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Animals of most species avoid close inbreeding, but the level of incest avoidance varies, and the ultimate causes of interspecies differences in the inbreeding tolerance are not quite clear. The subterranean lifestyle is associated with several characteristics which, in theory, should weaken incest avoidance. The available empirical data do not allow testing this prediction. In this laboratory study, the inbreeding avoidance in a strictly subterranean species, Zaisan mole vole (Ellobius tancrei) was estimated. The results provided evidence for incest avoidance between virgin female and closely related male (brother or father), whereas mother–son pairs displayed inbreeding tolerance. The odds ratio for the reproduction in unrelated vs sibling pairs was further used as a proxy index of inbreeding avoidance level to compare this characteristic in E. tancrei and 11 non-subterranean voles. In agreement with the predictions, (i) among non-subterranean voles, monogamous species displayed stronger incest avoidance than polygamous species; and (ii) subterranean monogamous species, E. tancrei, displayed higher inbreeding tolerance than non-subterranean monogamous species.

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.

Non-invasive age estimation is critically important for many field studies but often it represents a significant challenge. In rodents, upper incisors represent a part of a cranium which can be readily measured in an alive animal. We propose an age estimation method based on the measurements of both upper incisors’ width (IW) for a subterranean rodent, Ellobius tancrei. The IW measurements for 77 laboratory-born females and 81 males were fitted, separately for the sexes, by sigmoidal Gompertz growth functions to obtain the asymptotic values. Based on the data set encompassing pre-asymptotic ages, we then derived a polynomial regression model with log-transformed age as а predictor. The analysis revealed no statistically significant sex difference in growth patterns. Derived model explained 91% of IW variation and was used to obtain predicted values of age and their 95% prediction intervals through inverse calculations. We conclude that IW is a potentially useful age indicator for mole voles and possibly other rodents in cases when invasive or time-consuming methods are non-appropriate.

Group-living species differ in how the reproduction is shared among same-sex individuals and how the reproductive skew is attained. In mammals, the highest level of reproductive skew among females is known for some social African mole-rats. Mole voles (Ellobius, Arvicolinae) are similar to these well-studied subterranean rodents in both ecological specialization and social structure. At present, there is no information about the proximate mechanisms underlying singular breeding in any Ellobius species. In this study of the Zaisan mole voles, E. tancrei, we tested the mother’s influence on reproduction and survival of the young females exposed to an unrelated mate. Nine of 15 daughters housed in pairs bred, and all pairs persisted until the end of the experiment (6 months). The reproduction in the matrifilial trios (n = 12) was skewed towards mothers: only one daughter delivered but did not wean the litter. The latency until conception was significantly longer in paired daughters than in mothers from trios. Thus, the reproductive skew in trios may be initially generated by the age or experience difference rather than dominance asymmetry. Only 4 trios persisted for 6 months due to high female mortality. The heavier and older was a mother, and the younger was a daughter at male introduction, the more stable was the trio. The influence of females’ ages on group tenacity may be mediated by the daughter’s age-related reproductive activation. The despotic reproductive monopoly with extreme intolerance between kin reproductive females is unusual for voles and indicates a strong female–female competition in E. tancrei in nature.

Mole voles are the most specialized subterranean members of the subfamily Arvicolinae. We assess the basic reproductive parameters of the Zaisan mole vole (Ellobius tancrei Blasius, 1884) and compare our data with the characteristics reported for other Ellobius species and surface-dwelling voles. In most respects, reproduction of the E. tancrei follows the pattern that is typical for voles. Females undergo postpartum estrus, but rarely combine pregnancy with lactation. The rate of embryonic and postembryonic growth (0.13 and 0.54 g/day, respectively) are slightly lower, whereas the relative neonate and weanling masses (8% and 40% of maternal mass, respectively) are slightly higher than the respective values predicted for non-subterranean arvicolines. The combination of these trends results in the protracted pregnancy and lactation (both ∼30 days). The age at first breeding is delayed (>2.5 months). Despite heavy weanlings, total maternal investment per litter in E. tancrei is low due to small litter size (2.31). Although the species of Ellobius are similar to each other by the parameters of developmental time, they vary by litter size, total investment per litter, and possibly by relative neonate body mass. This is consistent with the idea that when body-size effect is removed, fecundity variables and degree of precociality at birth are dissociated from timing variables.

The generic status of Lasiopodomys and its division into subgenera Lasiopodomys (L. mandarinus, L. brandtii) and Stenocranius (L. gregalis, L. raddei) are not generally accepted because of contradictions between the morphological and molecular data. To obtain cytogenetic evidence for the Lasiopodomys genus and its subgenera and to test the autosome to sex chromosome translocation hypothesis of sex chromosome complex origin in L. mandarinus proposed previously, we hybridized chromosome painting probes from the field vole (Microtus agrestis, MAG) and the Arctic lemming (Dicrostonyx torquatus, DTO) onto the metaphases of a female Mandarin vole (L. mandarinus, 2n = 47) and a male Brandt's vole (L. brandtii, 2n = 34). In addition, we hybridized Arctic lemming painting probes onto chromosomes of a female narrow-headed vole (L. gregalis, 2n = 36). Cross-species painting revealed three cytogenetic signatures (MAG12/18, 17a/19, and 22/24) that could validate the genus Lasiopodomys and indicate the evolutionary affinity of L. gregalis to the genus. Moreover, all three species retained the associations MAG1bc/17b and 2/8a detected previously in karyotypes of all arvicolins studied. The associations MAG2a/8a/19b, 8b/21, 9b/23, 11/13b, 12b/18, 17a/19a, and 5 fissions of ancestral segments appear to be characteristic for the subgenus Lasiopodomys. We also validated the autosome to sex chromosome translocation hypothesis on the origin of complex sex chromosomes in L. mandarinus. Two translocations of autosomes onto the ancestral X chromosome in L. mandarinus led to a complex of neo-X1, neo-X2, and neo-X3 elements. Our results demonstrate that genus Lasiopodomys represents a striking example of rapid chromosome evolution involving both autosomes and sex chromosomes. Multiple reshuffling events including Robertsonian fusions, chromosomal fissions, inversions and heterochromatin expansion have led to the formation of modern species karyotypes in a very short time, about 2.4 MY.