Gray Vole Research Articles

Small mammals from the Strashnaya cave (Northwest Altai, West Siberia, Russia)

A sequence of small mammal associations has been studied from the Paleolithic site of Strashnaya cave (Altai Mountains, West Siberia, Russia). The total faunal composition includes 45 species of rodents, bats, insectivores, and lagomorphs. The dominant groups in each of 10 layers that included small mammal remains are rock voles, grey voles and zokors. Co-dominating groups are ground squirrel, marmots, steppe lemmings, and red-backed voles. Small mammals from the Strashnaya cave indicate that during Late Pleistocene winters in the region could have been warmer than now. They also suggest highly mosaic biotopes around the cave in Late Pleistocene that includes open steppe, desert, floodplain, and forest. Small mammals show open areas such as steppes, floodplain and meadows in the early Holocene. The modern small mammal fauna confidently indicate taiga forest environments.

Comparison of genetic and morphological characters in fossil teeth of grey voles from the Russian Far East (Rodentia: Cricetidae: Alexandromys)

Far-Eastern grey voles of the genus Alexandromys are a group of 12 species distributed exclusively in the Eastern Palearctic. Morphologically they are hard to be distinguished due to interspecific overlapping of several characters. In recent material of Alexandromys morphometric analyses of teeth (in particular the first lower molar) proved to be a good tool for species identification, although there are overlaps in several measurements. In subfossil and fossil material, preliminary analyses indicated considerable variation in tooth morphology and, in comparison to extant species, the presence of additional morphologically ambiguous forms. In the present study we tested in subfossil and fossil teeth of the genus Alexandromys from Russian Far East whether taxonomic classification based on morphology is in concordance with species determination based on DNA analysis. We also asked whether the morphologically ambiguous forms could be assigned to described species by means of DNA sequence analysis. The material originated from Medvezhyi Klyk Cave Deposits (Primorskyi Krai, Russia) and had an age of 2000–40,000 years. The results showed that the success rate in PCR amplification was ∼50% and it was possible to obtain PCR products of >400bp. The concordance between taxonomic assignment based on morphology and genetics was high. Out of 17 samples that were successful in the sequence analysis, only one yielded a classification that contradicts morphology and one specimen could not be classified since the delivered sequence most probably is a numt (nuclear copy of mitochondrial origin). Although only one of the four unidentified teeth in our sample was successful in the DNA analysis and allowed taxonomic assignment, our results suggest that genetic species determination could be a valuable tool to classify subfossil and fossil teeth in Arvicolinae.

Analysis of shape and size variation of the first lower molar in Far-Eastern grey voles of genus Alexandromys (Rodentia: Cricetidae) from Russian fauna using geometric morphometrics

Analysis of shape and size variation of the first lower molar in Far-Eastern grey voles of genus Alexandromys (Rodentia: Cricetidae) from Russian fauna using geometric morphometrics

The structure of craniometrical diversity of grey voles Microtus subgenus Alexandromys

The sample of 1671 intact skulls (15 measurements) of grey voles from Alexandromys subgenus and Microtus oeconomus was studied. Representatives of M. oeconomus and M. middendorffii are very similar in craniometrical features. The race M. o. kharanurensis is morphologically distant from other representatives of M. oeconomus, and possibly should not be included into this species. M. sachalinensis morphologically is similar to M. fortis. The specimens of M. gromovi are located inside the limits of internal variation of M. middendorffii. The both latter species are similar to M. mongolicus. There are western and eastern groups found inside M. mongolicus. The level of morphological differences between M. maximowiczii, M. mujanensis and M. evoronensis does not differ from the same between two groups of M. mongolicus or between races of M. fortis. The Russian part of the range of M. maximowiczii should be enlarged due to finding of the population of this species from the floodmeadows of Ussuri River. The morphological similarity between M. limnophilus and M. mongolicus is revealed. The voles M. l. malygini does not display similarity with the type specimen of M. limnophilus. The propriety for considering malygini as a race of M. limnophilus should be questioned.

Multiple independent evolutionary losses of XY pairing at meiosis in the grey voles

In many eutherian mammals, X-Y chromosome pairing and recombination is required for meiotic progression and correct sex chromosome disjunction. Arvicoline rodents present a notable exception to this meiotic rule, with multiple species possessing asynaptic sex chromosomes. Most asynaptic vole species belong to the genus Microtus sensu lato. However, many of the species both inside and outside the genus Microtus display normal X-Y synapsis at meiosis. These observations suggest that the synaptic condition was present in the common ancestor of all voles, but gaps in current taxonomic sampling across the arvicoline phylogeny prevent identification of the lineage(s) along which the asynaptic state arose. In this study, we use electron and immunofluorescent microscopy to assess heterogametic sex chromosome pairing in 12 additional arvicoline species. Our sample includes ten species of the tribe Microtini and two species of the tribe Lagurini. This increased breadth of sampling allowed us to identify asynaptic species in each major Microtine lineage. Evidently, the ability of the sex chromosomes to pair and recombine in male meiosis has been independently lost at least three times during the evolution of Microtine rodents. These results suggest a lack of evolutionary constraint on X-Y synapsis in Microtini, hinting at the presence of alternative molecular mechanisms for sex chromosome segregation in this large mammalian tribe.

Meiosis in gray voles of the subgenus Microtus (Rodentia, Arvicolinae) and in their hybrids

The results of light and electron microscopic (EM) studies of meiosis in Microtus arvalis males of the karyoform "arvalis" (2n = 46, NFa = 80), in hybrids between the chromosomal forms arvalis and obscurus (2n = 46, NFa = 68), in M. rossiaemeridionalis voles (2n = 54, NFa = 54), and in a hybrid between the species M. rossiaemeridionalis and M. kermanensis (2n = 54, NFa = 54) are presented. SC (synaptonemal complex) karyotypes of the parental forms and the hybrids were constructed on the basis of measurements of the length ofautosomal SCs revealed by the EM analysis in spermatocytes at the stage of middle pachytene. The SC karyotypes of M. arvalis and the hybrids female obscurus x male arvalis consist of 22 synaptonemal complexes of autosomal bivalents and the axial elements of the synaptonemal complexes of the sex chromosomes X and Y. The SC karyotypes of M. rossiaemeridionalis and the hybrid M. rossiaemeridionalis x M. kermanensis consist of 26 synaptonemal complexes of autosomal bivalents and a sex bivalent; they differ only in the length of the Y chromosome axis (Y chromosome in the hybrid was inherited from M. kermanensis). Asynaptic configurations of the autosomal SCs were not observed in the hybrids. The SC axial elements of the X and Y chromosomes in the parental forms and in the hybrids were located close to each other throughout pachytene, but they did not form a synaptic region. The normal synapsis in sterile hybrids (M. rossiaemeridionalis x M. kermanensis) and the behavior of the sex chromosomes in meiosis in fertile and sterile hybrids are discussed in the context of specific features of meiosis and reproductive isolation.

X-Y Chromosome Synapsis and Recombination in 3 Vole Species of Asian Lineage of the Genus Microtus (Rodentia: Arvicolinae)

The pattern of X-Y chromosome pairing in male meiosis is an important taxonomic feature of grey voles of the genus Microtus. Asynaptic sex chromosomes have been found in the majority of species of the Palearctic phylogenetic lineage of this genus, while normal X-Y synapsis has been observed in the species of subgenus Pallasiinus belonging to the Asian phylogenetic lineage. We analyzed sex chromosome pairing and recombination in M. maximowiczii, M. mujanensis and M. fortis which also belong to the Asian phylogenetic lineage (subgenus Alexandromys). Using immunostaining for the proteins of the synaptonemal complex (SCP3) and recombination nodules (MLH1) we demonstrated that X and Y chromosomes of these species paired and recombined in a short subtelomeric region. This indicates that the sex chromosomes of these species retain an ancestral fully functional pseudoautosomal region, which has been lost or rearranged in the asynaptic species of the genus Microtus.

Radiation events in the subfamily Arvicolinae (Rodentia): Evidence from nuclear genes

Voles and lemmings (subfamily Arvicolinae) areone of the youngest and speciesrich groups of myomorphic rodents prevailing in different landscapezones of the northern hemisphere. Because of unprecedented fossil records, as well as rapid and continuingmorphogenesis, they became leading forms in correlation and biostratigraphy of late Cenozoic continentaldeposits. For the same reasons, they are an almostideal model group for testing various evolutionary scenarios and phylogenetic hypotheses on the one hand,and for comparison of the possibilities and limitationsof different methodical approaches to phylogeny analysis and system generation, on the other hand.This study consisted in analysis of two nuclear genevariation, which demonstrated that mole lemmings(Ellobuisini), steppe lemmings (Lagurini) and grayvoles (Arvicolini) were sister groups. This divergencewas the latest, third step of subfamily radiation. Thenew data on close sister relationships of mole lemmings, gray voles, and steppe lemmings and on the latemole lemming radiation are unexpected and contradictory to traditional views.Originally, system generation and relationshipanalysis within the subfamily were based on comparatively studying the morphological traits in the modernand extinct forms; the most important results werereported in summary monographs and articles [1–4].As new approaches (karyological, allozyme analysis, molecular methods) appeared, modified schemeswere developed based on the new data [5–12]. Comprehensively studying the group revealed some distincthigher categories of the tribal rank in all summariesand systems, including the latest ones [11]. At thesame time, their composition, relationships, and thetime of divergence still remain obscure. Morphological approaches fail to reconstruct the evolutionary history and relationships of such a young and rapidlyevolving group because of a few available traits andnumerous parallelisms.The study of Arvicolinae molecular phylogeny hasbeen so far based on the mitochondrial cytochrome

Supraspecies relationships in the subfamily Arvicolinae (Rodentia, Cricetidae): An unexpected result of nuclear gene analysis

Phylogenetic analysis of the supraspecies relationships was carried out using partial sequences of two nuclear genes in the subfamily Arvicolinae, which is one of the youngest and species-rich groups of myomorph rodents. The analysis with the new data resolved the majority of polytomy nodes in the phylogenetic trees reported for Arvicolinae, suggesting a gradual, rather than a saltatory, mode for their evolution. Mole voles Ellobiusini, steppe voles Lagurini, and gray voles Arvicolini were fount to be a monophyletic group that corresponds to the latest third wave of radiation within the subfamily. Red-back voles Myodini (=Clethrionomini) are a sister clade to this group and correspond to the second radiation wave. The order of divergence remained unresolved for the earliest radiation wave (Ondatrini, Prometheomyini, Dicrostonychini, and Lemmini). The close relationships observed for mole, gray, and steppe voles are unexpected and contradict the conventional views that Ellobiusini are an ancient group and are separate from all other voles on evidence of the extreme simplicity of their rooted molars and the peculiar structure of their skull and postcranial skeleton. It was assumed that many of these morphological characters indicate adaptation to subterranean life and provide no phylogenetic signal.

Taxonomic position of Afghan vole (Subgenus Blanfordimys) by the sequence of the mitochondrial cytb gene

It is rather difficult to construct a system of gray voles of the tribe Microtini by a set of morphological and karyological characters because form generation is mosaic at these organization levels. The sequence of the mitochondrial cytochrome b gene was used to study the phylogenetic relationships and taxonomic position of the Central Asian subgenus Blanfordimys. Afghan vole Microtus (Blanfordimys) afghanus and Bucharian vole M. (Blanfordimys) bucharensis clustered with Pamir vole M. (Neodon) juldaschi, which is conventionally assigned to another subgenus. The last two species proved to be significantly closer to each other than either of them was to M. (Blanfordimys) afghanus, which disagrees with the monophyletic origin accepted for Blanfordimys. The genetic distances between the species of the subgenus Blanfordmys and M. juldaschi were comparable with the distances between the sister subgenera Microtus s. str. and Sumeriomys or Pallasiinus and Alexandromys and with the basal divergence of supraspecific clades in the subgenus Terricola. It was assumed that a special Central Asian group of species exists within the tribe Microtini and includes species of the subgenus Blanfordimys and Ml juldaschi and that the subgenera Neodon and Blanfordimys should be revised.

Comparative mapping of X chromosomes in vole species of the genus Microtus.

Comparative mapping of X-linked genes has progressed rapidly since Ohno's prediction that genes on the X chromosome should be conserved as a syntenic group in all mammals. Although several conserved blocks of homology between human and mouse have been discovered, rearrangements within the X chromosome have also been characterized. More recently, some exceptions to Ohno's law have been reported. We have used fluorescence in situ hybridization (FISH) to map five genes, Gla, G6pd, Hprt, Pgk1 and Xist, to two of the largest conserved segments of X material in five members of the genus Microtus (grey vole) and show that vole X chromosomes demonstrate greater homology to human than to mouse. Cytogenetic analysis indicates a relatively high frequency of rearrangement during vole evolution, although certain blocks of homology appear to be highly conserved in all species studied to date. On this basis we were able to predict the probable location of the rat X inactivation centre (Xic) based solely on high-resolution G-banding. Our prediction was then confirmed by mapping the rat Xist gene by FISH. The possible significance of conserving long-range chromosome structure in the vicinity of the Xic is discussed with respect to the mechanism of X inactivation.

The Vole Gene Map

Gray voles belong to the Arvicolidae family and, together with mouse and rat, to the vast Muroidea superfamily. All representatives of the genus Microtus look quite similar; a nonspecialist can see hardly any differences between them, except perhaps their slight variations in size and fur color. Voles are small rodents, with body sizes ranging between 80 and 145 mm, depending on species and sex. They have short tails (approximately one third their body length) with light gray to dark brown fur (Meyer and others 1996). They can be maintained in captivity relatively easily, and the conditions reported previously are suitable (Jackson 1997). The taxonomic status of different species of genus Microtus has been revised many times, and the exact status of some species of voles is still questionable. The relative rank of voles is complicated by the high morphological similarity of different representatives of gray voles, which led to misidentification of species using zoological criteria. The karyological approach shed more light on vole taxonomy and allowed identification of groups of species instead of a single polytypical species. This article describes the result of our efforts in mapping the genomes of 5 species of gray voles: M. arvalis, M. rossiaemeridionalis, M. kirgisorum, M. transcaspicus, and M. agrestis. Many revisions have been made to the status of Microtus arvalis (common vole). Initial, unsuccessful attempts to describe its chromosome set date back to the late 1930s, when Renaud first reported the correct number as 2n=46 (Renaud 1938). Additional research on the species has revealed many chromosome forms that had previously been considered subspecies. In 1965, the chromosome sets of voles were studied from subspecies M. arvalis duplicatus captured in the Leningrad region of Russia, and the diploid number was identified as 54, not 46, chromosomes (Meyer and others 1967). Later, sympatric sibling species were reported (Meyer and others