Mitogenomic phylogenetics of the bank vole Clethrionomys glareolus, a model system for studying end-glacial colonization of Europe.

Abstract

We have revisited the mtDNA phylogeny of the bank vole Clethrionomys glareolus based on Sanger and next-generation Illumina sequencing of 32 complete mitochondrial genomes. The bank vole is a key study species for understanding the response of European fauna to the climate change following the Last Glacial Maximum (LGM) and one of the most convincing examples of a woodland mammal surviving in cryptic northern glacial refugia in Europe. The genomes sequenced included multiple representatives of each of the eight bank vole clades previously described based on cytochrome b (cob) sequences. All clades with the exception of the Basque - likely a misidentified pseudogene clade - were highly supported in all phylogenetic analyses and the relationships between the clades were resolved with high confidence. Our data extend the distribution of the Carpathian clade, the marker of a northern glacial refugium in the Carpathian Mountains, to include Britain and Fennoscandia (but not adjacent areas of continental Europe). The Carpathian sub-clade that colonized Britain and Fennoscandia had a somewhat different history from the sub-clade currently found in or close to the Carpathians and may have derived from a more north-westerly refugial area. The two bank vole populations that colonized Britain at the end of the last glaciation are for the first time linked with particular continental clades, the first colonists with the Carpathian clade and the second colonists with the western clade originating in a more southerly refugium in the vicinity of the Alps. We however found no evidence that a functional divergence of proteins encoded in the mitochondrial genome promoted the partial genetic replacement of the first colonists by the second colonists detected previously in southern Britain. We did identify one codon site that changed more often and more radically in the tree than expected and where the observed amino acid change may affect the reductase activity of the cytochrome bc1 complex, but the change was not specific to a particular clade. We also found an excess of radical changes to the primary protein structure for geographically restricted clades from southern Italy and Norway, respectively, possibly related to stronger selective pressure at the latitudinal extremes of the bank vole distribution. However, overall, we find little evidence of pervasive effects of deviation from neutrality on bank vole mtDNA phylogeography.