Search

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.

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 current study evaluates the selection signals in the evolution of 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: E. talpinus, E. fuscocapillus and E. lutescens, two species of the genus Terricola: T. subterraneus and T. daghestanicus, Lasiopodomys mandarinus and Hyperacrius fertilis) and their closest aboveground relatives using codon-substitution models was applied. The highest number of selection signatures was detected in genes ATP8 and CYTB. The relaxation of selection was observed in most mtDNA protein-coding genes. In mole voles (genus Ellobius) the signatures of adaptive evolution of mitochondrial genes related to subterranean niche were most pronounced. 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 adaptations in individual mitochondrial protein-coding genes associated with the colonization of the subterranean niche may appear within a rather short evolutionary timespan.

Revealing the species- and age-specific effects of social conditions on reproduction can provide insight into the dynamics and evolution of animal social systems. Lagurus lagurus is an arvicoline rodent inhabiting the steppes of Eurasia. Living in extensive habitats and establishing monogamous groups, reported for this species, have been predicted to favour the mechanisms of social control of reproduction. On the other hand, any delay in breeding should be extremely costly for spring-born females in a short-lived multivoltine species. We performed two laboratory experiments to estimate incest avoidance and reproductive suppression by a same-sex competitor, in relation to the age of a focal female of L. lagurus. We also tested if the female reproductive rate in communal groups was affected by dominance asymmetry. In our first experiment, lemmings, independently of female age, displayed strong inbreeding avoidance. In the second experiment, female mortality tended to be higher in polygynous groups than in pairs, but there was no monopolization of reproduction in either sister or matrilineal trios. Latency to the birth of a litter was longer in polygynous than in monogamous primiparous females, but dominance asymmetry did not influence this characteristic. No age-related differences were revealed in the readiness to breed as a member of a communal group. Polygyny reduced the per-female reproductive success of older (about 3 months of age) primiparous females, whereas there was no such effect for younger (about 1 month of age) females.

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.

The social environment can be stressful for at least some group members, resulting in elevated levels of glucocorticoid stress hormones (GC). Patterns of the relationships between social rank and GC levels vary between species. In carnivores, primates and birds that live in permanent cooperative groups, helpers do not usually display physiological indicators of stress. Very little is known about status-related GC differences within cooperative groups of rodents. In this laboratory study, we compared GC concentrations in dominant (fathers) and subordinate (natal sons) males of a cooperative subterranean vole, Ellobius tancrei. The assessment of adrenocortical activity by measuring urine glucocorticoid metabolites (UGM) was previously validated for this species through an ACTH challenge test. We observed clear peaks of UGM in the second or third urine samples taken after the administration of ACTH (lag time equal to 2.5–3 h). Thus, UGM is suitable to estimate physiological stress in Ellobius. Postpubertal sons living in natal groups had significantly higher UGM concentrations than their fathers. The average UGM levels of sons were positively associated with their ages and paternal body masses, and negatively associated with paternal ages. Hence, son-father interactions rather than just younger ages of sons appear to contribute to GC differences. The revealed pattern was not consistent with that reported for most cooperative species from other taxa, highlighting the importance of comparative studies.

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.

Subterranean rodents are a good model system to examine adaptive evolution of social organization. Life underground has been proposed either to favor solitariness or, to the contrary, to promote sociality. In concordance with the first idea, most specialized diggers are solitary. However, group-living in several unrelated subterranean rodent species and especially eusociality in two genera of African mole-rats, the Bathyergidae, seem to support the second hypothesis. Thus, none of the two models is fully consistent with empirical data. Here we apply the comparative phylogenetic method to test an evolutionary correlation between fossoriality and female social strategy (solitary breeding vs breeding in group). Both characters show very strong phylogenetic signal, and we found a significant correlation between them. Subterranean lifestyle is readily acquired under female sociality. By contrast, the transition to life underground is extremely unlikely under female solitariness. Thus, not only social behavior may be affected by ecological specialization as it is widely assumed, but it can itself restrain the range of possible specializations. The rates of transition from sociality to solitariness are equal under subterranean and surface-dwelling lifestyle. Sociality loss is irreversible in subterranean lineages, unlike surface-dwelling lineages. Based on the revealed transition rates we suggest that all lineages of subterranean rodents have gone through the stage of cooperation at the beginning of their evolutionary track, whereas group-living is selected against in highly specialized diggers. An odd pattern of distribution of sociality across and within truly subterranean taxa probably derives from the influence of extrinsic factors in combination with phylogenetic inertia.

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.