Hystrix It. J. Mamm. (n.s.) 21(1) (2010): 89-96

KARYOTYPES OF NANNOSPALAX (PALMER 1903) POPU- LATIONS (RODENTIA: SPALACIDAE) FROM CENTRAL- EASTERN ,

YÜKSEL COùKUN*, SERVET ULUTÜRK, ALAETTIN KAYA

Dicle University, Science Faculty, Biology Department, 21280 Diyarbakır, Turkey * Corresponding author, E-mail: yukselc@.edu.tr

Received 23 September 2009; accepted 26 March 2010

RIASSUNTO - Cariotipi di Nannospalax (Palmer 1903) (Rodentia, Spalacidae) dell’Anatolia centro-orientale, Turchia. Sono stati analizzati i cariotipi di 20 (11 maschi e 9 femmine) Nannospalax catturati, nel periodo 2006-2009, in 11 località dell’Anatolia cen- tro-orientale (Turchia). Sono state individuate sei diverse forme cromosomiche (2n=49; 2n=50; 2n=52; 2n=54; 2n=60a e 2n=60b), corrispondenti a N. nehringi (N = 3), N. ehren- bergi, N. munzuri e N. tuncelicus. Nella provincia di è stata confermata la presenza di due popolazioni (2n=60a e 2n=60b), separate dal fiume Thoma. La forma 2n = 49, rinve- nuta presso Pülümür, potrebbe essere un nuovo taxon.

Key words: Spalax, Nannospalax, autosomi, forme cromosomiche, Turchia

The subterranean mole rats (Family: spalacids to the genus Nannospalax, the Spalacidae) are exceptionally variable - species of the genus Spalax having no ac- mals with respect to the morphology and rocentric chromosomes in their karyotypes karyology of their chromosomes. The ge- (Lyapunova et al., 1974; Zima and Kral, nus Nannospalax underwent a rapid chro- 1984). Two other species, Nannospalax mosomal evolutionary radiation that re- munzuri from - Ovacık and N. tun- sulted in the 59 chromosomal form, wide- celicus from Tunceli - Bingöl - Elazı÷ spread throughout the Palaearctic region province, have been described by Coúkun (Musser and Carleton, 2005). In Turkey (1996, 2004). two species (Spalax leucodon and S. Karyological studies on Turkish mole rats ehrenbergi) of mole rats have been defined were initiated by Soldatovic and Savic in morphological terms (Mursalo÷lu 1979; (1978). Currently, about150 populations of Kıvanç 1988 and Nevo et al., 1995). None- mole rats have been karyotyped. theless, contrary to Musser and Carleton Since 1984, investigations on Nannospalax (2005), we agree with Gromov and populations (Coúkun et al., 2006 and refer- Baranova (1981) in attributing all Turkish ences therein) showed that in Turkey there

89 Coúkun et al. are different allopatric chromosomal forms Voucher specimens were deposited at the (without hybrid zones) of this genus (Nevo Department of Biology, Science and Art et al., 1994, 1995; Tez et al., 2001; Faculty, University of Dicle. Coúkun, 2003). Yüksel (1984) recorded 2n Materials: (1) - Divri÷i - Hıdırlık vil- = 52 for specimens from Elazı÷, while 2n = lage (39o23'N 37o54'E) 1ƃƃ; (2) - 60 was reported for - Dutluca village (39o08'N (Yüksel, 1984; Ivanitskaya et al., 1997 and 38o36'E) 1ƂƂ; (3) Erzincan - Kemaliye - Nevo et al., 1995). In the same province, Çitköy village (39o06'N 38o34'E) 1ƂƂ; (4) Gülkaç and Yüksel (1989) found that the Elazı÷ - - village (38o50'N chromosome morphology of the specimens 38o50'E) 2ƂƂ, 1ƃƃ; (5) Malatya – from was different from that Akçada÷ - Kürecik Road (38o20'N 37o45'E) showed by individuals from other locali- 1 ƃƃ; (6) Malatya – Do÷anúehir - Örnek ties. Finally, 2n = 58 Nannospalax munzuri village (38o06'N 37o53'E) 2 ƃƃ; (7) and 2n = 54 N. tuncelicus were reported by Malatya – Kale - øzol (38o24'N 38o45'E) 2 Coúkun (2004). ƃƃ, 1ƂƂ; (8) Elazı÷ - Keban - Çirkan vil- This study aimed to describe the Nanno- lage (38o46'N 38o46'E); 1 ƂƂ, 1ƃƃ; (9) spalax karyotypes from the Central East Erzincan - Kemaliye - Esentepe village Anatolian region, for which there still was (39o16'N 38o29'E) 1ƃƃ; (10) Tunceli - Ho- lack of sound information. zat - Akmezra village (39o05'N 39o13'E) Between 2006 and 2009, twenty mole rats 1ƂƂ, 1ƃƃ; (11) Tunceli – Pülümür - Kan- were trapped in their burrows in 11 differ- gallı village (39o27'N 39o51'E) 2Ƃ Ƃ, 1ƃƃ. ent locations of Central East Anatolia, a On the whole six different chromosomal region characterized by high mountains (up populations from the Central East Anato- to 3200 m a.s.l.) and large undulating pla- lian region were identified (Fig. 1) and teaus between 900 and 2100 m a.s.l.. their diagnostic features described (Tab. 1). Chromosomes were extracted from bone Three belonged to N. nehringi, one to N. marrow cell suspensions stained with a 4% ehrenbergi, one to N. munzuri and one to Giemsa solution, by a standard air drying N. tuncelicus. The presence of two chromo- method modified from Lee and Elder somal forms previously described in (1980). Karyotypes were arranged in pairs Malatya province, 2n = 60a (Gülkaç and according to their size and centromere posi- Yüksel, 1989; Ulutürk et al., 2009) and 2n tion from the best metaphase spreads. The = 60b (Yüksel, 1984) was confirmed. fundamental number of chromosome arms These two forms seem to be separated by (NF) and autosomal number of chromo- the River Tohma. some arms (NFa) were computed by count- The karyotypes of six specimens from four ing bi-armed autosomes as two arms and localities (1-4) belonged to the first form ( acrocentric autosomes as one arm. The 2n = 60a) and showed NF = 82 and NFa = morphology of the chromosomes was iden- 78. Their karyotypes consisted of 10 pairs tified according to Levan et al. (1964). of meta- and submetacentric autosomes and

90 Karyotypes of Nannospalax inTurkey

Figure 1 - Sampling localities and geographical distribution of chromosomal forms in the region. (1) Sivas - Divri÷i - Hıdırlık village, (2) Erzincan - Kemaliye - Dutluca village, (3) Erzincan - Kemaliye - Çitköy village, (4) Elazı÷ - Keban - Denizli village, (5) Malatya – Akçada÷ - Kürecik Road, (6) Malatya – Do÷anúehir - Örnek village, (7) Malatya – Kale – øzol, (8) Elazı÷ - Keban - Çirkan village, (9) Erzincan – Kemaliye - Esentepe village, (10) Tunceli - - Akmezra village, (11) Tunceli – Pülümür - Kangallı village.

19 pairs of acrocentric ones. The X chro- tric (Fig. 2B). mosomes were large and submetacentric Our results agreed with those of Nevo et al. (Fig. 2A), whereas the Y chromosome was (1995) and Ivanitskaya et al. (1997), whilst very small and acrocentric. differed from the karyotypes (2n = 60, NF The karyotypes of six specimens from three = 80 and NFa = 76) described by Yüksel localities (5-7) had 2n = 60b, NF = 78 and (1984) and Gülkaç and Yüksel (1989). NFa = 74. Their karyotypes consisted of 8 Two specimens from Çirkan village pairs of meta- and submetacentric auto- (Elazı÷-Keban province, locality 8) be- somes and 21 pairs of acrocentric ones. The longed to N. ehrenbergi, showing 2n = 52, X chromosomes were small and submeta- NF = 76 and NFa = 72 (Fig. 2C). The auto- centric, whereas the Y somal complement consisted of 11 meta- chromosome was very small and acrocen- and submetacentric and 14 acrocentric pairs.

91 Coúkun et al.

Table 1 - Chromosomal records of Nannospalax from the Central-, Turkey (sm: submetacentric, st: subtelocentric, a: acrocentric, m: metacentric, 2n: diploid chromosome number, NF: chromosome arm number, NFa: fundamental (autosomal) number (ƂƂ).

Autosome Gonosomes Population Locality 2n NFa NF References m/sm/sit a X Y Arguvan st Gülkaç & Yüksel, 1989

Hekimhan Malatya Arguvan Ulutürk et al., 2009

Arapgir

2n=60a Elazı÷ Keban-Denizli 60 10 19 78 82 sm a Çitköy This study Erzincan Kemaliye Dutluca Divri÷i-Karasar Ulutürk et al., 2009 Sivas -Davuto÷lu Divri÷i-Hıdırlık This study Yazıhan Yüksel, 1984 60 9 20 76 80 sm st Akçada÷ Gülkaç & Yüksel, 1989 30 km W of Malatya Nevo et al., 1995

2n=60b Malatya 12 km E of Malatya Ivanitskaya et al., 1997

Do÷anúehir-Örnek 60 8 21 74 78 sm a

Kale-øzol This study Akçada÷-Kürecik st Yüksel, 1984

Sivrice Ivanitskaya et al., 1997 2n=52 Elazı÷ 52 11 14 72 76 sm Gözeli a Coúkun et al., 2006 Keban-Çirkan This study

Tunceli Ovacık Coúkun, 2004 2n=58 58 4 24 64 68 sm a Erzincan Kemaliye-Esentepe This study

Kovancılar Elazı÷ Palu

Kocakoç Coúkun, 2004 2n=54 54 9 17 70 74 sm a Tunceli Niúantaúı Hozat-Akmezra This study

2n=49 Tunceli Pülümür-Kangallı 49 12+1 11 72 76 sm a This study

92 Karyotypes of Nannospalax inTurkey

Figure 2 - Karyotypes of Nannospalax populations from central-eastern Anatolia. (A) 2n = 60a, (B) 2n = 60b, (C) 2n = 52, (D) 2n = 58, (E) 2n = 54, (F) 2n = 49.

The submetacentric X chromosomes and N. ehrenbergi is widespread in Southeast- the acrocentric Y chromosome were both ern Anatolia. small-sized. The karyotypes resulted iden- N. munzuri (2n = 58, NF = 68, NFa = 64) tical to those described by Yüksel (1984) was found on the eastern bank of the River and Coúkun et al. (2006) from Elazı÷, , Esentepe village (Erzincan- Ivanitskaya et al. (1997) from Elazı÷ and Kemaliye province, locality 9). Till now ùanlıurfa, Gülkaç and Yüksel (1989) from this species had been described only from Adıyaman and , Nevo et al. (1995) Tunceli – Ovacık (Coúkun, 2004). The from Diyarbakır, Coúkun (1998) from river probably acts as a geographic barrier ùırnak, suggesting that the 2n = 52 form of between 2n = 60a and 2n = 58 chromoso-

93 Coúkun et al. mal forms (Fig. 1). The autosomal com- of biarmed chromosomes. The results of plement consisted of 4 meta- and submeta- this study expanded the range of the 2n = centric and 24 acrocentric pairs. The X 52 chromosomal form of N. ehrenbergi to chromosomes were small sized and meta- the Lake and possibly ex- centric, while the small Y chromosome was tended the list of karyotypes of Nanno- acrocentric (Fig. 2D). spalax with one new form from Central The karyotypes of two specimens from East Anatolia, although further evidence Akmezra village (Tunceli-Hozat province, needs to be collected. Nevo et al. (1988, locality10) belonged to N. tuncelicus, 1995) pointed out that each chromosomal showing 2n = 54, NF = 74 and NFa = 70. form could be assigned to a separate bio- Their karyotypes consisted of 9 pairs of logical species, inhabiting a specific eco- meta- submetacentric and 17 pairs of acro- geographical region. According to this hy- centric autosomes (Fig. 2E). The X chro- pothesis, there presumably are about 30 mosomes were large and submetacentric, such species in Turkey. Our results suggest whereas the small Y chromosome was ac- that adaptive differentiation and speciation rocentric. are still in progress. The NF and NFa values of this population were different from those described by ACKNOWLEDGEMENTS Nevo et al. (1995) from , whilst agreed with those reported by Coúkun This study was partly supported by the Sci- (2004) from Bingöl, Elazı÷ and Tunceli entific and Technical Research Council of and, except for the morphology of the Y Turkey (TÜBøTAK-Project No. 105T192). chromosome, those recorded by Yüksel and Gülkaç (2001) from Kızılırmak Basin. REFERENCES The karyotypes of three specimens from Kangallı village, 20 km south of Pülümür Coúkun Y. 1996. A new subspecies of (Tunceli-Pülümür province, locality 11), Nannospalax nehringi (Satunin, 1898) showed 2n = 49, NF = 76 and NFa = 72. (Rodentia: Spalacidae) from Turkey. Their karyotypes consisted of 12 pairs and Säugetierkundliche Mitteilungen, 37: 1 univalent meta- submetacentric auto- 103-109. somes and 11 pairs of acrocentric ones. The Coúkun Y. 1998. Morphological and X chromosomes were large and submeta- Karyological characteristics of the centric, whereas the Y chromosome was species, Spalax ehrenbergi, Nehring small and acrocentric (Fig. 2F). Consider- 1897 (Rodentia: Spalacidae) from ing that, to our knowledge, there is no con- ùırnak province. XIV. National Bio- tact between the current ranges of the two logical Congress, 3: 114-122 (in Turk- forms 2n = 50 and 2n = 48, the karyotype ish). could represents a cytogenetically distinct Coúkun Y. 2003. A study on the morphol- taxon, characterised by a high percentage ogy and karyology of Nannospalax

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