Chromosomal forms of the Mole Rat, Nannospalax nehringi (Satunin, 1898), from the Van Lake Basin in Eastern Turkey
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2 Chromosomal forms of the Mole Rat, Nannospalax nehringi (Satunin, 1898), from the Van Lake Basin in Eastern Turkey (\lammalia: Rodentia) Yiiksel COjkun, Alaettin Kaya, Gokhan Yiiriimez Abstract. Two different chromosomal foons of the Mole Rat. Nannospalax nehringi (Satunin, 1898). have been found in the Van Basin, Eastern Turkey: a population around the city of Van with 20=48, NF=72 and t-:fa=68. and a population around the city of Bitlis with 20=54, NF=74 and t\fa=70. Both populations are confined to well-defined distribution areas. While both populations are separated in the south by Mt SOphan, an extinct volcano over 4000 m high. there is no geographic barrier between both populations in the north, and there seems to be a secondary contact zone. The Van population constitutes a new chromosomal form of Mole Rat in Turkey, and could bc rcgarded as a sibling species. However, no taxomomic decision is taken until more evidence on the evolution of these fontis has become available. Kc)' words: Rodentia, Spalacidae, Nanno.'palax nehringi, karyotype, Turkey, Introduction Mole rats of the genus Nannospalax have been widely studied in recent years to clarify species boundaries and phylogenetic relationships. Approximately 30 karyotypcs of Nannospalax have been reported from Turkey so far. The diploid number (2n) of chromosomes ranges from 38 to 62 (see e.g. GOLKA<;& YOKSEL 1989, IVANITSKAYA et al. 1997, TEZ et al. 2002), and the fundamental number of chromosomal arms (NF) varies between 66 and 92, while the fundamental number of autosomal arms (NFa) ranges from 62 to 88 (CO:';iKUN 2004a, b, C, S6ZEN et al. 2000, S6ZEN 2004, CO>KUN ct al. 2006, and references therein). Unfortunalely, karyulugical studies of the Nannospalax populations within the territory of Turkey are, on the whole, far from satisfactory for clarifying the distribution pattern and evolution of these chromosomal forms. The range of Nannmpalax nehringi (Satunin, 1898), first described as Spa/ax nehringi, is confined to the Caucasus and Eastern Turkey (TOPACHEVSKII 1969), It has been regarded as conspecific with Spal(L'(leI/codon Nordmann, 1840 (ELLERMAN & MORRISO!\,'-SCOTT 1951), but, following GRmtOV & BARANOVA (1981) who differentiated Nallnospalax from Spalax based on morphological characters, we consider this taxon to be a distinct species. The first studies on the karyological peculiarities of N. nehringi were carried out by MAT- TIlEY (1959), who recorded 2n~48 in samples from the Caucasus. Later, NEVO et al. (1995) reported the diploid number of chromosomes of specimens from Erzurum and Kars (Sankaml,) as 2n~50. S6ZEN et al. (2000) found 2n~50 and NF~72 in the populations from Kars (Susuz), Erzurum and Ardahan, CO>KUN (2003) 2n~48, NF~68 and NFa~64 from AgTl and Zoology in the Middle East 48,2009: ISSN Kasparek Verlag, Heidelberg
3 18 Zoology in the Middle East 48, 2009 Van-(aldlran, and again COSKUN (2003) 2n~50, NF~70, NFF66 from Erzurum and the Kars province. \Ve have studied the karyology of the Mole Rat in the Van Basin, which is relatively isolated and where different climate regions occur. \Vc wanted to determine how the karyological characteristics have evolved in different, relatively isolated populations. Material and methods The Mole rat specimens used in this study were collected in the Van Lake basin (Mu~, 8itlis and Van districts) in Eastern Turkey (37 58'-39 40'N; '-44 30'E). The region is characterised by high mountains (average altitude around 2000 m) and by large undulating plateaus at an altitude of ITI. The high plateaus arc subject to cold which limits arboreal vegetation, so that the region is covered mostly by steppe vegetation. Annual rainfall occurs more or less evenly throughout the year and varies between 400 and 600 mm. However, the rain shadow from large mountains, such as Agn, has rum rainfall, whilst the regions surrounding the large lakes may have rum rainfall. A total of21 Mole Rals (12 0, 99) was captured at 7 different localities in the Van Lake basin of Eastern Turkey (Fig. I) during three surveys in We opened burrow systems and collected the animals with hoes when they came up to plug the opening. Voucher specimens were deposited at the Department of Biology, Science and Art Faculty, University of Dick, Turkey. Karyotyping was carried out according to standard procedures (see e.g. COSKUN ct a!. 2006). Results According to our karyotype analyses, two different populations of N. nehringi occur in the Van Lake basin in Eastern Turkey. The diagnostic features of the different karyotypes are described below and summarised in Table 1, which provides an overview of all the populations of N. nehringi from Eastern Turkey that have been analysed so far. The approximate geographic area of each chromosomal form is shown in Fig. I. Van population. The specimens of the Van population were collected near the type locality (Kars~Gaziler Kaskoparan) of Nannospalax nehringi. The karyotypes of the two specimens from the city of east Mu~ (Malazgirt town) and the four specimens from the city of Van (town of Erci~ - Bozyaka village) have 2n=48, chromosomal arms NF=72, and autosomal arms NFa=68 (Table I). Their karyotypes consist of 11 pairs of metalsubmetacentric auto somes and 12 pairs of acrocentric autosomes. The X chromosomes are largc and submetacentric, whereas the Y chromosomes are large and acrocentric (Fig. 2A). The karyotype of this population represents a cytogenetically distinct taxon, with a high percentage ofbiarmed chromosomes. Hence, the records from Mu~ (Malazgirt town) and from Van (Erci~-Bozyaka village) have enlarged the distribution range of the 2n=48 form to the south and west. However, whilst the karyotype of these populations has the same diploid chromosome number (Le. 2n=48), the proportion of chromosomal and autosomal arms is variable. The karyotype of this population was first defined by COSKUN (2003) as 2n ~ 48, NF ~ 68, NFa ~ 64, and the karyotypes observed here are different from those.
4 \fammalia 19 -'" TURKEY. r A RI, VAN.('itif'~ Town "HilJ,b'loUDlllin~ ~Colle<:lionIO<lIlil;e~ (T1n!Udy! AOldrt'corch (C."ll WOJ) FIg. I. Sampling localities and geographic distribution of chromosomal forms of Nanllospalax nehringi in eastern Turkey (locality names are given in the sequence province - district - village). Billis Population: (I) BIlIi!'.- Ilizan - Ta~top village (3 specimens); (2) Bitlis Tatvan - A~aglkolba~1 village (4 specimens); (3) Hitlis -.-\hlat - Uludere village (4 specimens); (4) Mu:;; - Bulamk - Erentepe village (3 specimens); (5) Mu~ - Kum- "=-et village (I specimen). - Van Population: (6) Van - Erci~ Bozyaka village (4 specimens); (7) Mu:;; _ 'Ialazgirt (2 specimens). Old records: (8) Bitlis - Tatvan - Kuskunklfan; (9) Van - I km east ofc;:aldjran; (10) \gn - Ta~Il(;:ay- Yanalyol; (II) Agn - KiipkJran [data from localities 8-11 taken from COSKtP.\l (2003)]. Bitlis Population. The specimens of the Bitlis population were collecled from five localities: three specimens at Ta~top village near Hizan, four specimens at A~aglkolbaSI village near Tatyan, four specimens at Uludere village near Ahlat, three specimens at Erentepe village Dear Bulal11k, and one specimen at Ktimbet village near Mu~. The karyotypes of the 15 specimens from the Bitlis and Mu~ (Erentepe and Ktimbet village) populations have 2n=54, chromosomal arms NF=74, and autosomal arms NFa=70 Table I). The karyotypes consist of nine pairs of meta/submetacentric autosomes and l7 pairs of acrocentric autosomes. The X chromosomes are large and submetacentric, whereas the Y chromosomes are minute and acrocentric (Fig. 2B). This karyotype form is new to Turkey (Table I), This 2n~54 karyotype is different from the 2n~54 karyolypes described from Bingo] SE\'O et al. 1995), Yozgat (YOKSEL & GOLKA<;2001), Karabiik province (SOZE~ 2004) and Kastamonu (SOLEN et al. 2006b), but has the same chromosome arm numbers (NF and NFa) ~ the 20=54 karyotypes of Nannospalax tunceliclis (Co~kun, 1996) from Tunceli, Elazlg, 1lld Bingol (COSKUN 2004a) (Table 2),
5 20 Zoology in the rvtidd1c East Table 1. Chromosomal records of Nannospalax nehringi from Eastern Turkey. Abbreviations: sm = submctacentric; st = subtc1ocentric; a = acrocentric; III = metacentric; 20 = diploid chromosome number; NF = fundamental chromosome arm number; NFa = fundamental autosomal ann number; X = X chromosome; Y = Y chromosome. Autosomes 2n Bianncd: NFa NF X Y References a m,srn,st AUf! and alduan Sill a CO~KUN2003 ~fus (Malazc:irt), Van (Ercis) 48 II Sm a This study Erzurum. Kars (Sankamls) sm NEva ct al Erzurum and Kars ,m a COSKUN 2003 Erzurum, Kars (Susuz), Ardahan sm a SOZE;\ et a Bingol NEVO ct al. ]995 Tunceli, Elaw!. Bin»o! sm a COSKUN 2004a Bitlis, Mus sm a This study Table 2. Survey of the 20=54 and 20=48 chromosomal forms of Nannospa/a.'( described from Turkey (abbreviations as in Table 1). Autosomcs NF 2n Biarmed: NF X Y References a a m,sm,sl Karabuk sm a SOZEN 2004 Kastamonu sm a S{)ZEN et al.2006b Tunceli, Bin2:o1,Elazll! sm a COSKUN 2004a Bolu sm - NEva et al.1995 Bim!:ol sm - NEva et al Yozgat sm st YUKSEL &GULKA( 200] BitlisMus sm a Thisstu~ Agn, ( aldlran sm a COSKUK 2003 Uumushane Sm - SOZEN et al.2006a ;vius.van Sm a This study Discussion The karyotype of the N. nehringi specimens collected from Malazgirt, Mu~ province (locality 7) and Bozyaka village, Van provionce (locality 6), which are called the Van population, differs in the number of chromosomal arms from the specimens collected in Agn, <;aldtran and Glimli,hane (Ca,KuN 2003, SOZEN et al.2006a) (Table 1-2). The 2n=54 chromosomal fonn shows a great variability in the number of chromosomal arms (NF and NFa) among the various populations (Table 2). 2n=54 karyotypes have been recorded lrom Bolu and Bingol (NEva cl al. 1994, 1995), Yozgat (YOKSEL & GOLKAt; 2001), Karablik province (SOZEN 2004), Kastamonu (SOZEN et al.2006b) and Tokal (SOZEN et al.2006a). The chromosome morphology of the Bingol population studied by NEva et al. (1995) is actually unknown since the figure given for the 2n=54 karyotype is for the Bolu population. However, the karyotype of the populations from Bitlis (this study) is similar (2n~54, NF~74, NFa~70) 10 Ihat of the POpulalion from Yozgal reported by YOKSEL &
6 Mammalia 21 l ~ I " t 9 10 II I, X Y t "" Mu~-Malazgirt.Merkez. No: 580. Male ld] Bitlis Tatvan- A~glkolba~lk5ytl, No: 592, Male.1 II IIIIII II " " " " n.1s I' I~KK als AJ Ir. "" a 4 I xv - 00 t'1\ -.ft "", A'"...,.. A, T\n;C\i.-KQl:MOli.(',mnen vii., No,;'97, Male I. x, Fig. 2. Standard kai)'otypes of Nannospala.. nehringi: (A) Van population (.~'.No: 580), with 20 = 48: (8) Bitlis population (2.1'\0: 592) with 20 = 54; (e)nanno!>pala.. tllncelicus population (::3'.N"o: 397), with 20 = 54 (CO:)KUN 2004a).
7 22 Zoology in the Middle East 415,2009 Fig. 3. Nannospalax nehrinki, male (Photo; Y. CO~Kl.:" , Bitlis- Hizan- Ta~top village, No. 576). GDLKA( (2001). However, these two areas are geographically very distant one from another. The forms from Yozgat and from Bitlis are therefore regarded as different (Tables 1-2). The karyotype 2n~54, NF~74, NFa~70 ofthc Bitlis population of N. nehringi (this study) is also similar to that of the Nannospalax tuncelicus populations from Elazlg, Tunceli, and Bingo] (COSKUN 2004a), but the chromosome morphology is different. The main difference is the presence of only one large biarmed and one large (first pair) acrocentric chromosome pair in N. nehrin);i, while N. tunce/icus has two pairs bianned and no large acrocentric pair (Figs 2B-C). According to these results, the Van and Bitlis populations represent two different chromosomal forms of the species N. nehringi, even though there arc no significant geographic barriers between these two populations (from the Malazgirt and Bulallik districts). However, each karyotype form occupies a well-defined geographic range, and so some ecological barriers may limit its expansion. No hybrids have been found between these two populations. NEva et a1. (1995) stated that each chromosomal form should be assigned to a separate biological species and that there are presumably about 30 such species in Turkey. While the chromosomal diversity in Turkish N. nehringi is rather great, it is difficult at this time to decide whether or not a particular karyotype represents a separate species. ULUTURK & COSKUN (2000) showed that the Bitlis population possesses morphological characters different from other populations. This could indicate that the Bitlis population is a separate subspecies of Nannospalax nehringi (Fig. 3). According to the karyotype analyses in this study. however, the Bitlis population of lv'.nehringi could even be considered a separate species.
8 Mammalia 23 Acknowledgements. This shldy was supported by the Scicntific and Technical Research Council of Turkey (TUSITAK Project No. 105Tl92). We arc grateful to T. PAVLICEK(Haifa. Israel) for his comments on the manuscript. References COSKUN. Y. (2003): A study on the morphology and karyology of Nannospalax nehringi (Satunin, 1H98) (Rodentia: Spalacidae) from North-eastern Anatolia. Turkey. - Turkish Journal of Zoology 27: COSKUN. Y. (2004a): A new species of mole rat,,vannospalax mun:=urisp. n. and karyotype of Nannospalax lllnceliclls (Co~kun, 1996) (Rodentia: Spalacidae) in eastern Anatolia. ~ Zoology in the Middle East 33: CO~KUN, Y. (2004b): Morphological and karyological charactcristies of Nannospalax ehrenbergi (Nehring, 1898) (Rodentia: Spalacidae) from Hatay Province, Turkey. - Turkish Journal of Zoology 28: CO~KUN, Y. (2004c): A new chromosomal fonn of Nannospalax ehrenbergi from Turkey. - Folia Zoologiea 53: 35 I COSKUN, Y., S. ULUTORK & G. YURUMEZ (2006): Chromosomal diversity in mole-rats of the species Nannospalax ehrenbergi (Rodentia: Spalacidae) from South Anatolia, Turkey. - Mammalian Biology - Zeitschtift flir Saugetierkunde 71: ELLEIZMAN, J. R. & T. S. C MORRISON-SCOTT (195 I): Checklist of Palaearctic and Indian Mammals British r..1useum Natural Ilistory, London. GROMOV, I. M. & G. I. BARANOVA (1981): Catalogue of Mammals in USSR. - Nauka, Leningrad. I\'ANITSKAYA, E., Y. COSKUN & E. NEVO (1997): Banded karyotypes of mole rats (Spalax, Spalacidae, Rodentia) from Turkey: A comparative analysis. - Journal of Zoological Systematics and Evolutionary Research 35: \IATTHEY, R. (1959): Formules chromosomiques de Muridae et Spalacidae. La question du polymorphisme chromosomique chez les mammiferes. - Revue Suisse de Zoologic 66: ~EVO, E., M. G. FIUPPUCCI, C. REDI, A. KOROL & A. BElLES (1994): Chromosomal speciation and adaptive radiation of mole rats in Asia Minor correlated v....ith increased ecological stress. ~ Proceedings of the National Academy of Sciences ofthe United States of America 91 : 8 I60-8 I64. ~EVO E., M. G. FIUPPUCCI, C. REDI, S. SIMSON, G. HETH & A. BElLES (1995): Karyotype and genetic evolution in speciation of subterranean mole rats of the genus Spalar in Turkey. - Biological Journal of the Linnean Society 54: S6ZE.\I, M. (2004): A karyological study on subterranean mole rats of the Spalax leucodon Nordmann, 1840, superspccies in Turkey. - Zeitschrift fur Saugetierkunde 6: SOZE.\I, M., E. COLAK & N. YIGIT (2000): Contributions to the karyology and taxonomy of Spala>; leucodon nehringi Satunin. 1898, and Spalax leucodon armcniacus Mehely, 1909 (Mammalia: Rodentia) in Turkey. - Zeitschrift flir Saugetierkunde 65: SOZEN, M., F. MATUR, E. COLAK,~. OZKURT & A. KARATAS (2006a): Some karyological records and a new chromosomal form for Spalax (Mammalia: Rodentia) in Turkey. - Folia Zoologica 55: SOZEN, M.. M. SEVI.\IDlK & F. MATUR (2006b): Karyological and some morphological characteristics of Spalax leucodon Nordmann, 1840 (Mammalia: Rodentia) superspecies around Kastamonu Province, Turkey. - Turkish Journal of Zoology 30: TEl. C., i. GONDUZ & II. KEFELIOGLU (2002): New data on the distribution of2n =38 Spalax leucodon :-.Jordmann, 1840 cytotypc in Turkey. - Israel Journal of Zoology 48: TOPACHEVSKJI, V. A. (1969): The Fauna of the USSR: Mammals. Mole Rats, Spalacidae [English Translation]. Vol. III, No.3. - Leningrad.
9 24 Zoology in the Middle East 48, 2009 ULUTURK, S. & Y. COSKUN (2000): Morphological peculiarities of Mole Rats from Bitlis Province, Turkey. - Proceedings of the XVth National Congress of Biology, Ankara [in Turkish with English summary]. YOKSEL, E & M. D. GOLKA(: (2001): The cytogenetical comparison of Spa/ax (Rodentia: Spalacidac) populations from middle KlZlhrmak basin, Turkey. - Turkish Journal of Biology 25: Authors' address: Yiikscl Co~kun, Alaettin Kaya and Gakhan YiirUmez, Dicle University, and Art Faculty, Biology Department, Diyarbaklf, Turkey. - yuksclc@dic\c.cdu.tr. Science
10 """...,.-"'-- Sustainability has Many Faces A series for the UN Decade of Education for Sustainable Development Preserving biological and cultural diversity pre pares the ground for human development. The examples included in this series present various "faces" of sustainability, offering ideas, contributions and suggestions on education for sustainable development both in and out of school. Development Needs Diversity I'ooplt... ~..-l-.onol -~Ir<>rn...-"' """'" Each of the nine publications includes both a CD and DVD for education materials. Available in English, German, French, and Spanish. Price: Euro each Further information at gtz 1::::...""'-,-- Articles to be published in forthcoming Zoology in the Middle East (selection of already accepted manuscripts) issues of Manuscripts already accepted for publication include: Investigation of two dolphin mass mortality events in the Gulf in autumn 2007 Sexual dimorphism of Black Rock Agama, Laudakia me/anura llrata in Iran Assessment of the origin of a Loggerhead Turtle in the Arabian Gulf using mitochondrial DNA Honeycomb Stingray at the Syrian coast Genetic structure of a Silver Pomfret population as revealed by microsatellite variation Occurrence, behaviour, and habitat preference of the Levant Pincertail New records of shallow-water Oribatid mites new to the fauna of Iran sea spiders from Turkey Cover picture: A male Mole Rat, Nannospa/ax nehringi, (Photo: Y. CO$KUN, Bitlis/Turkey, )
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