This study provides the first evidence of ultrasonic vocalisations (USVs) in a truly subterranean rodent, the northern mole vole Ellobius talpinus. Calls were recorded by attracting callers with a bait to burrow entrances, where they were mostly visible to researchers. USVs recorded from 14 different burrows in southern Russia were verified as belonging to Ellobius talpinus by comparison with USVs of two wild-captured young males and by comparison with USVs of four adults from a captive colony. As a first attempt at exploring the function of USV diversity, we defined upward-intense USVs, with a maximum fundamental frequency (f0) of 35.32 ± 5.11 kHz, and variable-faint USVs, with a maximum f0 of 31.40 ± 7.78 kHz. Compared to variable-faint USVs, the upward-intense USVs were longer, had a larger depth of frequency modulation and were produced at high intensity in regular series. The upward-intense USVs were lower in the maximum and peak frequencies in the wild than in captivity, whereas the variable-faint USVs did not differ between recordings from the wild and from captivity. We discuss that similar ranges of acoustic variables found in USVs of Ellobius talpinus and surface-dwelling Arvicolinae species do not support the hypothesis that subterranean life has drastically reduced ultrasonic vocalisation in rodents.

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.

The mandarin vole, Lasiopodomys mandarinus, is one of the most intriguing species among mammals with non-XX/XY sex chromosome system. It combines polymorphism in diploid chromosome numbers, variation in the morphology of autosomes, heteromorphism of X chromosomes, and several sex chromosome systems the origin of which remains unexplained. Here we elucidate the sex determination system in Lasiopodomys mandarinus vinogradovi using extensive karyotyping, crossbreeding experiments, molecular cytogenetic methods, and single chromosome DNA sequencing. Among 205 karyotyped voles, one male and three female combinations of sex chromosomes were revealed. The chromosome segregation pattern and karyomorph-related reproductive performances suggested an aberrant sex determination with almost half of the females carrying neo-X/neo-Y combination. The comparative chromosome painting strongly supported this proposition and revealed the mandarin vole sex chromosome systems originated due to at least two de novo autosomal translocations onto the ancestral X chromosome. The polymorphism in autosome 2 was not related to sex chromosome variability and was proved to result from pericentric inversions. Sequencing of microdissection derived of sex chromosomes allowed the determination of the coordinates for syntenic regions but did not reveal any Y-specific sequences. Several possible sex determination mechanisms as well as interpopulation karyological differences are discussed.