we used a laboratory model of vertebrate adaptive radiation to investigate the genetic basis of the response to selection for predatory behavior and compare it with evolution of aerobic capacity reported in an earlier work. After 13 generations of selection, the proportion of bank voles (Myodes [=Clethrionomys] glareolus) showing predatory behavior was five times higher in selected lines than in controls. We analyzed the hippocampus and liver transcriptomes and found repeatable changes in allele frequencies and gene expression. Genes with the largest differences between predatory and control lines are associated with hunger, aggression, biological rhythms, and functioning of the nervous system. Evolution of predatory behavior could be meaningfully compared with evolution of high aerobic capacity, because the experiments and analyses were performed in the same methodological framework. The number of genes that changed expression was much smaller in predatory lines, and allele frequencies changed repeatably in predatory but not in aerobic lines. This suggests that more variants of smaller effects underlie variation in aerobic performance, whereas fewer variants of larger effects underlie variation in predatory behavior. Our results thus contradict the view that comparable selection pressures for different quantitative traits produce similar molecular patterns. Therefore, to gain knowledge about molecular-level response to selection for complex traits, we need to investigate not only multiple replicate populations but also multiple quantitative traits.

Current species distributions at high latitudes are the product of expansion from glacial refugia into previously uninhabitable areas at the end of the last glaciation. The traditional view of postglacial colonization is that southern populations expanded their ranges into unoccupied northern territories. Recent findings on mitochondrial DNA (mtDNA) of British small mammals have challenged this simple colonization scenario by demonstrating a more complex genetic turnover in Britain during the Pleistocene–Holocene transition where one mtDNA clade of each species was replaced by another mtDNA clade of the same species. Here, we provide evidence from one of those small mammals, the bank vole (Clethrionomys glareolus), that the replacement was genome-wide. Using more than 10 000 autosomal SNPs we found that similar to mtDNA, bank vole genomes in Britain form two (north and south) clusters which admix. Therefore, the genome of the original postglacial colonists (the northern cluster) was probably replaced by another wave of migration from a different continental European population (the southern cluster), and we gained support for this by modelling with approximate Bayesian computation. This finding emphasizes the importance of analysis of genome-wide diversity within species under changing climate in creating opportunities for sophisticated testing of population history scenarios.