Voles and Lemmings

Family Muridae (Arvicolinae)

Mammalian Hybrids

Arvicolinae
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EUGENE M. MCCARTHY, PHD GENETICS

     
European Water Vole
European Water Vole
(Arvicola terrestris)

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Alticola barakshin [Gobi Altai Mountain Vole]
× Alticola semicanus (♂) [Mongolian Silver Vole] CHR. CON: southern Siberia, Mongolia. Stubbe et al. (1994) reported three hybrid embryos.

Alticola macrotis [Large-eared Mountain Vole]
× Alticola roylei [Royle’s Mountain Vole] CHR. DRS? Bolshakov et al. 1982a.

Alticola roylei [Royle’s Mountain Vole] (= vinogradovi) See: Alticola macrotis.

Alticola semicanus [Mongolian Silver Vole] See: Alticola barakshin.

Arvicola terrestris [European Water Vole]
× Mesocricetus auratus (♀) [Golden Hamster] Mating was observed in captivity, but no hybrids were reported. M. auratus is usually assigned to the subfamily Cricetinae (hamsters) of family Muridae. Petzsch 1953, 1956.

Note: Myodes and Evotomys are a synonyms of Clethrionomys.

Clethrionomys centralis [Tien Shan Red-backed Vole]
× Clethrionomys glareolus (↔) [Bank Vole] CHR. CON: central Asia. HPF(♀♀). Zimmermann says that in hybrids the reddish brown of C. glareolus is dominant over the reddish gray of C. centralis, but various morphometric traits are intermediate. Ognev (p. 62) says the Asia Minor Bank Vole (C. g. ponticus) is morphologically intermediate in several respects, but not geographically intermediate, between C. centralis and C. glareolus. Kral et al. 1972 (p. 58); Ognev 1964; Orlov 1968; Rauschert 1963; Zimmermann 1965.
× Clethrionomys rutilus [Ruddy Vole] CHR. CON: eastern central Asia. Kral et al. 1972 (p. 58); Orlov 1968.

Clethrionomys gapperi [Southern Red-backed Vole]
× Clethrionomys glareolus (↔) [Bank Vole] CHR. DRS. HPF. Grant 1974.
× Clethrionomys rutilus [Ruddy Vole] ENHR. To analyze hybridization between these two voles, Runck et al. (2009) used variation in skeletal features and both mitochondrial and nuclear loci of individuals sampled from an approximately 550-km-long transect extending across the zone of contact (hybrid zone). The transect extended along the northern Pacific coast of North America. Identification of M. rutilus and M. gapperi based on the degree of closure of the post-palatal bridge was concordant with the distribution of diagnostic nuclear MYH6 alleles; however, an 80-km-wide hybrid zone was identified where such concordance was lacking. The hybrid form is characterized by having mitochondrial haplotypes closely related to the northern M. rutilus on a nuclear background and morphological characteristics of southern M. gapperi. Pure populations of M. rutilus are now isolated to the north of the hybrid zone, and pure M. gapperi by the LeConte Glacier. As they did not find pure M. rutilus or M. gapperi individuals within the hybrid zone, Runck et al. concluded that the hybrid population is self-sustaining and does not require continued hybridization between the pure parental forms for it's maintenance.

Note: Various island populations alstoni (Mull, Inner Hebrides), caesariaus (Jersey, Channel Islands); erica (Raasay, Inner Hebrides), skomerensis (Skomer, Wales), are now treated as races of Clethrionomys glareolus, but were treated as separate species until they were found to hybridize with mainland glareolus under captive conditions. Crowcroft and Godfrey 1960; Godfrey 1957, 1958; Grant 1974 (p. 245); Steven 1953, 1955.

Clethrionomys glareolus [Bank Vole]
See also: Clethrionomys centralis, C. gapperi.
× Clethrionomys rutilus (↔) [Ruddy Vole] CAENHR(n Scandinavia). HPF(♀♀). In regions adjacent to the range of C. rutilus voles that are phenotypically C. glareolus have C. rutilus mtDNA. In captive crosses Zimmermann found litter size and birth weight were slightly higher than in either parental type. Backcross hybrids of both sexes are partially fertile. Boratynski et al. 2011; Rauschert 1963; Spannhof 1959; Tegelström 1987; Tegelström et al. 1988; Zimmermann 1965.

Clethrionomys rutilus [Ruddy Vole] See: Clethrionomys centralis; C. glareolus.

Note: The various types of collared lemmings (genus Dicrostonyx) resemble each other morphologically, but vary greatly in karyotype. Their morphological similarity has led to lumping, their karyotypic variability, to splitting.

Dicrostonyx exsul [St. Lawrence Island Collared Lemming]
× Dicrostonyx groenlandicus [Northern Collared Lemming] CHR. DRS. HPF. Though these taxa have often been treated separately, Jarrell and Fredga (1993, p. 55) say they should be lumped because Rausch and Rausch (1972) found that they produced partially fertile hybrids in captivity. Duff and Lawson (2004) lump these taxa.
× Dicrostonyx nelsoni [Nelson’s Collared Lemming] CHR. DRS. HPF. These taxa were lumped by Duff and Lawson (2000). Rausch and Rausch 1972 (p. 381).
× Dicrostonyx torquatus [Arctic Collared Lemming] CHR. DRS. HPF. Rausch and Rausch 1972.
× Dicrostonyx unalascensis [Unalaskan Collared Lemming] CHR. DRS. These taxa were lumped by Duff and Lawson (2000). Rausch and Rausch 1972 (p. 375).

Note: Two populations (nelsoni, rubricatus), treated as races of Dicrostonyxgroenlandicus, differ in karyotype. Their hybrids have meiotic abnormalities (e.g., chromosome rings) and produce both gametes and progeny at reduced rates. Jarrell and Fredga 1993 (p. 54).

Dicrostonyx groenlandicus [Northern Collared Lemming]
See also: Dicrostonyx exsul.
× Dicrostonyx richardsoni [Richardson’s Collared Lemming] CAENHR(n Canada). Hybridization occurs in the region south of the Melville Peninsula and on Southampton Island. Scott and Fisher (1983) claimed that these hybrids are sterile when no progeny were obtained after carrying out 15 inter se matings and one backcross mating (sex of hybrid unspecified). Although their sample size is small, this finding suggests at least one sex is sterile (which by Haldane’s Rule would be the male). However, the matings that they report do not exclude the possibility that females may be partially fertile. Anderson 1946; Anderson and Rand 1945 (citing Degerbøl and Freuchen); Degerbøl and Freuchen 1935.
× Dicrostonyx torquatus [Arctic Collared Lemming] CHR. DRS. Rausch and Rausch reported hybridization of groenlandicus with rubricatus (which has been treated as a separate species, but was lumped with groenlandicus by Duff and Lawson 2004). Rausch and Rausch 1972 (p. 378).

Dicrostonyx nelsoni [Nelson’s Collared Lemming]
See also: Dicrostonyx exsul.
× Dicrostonyx rubricatus [Bering Collared Lemming] CHR. CON: northwestern Alaska? HPF(♂&♀). Since male hybrids are known to be partially fertile, it is here presumed that females are also partially fertile. The chromosomes of these lemmings differ with respect to several structural rearrangements which form ring structures during meiosis in the hybrids. Though they have often been treated separately, these taxa were lumped by Duff and Lawson (2004). Jarrell and Fredga 1993 (p. 52).

Dicrostonyx richardsoni [Richardson’s Collared Lemming]
See also: Dicrostonyx groenlandicus.
× Dicrostonyx torquatus [Arctic Collared Lemming] CHR. DRS. HPF. Rausch and Rausch 1972.

Dicrostonyx rubricatus [Bering Collared Lemming]
See also: Dicrostonyx nelsoni.
× Dicrostonyx unalascensis [Unalaskan Collared Lemming] CHR. DRS. These taxa were lumped by Duff and Lawson (2000). Rausch and Rausch 1972 (p. 380).

Dicrostonyx torquatus [Arctic Collared Lemming]
See also: Dicrostonyx exsul; D. groenlandicus; D. richardsoni.
× Dicrostonyx vinogradovi [Wrangel Collared Lemming] CHR. DRS. HPF(♀♀). These lemmings are morphologically similar, but their karyotypes differ by at least by 13 chromosomal rearrangements (fusions, fissions and inversions). Male F₁ spermatogenesis is arrested in early meiosis. In female F₁ hybrids, ovaries have fewer follicles, more atretic follicles, and accelerated folliculogenesis compared to parental types. Because of this acceleration, F₁ female show no reduction in mature follicles and ovulations. There is, however, an increase in prenatal losses in F₂ hybrids. Chernayavskij and Kozlovskij 1980; Gileva et al. 1994.

Dicrostonyx unalascensis [Unalaskan Collared Lemming] See: Dicrostonyx exsul; D. rubricatus.

Dicrostonyx vinogradovi [Wrangel Collared Lemming] See: Dicrostonyx torquatus.

Ellobius tancrei [Zaisan Mole-Vole] Captive hybridization of chromosomal races of E. tancrei (34-chromosome race × 54-chromosome race, and 36-chromosome race × 54-chromosome race) produced offspring at reduced rates and the hybrids themselves had reduced fertility. Bakloushinskaya and Lyapunova 2003; Kolomiets et al. 1985; Lyapunova and Yakimenko 1986; Lyapunova et al. 1990.

Note: A population in the northern Chukotka Peninsula, chrysogaster, was treated as a race of Lemmus sibiricus. However, chrysogaster’s karyotype differs from that of L. sibiricus and is identical to that of L. trimucronatus. For this reason Pokrovski et al. say chrysogaster and L. trimucronatus should be treated as conspecific. Nowak (1999, vol. 2, p. 1481) includes chrysogaster in L. trimucronatus. Hence, crosses listed here involving the taxon L. trimucronatus refer to reports of hybridization involving chrysogaster. Jarrell and Fredga 1993 (p. 49); Pokrovski et al. 1984.

Lemmus amurensis [Amur Lemming]
× Lemmus lemmus [Norway Lemming] CHR. DRS. HPF(♂&♀). Pokrovski et al. 1984 (p. 909).
× Lemmus sibiricus(↔) [Siberian Lemming] CHR. CON: northeastern Russia? HPF(♂&♀). Pokrovski et al. 1984 (p. 909).
× Lemmus trimucronatus (↔) [Brown Lemming] CHR. CON: northeastern Russia? HPF(♀♀). Pokrovski et al. 1984 (p. 909).

Lemmus lemmus [Norway Lemming]
See also: Lemmus amurensis.
× Lemmus sibiricus(↔) [Siberian Lemming] CHR. CON: northwestern Eurasia. HPF(♂&♀). Pokrovski et al. 1984.
× Lemmus trimucronatus (↔) [Brown Lemming] CHR. DRS. HPF(♀♀). Jarrell and Fredga 1993 (p. 49); Pokrovski et al. 1984.

Lemmus sibiricus [Siberian Lemming]
See also: Lemmus amurensis; L. lemmus.
× Lemmus trimucronatus [Brown Lemming] CHR. CON: e Russia (n Chukotka Peninsula). HPF(♀♀). Jarrell and Fredga 1993 (p. 49); Pokrovski et al. 1984.

Lemmus trimucronatus [Brown Lemming] See: Lemmus amurensis; L. lemmus; L. trimucronatus.

Note: Members of the genus Microtus show great variability in karyotype, but relatively little in morphology. Meylan 1972.

Microtus agrestis [Field Vole] M. agrestis includes a morphologically cryptic population in southwestern Europe that is genetically distinct the recognized type. Jaarola suggests that it should be treated as a separate species. Jaarola also mentions that another hybrid zone exists where a second genetically distinct population (“Lund”) comes into contact with ordinary M. agrestis in southern Sweden (Skåne and Blekinge). Internet Citations: JAAR.

Microtus arvalis [Common Vole]
× Microtus kirgisorum (↔) [Tien Shan Vole] CHR. DRS? LFH. Meier et al. (1981, p. 300) say this cross is “characterized by a low intensity of reproduction, absence of heterosis in hybrids and arrest of oogenesis [in hybrids] at an early stage.” Zakian et al. 1987, 1991.
× Microtus obscurus [Altai Vole] CHR. Parapatric contact zone (e Europe). HPF. Arvalis has 13 pairs of bi-armed chromosomes (metacentrics and submetacentrics) and 4 pairs of telocentrics; obscurus, 7 and 10 pairs respectively. Golenishchev et al. 2001; Mazurok et al. 2001; Mejer et al. 1972; Moska et al. 2004; Orlov and Malygin 1969; Zagorodnyuk 1991. Internet Citations: ZIN.
× Microtus orcadensis (♂) [Orkney Vole] CHR. HPF(♂&♀). DRS. Orkney voles are about twice as big as common voles. If caged together the two usually will not mate for several days. During this time the arvalis individual is often killed by the larger Orkney. Hybrids tails are long, as in orcadensis. Although formerly treated as a separate species, orcadensis is now usually treated as a race M. arvalis. Duff and Lawson (2004) do not treat them separately. In crosses between orcadensis and another vole, sarnius, formerly treated separately (Guernsey Vole), but now also lumped under M. arvalis, Crowcroft and Godfrey note that the long tail of sarnius was dominant over the short one of orcadensis. Zimmerman (p. 11) says that “the large vole of Orkney [i.e. orcadensis] differs very much from the small forms of central Europe in morphological and histological characters, but the complete fertility of the hybrids shows that it belongs to the species Microtus arvalis.” He also notes that adult hybrids are nearly as large as M. orcadensis, but intermediate in birth weight and litter size. Crowcroft and Godfrey 1962; Zimmerman 1959/60.
× Microtus rossiaemeridionalis (↔) [Sibling Vole] CAONHR(e Europe). HPF(♀♀). In hybrids spermatogenesis is blocked at the stage of primary spermatocytes. Ovulation, too, occurs at greatly reduced rates. However, according to Gileva et al. (2001, p. 568) “in very rare cases, the production and maturation of genetically balanced eggs and emergence of progeny as a result of backcrosses may occur in the hybrid females.“ Natural hybrids occur in the Urals. Gileva et al. 2000, 2001; Malygin and Sokolov 1983; Meier 1994; Meier et al. 1996; Rubtsov et al. 2002; Zakian et al. 1987, 1991; Zybina and Skholl 1972.
× Microtus transcaspicus (♀) [Transcaspian Vole] CHR. DRS? Meier et al. 1981; Zakian et al. 1991.

Microtus breweri [Beach Vole]
× Microtus pennsylvanicus [Meadow Vole] CHR. DRS. Wetherbee et al. 1972.

Note: Two populations (californicus, stephensi) are treated as races of Microtus californicus. Gill (1980) found that female hybrids between these types are about as fertile as pure type females, but that male hybrids are either sterile or of very low fertility. No sperm was formed and the testicular material was highly abnormal.

Microtus californicus [California Vole]
× Microtus montanus (♂) [Montane Vole] CHR. CON: western U.S. (California, Oregon). F₁ hybrid has sharp nose and small eyes of montanus, but its tail resembles californicus (dark above, light beneath). Hatfield 1935.

Microtus carruthersi [Carruther’s Vole]
× Microtus juldaschi (↔) [Juniper Vole] CAENHR(Turkestan). HPF(♂&♀). Due to hybridization, these taxa are sometimes lumped. Bolshakov 1969; Bolshakov et al. 1982b.

Microtus daghestanicus [Daghestan Pine Vole]
× Microtus majori [Major’s Pine Vole] ENHR. HPF. CON: Caucasus Mountains. Malygin et al. 2000.

Microtus duodecimcostatus [Mediterranean Pine Vole]
× Microtus multiplex (♂) [Alpine Pine Vole] CON: France? Meylan (1972) obtained a hybrid embryo.
× Microtus subterraneus (♂) [Common Pine Vole] CON: France? Meylan (1972) observed fertilization in this cross, but no hybrid embryos.

Microtus guentheri [Gunther’s Vole] (2n = 54)
× Microtus paradoxus [Paradox Vole] CHR. LFH. DRS. Golenishchev et al. 2002.
× Microtus qasvinensis [Qasvin Vole] CHR. Groves 2005 (p. 1014).
× Microtus schidlovskii [Schidlovsky’s Vole] CHR. LFH. DRS. Golenishchev et al. 2002.
× Microtus socialis [Social Vole] CHR. LFH. CON: Israel, Syria, Turkey. In hybrids between M. guentheri and M. s. binominatus (Talysh Mountains, Azerbaijan), which are heterozygous with respect to several chromosomal rearrangements, meiosis was disrupted; most cells contained 3-4 trivalents with lengthy regions of asynapsis; univalents and nonhomologous pairing were observed quite often in the hybrids. The sex chromosomes were not always completely paired. Golenishchev et al. 2002. Internet Citations: ZIN.

Microtus juldaschi [Juniper Vole] See: Microtus carruthersi.

Microtus kermanensis [Baluchistan Vole]
× Microtus rossiaemeridionalis [Sibling Vole] CHR. CON: southwestern Asia. HPF(♀♀). These voles differ in morphology, but have identical chromosome counts (2n = 54). Internet Citations: ZIN.

Microtus kirgisorum [Tien Shan Vole]
See also: Microtus arvalis.
× Microtus rossiaemeridionalis (♀) [Sibling Vole] CHR. DRS. Zakian et al. 1991.
× Microtus transcaspicus (♂) [Transcaspian Vole] NHR. Hybrids from Turkmenistan have been reported. Meier et al. 1981; Meyer 1980; Zakian et al. 1991.

Microtus levis [East European Vole]
× Microtus transcaspicus (♀) [Transcaspian Vole] CHR. DRS. Meyer et al. 1996.

Microtus majori [Major’s Pine Vole] See: Microtus daghestanicus.

Microtus mexicanus [Mexican Vole] Two populations (mongolensis, navaho), treated as races of this vole, have a narrow hybridize zone in central Arizona (Bradshaw Mountains. and south of Prescott). Hoffmeister 1986 (Map 5.98 and p. 443).

Microtus montanus [Montane Vole] See: Microtus californicus.

Microtus multiplex [Alpine Pine Vole]
See also: Microtus duodecimcostatus.
× Microtus subterraneus (↔) [Common Pine Vole] CHR. CON: southern Europe. HPF. Meylan (1972 produced many hybrids from this cross.

Microtus obscurus [Altai Vole] See: Microtus arvalis.

Microtus orcadensis [Orkney Vole] See: Microtus arvalis.

Microtus paradoxus [Paradox Vole] (2n = 62)
See also: Microtus guentheri.
× Microtus schidlovskii [Schidlovsky’s Vole] CHR. HPF(♀♀). DRS. Golenishchev et al. 2002.
× Microtus socialis [Social Vole] CHR. HPF. CON: northwestern Iran. HPF(♂&♀). Golenishchev et al. (2002) report that the karyotypes of these two voles are identical and that hybrids are easily obtained and develop normally.

Microtus pennsylvanicus [Meadow Vole] See: Microtus breweri. A vole occurring on Block Island (Rhode Island, U.S.) formerly treated as a separate species, M. provectus (Block Island Meadow Mouse) was lumped under pennsylvanicus by Chamberlain (1954). And yet, Wheeler (1952), who obtained hybrids between a pennsylvanicus maleand a provectus female, could not obtain the reciprocal cross.

Microtus qasvinensis [Qasvin Vole] See: Microtus guentheri.

Microtus rossiaemeridionalis [Sibling Vole] (=epiroticus, subarvalis]
See also: Microtus arvalis; M. kermanensis; M. kirgisorum.
× Microtus transcaspicus (↔) [Transcaspian Vole] CHR. HPF(♀♀). DRS. Meier et al. (1981, p. 300) say this cross is characterized by a high intensity of reproduction, heterosis, and low levels of abnormalities in hybrid oogenesis. Zakian et al. 1991.

Microtus savii [Savi’s Pine Vole] Two karyopopulations, brachycercus and savii, usually treated as races of this vole, hybridize in Italy. The brachycercus’sX and Y chromosomes are large, savii’s, of normal size. Galleni,Tellini et al. (1998) say spermatogenesis is impaired in hybrids. Galleni 1995; Galleni, Stanyon et al. 1998; Galleni, Tellini et al. 1994, 1998.

Microtus schidlovskii [Schidlovsky’s Vole] (2n = 60)
See also: Microtus guentheri, M. paradoxus.
× Microtus socialis (♂) [Social Vole] CHR. CON: Georgia, Armenia. HPF(♀♀). The only obvious difference between the karyotypes of these two voles is that the first (largest) autosome in M.schidlovskii is homologous to two separate chomosomes in M. socialis. Golenishchev et al. 2002.

Microtus socialis [Social Vole] See: Microtus guentheri, M. paradoxus; M. schidlovskii. In Azerbaijan, hybrids occur between two populations (aristovi, zaitsevi) treated as races of this vole. Golenishchev et al. 2002.

Microtus subterraneus [Common Pine Vole] See: Microtus duodecimcostatus; M. multiplex.

Microtus transcaspicus [Transcaspian Vole] See: Microtus arvalis; M. kirgisorum; M. lavis; M. rossiaemeridionalis.

Note: In addition to voles and lemmings, the muskrat (Ondatra zibethicus), too, is usually assigned to subfamily Arvicolinae.

Ondatra zibethicus [Muskrat] × Felis catus (♀) [Domestic Cat] George Lyman Kittredge (1916 p. 37) writes that in 1716 the New England Puritan minister and author Cotton Mather (1663-1728) reported to the Royal Society that a cat in Roxbury, Massachusetts had bred with a muskrat and brought forth a numerous litter of kittens, all of which were of a mixed form, some more resembling muskrat, others, cat. In the same article (p. 18), Kittredge states that “No historical student would think of denying that Cotton Mather was one of the best informed Americans of his time in scientific matters.” Kittredge (1860-1941) was a celebrated professor and scholar of English literature at Harvard University.

Phenacomys intermedius [Western Heather Vole]
× Phenacomys ungava [Eastern Heather Vole] ENHI. HPF(vh). Parapatric contact in British Columbia. Crowe et al. 1943; McAllister and Hoffmann 1988.

Phenacomys ungava [Eastern Heather Vole] See: Phenacomys intermedius.

Phaulomys andersoni [Japanese Red-backed Vole]
× Phaulomys smithii [Smith’s Vole] ENHR(Japan). HPF(♀♀). CON: southwestern Honshu (Kii Peninsula), central Honshu. ACZ (andersoni occurs above smithii). Iwasa and Suzuki 2003.

Phaulomys smithii [Smith’s Vole] See: Phaulomys andersoni.

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By the same author: Handbook of Avian Hybrids of the World, Oxford University Press (2006).


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