Interspecific introgression is a potentially important source of novel variation of adaptive significance. Although multiple cases of adaptive introgression are well documented, broader generalizations about its targets and mechanisms are lacking. Multiallelic balancing selection, particularly when acting through rare allele advantage, is an evolutionary mechanism expected to favor adaptive introgression. This is because introgressed alleles are likely to confer an immediate selective advantage, facilitating their establishment in the recipient species even in the face of strong genomic barriers to introgression. Vertebrate major histocompatibility complex genes are well-established targets of long-term multiallelic balancing selection, so widespread adaptive major histocompatibility complex introgression is expected. Here, we evaluate this hypothesis using data from 29 hybrid zones formed by fish, amphibians, squamates, turtles, birds, and mammals at advanced stages of speciation. The key prediction of more extensive major histocompatibility complex introgression compared to genome-wide introgression was tested with three complementary statistical approaches. We found evidence for widespread adaptive introgression of major histocompatibility complex genes, providing a link between the process of adaptive introgression and an underlying mechanism. Our work identifies major histocompatibility complex introgression as a general mechanism by which species can acquire novel, and possibly regain previously lost, variation that may enhance defense against pathogens and increase adaptive potential.

• Keywords
• MHC, adaptation, host–pathogen coevolution, hybridization, introgression,
• MeSH
• Genetic Introgression * MeSH
• Major Histocompatibility Complex * genetics   MeSH
• Hybridization, Genetic * MeSH
• Evolution, Molecular MeSH
• Vertebrates * genetics   MeSH
• Selection, Genetic MeSH
• Genetic Speciation MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH

Genetic admixture introduces new variants at relatively high frequencies, potentially aiding rapid responses to environmental changes. Here, we evaluate its role in adaptive variation related to climatic conditions in bank voles (Clethrionomys glareolus) in Britain, using whole-genome data. Our results reveal loci showing excess ancestry from one of the two postglacial colonist populations inconsistent with overall admixture patterns. Notably, loci associated with climate adaptation exhibit disproportionate amounts of excess ancestry, highlighting the impact of admixture between colonist populations on local adaptation. The results suggest strong and localized selection on climate-adaptive loci, as indicated by steep clines and/or shifted cline centres, during population replacement. A subset, including a haemoglobin gene, is associated with oxidative stress responses, underscoring a role of oxidative stress in local adaptation. Our study highlights the important contribution of admixture during secondary contact between populations from distinct climatic refugia enriching adaptive diversity. Understanding these dynamics is crucial for predicting future adaptive capacity to anthropogenic climate change.

• MeSH
• Acclimatization genetics   MeSH
• Arvicolinae * genetics   physiology   MeSH
• Adaptation, Physiological genetics   MeSH
• Genetic Variation MeSH
• Polymorphism, Single Nucleotide MeSH
• Climate Change * MeSH
• Climate MeSH
• Genetics, Population MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Geographicals
• United Kingdom MeSH

Evidence for divergent selection and adaptive variation across the landscape can provide insight into a species' ability to adapt to different environments. However, despite recent advances in genomics, it remains difficult to detect the footprints of climate-mediated selection in natural populations. Here, we analysed ddRAD sequencing data (21,892 SNPs) in conjunction with geographic climate variation to search for signatures of adaptive differentiation in twelve populations of the bank vole (Clethrionomys glareolus) distributed across Europe. To identify the loci subject to selection associated with climate variation, we applied multiple genotype-environment association methods, two univariate and one multivariate, and controlled for the effect of population structure. In total, we identified 213 candidate loci for adaptation, 74 of which were located within genes. In particular, we identified signatures of selection in candidate genes with functions related to lipid metabolism and the immune system. Using the results of redundancy analysis, we demonstrated that population history and climate have joint effects on the genetic variation in the pan-European metapopulation. Furthermore, by examining only candidate loci, we found that annual mean temperature is an important factor shaping adaptive genetic variation in the bank vole. By combining landscape genomic approaches, our study sheds light on genome-wide adaptive differentiation and the spatial distribution of variants underlying adaptive variation influenced by local climate in bank voles.

• Keywords
• Clethrionomys glareolus, climate gradient, genomic analysis, local adaptations, rodent,
• Publication type
• Journal Article MeSH

The elateroid family Lycidae is known for limited dispersal propensity and high species-level endemism. The red net-winged beetle, Dictyoptera aurora (Herbst, 1874), differs from all relatives by the range comprising almost the entire Holarctic region. Based on a five-marker phylogeny and 67 barcode entries (cox1-5' mtDNA) from the whole range, we recovered two genetically distinct species within traditionally defined D. aurora and resurrected the name D. coccinata (Say, 1835) as the oldest available synonym for Nearctic populations. Yet, no reliable morphological trait distinguishes these species except for minute differences in the male genitalia. D. coccinata is a monophylum resulting from a single Miocene dispersal event, ~15.8 million years ago, and genetic divergence implies long-term isolation by the Bering Strait. Far East Asian and west European populations are also genetically distinct, although to a lower extent. Two independent colonization events established the Fennoscandian populations after the last glacial maximum. Besides intrinsic factors, the high morphological similarity might result from stabilizing selection for shared aposematic signals. The rapidly accumulating barcode data provide valuable information on the evolutionary history and the origins of regional faunas.

• Keywords
• Müllerian mimicry, aposematic signal, barcode, cryptic species, dispersal, last glacial maximum, morphological stasis, mtDNA, rRNA, taxonomy,
• Publication type
• Journal Article MeSH

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.

• Keywords
• Myodes glareolus, SNP, admixture, genotyping‐by‐sequencing, postglacial colonization,
• Publication type
• Journal Article MeSH

Species-level environmental niche modeling has been crucial in efforts to understand how species respond to climate variation and change. However, species often exhibit local adaptation and intraspecific niche differences that may be important to consider in predicting responses to climate. Here, we explore whether phylogeographic lineages of the bank vole originating from different glacial refugia (Carpathian, Western, Eastern, and Southern) show niche differentiation, which would suggest a role for local adaptation in biogeography of this widespread Eurasian small mammal. We first model the environmental requirements for the bank vole using species-wide occurrences (210 filtered records) and then model each lineage separately to examine niche overlap and test for niche differentiation in geographic and environmental space. We then use the models to estimate past [Last Glacial Maximum (LGM) and mid-Holocene] habitat suitability to compare with previously hypothesized glacial refugia for this species. Environmental niches are statistically significantly different from each other for all pairs of lineages in geographic and environmental space, and these differences cannot be explained by habitat availability within their respective ranges. Together with the inability of most of the lineages to correctly predict the distributions of other lineages, these results support intraspecific ecological differentiation in the bank vole. Model projections of habitat suitability during the LGM support glacial survival of the bank vole in the Mediterranean region and in central and western Europe. Niche differences between lineages and the resulting spatial segregation of habitat suitability suggest ecological differentiation has played a role in determining the present phylogeographic patterns in the bank vole. Our study illustrates that models pooling lineages within a species may obscure the potential for different responses to climate change among populations.

• Keywords
• Last Glacial Maximum, MaxEnt, Myodesglareolus, cryptic refugia, ecological niche modeling, intraspecific variation,
• Publication type
• Journal Article MeSH