Turkish Journal of Zoology Turk J Zool (2016) 40: 831-841 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Review Article doi:10.3906/zoo-1509-53

Review of unique odd chromosome-numbered underground rodent species of the Palearctic region: Ellobius lutescens Thomas 1897 (Rodentia: Cricetidae)

Yüksel COŞKUN* Department of Biology, Faculty of Science, Dicle University, Diyarbakır, Turkey

Received: 29.09.2015 Accepted/Published Online: 24.12.2015 Final Version: 06.12.2016

Abstract: A review of the species within the genus Ellobius from Turkey is provided. The Transcaucasian mole vole, Ellobius lutescens, is the westernmost representative of the genus and among the most enigmatic and yet most neglected of the Palearctic placental mammals. Currently, its distribution is thought to be restricted to eastern Anatolia. The Transcaucasian mole voles inhabit a wide variety of habitats across this distribution area in semiarid or grassland territories and high-elevation cultivated fields. The species’ distribution, feeding ecology, population structure, behavior, reproduction, genetics, and fossil records are reviewed here for Turkey. This paper brings together information published during the last century in books and scientific papers. Future research needs to include collation of further data on population dynamics, maximum length of the breeding season, reliable abundance estimates, and studies of distribution and migration. Other areas worthy of investigation are the identification of wintering areas, acquisition of up-to- date data on reproduction and mortality, and investigations into the consequences of environmental changes for the species.

Key words: Mammalia, Rodentia, Cricetidae, Arvicolinae, Ellobius lutescens, review, Turkey

1. Introduction ridges are closely approximated throughout, tending to The genusEllobius Fischer, 1814 belongs to the family fuse or in old age fusing to form a sagittal crest extending Cricetidae and is characterized by exclusively subterranean from the interorbital region backwards to the occiput. habitation. It is highly specialized for fossorial habits; the fur The outer wall of the infraorbital foramen is absent, and is very fine, short, dense, and mole-like; the eyes are small; the foramen is more rounded than in allied genera. The the ears are reduced to a mere fold of naked integument rostrum in a ventral view is long and slender; the anterior surrounding the external meatus and completely hidden palatal foramina are very small. The auditory bullae are in the fur. External ear conches are undeveloped (Ognev, very small and but slightly inflated. The mandible has lofty 1963; Harrison, 1972). The fore and hind feet are of recurved coronoid processes, and the angular processes moderate size, armed with very small claws, and with are reduced in each ramus to a mere ridge bordering naked soles; there are five palmar and six plantar pads as the alveolar sheath to the lower incisor as it ascends the usual, the plantar pads being all moderately developed condylar process (Hinton, 1926; Ellerman, 1948). or small. The lateral borders of the fore and hind feet are Upper and lower incisors are enormously enlarged and fringed with stiff hairs, those on the outer margins being thrown forwards; lower incisors form a prominent knob especially well developed. The tail is very short, rounded terminally, and fully clothed with stiff hairs, which form on the outer side of the mandible. Cheek-teeth are rooted a long thin terminal pencil, usually shorter than the hind in adults. The third upper and lower molars are reduced foot (Hinton, 1926; Ellerman, 1941). in size. Enamel loops of molars not forming completely The skull shows extreme fossorial specialization, being closed triangles. The enamel is rather thin (Hinton, 1926; cuneate in profile, with straightened and far-protruding Ellerman, 1948; Vinogradov and Argiropulo, 1968). incisors, extremely shallow and slender rostrum, Based on morphological and karyological studies, the depressed anterior nares, flattened dorsal surface, and genus Ellobius comprises five species. Ellobius fuscocapillus, slightly inclined occiput. The zygomata are moderately E. lutescens, E. talpinus, E. tancrei, and E. alaicus exist at the stout and diverge posteriorly. The interorbital region is present time. As shown in Figure 1, these species exhibit short and wide, about as broad as a rostrum. The temporal allopatric distribution (Panteleyev, 1998).

* Correspondence: [email protected] 831 COŞKUN / Turk J Zool

Figure 1. Geographic distribution of genus Ellobius. Species are: 1- E. fuscocapillus, 2- E. lutescens, 3- E. talpinus, 4- E. tancrei, 5- E. alaicus. Map redrawn from Panteleyev (1998) with modifications.

2. Ellobius lutescens Thomas 1897 (Transcaucasian mole dark, ash-gray, or grayish brown. Sagittal crest of adults vole) not reaching the lambdoid region and branching anteriorly The Transcaucasian mole vole, Ellobius lutescens, was first to the lambdoid crest (Ellerman, 1948). Thomas (1897) described by Thomas in 1897, on the basis of specimens provided the following measurements: head and body 125 collected from Erçek near Van, eastern Anatolia (Thomas, mm; tail 14 mm; hind foot 22 mm. Skull: basal length 31 1897). Ellobius lutescens (Figure 2) has a lower diploid mm; basilar length 28 mm; greatest breadth 24 mm; palate chromosome number, 2n = 17. The following characters length from henselion 187 mm; diastema 12 mm; length of are gathered from several sources and at best are diagnostic upper molar series 7.2 mm. only when used in combination. Its dorsal side is rather Average and extreme figures from four skulls’ measurements are detailed below, including the type from Van, Turkey: occipitonasal 26.1–28.5 (27) mm, tooth-row 6.7–7.0 (6.9) mm, frontals 5.5–6.1 (5.8) mm. A specimen was also examined from Talysh, Transcaucasia. Average and extreme measurements of eight skins, including the type, from Van, Turkey and Kazvin, North Persia: head and body 102–132 (118) mm, tail 10–15 (11) mm, hind foot 20–25 (22) mm (Ellerman, 1948). 2.1. General characters Thomas (1897) described Ellobius lutescens as follows: “General colour dull slaty buff, quite different from the bright yellowish of the Eastern species, with which it agrees in tooth-structure, and more similar to dark examples of E. talpinus from the Volga. Head but little darker than body. Belly scarcely lighter than back, the Figure 2. Photograph of an adult Ellobius lutescens from Iğdır, line of demarcation quite gradual. Everywhere, above and Turkey. Photograph by Y Coşkun, collected on 24 April 2013.

832 COŞKUN / Turk J Zool below, the hairs are dark slaty grey with buffy tips. Skull 2.2. Distribution with a long slender muzzle [see (Figure 2)]. Nasals long Ellobius lutescens is a Palearctic species that is distributed and very narrow, much compressed for their posterior two in Iran, Iraq, Azerbaijan, Armenia, Transcaucasia, and East thirds. Zygomata boldly expanded, starting out anteriorly Anatolia (Thomas, 1905; Ellerman and Morrison-Scott, at a right angle to the general line of the skull. Lambdoid 1951; Darlington, 1957; Osborn, 1962; Walker, 1964; Lay, crest curving forwards mesially, not forming an angle in 1967; Hassinger, 1973; Roberts, 1977; Corbet, 1978; Corbet the middle line. Posterior plate much as in E. fuscocapillus, and Hill, 1991; Wilson and Reeder, 2005; Coşkun, 1997; but inner part of bullae rising much higher above the level Nowak, 1999) (Figure 1). The elevational distribution is of the basioccipital and basisphenoid than in that species.” from ca. 1500 to about 2800 m in East Anatolia including The pelage is short and soft. Beneath the fur is gray, Van, Hakkari, Ağrı, and Iğdır provinces (Figure 3) (Coşkun and tips are gray to pale brown. The summer pelage of E. and Ulutürk, 2001; Kaya and Coşkun, 2015). Live mole lutescens is considerably grayer than its buffy winter coat, voles allowed to wander freely frequently fell into holes, due seemingly to greater exposure of the slate-colored over drop-offs, and into streams, an indication that they basal parts of the hairs. This black-buff color relationship may have poor vision (Lay, 1967). is identical to that of topotypes from Van, Turkey, of E. 2.3. Skull morphology lutescens (FMNH 82162–3) and the Azerbaijan series (Lay, The skull is robust. Incisive foramina are small. Interparietal 1967). Demarcation is not clear. The ventral part of body is is absent. Zygomatic arches are widely separated and darker than the dorsal side. Eyes are small, pinnae absent, broadened in the middle. The sagittal crest of adults does and ear openings hidden in the fur. Its tail is short, and the not reach the occipital region and branches into two crests, tip is broader than the base. The fore and hind feet have which enclose a small triangular area (Figure 4a). five digits, weak nails, and naked soles, and the hind feet Dental formula is incisive 1/1, canine 0/0, premolar possess six tubercles (Coşkun, 2001). 0/0, molars 3/3, total 16 (Figure 4b). The incisor teeth Ranges (in mm) for cranial measurements of 7 are highly specialized; they are much lengthened and specimens are as follows: overall length of skull 28.2–29.8 straightened (Figure 4c), forming smaller segments of mm; basilar length 28.0–31.2; condylobasal length 30–31; much larger circles than usual; they are without grooves, interorbital width 6.0–6.3; zygomatic width 23.2–24.0; and as is very commonly the case in rodent incisors length of nasals 8.2–8.8; width of braincase 15.6–15.8; showing fossorial adaptation, their enamel is white and they tend to be rounded in transverse section. Pups have diastema 10.3–12.2; length of palatal foramina 3.0–3.1; incisors at birth; however, these incisors appear different length of upper molar tooth row 7.2–7.7; height of skull from the normal incisors of adults. These incisors were 11.2–12.2; length of body 101–108; hind foot 22.3–23.2 yellowish and bent sideways at the tips. They could be used (Ognev, 1963). to seize nipples that were too small (Kaya and Coşkun, For Turkey, averages and ranges of body dimensions 2015). The upper incisors extend much further backwards (in mm) of 16 specimens (Coşkun, 2001) from the Van in the maxillary bones than in any other Microtinae and Hakkari regions are: head and body length 121.4 (Hinton, 1926; Ognev, 1963; Roberts, 1977; Harrison and (106–130); tail length 10.0 (7–12); hind foot length 22.4 Bates, 1991). The angular processes are weak; condyloid (20–23) mm; weight (g) 70.4 (58–84); condylobasal length process is fused with the alveolar process. The coronoids 29.2 (27.1–32.2); zygomatic breadth 22.9 (21.3–24.7); skull are tall, finely pointed, and curved (Coşkun, 2001) (Figure height 11.5 (10.6–12.5); interorbital width 6.2 (5.3–6.6); 4d). nasal length 8.6 (7.4–10.3); incisive foramen length 1.76 The cheek-teeth are rooted and hypsodont. There is (1–2.2); upper molar row length 7.06 (6.4–7.6); upper no root in the molars of the young specimens but 2 roots diastema length 11.4 (10.3–12.5); mandible length 21.0 3 exist in adult ones. Both M (upper 3rd molars) and M3 (18.7–22.9); coronoid process height 11.8 (10.3–13.1). (lower 3rd molars) are reduced and smaller than the other Means and ranges (in parentheses) of selected external and molars. M1,2 have two inner and two outer reentrant folds, skull measurements (in mm) for 99 specimens (Gharkheloo 3 whereas M has two outer and one inner fold. M1 has three and Kıvanç, 2003) from Iran are: total length 125.7 (100– inner and outer folds, and M2,3 have two inner and two 140); tail 13.4 (9–19); hind foot 22.3 (17–26); weight (g) outer reentrant folds (Figure 5). There are no molar crest 62.0 (24.8–81.5); greatest length of skull 33.1 (28.8–35.6); pattern differences among the young and old specimens condylobasal length 28.3 (22–30.9); nasal length 8.8 (7.5– (Coşkun, 2001). The first and second upper molars have 3 10.2); upper tooth row 6.9 (6.2–8.8); diastema 11.4 (9.7– triangles in the lingual and labials (Figure 5). However, the 12.8); zygomatic breadth 22.4 (19.3–22.6); tympanic bulla reentrant among the first and the second triangles in the length 7.9 (7.2–8.9); incisive foramen length 2.4 (1.9–3). lingual is more superficial (Gharkheloo and Kıvanç, 2003).

833 COŞKUN / Turk J Zool

Lake Van

Figure 3. Distribution area of Ellobius lutescens in Turkey. *: Erçek is the type locality.

2.4. Reproduction Walker (1964) stated that E. lutescens can bear one Mole voles can live to be 1–6 years old and can reach to seven pups (usually three to five) twice a year. Five sexual maturity after the first wintering at the age of individuals were observed in a burrow; therefore, at least about 1 year. The dispersal of the young occurs mainly three pups live in a burrow system (Coşkun, 2000). This after the first wintering. Some animals disperse after the species is a poor breeder in captivity; only one pup was second wintering. The gestation period for mole voles is produced in March from a couple of E. lutescens kept in approximately 1 month (Evdokimov, 1997, 2002). a cage for more than 1 year. They bear one to three pups The Transcaucasian mole vole typically has 3 paired twice a year, in March–April and October–November mammae, two pairs pectoral and one pair inguinal. For (Coşkun, 1997, 2000; Coşkun and Ulutürk, 2001, 2003). this study, some E. lutescens pups were captured in May. 2.5. Behavior They can give birth in early May or late April. Females of The social behavior of the mole vole is strictly familial, and E. lutescens captured near Muradiye, Van, during October when the entire family is in the nest, the animals have to were pregnant. Four embryos were observed in the uterus settle themselves into several “tiers” (Evdokimov, 2002). of a female; they could give birth in autumn for a second Individuals of E. lutescens live as a family society, not in time. The uterus is short and wide with long narrow groups. Mole voles tolerate high densities in captivity, uterine horns (Coşkun and Ulutürk, 2001). The pups were although they do not exhibit ‘normal’ behavioral patterns; weaned on days 33–35. Postnatal development is shown individuals kept in the laboratory for more than 1 year did in Figure 6 (Kaya and Coşkun, 2015). The duration of not hibernate or aestivate. Cage-mates groom each other the pups to both suckle and feed on vegetables was about and sleep in contact with each other. Sleeping position 8–10 days (Kaya and Coşkun, 2015). Os penis extremely varies with the temperature; when the temperature of the minute, basally extremely expanded, terminally rounded laboratory increases, the animals lie on their backs and (Ognev, 1963). try to cool down by opening their fore and hind limbs

834 COŞKUN / Turk J Zool

Figure 4. Dorsal (a), ventral (b), and lateral (c) views of cranium and lateral view (d) of mandible of an adult male Ellobius lutescens (Dicle University, Faculty of Science, Department of Biology, Zoology Lab. Mammal collection number 741, from 20 km south of Iğdır, Turkey).

Figure 5. Chewing surface variations of upper (left) and lower (right) rows of permanent molars teeth of Ellobius lutescens. Ant. Anterior, Post. posterior, lab. labial, lin. lingual side. laterally. In cold conditions they huddle together in the mostly during morning and evening. They usually fed in nest. When another couple is put in the cage, these families the morning (Kaya and Coşkun, 2015). live together in peace, and all individuals guard the pups 2.6. Ecology (Coşkun and Ulutürk, 2001, 2003). They were active Mole voles are distributed in all soil types with the (feeding, digging, grooming) almost all day and night, but exception of moving sand. Generally, mole voles inhabit

835 COŞKUN / Turk J Zool

)

T me (day)

Figure 6. Mean mass and linear measurements of E. lutescens from birth to 98 days of age (ToL: total length, HFL: hind foot length, TL: tail length) (Kaya and Coşkun, 2015). open areas. The mole vole prepares its underground in emergencies descend to a depth of 54–90 cm from the tunnels by scratching the soil with its incisors and pushing surface at an angle of 45° (Coşkun, 2001). the loosened soil behind its body with its fore and hind This species makes its nest close to the surface, and limbs. It then turns and transports the excavated soil with there are many tunnels connected to it. There are soft the head, fore feet, and breast, so that the mounds occur materials (nylon, pieces of cloth, dry grass, etc.) and food on the surface. These mounds may be confused with those in the nest. The food is stored in expanded rooms near the of Talpa and Spalax. There are 22–35 mounds 5 m × 3.6 nest and there is no other food storage room. However, m in an area, which are usually established in or around the gallery systems of each family differ in terms of soil cultivated or grassy fields. The top and base diameter of structure and food; it is impossible to determine a typical these mounds are 8–21 cm and 24–50 cm, respectively. gallery system. The size of the home range of each family The height is 9–14 cm. The distance between mounds is about 12 m × 9 m. Its size changes with the amount of varies from 4 cm to 70 cm. Each burrow system contains a food. Each burrow system contains one male, one female, pair of mole voles (male and female with offsprings during and at least one pup. The population is estimated such that the breeding season). The diameter of the forage tunnels is there would be 24,000 individuals in an area of 1 km2 in more or less constant throughout each burrow system. The Turkey (Coşkun and Ulutürk, 2003). vertical and horizontal diameters of the tunnels are 5–8 The mole vole is a generalist and collects a variety of cm and 6–9 cm, respectively. The tunnel diameter is only food species. They eat all kinds of vegetation and feed slightly greater than the body diameter of the occupant primarily on large subterranean edible parts of plants (i.e. animal. The average depth of forage tunnels was 27 ± 5.8 corns, bulbs, tubers, rosettes), which they collect while cm (16–48 cm). The main tunnel system is connected to burrowing through the ground and hoard in their nests feeding tunnels. Feeding tunnels are dug only when there and mound stores. They often distinguish between food is a greater probability of finding food in the vicinity of types and store them in separate chambers of their nest the main tunnel. The depth of the mole vole’s feeding mound. Collections include bulbs of the genera Geranium, tunnels is probably determined primarily by the level of Bunium, and Allium. They do not drink water; rather, they underground parts of plants that serve as food materials obtain water from their food (Coşkun, 2001). Their food for the animals. The tunnels in which the animal shelters is composed of potatoes, carrots, beets, clover roots, and

836 COŞKUN / Turk J Zool onions near cultivated areas. In clover fields, they rend their area showed stability of the chromosome number clover roots at 10–12 cm below the surface. About 298 g of and morphology in both of these species (Lyapunova et stored food was removed from a burrow that included one al., 1980). According to Vorontsov and Lyapunova (1984), pup, one male, and one female. This species cuts the roots seismically active regions may bring about increased of plants while scratching tunnels in agricultural areas chromosome variation, particularly in fossorial forms (Coşkun and Ulutürk, 2001, 2003). such as Ellobius. The genusEllobius may serve as an In captivity, the amount of food consumed varies from interesting example of the mosaic character of evolution. 0.57 to 0.74 or 1.08 g per gram of the animal’s weight. A unique system of sex determination was described for Animals kept together in a cage consume less food than them. Only E. fuscocapillus has 2n = 36 and an XX-XY sex animals kept alone. A single animal consumes 0.91 g determination system unusual for mammals; E. lutescens food per gram of weight, while couples consume 0.68 g has odd diploid number 2n = 17 and XO-XO system in each. It is observed that E. lutescens, when kept in a cage, both sexes. E. talpinus s. str. has 2n = 54, NF = 54, and consumes 79.66 ± 2.89 (19–166) g of food daily. There isomorphic sex chromosomes XX-XX; E. tancrei (2n = 54, is a linear relationship between the weight of the animal NF = 56) and E. alaicus (2n = 52, NF = 56) have normally and consumed food (r = 0.63). These animals primarily XX-XX to (one X inactive). Moreover, E. tancrei is a unique preferred carrots to potatoes, beets, radishes, and onions in example of broad chromosomal changes, 2n = 54–31. It is laboratory conditions. The consumption of carrot is higher quite obvious that the evolutionary changes in the species than that of potato. The females consume more food than Ellobius lutescens involved significant transformations both males (Coşkun and Ulutürk, 2003). Cannibalism was seen in the sex chromosomes from the type (XX, XY) to (XO) in a cage occupied by adults and older pups (Kaya and in males and females and the autosomal chromosomes on Coşkun, 2015). the way from 2n = 54 to 2n = 17 (Borisov et al., 1991, 1999; The mole vole’s adaptations to the continental climate of Kolomiets et al., 1991; Bakloushinskaya and Lyapunova, southern Siberia are based on distinct seasonal variations 2003). in the thermoregulation. In summer, thermoregulatory The karyotype of Ellobius lutescens is unique for mechanisms are similar to those of desert eusocial fossorial mammals (Figure 7). The chromosomes of the males of species, but in spring and autumn, mole voles share the this species are identical to those of the females in number thermoregulatory strategies of boreal terrestrial rodents and morphology, with the same odd number (2n = 17) (Moshkin et al., 2001). being present in both sexes, the number of autosomal Vormela peregusna (Marbled polecat) and Vulpes vulpes arms being NFa = 32, and the fundamental number (Red fox) (Roberts, 1977) and snakes, species of Erycinae, being NF = 34. The karyotype in both males and females Eryx tataricus and Eryx millaris (Rodriguez-Robles et al., consists of 8 pairs of biarmed autosomes and a single small 1999), prey upon mole voles. submetacentric chromosome (Figure 7). Both sexes have Endoparasites, such as Calodium hepaticum, which is a the chromosome constitution XO (Matthey, 1953, 1957; cosmopolitan parasite of the liver parenchyma, have been Hsu and Benirschke, 1969; Vorontsov et al., 1969; Zima reported from the genus Ellobius (Anderson, 2000). and Kral, 1984; Coşkun, 1997; Gharkheloo and Kıvanç, 2.7. Genetics 2003; Graphodatsky et al., 2011). The odd chromosome The genus Ellobius is characterized by the highest is the X chromo­some (chromosome 9), and it constitutes intragenic variability of diploid numbers found in approximately 5% of the haploid genome. At prophase I placental mammals (2n = 17–54). At the same time, the the unpaired chromosome 9 is not involved in synapsis study of specimens of E. lutescens Thomas (2n = 17) and with other chromosomes and forms a sex body at the E. fuscocapillus Blyth (2n = 36) from different parts of end of pachytene (Kolomiets et al., 1991). The G-banding

Figure 7. Karyotype of a female Ellobius lutescens from Iğdır province, Turkey.

837 COŞKUN / Turk J Zool pattern of the unpaired sex chromosome (chromosome 9) population size via the embryonic death of genotypes of Ellobius lutescens is similar to that of the X chromosome XX and OO would be beneficial for all Ellobius species. of Ellobius fuscocapillus (Kolomiets et al., 1991), whereby Nevertheless, this peculiar evolutionary progressive chromosome 9 has been indirectly identified as the X mechanism has been acquired merely by Ellobius lutescens chromosome (White, 1957, 1960, 1973; Wolf et al., 1979; (Kolomiets et al., 1991). Djalali et al., 1986). Convincing evidence substantiating 2.8. Fossil records that the unpaired chromosome 9 can be considered as an Topachevskii and Rekovets (1982) interpreted relationships X chromosome of this species was obtained by Vogel et al. and morphological trends in diversification within the (1988). genus from the late Pliocene to Recent. The present range The mechanism of sex determination in Ellobius of Ellobius is only part of a wider distribution that once lutescens is still unknown and both males and females of embraced Israel and North Africa in the middle to late this species have the formula XO (Vorontsov et al., 1980). Pleistocene (Jaeger, 1988; Kowalski and Rzebik-Kowalska, For many years, it was thought that the sex-determining 1991). and sex-differentiating genes on Y had merely been Gromov and Baranova (1981) stated that the genus translocated to another chromosome in the complement. Ellobius has existed since the mid-Pleistocene. Erbajeva However, it is now clear that although the E. fuscocapillus Y and Alexeeva (2000) and Alexeeva et al. (2001) recognized bears a quite normal Sry (sex-determining region on the Y the Early, Middle, and Late Pleistocene fossils from chromosome) and Zfy (the zinc finger Y gene, considered Trans-Baikal area. Representatives of the genus Ellobius are as the testis-determining gene before Sry), there is no Sry characterized by a tendency towards size and crown height or Zfy in E. lutescens (Vogel et al., 1998; Marchal et al., increases, reduction in prismatic folding, and complication 2003; Kuroiwa, 2012). Evidently, a new sex-determining system took over in a common Ellobius ancestor (Graves, of M/l, which may be possible in M/3. Two developmental 2002; Kuroiwa, 2012). lineages are traced: Ellobius and Afganomys. Within the Just et al. (1995) demonstrated that E. lutescens lacks subgenus Ellobius, forms from Central Asia were singled the Sry gene and sex determination occurs in the absence out, which had led to E. tancrei retaining a number of ancient characters (prismatic fold and complicated M ). of a Y chromosome. Vogel et al. (1998) reported that Sry 3 and Zyf are missing in Ellobius lutescens. Nr5a1 (nuclear The subgenus Afganomys developed autonomously and receptor subfamily 5, group A, member 1) is not the independently, although its history has not been studied in key male sex-determining gene in E. lutescens (Just et detail (Rekovets, 1994). al., 2002). Sry induces testis differentiation in males. Sry Remains of cf. Ellobius have been reported for the contains SOX9 (Sry-related high mobility group box, Pliocene (Late Villanyian), collected in the karst fissure in gene 9). SOX9 is the sex-determining gene in E. lutescens, Rivoli Veronese, northeastern Italy, and the west of Ukraine having two alleles with one of them acting either in a (Sala et al., 1994); for the Early Pliocene (Ruscinian) in male- or in a female-dominant way to induce or repress Kotovka, Odessa-Ukraine (Nesin and Nadachowski, testis differentiation, respectively (Baumstark et al., 2001). 2001); and for the Acheulian in Kyrgyzstan (Markova, Southern blot analysis demonstrated that Zfy, like Sry, is 1992) and the Upper Pleistocene in Israel (Tchernov, lost in E. lutescens. These results support the assumption 1968). E. lutescens was found in Iraq (Bate, 1930) in the that the entire Y chromosome has been lost from the layers of Hazar Merd, aged 25,000 years. Storch (1980) genome of this species (Marchal et al., 2003). reported subrecent deposits from caves in northern Iran. Embryonic mortality is high. Combinations of Hashemi et al. (2006) noted that the Late Pleistocene and gametes with chromosomal numbers of 8+8 or 9+9 were Early Holocene remains of E. lutescens were found in lethal. The existence of the unpaired sex chromosome in cave Kani Mikaeil (Kordestan) Qalaloun near Kouhdasht, E. lutescens is connected with a specific mechanism that Yafteh Gar, and Arjeneh near Khoramabad (Lorestan) in reduces the size of litters (Lyapunova et al., 1975). western and northwestern Iran. Ultrastructure, meiotic behavior, and evolution of The presence of fossil remains in Konya (Turkey) shows sex chromosomes were discussed by Kolomiets et al. that the members of the genus Ellobius were distributed (1991). The X remains un­paired at meiosis. Meiosis and over a wide area during the Pleistocene periods in West spermatogenesis are maintained without a Y chromosome Anatolia, and nowadays they only exist in East Anatolia (Castro-Sierra and Wolf, 1968; Chandra, 1999). The (Coşkun and Ulutürk, 2003). mammalian sex-determining gene SRY is absent in XO During the Middle Pleistocene Ellobius evolved species of Ellobius (Kuroiwa, 2012). through the succession of E. africanus, E. atlanticus, E. The lethality in young rodents of such habitats is, barbarus, and E. zimae. The widest distribution of Ellobius obviously, significantly lower compared to the underground probably occurred in the Pliocene, when it reached North species. From this point of view, the mechanism regulating Africa (Jaeger, 1988; Raynal et al., 2001).

838 COŞKUN / Turk J Zool

2.9. Remarks maximum length of the breeding season, reliable E. lutescens was described as a species by Thomas (1897) abundance estimates, and studies of distribution and but was considered a subspecies of E. fuscocapillus by migration. Other areas worthy of investigation are the Ognev (1963). It is determined that this species is not identification of wintering areas, acquisition of up-to-date endangered, and therefore it does not need any protection data on reproduction and mortality, and investigations at present (Coşkun and Ulutürk, 2001, 2003).The generic into the consequences of environmental changes for the name, Ellobius, is from Greek. The specific name lutescens species. comes from the Latin “lutes”, meaning “yellowish”, the fur color of the earliest specimens collected in Turkey. Acknowledgment In conclusion, future research needs to include I would like to thank Ms Emma Sherlock of the Natural the collation of further data on population dynamics, History Museum of London for English editing.

References

Alexeeva NV, Erbajeva MA, Şen Ş (2001). Geology and fauna and Coşkun Y (2000). Some peculiarities of the species Ellobius lutescens preliminary correlation of sediments of the main late Cenoic from Turkey. In: Proceedings of XVIIth International Congress sites of the Transbaikal area. Quatern Int 80-81: 93-100. of Zoology, Athens, Greece, p. 179. Anderson RC (2000). Nematode Parasites of Vertebrates. Their Coşkun Y (2001). On distribution, morphology and biology of Development and Transmission. 2nd ed. Wallingford, UK: the mole vole, Ellobius lutescens Thomas 1897 (Mammalia: CABI Publishing. Rodentia) in Eastern Turkey. Zool Middle East 23: 5-12. Bakloushinskaya IYu, Lyapunova EA (2003). History of study and Coşkun Y, Ulutürk S (2001). Taxonomy, Distribution and Karyology evolutionary significance of wide Robertsonian variability in of the Genus Ellobius (Rodentia: Mammalia) in Turkey. TBAG mole-voles Ellobius tancrei s. l. (Mammalia, Rodentia). In: Research Project No. 1751. Ankara, Turkey: TÜBİTAK. Kryukov AP, Yakimenko LV, editors. Problems of Evolution, Coşkun Y, Ulutürk S (2003). Observations on the mole vole, Ellobius Vol. 5. Vladivostok, Russia: Dalnauka, pp. 114-126. lutescens Thomas 1897, (Mammalia: Rodentia) in Turkey. Turk Bate DMA (1930). Animal remains from the Dark Cave, Hazar Merd. J Zool 27: 81-87. American School of Prehistoric Research Bulletins 6: 38-41. Darlington PJ (1957). Zoogeography: The Geographical Distribution Baumstark A, Akhverdyan M, Schulze A, Reisert I, Vogel W, Just W of Animals. New York, NY, USA: John Wiley & Sons. (2001). Exclusion of SOX9 as the testis determining factor in Djalali M, Hameister H, Vogel W (1986). Further chromosomal Ellobius lutescens: evidence for another testis determining gene studies on Ellobius lutescens: heteromorphism of chromosome besides SRY and SOX9. Mol Genet Metab 72: 61-66. No. 1 is not associated with sex determination. Experientia 42: Borisov YM, Lyapunova E A, Vorontsov NN (1991). Karyotype 1281-1282. evolution in the genus Ellobius (Microtinae, Rodentia). Ellerman JR (1941). The Families and Genera of Living Rodents. Vol. Genetika 27: 523-532. II, Family Muridae. London, UK: British Museum (Natural Borisov YM, Lyapunova EA, Vorontsov NN (1999). Karyotype History). evolution in the genus Ellobius (Arvicolinae, Rodentia). In: Ellerman JR (1948). Key to the rodents of South-west Asia in the Proceedings of the 3rd European Congress of Mammalogy, British Museum collection. P Zool Soc Lond 118: 780-781. Jyvaskyla, Finland, p. 78. Ellerman JR, Morrison-Scott TCS (1951). Checklist of Palaearctic Castro-Sierra E, Wolf U (1968). Studies on the male meiosis of and Indian Mammals, 1758 to 1946. London, UK: British Ellobius lutescens Th. Cytogenetics 7: 241-248. Museum (Natural History). Chandra HS (1999). Another way of looking at the enigma of sex Erbajeva MA, Alexeeva NV (2000). Pliocene and Pleistocene determination in Ellobius lutescens. Curr Sci India 76 : 1072- biostratigraphic succession of Transbaikalia with emphasis on 1073. small mammals. Quatern Int 68-71: 67-75. Corbet GB (1978). The Mammals of the Palaearctic Region: A Evdokimov NG (1997). Population dynamics in the common mole Taxonomic Review. London, UK: British Museum (Natural vole (Ellobius talpinus Pall.). Doklady Biological Sciences 356: History). 478-481. Corbet GB, Hill JE (1991). A World List of Mammalian Species. 3rd Evdokimov NG (2002). The Northern mole vole: Is it hibernator? ed. London, UK: British Museum (Natural History). Russ J Ecol 33: 32-37. Coşkun Y (1997). Morphological and karyological peculiarities of the Gharkheloo MM, Kıvanç E (2003). A study on the morphology, species Ellobius lutescens Thomas, 1897 (Rodentia: Cricetidae) karyology and distribution of Ellobius Fisher, 1814 (Mammalia: in Turkey. Turk J Zool 21: 349-354. Rodentia) in Iran. Turk J Zool 27: 281-292.

839 COŞKUN / Turk J Zool

Graphodatsky AS, Trifonov VA, Stanyon R (2011). The genome Lyapunova EA, Vorontsov NN, Zakarjan GG (1975). Zygomatic diversity and karyotype evolution of mammals. Molecular mortality in Ellobius lutescens (Rodentia: Microtinae). Cytogenetics 4: 22. Experientia 31: 417. Graves JAM (2002). The rise and fall of SRY. Trends Genet 18: 259- Marchal JA, Acosta MJ, Bullejos M, Diaz De La Guardia R, Sanchez 264. A (2003). Sex chromosomes, sex determination, and sex- Gromov IM, Baranova GI (1981). Catalogue of Mammals in USSR. linked sequences in Microtidae. Cytogenet Genome Res. 101: Leningrad, Russia: Nauka. 266-273. Harrison DL (1972). The Mammals of Arabia. Vol. 3. Lagomorpha- Markova A (1992). Fossil rodents (Rodentia, Mammalia) from the Rodentia. London, UK: Ernest Benn Ltd. Sel’-Ungur Acheulian cave site (Kirghizstan). Acta Zoologica Cracoviensia 35: 217-239. Harrison DL, Bates PJJ (1991). The Mammals of Arabia. 2nd ed. Sevenoaks, UK: Harrison Zoological Museum. Matthey R (1953). Un nouveau type de chromosomes sexuels chez un mammifere (Ellobius lutescens Thomas Rodentia- Hashemi N, Darvish J, Mashkour M, Biglari F (2006). Rodents and Microtinae). Experientia 10: 18 (in French). Lagomorphs remains from late Pleistocene and early Holocene Caves and Rochshelter sites in the Zagros region, Iran. Iranian Matthey R (1957). Cytologie comparee, systematique et phylogenie Journal of Animal Biosystematics 2: 25-33. des Microtinae (Rodentia-Muridae). Rev Suisse Zool 64: 52- Hassinger JD (1973). A survey of the mammals of Afghanistan: 53 (in French). Resulting from the 1965 Street Expedition (Excluding Bats). Moshkin MP, Novikov EA, Petrovski DV (2001). Seasonal changes Fieldiana Zoology, Vol. 60. Chicago, IL, USA: Field Museum of thermoregulation in the mole vole Ellobius talpinus. of Natural History. Physiol Biochem Zool 74: 867-875. Hinton MAC (1926). Monograph of the Voles and Lemmings. Nesin VA, Nadachowski A (2001). Late Miocene and Pliocene London, UK: British Museum (Natural History). small mammal faunas (Insectivora, Lagomorpha, Rodentia) Hsu TC, Benirschke K (1969). An Atlas of Mammalian of Southeastern Europe. Acta Zoologica Cracoviensia 44: Chromosomes. Vol. 3, Folio 112. Berlin, Germany: Springer. 107-135. Jaeger JJ (1988). Origine et evolution du genre Ellobius (Mammalia, Nowak RM (1999). Walker’s Mammals of the World. 6th ed. Rodentia) en Afrique Nord-Occidentale. Folia Quaternaria Baltimore, MD, USA: The Johns Hopkins University Press. 57: 3-50 (in French). Ognev SI (1963). Mammals of the USSR and Adjacent Countries. Just W, Baumstark A, Hameister H, Schreiner B, Reisert I, Vol. V. Rodents. Jerusalem, Israel: IPST. Hakhverdian M, Vogel W (2002). The sex determination in Osborn DJ (1962). Rodents of the subfamily Microtinae from Ellobius lutescens remains bizarre. Cytogenet Genome Res 96: Turkey. J Mammal 43: 515-529. 146-153. Panteleyev PA (1998). The Rodents of the Palaearctic. Composition Just W, Rau W, Vogel W, Akhverdian M, Fredga K, Graves JAM, and Areas. Moscow, Russia: Russian Academy of Science, Lyapunova EA (1995). Absence of Sry in species of the vole A.N. Severtzov Institute of Ecology and Evolution. Ellobius. Nat Genet 11: 117-118. Raynal JP, Alaoui FZS, Geraads D, Magoga L, Mohi A (2001). Kaya A, Coşkun Y (2015). Reproduction, postnatal development, The earliest occupation of North-Africa: the Moroccan and social behavior of Ellobius lutescens Thomas, 1897 perspective. Quatern Int 75: 65-75. (Mammalia: Rodentia) in captivity. Turk J Zool 39: 425-431. Rekovets LI (1994). History and phylogeny of Arvicolidae Kolomiets OL, Vorontsov NN, Lyapunova EA, Mazurova TF (1991). Ultrastructure, meiotic behavior, and evolution of sex (Rodentia) in Pleistocene of Eastern Europe. Polish chromosomes of the genus Ellobius. Genetica 84: 179-189. Ecological Studies 20: 553-558. Kowalski K, Rzebik-Kowalska B (1991). Mammals of Algeria. Roberts TJ (1977). The Mammals of Pakistan. London, UK: Ernst Warsaw, Poland: Polish Academy of Science. Benn Ltd. Kuroiwa A (2012). The fate of the Y chromosome. In: D’Aquino Rodriguez-Robles JA, Bell CJ, Greene W (1999). Gape size and M, Stallone V, editors. Sex Chromosomes: New Research. evolution of diet in snakes. Feeding ecology of erycine boas. Hauppauge, NY, USA: Nova Science Publishers, pp. 87-107. J Zool 248: 49-58. Lay DM (1967). A Study of the Mammals of Iran. Resulting from Sala B, Masini F, Torre D (1994). Villanyian arvicolids from the Street Expedition of 1962-63. Fieldiana Zoology, Vol. 54. Veronese, a karst fissure in the Adige valley, Northeastern Chicago, IL, USA: Field Museum of Natural History. Italy. Boll Soc Paleontol I 33: 3-11. Lyapunova EA, Vorontsov NN, Korobitsyna KV, Ivanitskaya Storch G (1980). Spatglaziale kleinsauger der Ali Tepeh-Höhle EYu, Borisov MYu, Yakimenko LV, Dovgal VYe (1980). A (Behsnar). Zur klima-ökologischen faunengeschichte in NE- Robertsonian fan in Ellobius talpinus. Genetica 52-53: 239- Iran (Mammalia: Insectivora, Rodentia). Senckenbergiana 247. Biologica 60: 285-302 (in German).

840 COŞKUN / Turk J Zool

Tchernov E (1968). Succession of Rodent Faunas During the Upper Vorontsov NN, Lyapunova EA, Zakaryan GG, Ivanov VG (1969). The Pleistocene of Israel. Mammalia Depicta. Hamburg, Germany: karyology and taxonomy of the genus Ellobius (Microtinae, Paul Parey. Rodentia). In: The Mammals, Evolution, Karyology, Taxonomy, Fauna. 2nd All-Union Mammalogy Conference, Moscow. Thomas O (1897). On two new rodents from Van, Kurdistan. Annals and Magazine of Natural History 20: 308-310. Walker EP (1964). Mammals of the World. Vol. 2. Baltimore, MD, USA: The Johns Hopkins Press. Thomas O (1905). On a collection of mammals from Persia and Armenia presented to the British Museum by Col. A.C. White MJD (1957). An Interpretation of the Unique Sex- Bailward. P Zool Soc Lond 2: 519-527. Chromosome Mechanism of the Rodent Ellobius lutescens Thomas. Calcutta, India: Proceedings of the Zoological Society Topachevskii VA, Rekovets LI (1982). New material for systematic of Calcutta, Mookerjee Memoir. and evolution of the mole vole, nominative subgenus and genus Ellobius (Rodentia, Cricetidae). Vestnik Zoologii 5: 47-54. White MJD (1960). Are there no mammal species with XO males - and if not, why not? Am Nat 95: 315-321. Vinogradov BS, Argiropulo AI (1968). Fauna of the USSR. Key to Rodents. Jerusalem, Israel: IPST. White MJD (1973). Animal Cytology and Evolution. 3rd ed. Cambridge, UK: Cambridge University Press. Vogel W, Janitas S, Rau W, Geerkens C, Baumstark A, Correa-Cerro LS, Ebenhoch C, Just W (1998). Sex determination in Ellobius Wilson DE, Reeder DM (2005). Mammal Species of the World. lutescens: the story of an enigma. Cytogenet Cell Genet 80: 214- Washington, DC, USA: Smithsonian Institution Scholarly 221. Press. Vogel W, Steinbach P, Djalali M, Mehnert K, Ali S, Epplen JT (1988). Wolf M, Schempp W, Vogel W (1979). Ellobius lutescens Th. Chromosome 9 of Ellobius lutescens is the X chromosome. (Rodentia, Microtinae): Q-, R-, and replication banding Chromosome (Berl) 90: 112-118. patterns. Cytogenet Cell Genet 23: 117-123. Vorontsov NN, Lyapunova EA (1984). Explosive chromosomal Zima J, Kral B (1984). Karyotypes of European mammals. II. speciation in seismic active regions. Chromosome Today 8: Acta Scientiarum Naturalium Academiae Scientarium 279-294. Bohemoslovacae (Brno) 18: 1-62. Vorontsov NN, Lyapunova EA, Borisov YuM, Dovgal VE (1980). Variability of sex chromosomes in mammals. Genetica 52-53: 361-372.

841