Arvicolinae is one of the most impressive placental radiations with over 150 extant and numerous extinct species that emerged since the Miocene in the Northern Hemisphere. The phylogeny of Arvicolinae has been studied intensively for several decades using morphological and genetic methods. Here, we sequenced 30 new mitochondrial genomes to better understand the evolutionary relationships among the major tribes and genera within the subfamily. The phylogenetic and molecular dating analyses based on 11,391 bp concatenated alignment of protein-coding mitochondrial genes confirmed the monophyly of the subfamily. While Bayesian analysis provided a high resolution across the entire tree, Maximum Likelihood tree reconstruction showed weak support for the ordering of divergence and interrelationships of tribal level taxa within the most ancient radiation. Both the interrelationships among tribes Lagurini, Ellobiusini and Arvicolini, comprising the largest radiation and the position of the genus Dinaromys within it also remained unresolved. For the first time complex relationships between genus level taxa within the species-rich tribe Arvicolini received full resolution. Particularly Lemmiscus was robustly placed as sister to the snow voles Chionomys in the tribe Arvicolini in contrast with a long-held belief of its affinity with Lagurini. Molecular dating of the origin of Arvicolinae and early divergences obtained from the mitogenome data were consistent with fossil records. The mtDNA estimates for putative ancestors of the most genera within Arvicolini appeared to be much older than it was previously proposed in paleontological studies.

Supplementary data are available at Bioinformatics online.

In this article, we present the nearly complete mitochondrial genome of the Subalpine Kashmir vole Hyperacrius fertilis (Arvicolinae, Cricetidae, Rodentia), assembled using data from Illumina next-generation sequencing (NGS) of the DNA from a century-old museum specimen. De novo assembly consisted of 16,341 bp and included all mitogenome protein-coding genes as well as 12S and 16S RNAs, tRNAs and D-loop. Using the alignment of protein-coding genes of 14 previously published Arvicolini tribe mitogenomes, seven Clethrionomyini mitogenomes, and also Ondatra and Dicrostonyx outgroups, we conducted phylogenetic reconstructions based on a dataset of 13 protein-coding genes (PCGs) under maximum likelihood and Bayesian inference. Phylogenetic analyses robustly supported the phylogenetic position of this species within the tribe Arvicolini. Among the Arvicolini, Hyperacrius represents one of the early-diverged lineages. This result of phylogenetic analysis altered the conventional view on phylogenetic relatedness between Hyperacrius and Alticola and prompted the revision of morphological characters underlying the former assumption. Morphological analysis performed here confirmed molecular data and provided additional evidence for taxonomic replacement of the genus Hyperacrius from the tribe Clethrionomyini to the tribe Arvicolini.

The subterranean voles of the genus Ellobius are species of subfamily Arvicolinae well adapted to underground life. In this paper, we report the assemblies of complete mitochondrial genomes for three mole voles from genus Ellobiusnorthern mole vole Ellobius talpinus (16,376 bp), transcaucasian mole vole E. lutescens (16,540 bp), and southern mole vole E. fuscocapillus (16,388 bp). Each of three mitogenomes encode for 12S and 16S rRNAs, 22 tRNAs, 13 protein-coding genes, and D-loop in the characteristic arrangement of subfamily Arvicolinae (Rodentia: Cricetidae). This study verifies the evolutionary status of subgenera Bramus and Ellobius within the genus Ellobius at the molecular level. The mitochondrial genome would be a significant supplement for the Ellobius genetic background. The three Ellobius species formed a monophyletic group with the high bootstrap value (100%) in all examinations.

Background Mitochondrial genes encode proteins involved in oxidative phosphorylation. Variations in lifestyle and ecological niche can be directly reflected in metabolic performance. Subterranean rodents represent a good model for testing hypotheses on adaptive evolution driven by important ecological shifts. Voles and lemmings of the subfamily Arvicolinae (Rodentia: Cricetidae) provide a good example for studies of adaptive radiation. This is the youngest group within the order Rodentia showing the fastest rates of diversification, including the transition to the subterranean lifestyle in several phylogenetically independent lineages. Results We evaluated the signatures of selection in the mitochondrial cytochrome b (cytB) gene in 62 Arvicolinae species characterized by either subterranean or surface-dwelling lifestyle by assessing amino acid sequence variation, exploring the functional consequences of the observed variation in the tertiary protein structure, and estimating selection pressure. Our analysis revealed that: (1) three of the convergent amino acid substitutions were found among phylogenetically distant subterranean species and (2) these substitutions may have an influence on the protein complex structure, (3) cytB showed an increased ω and evidence of relaxed selection in subterranean lineages, relative to non-subterranean, and (4) eight protein domains possess increased nonsynonymous substitutions ratio in subterranean species. Conclusions Our study provides insights into the adaptive evolution of the cytochrome b gene in the Arvicolinae subfamily and its potential implications in the molecular mechanism of adaptation. We present a framework for future characterizations of the impact of specific mutations on the function, physiology, and interactions of the mtDNA-encoded proteins involved in oxidative phosphorylation.

Life under the earth surface is highly challenging and associated with a number of morphological, physiological and behavioral modifications. Subterranean niche protects animals from predators, fluctuations in environmental parameters, but is characterized by high levels of carbon dioxide and low levels of oxygen and implies high energy requirements associated with burrowing. Moreover, it lacks most of the sensory inputs available above ground. The current study describes results from RNA-seq analysis of four subterranean voles from subfamily Arvicolinae: Prometheomys schaposchnikowi, Ellobius lutescens, Terricola subterraneus, and Lasiopodomys mandarinus. Original RNA-seq data were obtained for eight species, for nine species, SRA data were downloaded from the NCBI SRA database. Additionally assembled transcriptomes of Mynomes ochrogaster and Cricetulus griseus were included in the analysis. We searched for the selection signatures and parallel amino acid substitutions in a total of 19 species. Even within this limited data set, we found significant changes of dN/dS ratio by free-ratio model analysis for subterranean Arvicolinae. Parallel substitutions were detected in genes RAD23B and PYCR2. These genes are associated with DNA repair processes and response to oxidative stress. Similar substitutions were discovered in the RAD23 genes for highly specialized subterranean Heterocephalus glaber and Fukomys damarensis. The most pronounced signatures of adaptive evolution related to subterranean niche within species of Arvicolinae subfamily were detected for Ellobius lutescens. Our results suggest that genomic adaptations can occur very quickly so far as the amount of selection signatures was found to be compliant with the degree of specialization to the subterranean niche and independent from the evolutionary age of the taxon. We found that the number of genomic signatures of selection does not depend on the age of the taxon, but is positively correlated with the degree of specialization to the subterranean niche.

In this paper, we report the complete mitochondrial genome of the common pine vole Microtus (Terricola) subterraneus, which was sequenced for the first time using Illumina next-generation sequencing (NGS) technology. The total length of the mitogenome was 16,398 bp and contained 12S, 16S rRNAs, 22 tRNAs, 13 protein-coding genes, and a 883 bp D-loop in the characteristic arrangement of subfamily Arvicolinae, Rodentia. Overall base composition of the complete mitochondrial DNA is A (33.0%), C (26.5%), G (13.4%), and T (27.0%), respectively. Phylogenetic analysis of mitochondrial genomes showed a classic taxon pattern, identified using individual phylogenetic markers.

This study evaluates signatures of selection in the evolution of the mitochondrial DNA of voles, subfamily Arvicolinae, during the colonization of subterranean environments. The comparative sequence analysis of mitochondrial protein-coding genes of eight subterranean vole species (Prometheomys schaposchnikowi, three species of the genus Ellobius: Ellobius talpinus, Ellobius fuscocapillus and Ellobius lutescens, two species of the genus Terricola: Terricola subterraneus and Terricola daghestanicus, Lasiopodomys mandarinus, and Hyperacrius fertilis) and their closest aboveground relatives was applied using codon-substitution models. The highest number of selection signatures was detected in genes ATP8 and CYTB. The relaxation of selection was observed in most mitochondrial DNA protein-coding genes for subterranean species. The largest amount of relaxed genes is discovered in mole voles (genus Ellobius). The number of selection signatures was found to be independent of the evolutionary age of the lineage but fits the degree of specialization to the subterranean niche. The common trends of selective pressures were observed among the evolutionary ancient and highly specialized subterranean rodent families and phylogenetically young lineages of voles. It suggests that the signatures of adaptation in individual mitochondrial protein-coding genes associated with the colonization of the subterranean niche may appear within a rather short evolutionary timespan.