Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus)

Abstract

This study details the phylogeographic pattern of the bank vole, Clethrionomys glareolus, a European rodent species strongly associated with forest habitat. We used sequences of 1011 base pairs of the mitochondrial DNA cytochrome b gene from 207 bank voles collected in 62 localities spread throughout its distribution area. Our results reveal the presence of three Mediterranean (Spanish, Italian and Balkan) and three continental (western, eastern and 'Ural') phylogroups. The endemic Mediterranean phylogroups did not contribute to the post-glacial recolonization of much of the Palaearctic range of species. Instead, the major part of this region was apparently recolonized by bank voles that survived in glacial refugia in central Europe. Moreover, our phylogeographic analyses also reveal differentiated populations of bank voles in the Ural mountains and elsewhere, which carry the mitochondrial DNA of another related vole species, the ruddy vole (Clethrionomys rutilus). In conclusion, this study demonstrates a complex phylogeographic history for a forest species in Europe which is sufficiently adaptable that, facing climate change, survives in relict southern and northern habitats. The high level of genetic diversity characterizing vole populations from parts of central Europe also highlights the importance of such regions as a source of intraspecific genetic biodiversity.

Molecular and ecological signs of mitochondrial adaptation: consequences for introgression?

“…Therefore, similar to other small mammals (Fløjgaard et al, 2009) the distribution of M. glareolus appears to be related to productivity in the environment (Stephenson, 1998). This result suggest that introgressed M. rutilus mitotype in M. glareolus background could have facilitated the invasion of this species to more severe environments, assuming that hybridization happened before the invasion (as suggested by some of the previous studies: Tegelström, 1987;Deffontaine et al, 2005). These evidences also suggest that different mitotypes (and likely also key OXPHOS nuclear units) populate different climatic regions that may have allowed local adaptation.…”

“…Whether massive mtDNA introgression results from purely neutral processes or it can be significantly affected by natural selection remains a matter of debate (Cheviron and Brumfield, 2009;Arnold et al, 2011;Pons et al, 2013). For example, studies on the Eurasian bank vole Myodes (or Clethrionomys) glareolus have shown that its northeastern, and some eastern, populations harbour an mtDNA lineage that introgressed from its neighbour, Myodes rutilus, that has even become fixed in some populations (Tegelström, 1987;Deffontaine et al, 2005;Boratyń ski et al, 2011). This observation led to the hypothesis that colonization of northeastern Europe and western Asia by M. glareolus was facilitated by the introgression (before or during colonization of currently occupied regions), through hybridization, of physiological mechanisms that allowed it to inhabit more severe habitats (Boratyń ski et al, 2011;Šíchová et al, 2014).…”

Geography and host biogeography matter for understanding the phylogeography of a parasite

“…1). Similarly, some species such as the brown bear (Ursus arctos) (Taberlet et al, 1998) or different small mammal species [Clethrionomys glareolus (Deffontaine et al, 2005); Sorex minutus and S. araneus (Bilton et al, 1998) and M. arvalis (Jaarola and Searle, 2004) and M. oeconomus (Brunhoff et al, 2003)] display genetic lineages suggesting that these species also survived in more easterly refuges (the Caucasus or the southern Urals) and in Central Europe (Kotlı´k et al, 2006). Moreover, the examination of the fossil record of European temperate species during the last ice age (26000-13000 years ago) reveals that environmental conditions were not severe enough in these regions to prevent the survival of forest-dependent species, notably in Poland (Sommer and Nadachowski, 2006).…”

Postglacial recolonisation of European Russia by the common shrew Sorex araneus

“…Such species traditionally have been considered to have spread northwards from refugia in Southern Europe at the end of the glaciation (Hewitt, 1999). However, mitochondrial DNA studies on some widespread species of small mammal suggest that colonisation may have occurred from glacial refugia in central Europe (Bilton et al, 1998;Deffontaine et al, 2005). Chromosome studies on the common shrew suggest that postglacial colonisation of Northern Europe may have occurred from the Urals (Polyakov et al, 1997(Polyakov et al, , 2000 and from a refugium near the Black Sea coast along the northern slopes of the Carpathian Mts.…”