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.

Understanding the historical contributions of differing glacial refugia is key to evaluating the roles of microevolutionary forces, such as isolation, introgression, and selection in shaping genomic diversity in present‐day populations. In Europe, where both Mediterranean and extra‐Mediterranean (e.g., Carpathian) refugia of the bank vole (Clethrionomys glareolus) have been identified, mtDNA indicates that extra‐Mediterranean refugia were the main source of colonization across the species range, while Mediterranean peninsulas harbor isolated, endemic lineages. Here, we critically evaluate this hypothesis using previously generated genomic data (>6,000 SNPs) for over 800 voles, focusing on genomic contributions to bank voles in central Europe, a key geographic area in considering range‐wide colonization. The results provide clear evidence that both extra‐Mediterranean (Carpathian) and Mediterranean (Spanish, Calabrian, and Balkan) refugia contributed to the ancestry and genomic diversity of bank vole populations across Europe. Few strong barriers to dispersal and frequent admixture events in central Europe have led to a prominent mid‐latitude peak in genomic diversity. Although the genomic contribution of the centrally located Carpathian refugium predominates, populations in different parts of Europe have admixed origins from Mediterranean (28%–47%) and the Carpathian (53%–72%) sources. We suggest that the admixture from Mediterranean refugia may have provisioned adaptive southern alleles to more northern populations, facilitating the end‐glacial spread of the admixed populations and contributing to increased bank vole diversity in central Europe. This study adds critical details to the complex end‐glacial colonization history of this well‐studied organism and underscores the importance of genomic data in phylogeographic interpretation.

Increasing evidence suggests that adaptation to diverse environments often involves selection on existing variation rather than new mutations. A previous study identified a nonsynonymous single nucleotide polymorphism (SNP) in exon 2 of two paralogous β-globin genes of the bank vole (Clethrionomys glareolus) in Britain in which the ancestral serine (Ser) and the derived cysteine (Cys) allele represent geographically partitioned functional variation affecting the erythrocyte antioxidative capacity. Here we studied the geographical pattern of the two-locus Ser/Cys polymorphism throughout Europe and tested for the geographic correlation between environmental variables and allele frequency, expected if the polymorphism was under spatially heterogeneous environment-related selection. Although bank vole population history clearly is important in shaping the dispersal of the oxidative stress protective Cys allele, analyses correcting for population structure suggest the Europe-wide pattern is affected by geographical variation in environmental conditions. The β-globin phenotype is encoded by the major paralog HBB-T1 but we found evidence of bidirectional gene conversion of exon 2 with the low-expression paralog HBB-T2. Our data support the model where gene conversion reshuffling genotypes between high- and low- expressed paralogs enables tuning of erythrocyte thiol levels, which may help maintain intracellular redox balance under fluctuating environmental conditions. Therefore, our study suggests a possible role for gene conversion between differentially expressed gene duplicates as a mechanism of physiological adaptation of populations to new or changing environments.

The Iberian desman ( Galemys pyrenaicus ), a semiaquatic mammal endemic to southwestern Europe, is listed as Endangered by the IUCN due to substantial range and population decline in recent years, with its populations now largely limited to river headwaters. This restriction to upstream locations highlights the importance of documenting genetic variation and population connectivity in Iberian desmans for effective conservation strategies. While previous studies have revealed phylogeographic structure across the range of the species, gaps remain in our understanding of the microgeographic dynamics that shape genetic exchange within specific geographic regions. This study first combined our newly generated SNP data with previous datasets to further explore genetic structure across the entire Iberian desman distribution using the 115 individuals now available. Due to differences in methodology between our study and previous studies, only 110 SNPs were available for comparison across all individuals. Nevertheless, the analysis with these SNPs confirmed the presence of the five major phylogeographic units previously described and validated the assignment of our newly generated dataset to the Occidental phylogeographic unit. Focusing on our newly generated data, we explored the microgeographic dynamics of this Occidental phylogeographic unit with a higher-resolution genomic dataset (7,604 SNPs, 14 individuals). This analysis provided evidence of isolation-by-distance (IBD), suggesting that gene flow decreases with increasing geographic distance and that dispersal occurs primarily over short distances. Focussing on the Douro river system, our genomic clustering results showed both connectivity along the best-sampled river (Sabor) and between headwaters of this and headwaters from a closely located river (Tua). Our IBD results were consistent with this, indicating riverine dispersal as well as a combination of riverine and overland dispersal at headwaters. These results highlight the importance of both aquatic and terrestrial corridors in upstream areas for maintaining connectivity. Thus, conservation efforts should prioritize the protection and restoration of riparian and terrestrial corridors, particularly in fragmented landscapes, to mitigate isolation and preserve genetic diversity in the Iberian desman. This study underscores the value of genomic approaches in conservation and contributes to a deeper understanding of the ecological and evolutionary processes that maintain population connectivity in an endangered species.