NORTH-WESTERN JOURNAL OF ZOOLOGY 9 (1): 57-62 ©NwjZ, Oradea, Romania, 2013 Article No.: 131701 http://biozoojournals.3x.ro/nwjz/index.html

Karyotypes of three gerbil of the genera Tatera and from Turkey and Senegal

Atilla ARSLAN1, Jan ZIMA2,*, Darina KOUBÍNOVÁ3, Tarkan YORULMAZ4, Kubilay TOYRAN5 and Serdar GÖZÜTOK6

1. Department of Biology, Faculty of Science, Selçuk University, 42031 Konya, Turkey. 2. Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, 603 65 Brno, Czech Republic. 3. Department of Zoology, Faculty of Science, Charles University, 128 44 Praha, Czech Republic. 4. Department of Biology, Faculty of Science, Çankırı Karatekin University, Çankırı, Turkey. 5. Department of Biology, Faculty of Science and Arts, Bitlis Eren University, Bitlis Turkey. 6. Department of Biology, Faculty of Science and Arts, Kırıkkale University, 71450 Kırıkkale, Turkey. *Corresponding author, J. Zima, e-mail: [email protected]

Received: 11. November 2011 / Accepted: 05. November 2012 / Available online: 27. December 2012 / Printed: June 2013

Abstract. In this study, we examined karyotypes of three gerbil species of the genera Tatera and Gerbilliscus. The diploid number of 68 chromosomes was confirmed in all specimens of Tatera indica examined from southeastern Anatolia in Turkey. The C-band positive regions were distributed in centromeric areas of all the autosomal pairs and the X chromosome. The Y chromosome was stained uniformly and C-positively. The active NORs were localized in three out of eight pairs of biarmed autosomes (NF=86). Conventionally stained karyotypes were studied in two species of Gerbilliscus from Senegal, western Africa. The female karyotype of G. gambianus contained 52 chromosomes including one large subtelocentric, six submetacentric and 19 acrocentric pairs (NF=66). The female karyotype of G. guineae contained 50 chromosomes including a large metacentric, eight submetacentric and 16 acrocentric autosomal pairs (NF=68). Minor differences in chromosome morphology were observed in these studied species in comparison with previously published data.

Keywords: cytogenetics, , Gerbillinae, Asia Minor, western Africa.

Introduction data has been obtained by Matthey (1953), Rao et al. (1968), Aswanthanaryana and Manjunatha The gerbils (: Gerbillinae) represent a (1981), and Yosida (1981). In Turkey, the conven- distinct group defined by a set of derived morpho- tionally stained karyotype of T. indica was de- logical traits (Musser & Carleton 2005). Pavlinov et scribed by Yiğit et al. (2001) from Ceylanpınar. al. (1990) recognized two lineages of extant gerbil However, information on differentially stained species designated as Taterillinae and Gerbillinae. chromosomes and detailed structure of the karyo- The genera Tatera and Gerbilliscus, previously type is still lacking in this species. considered congeneric, were included in the for- The Gerbilliscus, previously included as mer lineage. Pavlinov et al. (1990) and Pavlinov a part of the Tatera genus, consists of about 11 (2001) regarded true Tatera to consist only of single species. The western Africa Gerbilliscus species Asian species, and separated the African endemic reveal a relatively high level of karyotype variabil- genus Gerbilliscus, with as its closest ity (Colangelo et al. 2001, Volobouev et al. 2007). relative. The Asian Tatera and African Gerbilliscus The species studied by us belong to well- are differentiated by certain morphological traits supported western clade including G. gambianus, (Musser & Carleton, 2005), and also karyotypes G. guineae, G. kempi, and possibly other not yet (Rao et al. 1968, Yosida 1981, Qumsiyeh and described species (Colangelo et al. 2007, Volo- Schlitter 1991, Yiğit et al. 2001). Cytogenetic data bouev et al. 2007). The northern savanna gerbil, G. for gerbils were summarized by Viegas-Péquinot gambianus (Wroughton, 1906) was listed as G. et al. (1986) and Qumsiyeh & Schlitter (1991). kempi by Musser and Carleton (2005) but the spe- The , T. indica (Hardwicke, 1807) cies nomenclature was revised and proposed to be occurs from Mesopotamia across Iran, Afghani- changed by Colangelo et al. (2007) and Volobouev stan, and Pakistan to India and Sri Lanka. The et al. (2007). The species is distributed in a vast species is known from south-eastern Turkey in the range throughout Sub-Saharan northern savanna area between Akçakale and Ceylanpınar (in Şanlı- from western to eastern Africa. The karyotype was urfa), close to the Syrian border (Kryštufek & studied from Senegal, Niger, Chad, and Mali Vohralík 2009). A number of dispersed karyotypic (Matthey 1969, Hubert et al. 1973, Dobigny et al. 58 A. Arslan et al.

2002, Granjon & Dobigny 2003, Volobouev et al. Results 2007). The diploid number of 52 chromosomes was uniformly reported. The Guinean gerbil, G. The karyotype of T. indica consists of 68 chromo- guineae (Thomas, 1910), with the partly sympatric somes including eight bi-armed pairs and 25 acro- range, was recorded from Gambia and Senegal centric pairs of autosomes (NFa = 82). The X through Guinea, Sierra Leone, and southern Mali chromosome is large and metacentric, while the Y to Burkina Faso and Ghana (Musser and Carleton chromosome is small acrocentric (NF = 86) (Fig. 1). 2005). The karyotype of this species was examined The C-banded karyotype of this species is illus- in Burkina Faso and Mali (Matthey & Petter 1970, trated in Fig. 2. Most of the autosomes possess Benazzou et al. 1984, Volobouev et al. 2007) and distinct pericentromeric C-bands. The X chromo- the chromosome diploid number of 2n=50 was some has a centromeric C-positive band and the Y reported. Colangelo et al. (2001) and Volobouev et chromosome appears to be uniformly and C- al. (2007) performed comparative chromosome positively stained. By using silver-nitrate staining, banding analyses of the western African gerbils of NORs are localized in the secondary constrictions the genus Gerbilliscus. in the short arms of the three bi-armed pairs (nos. The aim of this study is to evaluate chromo- 1, 2, and 4). All the observed NORs are homomor- somal differences between the two genera studied, phic and occur in both the homologues (Fig. 3). and to contribute to karyotype faunistic mapping The female karyotype of G. gambianus (Fig. 4) of the three species examined. In this respect, this consists of 52 chromosome that can be differenti- study is continuation of our survey of cytogenetic ated into one large subtelocentric pair, six me- characteristics of from Asia Minor and dium-sized and small submetacentric pairs, and 19 western Africa (Koubínová et al. 2010, Arslan & acrocentric pairs (NF=66). The largest subtelocen- Zima 2011, Arslan et al. 2011a,b). Chromosomal tric pair can be tentatively designated as the X banding analysis of the karyotype of T. indica with chromosomes (NFa=62), based on the comparison the use of C-banding and Ag-NOR staining is with other published data. aimed to facilitate further comparative cytogenetic The female karyotype of G. guineae (Fig. 5) studies among gerbils. consists of 50 chromosomes including single large metacentric pair, eight submetacentric pairs, and 16 acrocentric pairs (NF=68). The largest metacen- Materials and methods tric pair can be tentatively designated as the X

chromosomes considering the published data on The specimens of T. indica (6 males and 4 females) were collected in the Ceylanpinar, Şanlıurfa Province, south- karyotypes of the species. Consequently, NFa is eastern Turkey (36° 51´ N, 40° 04´ E). Single female of G. 64. gambianus was collected in Diala Koto, south-eastern Senegal (13°18´ N, 13°16´ E). Two females of G. guineae originated from Dar Salam, Senegal (13°16´ N, 13°12´ E). Discussion All the were collected with the permission and under supervision of the Senegal’s National Parks Gen- Aside from the distinct karyotypic differences eral Management. Karyotype preparations were obtained from the bone between the genera Tatera and Gerbilliscus, which marrow of animals treated with colchicine (Ford and play a role in the generic division, these species Hamerton 1956). After preparation of chromosome slides, share common features which well illustrate their conventional Giemsa-staining was carried out. In T. in- common belonging to a clade based on mt DNA dica, constitutive heterochromatin and nucleolus organ- data (Colangelo et al. 2007). Contrary to differ- izer regions (NORs) were detected in individual auto- ences in their number of chromosomal arms (86 in somal and sex chromosome pairs via C-banding (Sumner Tatera vs. 60-68 in Gerbilliscus, cf. Qumsiyeh and 1972) and Ag-NOR staining (Howell and Black 1980), respectively. From each specimen, 4 to 20 slides were Schlitter 1991, Volobouev et al. 2007), there is a prepared, and at least 20 well-spread metaphase plates similar proportion of bi-armed and uni-armed were analysed. autosomes, as well as the large X chromosomes Standard voucher specimens (skins and skulls) are which usually represent the largest elements of the deposited in collections of the Department of Biology, complement. Both the studied species of Gerbillis- Faculty of Science, Selçuk University, Konya, Turkey (T. cus have similar karyotypes that differ in the cen- indica), and the Institute of Vertebrate Biology ASCR, tromere position on their largest chromosome Brno, Czech Republic (Gerbilliscus spp. ) (presumably the X chromosome) and in the pro-

Karyotypes of gerbils 59

Figure 1. Metaphase spread and male karyotype of Tatera indica (Turkey).

Figure 2. Metaphase spread and C-banded male karyotype of Tatera indica.

portion of the bi-armed and uni-armed chromo- gelo et al. 2001). somes. An autosomal fusion may be assumed as a Certain differences can be found between the mechanism of divergence between the autosomal results reported in this study and published re- complements of both the species (Volobouev et al. cords in individual species. Matthey (1953) re- 2007). The banding analyses showed that the ported diploid number of 72 chromosomes, and variation in the morphology of the X chromosome fundamental number of 80 chromosomal arms in may be related to a pericentric inversion (Colan- T. indica. Different findings were reported by Rao

60 A. Arslan et al.

Figure 3. Silver-stained metaphase spread and male karyotype of Tatera indica. Arrows indicate the position of active Ag-NORs.

Figure 4. Metaphase spread and female karyotype of Gerbilliscus gambianus (Senegal).

et al (1968), Yosida (1981), and Aswanthanaryana arms (NF = 80-86) in the Indian subspecies T. in- and Manjunatha (1981) from India who found 2n dica hardwickei. Yosida (1981) described the karyo- = 68 in the somatic cells of the species. Aswan- type containing eight bi-armed and 25 acrocentric thanaryana and Manjunatha (1981) further re- autosomal pairs (NF=86 and NFa=82), a large and ported variation in the number of chromosomal metacentric X chromosome, and an acrocentric Y Karyotypes of gerbils 61

Figure 5. Metaphase spread and female karyotype of Gerbilliscus guineae (Senegal).

chromosome as in our case. Rao et al (1968) re- T. indica, these NORs were located in telomeric corded NF= 84 and NFa= 80 in the subspecies T. position on biarmed autosomes. indica cuverii, and the same fundamental numbers Chromosomal studies of G. gambianus from were reported in populations examined from Tur- various parts of western Africa (Matthey & Petter key (Yiğit et al. 2001). The differences between 1970, Hubert et al. 1973, Dobigny et al. 2002, Gran- published data are therefore caused by variable jon & Dobigny 2003) revealed similar results as proportion of the bi-armed and uni-armed auto- those reported in this paper, but a different num- somes reported in individual papers. However, ber of autosomal arms was recorded. The com- this variation reveals no clear geographical pat- plement described in this study contains seven bi- tern, and could be influenced by varying interpre- armed autosomal pairs (NFa=62) compared to tation of individual authors. eight bi-armed pairs reported in other studies According to Yosida (1981), almost all auto- (NFa=64). This difference may be related to auto- somes of Indian gerbil had a small centromeric C- somal heteromorphism recorded in a bi-armed band, and the X and Y chromosomes were rather pair in certain Gerbilliscus species from western uniformly stained. The whole body of the Y chro- Africa (Colangelo et al. 2001, Volobouev et al. mosome was always stained heavily, but the C- 2007). However, the homologous chromosomes in staining pattern of the X was somewhat variable. this heteromorphic pair were usually bi-armed In most cells, both arms of the X were also inten- (Volobouev et al. 2007), and the exact mechanism sively stained. This pattern of C-banding is con- of the observed variation thus remains unknown. gruent with our findings in the autosomal com- Certain differences between the published results plement but certain differences are indicated in can be found also in the centromere position in the staining of the X chromosome. Similar C-banding X chromosome (e. g., Matthey & Petter 1970), pattern with the positive regions in centromeric however, these differences may be explained by position in all autosomes was recorded also in the presumed misidentification of the sex chromo- Gerbilliscus species (Colangelo et al. 2001, Volo- somes (Volobouev et al. 2007). bouev et al. 2007). There are only few data about The data on the karyotype of G. guineae (Mat- the distribution of NORs in the karyotype of ger- they & Petter 1970, Benazzou et al. 1984, Volo- bils. Colangelo et al. (2001) reported the maximum bouev et al. 2007) are similar to the results re- number of four NORs in G. kempi. Similarly as in ported in this paper (2n=50, NF=68, NFa=64). We

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