Multilocus phylogeny and taxonomy of East Asian voles Alexandromys (Rodentia,Arvicolinae)

Phylogenetic relationships, taxonomy and nomenclature issues within East Asian voles Alexandromys were addressed using comprehensive species samples, including all 12 valid species of the genus, and multilocus analysis. We examined the mitochondrial cytochrome b (cytb) gene and three nuclear genes in 36 specimens. Additionally, we examined a data set of 106 specimens using only the cytb gene. Our results did not confirm the aggregation of A. kikuchii, A. montebelli and A. oeconomus into a separate clade, namely the subgenus Pallasiinus. Analysis of incomplete lineage sorting using JML software highlighted both the cases of mitochondrial introgression and incomplete lineage sorting within the genus. Thus, the sister position of A. sachalinensis and A. maximowiczii in mitochondrial trees could be explained by mitochondrial introgression, while the sister position of A. limnophilus and A. fortis in mitochondrial trees could be successfully explained by incomplete lineage sorting. Very short genetic distances, together with an absence of monophyly, of the three species, A. evoronensis, A. mujanensis and A. maximowiczii, is supported by multiple morphological data, which indicates that these three taxa should be one species—A. maximowiczii. Analysis of genetic distances and tree topology revealed that three species of short‐tailed voles—A. middendorffii, A. mongolicus and A. gromovi—are more closely related to each other than to other established species of Alexandromys. The lacustrine vole, A. limnophilus, is closely related to the group of short‐tailed voles. Analysis of the type specimens of limnophilus and flaviventris confirmed that these taxa form one species together with A. l. malygini. Our results suggest that the mountains of western Mongolia are inhabited by a new taxon of short‐tailed voles of the same rank as middendorffii, mongolicus and gromovi—A. m. alpinus ssp. n.     

Water metabolism in free-ranging pine voles (Microtus pinetorum)

Rates of body water turnover in free-ranging pine voles exceeded those reported for a large number of similarly sized mammals. Concentrations of urine obtained from free-ranging pine voles were significantly lower than values published for other free-ranging mammals and also for laboratory-maintained members of this species. Rates of body water turnover in this species were not correlated with seasonal changes in soil temperatures.     

Systematics of snow voles (Chionomys, Arvicolinae) revisited

To elucidate the evolutionary history of snow voles, genus Chionomys, we studied the phylogeography of Chionomysnivalis across its range and investigated its relationships with two congeneric species, Chionomysgud and Chionomysroberti, using independent molecular markers. Analyses were based on mitochondrial (~940 bp cyt b) and Y-chromosomal (~2020 bp from three introns) genetic variation. Our data provide conclusive evidence for a Caucasian and Middle Eastern origin for the three species and a subsequent westward expansion of C.nivalis. In addition, we discuss the taxonomic status of the genus Chionomys in relation to the genus Microtus.     

Molecular and morphological evidence for multiple species within Paranoplocephala omphalodes (Cestoda, Anoplocephalidae) in Microtus voles (Arvicolinae)

Haukisalmi, V., Wickström, L. M., Henttonen, H., Hantula, J. & Gubányi, A. (2004). Molecular and morphological evidence for multiple species within Paranoplocephala omphalodes (Cestoda, Anoplocephalidae) in Microtus voles (Arvicolinae). —Zoologica Scripta, 33, 277–290. The present study was designed to test the hypothesis that the anoplocephalid cestode Paranoplocephala omphalodes (Hermann, 1783), a Holarctic parasite of Microtus voles, is a complex of host‐specific species, rather than a single host‐generalist species, using uni‐ and multivariate morphometrics and DNA sequence data from the mitochondrial cytochrome oxidase I gene. The phylogenetic methods applied to the mtDNA sequence data showed consistently that the cestodes morphologically recognizable as P. omphalodes include four well‐supported monophyletic groups, representing at least three distinct, largely host‐specific species. Multivariate morphometrics (discriminant analysis) successfully distinguished the four main mtDNA clades of P. omphalodes‐like cestodes. The true P. omphalodes is shown to be a parasite of Microtus arvalis, M. agrestis and Clethrionomys glareolus in Europe. Microtus oeconomus harbours two host‐specific, allopatric and possibly conspecific clades, one with a Holarctic and another with an (eastern) Beringian (Alaskan) distribution. The eastern Beringian endemic M. miurus is also parasitized with a host‐specific, morphologically divergent species of Paranoplocephala. The cestode clades recognized in M. oeconomus and M. miurus represent 2–3 undescribed species. Molecular phylogenetic analyses supported the monophyly of the ‘northern clade’ of Paranoplocephala spp., an assemblage including P. kalelai from Clethrionomys spp., P. macrocephala from Microtus spp. and all clades of P. omphalodes‐like cestodes except those representing the true P. omphalodes from Europe. The intra‐ and interspecific phylogeny within the northern clade is compared tentatively with the known evolutionary history of the hosts.     

中国(鼲)亚科田鼠族(Microtini)分类学研究进展与中国已知种类

䶄亚科田鼠族（Microtini）是一个分布广、物种多、在分类学上存在争议也较多的类群。通常认为该族在全世界有10属81种,中国有7属24种。近年来,通过广泛采集标本,开展分类与系统发育研究,基本厘清了我国䶄亚科田鼠族分类与系统发育问题。确认田鼠族在全世界仅8属,分别是东方田鼠属（Alexandromys）、雪田鼠属（Chionomys）、毛足田鼠属（Lasiopodomys）、艾草田鼠属（Lemmiscus）、田鼠属（Microtus）、松田鼠属（Neodon）、沟牙田鼠属（Proedromys）和川西田鼠属（Volemys）。帕米尔田鼠属（Blanfordimys）被证明是田鼠属的亚属,白尾松田鼠属（Phaiomys）是松田鼠属 的同物异名,水䶄属（Arvicola）被证明不属于田鼠族。而东方田鼠属是从田鼠属的亚属提升为属。中国田鼠族包括6属26种。青海毛足田鼠（Lasiopodomys fuscus）、白尾松田鼠（Phaiomys leucurus）和克氏田鼠（Microtus clarkei）均是松田鼠属成员。凉山沟牙田鼠（Proedromys liangshanensis）、林芝松田鼠（Neodon linzhiensis）、聂拉木松田鼠（Neodon nyalamensis）和墨脱松田鼠 （Neodon medogensis）是近年来命名的新种。     

Ontogenetic variation in occlusal shape of evergrowing molars in voles: An intravital study in Microtus gregalis (Arvicolinae,Rodentia)

In order to reveal patterns of ontogenetic change in occlusal shape of evergrowing molars in arvicolines, an intravital tooth printing method was applied to 20 individuals of Microtus gregalis born in captivity. Complexity patterns of the first lower molar were assessed by morphotype analysis of the anteroconid complex. Morphotype dental patterns were monitored using tooth prints at 0.5, 1, 2, 3 months of age, and postmortem. Ontogenetic changes in molar complexity and bilateral symmetry among right and left molars of the same individual during the process of tooth wear were assessed. Our results suggested that morphotype dental patterns could not be clearly established in half-month old animals due to presence of juvenile characters. For animals of 1 month and older, age differences in morphotype dental patterns were non-significant and negligible compared to among-individual variation. Within-individual differences among right and left molars, when present, were not related to age of an animal suggesting that bilateral asymmetry of morphotype dental pattern could be regarded as inherent characteristic of an individual persisting during post-juvenile tooth wear.     

Cryptic variation in mole voles Ellobius (Arvicolinae,Rodentia) of Mongolia

The mole vole subgenus Ellobius is currently considered to include three species: Ellobius talpinus (distributed from SE Europe and Turkmenistan through Kazakhstan to SW Siberia), Ellobius alaicus (S Tianshan, Pamir-Alay) and Ellobius tancrei (East and West Central Asia, from the Amu-Darya to Mongolia and N China). A study focusing on the genetic variation in Ellobius from Mongolia was conducted using one mitochondrial and three nuclear markers. Two divergent allopatric lineages endemic to East Central Asia were revealed. The first lineage occurs from Dzungaria eastwards to central Mongolia and represents E. tancrei sensu stricto. The second lineage is found in East Gobi only and corresponds to a taxon described as Ellobius orientalis, which has been traditionally treated as a subspecies of E. tancrei. However, molecular and chromosome data indicate that orientalis is related not to E. tancrei but to E. talpinus, which is separated from the former by a distribution gap of ~2,000 km. The taxonomic status of the East Gobi mole vole is ambiguous, and its genetic distance from E. talpinus s. str. falls into the range characteristic for closely related vole species or semi-species. According to molecular estimates, the two taxa have been isolated since the late Middle Pleistocene. A similar divergence is observed between the East and West Central Asian lineages of E. tancrei. E. alaicus is placed as sister to the latter rendering E. tancrei sensu lato paraphyletic. The revealed phylogeographic pattern implies that East Central Asia was colonized by mole voles through multiple eastward dispersal events.     

Male siblings inhibit reproductive activity in female pine voles, Microtus pinetorum

Pine vole females paired in breeding cages with male siblings remain unreproductive beyond the age of puberty onset. In this study only 10% of females caged with their brothers reproduced, whereas 85% of females placed with strange males had litters. Mating between a female and a strange male was also suppressed by the presence of a male sibling sequestered behind a wire mesh barrier in the breeding cage. When the sibling male was removed from the cage after 1 day, 78% of the females produced litters. When the sibling remained behind the barrier in the breeding cage, only 42% gave birth to young conceived in his presence. Conception of second litters during the postpartum estrus occurred in over 80% of females caged with strange males alone and only 10% of females caged with sibling males. Female pine voles are induced to become reproductively active by strange males but this activity is depressed by the presence of a brother, and once initiated it does not continue if the female is caged with her brother.     

Systematic relationships within the Microtus arvalis (Rodentia: Cricetidae) group in Iran,inferred from cytogenetic analyses

The distribution of C-heterochromatin and nucleolar organizer regions (NORs) was studied in three species of voles of the Microtus arvalis group in Iran: M. mystacinus, M. kermanensis, and M. transcaspicus. The C-banding pattern and NORs distribution were similar in M. mystacinus and M. kermanensis suggesting taxonomic proximity of these two species. At the same time, the karyotypes of M. mystacinus from Iran were different in C-banding pattern from the complements of conspecific 54-chromosome voles from Europe and other regions of Asia. The most distinct difference was in size of the distal C-positive block of heterochromatin on the X chromosome. In this respect M. mystacinus from Iran and M. kermanensis resembled M. transcaspicus. Small size of the distal C-positive heterochromatic block may be ancestral whereas larger size is derived. The X chromosome of M. transcaspicus can be derived from that of M. mystacinus and M. kermanensis by a large inversion or centromeric shift.     

Ecophenotypic variation and phylogenetic inheritance in first lower molar shape of extant Italian populations of Microtus (Terricola) savii (Rodentia)

Seventeen extant populations of Microtus (Terricola) savii have been investigated for correlations of first lower molar shape to climatic variables by means of geometric morphometrics, and controlling for phylogenetic inheritance. Comparative methods revealed that climatic variables and phylogeography provide a very similar contribution to variation in first lower molars morphology, whereas tooth size does not appear to be affected by climatic conditions. Climate‐related changes have been recognized in the anteroconid portion of the tooth. This indicates that molar tooth variation is strongly influenced by climatic conditions, although in a complex way. Calabrian populations, often ascribed to Microtus (Terricola) brachycercus, form a distinct cluster, in agreement with the most recent genetic analyses. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 632–647.     

Following the rivers: historical reconstruction of California voles Microtus californicus (Rodentia: Cricetidae) in the deserts of eastern California

The California vole, Microtus californicus, restricted to habitat patches where water is available nearly year‐round, is a remnant of the mesic history of the southern Great Basin and Mojave deserts of eastern California. The history of voles in this region is a model for species‐edge population dynamics through periods of climatic change. We sampled voles from the eastern deserts of California and examined variation in the mitochondrial cytb gene, three nuclear intron regions, and across 12 nuclear microsatellite markers. Samples are allocated to two mitochondrial clades: one associated with southern California and the other with central and northern California. The limited mtDNA structure largely recovers the geographical distribution, replicated by both nuclear introns and microsatellites. The most remote population, Microtus californicus scirpensis at Tecopa near Death Valley, was the most distinct. This population shares microsatellite alleles with both mtDNA clades, and both its northern clade nuclear introns and southern clade mtDNA sequences support a hybrid origin for this endangered population. The overall patterns support two major invasions into the desert through an ancient system of riparian corridors along streams and lake margins during the latter part of the Pleistocene followed by local in situ divergence subsequent to late Pleistocene and Holocene drying events. Changes in current water resource use could easily remove California voles from parts of the desert landscape.     

Puberty in pine voles, Microtus pinetorum, and the influence of chemosignals on female reproduction

We investigated the reproductive biology of an induced ovulator, the pine vole (Microtus pinetorum). Male puberty, measured as age at first impregnation, was found to occur as early as 44 days of age. Female puberty measured as age at first conception, was found to occur as early as 32 days of age, considerably earlier than previously reported. Females paired with stud males exhibited a doubling of uterine weight within 12 h, and vaginal sperm were present after 48 h. This indicates that although behavioral responses to males--including mating--require prolonged contact, physiological responses to males occur rapidly. Chemosignals from males slightly increased uterine and ovarian weights of females, but chemosignals from other females did not. Young females paired with stud males for 48 h in the presence of soiled bedding from the female's family had significantly smaller increases in ovarian and uterine weights than similar females paired on clean bedding. Suppression of reproduction in female offspring while they remain with the extended family unit is discussed as a life-history tactic and as a possible mechanism for inbreeding avoidance.     

Karyology of the Savi pine vole, Microtus savii (De Sélys-Longchamps, 1838) (Rodentia, Arvicolidae): G-, C-, DA/DAPI-, and AluI-bands.

Specimens of the Savi pine vole (Microtus savii) were collected from three localities in central (Pisa and Viterbo) and southern Italy (Rosarno, Calabria) and were karyotyped using G-, C-, DA/DAPI-, and AluI-banding. All karyotypes had 2n = 54 chromosomes and seemingly identical autosomal banding. The sex chromosomes of the southern Italian specimens, M. savii brachycercus, showed additional large blocks of heterochromatin. In the northern specimens, M. savii savii, the X chromosome is metacentric, whereas in the southern specimens of M. savii brachycercus the X chromosome is a much larger submetacentric chromosome, and the Y chromosome is more than twice the size of the Y in the northern specimens. DA/DAPI staining reveals three levels of fluorescent intensity in the sex chromosomes of the Calabrian specimens. The sex chromosomes of M. savii brachycercus also have the only AluI bands seen in either chromosome set. These data suggest a heterogeneous origin and composition of the C-band regions of these chromosomes. Preliminary data suggest that fertility is reduced in crosses between the two karyomorphs.     

Helping by juvenile pine voles (Microtus pinetorum), growth and survival of younger siblings, and the evolution of pine vole sociality

We quantified the behavior of juvenile pine voles (Microtuspinetorum) in families maintained in outdoor enclosures protectedfrom rain and predators and determined the effects of numberof juveniles present (0–3) on their younger siblings andtheir parents. Juveniles exhibited behaviors characteristicof helpers in cooperative breeding species: brooding, grooming,and retrieving younger siblings, and maintaining nests, runways,and food caches. The number of juveniles had no effect on weights,growth rates, or survival of younger siblings or on survivalof parents, but families with three juveniles had shorter interlitterintervals than other families. There was a trend toward lowerweights for younger siblings when juveniles continued to nursefrom their mothers. Juveniles brooded and groomed younger siblingsmore when their mothers were absent than when mothers were present.In families with juveniles, younger siblings were alone significandyless often than in families without juveniles, but number ofjuveniles in the family had little effect on duration or frequencywith which juveniles brooded or groomed younger siblings. Thesedata are consistent with cooperative breeding having evolvedvia individual selection for delayed dispersal. We argue thatthe limited availability of vacant tunnel systems and the highcost of digging new tunnel systems constrains dispersal in pinevoles and has led to the evolution of cooperative breeding.     

Climatic niche conservatism and ecological opportunity in the explosive radiation of arvicoline rodents (Arvicolinae,Cricetidae)

Climatic niche conservatism shapes patterns of diversity in many taxonomic groups, while ecological opportunity (EO) can trigger rapid speciation that is less constrained by the amount of time a lineage has occupied a given habitat. These two processes are well studied, but limited research has considered their joint and relative roles in shaping diversity patterns. We characterized climatic and biogeographic variables for 102 species of arvicoline rodents (Arvicolinae, Cricetidae), testing the effects of climatic niche conservatism and EO on arvicoline diversification as lineages transitioned between biogeographic regions. We found that the amount of time a lineage has occupied a precipitation niche is positively correlated with diversity along a precipitation gradient, suggesting climatic niche conservatism. In contrast, shift in diversification rate explained diversity patterns along a temperature gradient. Our results suggest that an indirect relationship exists between temperature and diversification that is associated with EO as arvicoline rodents colonized warm Palearctic environments. Climatic niche conservatism alone did not fully explain diversity patterns under density‐dependence, highlighting the additional importance of EO‐related processes in promoting the explosive radiation in arvicoline rodents and shaping diversity pattern among biogeographic regions and along climatic gradients.     

Integrative taxonomy, systematics and distribution of the genus Eligmodontia (Rodentia, Cricetidae, Sigmodontinae) in the temperate Monte Desert of Argentina

The systematics and distribution of South American sigmodontine rodents a matter of continuous revision and debate. The silky mice, genus Eligmodontia Cuvier, 1837, are among the most specialized murid rodents endemic to South America and its diversification for desert existence is associated with the uplift of the Andes and the early development of arid landscapes. Aiming to clarify the systematics of the species of silky mice occurring in the driest portion of the temperate Monte Desert in Argentina, qualitative and quantitative external and cranial characters, cytogenetics and molecular relationships, were studied. We characterized three karyotypes of Eligmodontia; two of which are described for the first time, and allocated them to previously named species. E. moreni Thomas, 1896 (2n=52 and FN=50), E. typus Cuvier, 1837 (2n=44 and FN=44) and E. marica Thomas, 1918. The later shows the same diploid number of E. typus, but its X—chromosome is not METACENTRIC but ACROCENTRIC . A discriminant analysis of external and cranial data separates E. moreni from E. typus and E. marica. Whereas these last ones show some degree of overlap. The morphological and chromosomal differentiation of Eligmodontia is sustained by DNA distances. Phylogenetic analyses show two major clades. One formed by E. moreni, E. puerulus and E. hirtipes, sharing a high FN and a northern distribution, and THE other formed by E. typus, E. marica and E. morgani with low FN and a central-southern distribution. Two centers of diversification are proposed to explain the evolution of Eligmodontia.     

Heterochromatin study and geographical distribution of Microtus species (Rodentia,Arvicolinae) from Greece

In a sample of 108 underground voles from 23 Greek localities, the species Microtus felteni, M. guentheri, M. rossiaemeridionalis and M. subterraneus were identified, based on external body morphology and karyotype. Moreover, the implemented C-banding staining technique revealed the heterochromatin distribution in the chromosomes of the above species. All M. guentheri (2n=54, FN=54) and M. rossiaemeridionalis (2n=54, FN=56) specimens displayed the typical karyotypes of these species, respectively. The M. subterraneus specimens belonged to the chromosomal race with 2n=52, FN=60 of this species, apart from a single individual that demonstrated a medium-sized, subtelocentric autosome in heterozygous condition (2n=52, FN=61). Furthermore, M. felteni individuals, trapped again after many years, were karyologically studied (2n=54, FN=56) and the C-banding pattern for this species is hereby presented for the first time. Finally, the study of meiotic preparations in M. guentheri and M. rossiaemeridionalis males verified the asynaptic behaviour of their sex chromosomes. The karyotype of the four studied Microtus species does not seem to have diversified much from the putative ancestral arvicoline karyotype (2n=56, FN=56). On the other hand, the heterochromatin accumulation in the sex chromosomes, particularly prominent in M. felteni and M. rossiaemeridionalis, represents this common tendency in several Microtus species.