High molecular variability in three pine vole species of the subgenus Terricola ( Microtus , Arvicolinae) and plausible source of polymorphism

Abstract

We studied molecular variability to clarify intraspecific differentiation and phylogenetic relationships in three pine vole species (genus Microtus, subgenus Terricola): Microtus subterraneus, Microtus daghestanicus, and Microtus majori. Multilocus analysis was performed using the entire mitochondrial cytb gene and fragments of nuclear BRCA1, IRBP, and XIST genes. Results confirmed separation of the species, especially M. majori compared with M. daghestanicus and M. subterraneus. These species showed different molecular polymorphism in the genetic markers. We identified two close forms of M. majori, differing in cytb gene and the nuclear gene XIST; one form inhabits the northern slopes of the Greater Caucasus, another the Transcaucasia. Separation of M. daghestanicus populations from North Ossetia and the others was clear. Microtus subterraneus populations from southern Europe and Asia Minor were characterized by maximal genetic heterogeneity; the specimen from Samsun (northern Asia Minor) appeared to be most distant from the others. Despite polymorphism in the chromosome number in M. subterraneus populations from the East European Plain, they possess a depleted gene pool. Results indicated that M. subterraneus colonized the East European Plain in the Holocene, and chromosome variability originated in this part of the species' range as a result of chromosomal fission and quick fixation of the arrangement in northern populations. We argue that differences in the genetic differentiation patterns of Terricola species are mainly due to their ecological peculiarities.

Geographic Mosaic of Extensive Genetic Variations in Subterranean Mole Voles Ellobius alaicus as a Consequence of Habitat Fragmentation and Hybridization

“…One of the most striking examples is a group of pine voles of the subgenus Terricola (genus Microtus ), which includes several species with different patterns of chromosomal polymorphism. As demonstrated in a recent work involving molecular markers [ 28 ], in the Caucasus pine vole M. daghestanicus , along with a wide Robertsonian chromosome fan, significant variability of mitochondrial cytb gene and even nuclear BRCA1 gene was observed, where their different variants existed in the same chromosome form and even the same population. It should be noted that the wide molecular polymorphism was explained by ecological peculiarities of Caucasus pine voles, inhabiting alpine meadows (likely mole voles) and evolving in small isolated populations.…”

“…We assumed that for the reconstruction of the sibling species phylogeny, data on the XIST gene (one of the actively used sex-linked markers) would be valuable [ 14 , 18 , 28 , 39 ]. Indeed, the analysis of the sequences of its two fragments transformed and added details to the above picture.…”

“…The sequences of the protein-coding genes ( cytb and IRBP ) were presented by entire codons. Marginal codon boundaries (i.e., the first nucleotide of the initial codon and the third nucleotide of the last codon) in the IRBP gene fragment were determined from its sequences in genomes of house mice [ 27 ] and pine voles of the Terricola subgenus [ 28 ]. Sites in which two overlapping peaks were reproducibly registered in chromatograms were coded and treated as heterozygous.…”

“…Dendrograms were built based on the Maximum Likelihood (ML) method using IQTree software, version 2.0-rc2 [ 29 , 30 ]; the ModelFinder option [ 31 ] was applied to achieve optimal model evaluation of nucleotide substitutions for each gene. Before statistical analysis, non-extended deletions (revealed in the XIST gene sequences of several specimens) were filled in by random nucleotides which were absent in the total mole voles’ sample; this approach was used in analysis of the XIST gene variability in pine voles of the Terricola subgenus [ 28 ]. Final images of phylogenetic trees rooted on the genetically remotest group (i.e., mole voles from Mongolia) in all cases were rendered in FigTree 1.4.3 ( (accessed on 25 November 2018)) and processed in Inkscape ( (accessed on 27 September 2021)).…”

Voles and Lemmings (Arvicolinae) of the Palaearctic Region

“…M. fingeri has thus far been held in synonymy of majori and afterwards of subterraneus. We rank it as a species in its own right on the basis of a deep divergence in Mt-sequences (Bogdanov et al 2021; our unpublished results).…”