Genetic structure and colonization processes in European populations of the common vole, Microtus arvalis.

The level of genetic differentiation within and between evolutionary lineages of the common vole (Microtus arvalis) in Europe was examined by analyzing mitochondrial sequences from the control region (mtDNA) and 12 nuclear microsatellite loci (nucDNA) for 338 voles from 18 populations. The distribution of evolutionary lineages and the affinity of populations to lineages were determined with additional sequence data from the mitochondrial cytochrome b gene. Our analyses demonstrated very high levels of differentiation between populations (overall FST: mtDNA 70%; nucDNA 17%). The affinity of populations to evolutionary lineages was strongly reflected in mtDNA but not in nucDNA variation. Patterns of genetic structure for both markers visualized in synthetic genetic maps suggest a postglacial range expansion of the species into the Alps, as well as a potentially more ancient colonization from the northeast to the southwest of Europe. This expansion is supported by estimates for the divergence times between evolutionary lineages and within the western European lineage, which predate the last glacial maximum (LGM). Furthermore, all measures of genetic diversity within populations increased significantly with longitude and showed a trend toward increase with latitude. We conclude that the detected patterns are difficult to explain only by range expansions from separate LGM refugia close to the Mediterranean. This suggests that some M. arvalis populations persisted during the LGM in suitable habitat further north and that the gradients in genetic diversity may represent traces of a more ancient colonization of Europe by the species.

Heckel G ，Burri R ，Fink S ，Desmet JF ，Excoffier L ... -  《EVOLUTION》

Transalpine colonisation and partial phylogeographic erosion by dispersal in the common vole (Microtus arvalis).

The colonisation history and genetic structure of the common vole (Microtus arvalis) was investigated in the region of the Alps by analysing the mitochondrial cytochrome b gene (mtDNA) and 19 microsatellite loci (nucDNA) for 137 voles from 52 localities. mtDNA data provided a much refined distribution of three highly divergent evolutionary lineages in the region compared to previous studies. Although high mountain ranges are widely accepted to be barriers for colonisation processes for many organisms and especially small terrestrial mammals, our phylogeographic analyses showed clear evidence of four transalpine colonisation events by the common vole. Individual-based phylogenetic analyses of nucDNA and two alternative Bayesian-clustering approaches revealed a deep genetic structure analogous to mtDNA. Incongruence between nucDNA and mtDNA at the individual level was restricted to the regions of contact between the lineages. mtDNA patterns and strong female philopatry in M. arvalis suggest that the crossings of the Alps occurred during the colonisation of the region when it was free from ice after the last glaciation. nucDNA patterns suggest that some of the transalpine elements of this phylogeographic pattern were subsequently eroded by male-biased gene flow. We conclude that the combination of phylogeography and landscape genetics at the individual level can provide very detailed insights into colonisation events and may even allow differentiation between historical and more recent processes.

Braaker S ，Heckel G 《-》

Mitochondrial gene diversity in the common vole Microtus arvalis shaped by historical divergence and local adaptations.

The phylogeography of the common vole (Microtus arvalis) was examined by analysing mitochondrial DNA (mtDNA) sequence variation in 1044 base pairs (bp) of the cytochrome b (cytb) gene and in 322 bp of the control region (ctr) among 106 individuals from 58 locations. The geographical distribution of four previously recognized cytb evolutionary lineages in Europe was refined and a new lineage was found in southern Germany. All lineages were distributed allopatrically, except in one sample that was probably located in a contact zone. The occurrence of several lineages in the Alps is in keeping with their recent recolonization from distinct sources. The translation of 84 cytb DNA sequences produced 33 distinct proteins with relationships that differed from those of the DNA haplotypes, suggesting that the mtDNA lineages did not diverge in response to selection. In comparison with M. agrestis, a neutrality test detected no overall evidence for selection in the cytb gene, but a closer examination of a structural model showed that evolutionarily conserved and functionally important positions were often affected. A new phylogeographical test of random accumulation of nonsynonymous mutations generated significant results in three lineages. We therefore conclude that the molecular diversity of cytb in M. arvalis is overall the result of the demographic history of the populations, but that there have been several episodes of local adaptation to peculiar environments.

Fink S ，Excoffier L ，Heckel G 《MOLECULAR ECOLOGY》

Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences.

Voles of the genus Microtus represent one of the most speciose mammalian genera in the Holarctic. We established a molecular phylogeny for Microtus to resolve contentious issues of systematic relationships and evolutionary history in this genus. A total of 81 specimens representing ten Microtus species endemic to Europe as well as eight Eurasian, six Asian and one Holarctic species were sequenced for the entire cytochrome b gene (1140 bp). A further 25 sequences were retrieved from GenBank, providing data on an additional 23, mainly Nearctic, Microtus species. Phylogenetic analysis of these 48 species generated four well-supported monophyletic lineages. The genus Chionomys, snow voles, formed a distinct and well-supported lineage separate from the genus Microtus. The subgenus Microtus formed the strongest supported lineage with two sublineages displaying a close relationship between the arvalis species group (common voles) and the socialis species group (social voles). Monophyly of the Palearctic pitymyid voles, subgenus Terricola, was supported, and this subgenus was also subdivided into two monophyletic species groups. Together, these groupings clarify long-standing taxonomic uncertainties in Microtus. In addition, the "Asian" and the Nearctic lineages reported previously were identified although the latter group was not supported. However, relationships among the main Microtus branches were not resolved, suggesting a rapid and potentially simultaneous radiation of a widespread ancestor early in the history of the genus. This and subsequent radiations discernible in the cytochrome b phylogeny, show the considerable potential of Microtus for analysis of historical and ecological determinants of speciation in small mammals. It is evident that speciation is an ongoing process in the genus and that the molecular data provides a vital insight into current species limits as well as cladogenic events of the past.

Jaarola M ，Martínková N ，Gündüz I ，Brunhoff C ，Zima J ，Nadachowski A ，Amori G ，Bulatova NS ，Chondropoulos B ，Fraguedakis-Tsolis S ，González-Esteban J ，José López-Fuster M ，Kandaurov AS ，Kefelioğlu H ，da Luz Mathias M ，Villate I ，Searle JB ... -  《MOLECULAR PHYLOGENETICS AND EVOLUTION》

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

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.

Deffontaine V ，Libois R ，Kotlík P ，Sommer R ，Nieberding C ，Paradis E ，Searle JB ，Michaux JR ... -  《MOLECULAR ECOLOGY》