Cytogenetics Study and Characterization of Sumatra Serow, Capricornis Sumatraensis (Artiodactyla, Bovidae) by Classical and FISH Techniques

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Cytogenetics Study and Characterization of Sumatra Serow, Capricornis sumatraensis (Artiodactyla, Bovidae) by Classical and FISH Techniques

Sitthisak Jantarat1, Alongklod Tanomtong2*, Isara Patawang3, Somkid Chaiphech4, Sukjai Rattanayuvakorn5 and Krit Phintong6

1 Biology Program, Department of Science, Faculty of Science and Technology, Prince of Songkla University (Pattani), Pattanee, Muang 94000, Thailand 2 Toxic Substances in Livestock and Aquatic Animals Research Group, Department of Biology, Faculty of Science, Khon Kaen University, Khon Kaen, Muang 40002, Thailand 3 Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, Muang 50200, Thailand 4 Department of Animal Science, Rajamangala University of Technology Srivijaya Nakhonsrithammarat Campus, Nakhonsrithammarat, Thungyai 80240, Thailand 5 Department of Science and Mathematics, Faculty of Agriculture and Technology, Rajamangala University of Technology Isan, Surin Campus, Surin, Muang 32000, Thailand 6 Department of Fundamental Science, Faculty of Science and Technology, Surindra Rajabhat University, Surin, Muang 32000, Thailand

Received April 19, 2016; accepted December 10, 2016

Summary Karyological analysis in the Sumatra serow (Capricornis sumatraensis) from Thailand were conduct- ed. Blood samples were taken from two male and two female serows. After standard whole blood lymphocytes had been cultured at 37°C for 72 h in the presence of colchicine, metaphase spreads were performed on microscopic slides and air-dried. Conventional, GTG-, high-resolution, Ag-NOR banding and ﬂuorescence in situ hybridization (FISH) were applied to stain the chromosomes. The results showed that the diploid chromosome number of C. sumatraensis was 2n=48 and the fundamental number (NF) for both sexes were 60. The types of autosomes were 2 large metacentric, 4 large submetacentric, 2 large acrocentric, 2 medium telocentric, 4 small submetacentric and 32 small telocentric chromosomes. The X chromosome was a medium telocentric chromosome and the Y chromosome was a smallest telocentric chromosome. From the GTG-banding and high-resolution techniques, the numbers of bands in the C. sumatraensis were 147 and 207, respectively, and each chromosome pair could be clearly differentiated. In addition, the long arm near telomere (subtelomeric region) of chromosome pairs 2, 3 and 4 showed clearly observable heteromorphic nucleolar organization regions (NORs) (2a2b, 3a3b, 4a4b). This is the

ﬁrst report on natural polymorphism of NORs. The microsatellites d(AC)15 accumulated at the telomeres of several pairs and interstitial sites of some chromosomes. The microsatellites d(CGG)10 highly accumulated at the correspondence sites of NORs. FISH with the telomeric probe revealed hybridization signals on each telomere of all chromosomes and interstitial telomeric sites were not detected. The karyotype formula could be deduced as: m sm a t sm t 2n (diploid) 48=L2422432 +L +L +M +S +S +sex-chromosomes

Key words Karyotype, Chromosome, Capricornis sumatraensis, Polymorphism.

The Sumatra serow (Capricornis sumatraensis) is rather short bodied, long-legged goat antelopes, and a classiﬁed under the order Artiodactyla, family Bo- short, thick neck. The coat is coarse and rather thin, the vidae, subfamilies Caprinae. All six species of serow, upper parts are usually black or grayish, with the legs namely, Japanese serow (Capricornis crispus), Tai- below the knees widely variable in color from black to wan serow (C. swinhoei), C. sumatraensis, Chinese gray. The lips are white and there is often a rufous or serow (C. milneedwardsii), red serow (C. rubidus) and white patch under the throat. The ears are long, nar- Himalayan serow (C. thar), were until recently also row and pointed, dark behind and white on the inner classiﬁed under genus Naemorhedus, which now only surface. The horns are rather thick, slightly curved and contains the gorals. They live in central or eastern Asia short with a record length of 280 mm, and the basal por- (Wilson and Reeder 2005). tion has numerous thin rings. The horns of females are The general characteristics of the C. sumatraensi are: shorter (25–50 mm), slightly thinner and less corrugated than those of males. The hoofs are short and solid with * Corresponding author, e-mail: [email protected] pedal glands on all four feet. There is also a well-devel- DOI: 10.1508/cytologia.82.127 oped facial gland located about 40 mm below the eye; the 128 S. Jantarat et al. Cytologia 82(2)

Fig. 1. General characteristics of Sumatra serow, Capricornis sumatraensis (Artiodactyla, Bovidae, Caprinae).

Fig. 2. Metaphase chromosome plates and karyotypes of male (A) and female (B) Sumatra serow (Capricornis sumatraensis), 2n=48 by conventional straining technique (scale bars=10 µm).

Table 1. Review of cytogenetic reports of the genus Capriconis (Artiodactyla, Bovidae).

Species 2n NF m sm a t X Y NORs Reference

C. crispus 50 60 10 0 38 0 a a ̶ Benirschke et al. (1972) C. sumatraensis 46 58 10 0 34 0 m m ̶ Fischer and Höhn (1972) 48 60 12 0 34 0 a a ̶ Soma et al. (1982) 48 ̶ ̶ ̶ ̶ ̶ ̶ ̶ ̶ Huang et al. (2005) 48 60 2 8 2 34 t t 2, 3, 4 Present study C. swinhoei 50 60 10 0 38 0 a a ̶ Soma et al. (1981)

Notes: 2n=diploid chromosome number, NF=fundamental number (number of chromosome arm), m=metacentric, sm=submetacentric, a=acrocentric, t=telocentric chromosome, X=X-chromosome, Y=Y-chromosome, NORs=nucleolar organizer regions and ̶=not available. 2017 Cytogenetics Study and Characterization of Sumatra Serow, Capricornis sumatraensis (Artiodactyla, Bovidae) by Classical and FISH Techniques 129

Fig. 3. Metaphase chromosome plates and karyotypes of male (A) and female (B) Sumatra serow (Capricornis sumatraensis), 2n=48 by GTG-banding technique (scale bars=10 µm). opening is not closed by a flap of skin as in sheep and ies on taxonomy and evolutionary relationships of this gazelles but is filled with numerous short hairs (Lekagul genus. Moreover, it provides useful basic information for and McNeely 1988) (Fig. 1). conservation and breeding practices, as well as for stud- The standardized karyotypes of cattle, buffalo, sheep ies on the chromosome evolution of this serow. and goat, which are the main domestic animals in the family Bovidae have been investigated by many workers Materials and methods using G-, C-, R-, Ag-NOR banding and high-resolution techniques (Di Berardino et al. 1990, Hayes et al. 1993, Blood samples of the C. sumatraensis (two males Kaftanovskaya and Serov 1994, Iannuzzi et al. 1995, and two female) were collected from Phang Nga Wild- Jantarat et al. 2009, Supanuam et al. 2010, Kenthao life Breeding Center, Thailand and then applied to et al. 2012), reflecting their economic importance. Re- cytogenetic studies by lymphocyte culture of whole cently, karyotypes of wild bovid have been reported. blood samples. The culture cells were treated with a Their bi-armed chromosomes are the result of Robertso- colchicine-hypotonic-fixation-air-drying technique fol- nian translocation or centric fusion (Cribiu et al. 1990, lowed by conventional staining, GTG-, high-resolution Claro et al. 1996, Robinson et al. 1996, Oh et al. 2011, and Ag-NOR banding techniques (Rooney 2001) as well Gomontean et al. 2009, Tanomtong et al. 2011). In genus as dual-color fluorescence in situ hybridization (FISH)

Capricornis, cytogenetic studies have been performed to detect the microsatellites d(AC)15, d(CGG)10 and telo- in three species, including C. crispus (Benirschke et al. mere sites. FISH was performed under high stringency 1972), C. sumatraensis (Fischer and Höhn 1972, Soma conditions on mitotic chromosome spreads (Pinkel et al. et al. 1982, Huang et al. 2005) and C. swinhoei (Soma 1986, Liehr 2009). For 20 cells of each individual chro- et al. 1981) (Table 1). Most of these species have 2n=48 mosome, checks, length measurements, karotyping and or 50 chromosomes consisting of bi-armed and mono- idiograming were accomplished by using a light micro- armed chromosomes. scope as previously described (Chaiyasut 1989). In the present article, we indicate the first finding of NOR polymorphism and chromosome analysis in the Results and discussion C. sumatraensis from Thailand. We provide the very first report on chromosome standardization, including Cytogenetic study of C. sumatraensis using lympho- chromosome measurements of shape and size, karyotype cyte culture demonstrated that the chromosome number formulation, and idiograming. The results obtained can is 2n (diploid)=48 (Fig. 2). This is the same chromosome provide more cytogenetic information for future stud- number for the C. sumatraensis as reported in previous 130 S. Jantarat et al. Cytologia 82(2)

Fig. 4. Prometaphase chromosome plates and karyotypes of male (A) and female (B) Sumatra serow (Capricornis sumatraensis), 2n=48 by high-resolution GTG-banding technique (scale bars=10 µm). studies (Soma et al. 1982, Huang et al. 2005). These mosome was a medium telocentric chromosome and the features are differences to that reported by Fischer and Y chromosome was the smallest telocentric chromo- Höhn (1972) indicating that C. sumatraensis had 2n=46. some. These features are differences to that reported The fundamental number (NF, number of chromosome by Soma et al. (1982) indicating that a C. sumatraensis arms) was 60 in both male and female, which is the same had an acrocentric X-chromosome and an acrocentric Y- as the report of Soma et al. (1982). According to the chromosome. Furthermore, Fischer and Höhn (1972) also chromosome characteristics of others in family Bovidae, reported that the sex chromosome of the C. sumatraensis gaur (2n=58, NF=58), banteng (2n=60, NF=58), cattle, had a metacentric X chromosome and a metacentric Y B. taurus (2n=60, NF=58), swamp buffalo (2n=48, chromosome. An important karyotypic difference be- NF=56), river buffalo (2n=50, NF=58), goat (2n=60, tween bovine and ovine species is the different shape of NF=58) sheep (2n=54, NF=58) and goral (2n=56, the X chromosomes. While those of cattle are submeta- NF=60), all of them have the range of 2n=48–60 and centric, X chromosomes in goat and sheep are acrocen- most have NF=58, except in swamp buffalo that has tric with short arms (Huang et al. 2005). NF=56 which its chromosome pair 1 derived from tan- The GTG-banded metaphase and high-resolution dem fusion of chromosome pair 4 and 9 of river buffalo GTG-banded prometaphase of the examined male and (Di Berardino and Iannuzzi 1981). female serows presented different chromosome lengths C. sumatraensis autosomes consist of 2 large meta- (Figs. 3 and 4). The autosomes of the serow were ar- centric, 4 large submetacentric, 2 large acrocentric, ranged according to decreasing size from chromosome 2 medium telocentric, 4 small submetacentric and 32 pair 1 to 23, and the karyotype was made with a single small telocentric chromosomes (2m+8sm+2a+34t). Dif- metaphase plate. The last small chromosomes (number ference chromosomal features were reported by Soma 19, 20, 21, 22 and 23) were difficult to identify because et al. (1982), which indicated that the C. sumatraensis of their similar band patterns. As these band patterns had 12 metacentric and 34 acrocentric chromosomes. differed depending on chromosome length, it was dif- As for the sex chromosome of this study, the X chro- ficult to find an overall band similarity between serow 2017 Cytogenetics Study and Characterization of Sumatra Serow, Capricornis sumatraensis (Artiodactyla, Bovidae) by Classical and FISH Techniques 131

Fig. 5. Metaphase chromosome plates and karyotypes of male Sumatra serow (Capricornis sumatraensis), 2n=48 by Ag-NOR banding technique. The q-arm of metacentric chromosome pair 2a, the q-arm of submetacentric chromosome pair 3a and the q-arm of acrocentric chromosome pair 4a showed clearly observable heteromorphic NORs (scale bars=10 µm). and goat. Studies have established a high degree of Yunis and Prakash (1982), which reported that the chro- similarity in the banding patterns of the Bovidae species mosome band number from the high-resolution tech- (Gallagher and Womack 1992, Hayes et al. 1991, Oh nique of prometaphase chromosomes is over 1000 bands et al. 2011). The conservation of band patterns indicates per haploid set. In this study, the chromosome scoring is that karyotype evolution has occurred by centric fusion done only with clearly visible bands, except for variable (Chowdhary et al. 1991, Hayes et al. 1991, Iannuzzi bands due to the small number of scored bands. et al. 1991, Oh et al. 2011). In Bovidae, it was reported For this case, the NORs of C. sumatraensis performed that chromosomes with Robertsonian translocation lost by the Ag-NOR staining technique are in the ﬁrst report centric heterochromatin during the course of the centric (Fig. 5). In C. sumatraensis, we found that the long arm fusion in the evolution (Iannuzzi et al. 1991). However, subtelomeric regions of the metacentric chromosome in serow, the present study revealed no evidence of Rob- pair 2a, submetacentric chromosome pair 3a and ac- ertsonian translocation (centric fusion). rocentric chromosome pair 4a have clearly observable The GTG-banding technique revealed that the number heteromorphic NORs (2a2b, 3a3b and 4a4b) in male. of GTG-bands on one set of haploid chromosomes (n), There also is the possibility that NOR site variations which includes autosomes, and the X and Y chromo- could prove useful as phyletic or systematic markers. somes, is 147 bands for the C. sumatraensis. The num- NORs have repetitive DNA that function in rRNA syn- ber of bands in one set of prometaphase haploid chromo- thesis, so the increase or decrease in the size of NORs somes from the high-resolution technique is 207. This in C. sumatraensis might inﬂuence the gene in protein can be compared with the study in human and apes by synthesis. There was polymorphism in macaques (genus 132 S. Jantarat et al. Cytologia 82(2)

Fig. 6. Fluorescence in situ hybridization with various repetitive DNA probes, including microsatellites d(AC)15 probe (A), d(CGG)10 probe (B) and telomere probe (C) on metaphase chromosomes of the male Sumatra serow (Capricornis sumatraensis), 2n=48, scale bars indicate 10 µm.

Macaca) from the report of Warburton et al. (1975). In sites were not detected (Fig. 6). addition, the report of Tantravahi et al. (1976) indicated In this paper, we present the chromosomal character- the presence of NORs on human chromosomes 13, 14, istics of male and female serows in Thailand. While se- 15, 21, 22 and also found that human satellite chromo- row is a member of the family Bovidae, it does not share somes have polymorphism by NOR-banding technique. any of the common chromosomal characteristics of this Microsatellites are usually located in the heterochro- group. Groves and Grubb (1985) suggested that goral matic regions (telomeres/centromeres) of mammal ge- and serow should be assigned to one genus on the basis nomes. The microsatellites d(CA)15 and d(CGG)10 probe, of morphological analysis, but the present study offers were used as probes and were synthesized as described no cytogenetic evidence to support their case. by Kubat et al. (2008). These sequences were directly The length in centimeters of the chromosomes in labeled with Cy3 at the 5′ terminus during synthesis mitotic metaphase cells for 20 cells were measured in by Sigma (St. Louis, MO, USA). The microsatellites males and females. The mean of length short arm chro- d(AC)15 probe accumulated at the telomeres of several mosome (Ls), length long arm chromosome (Ll), length pairs and interstitial sites of some chromosomes (chro- total arm chromosome (LT), relative length (RL), cen- mosomes pairs 1, 11, 12, 18 and the X-chromosome). tromeric index (CI), standard deviation (SD) of RL, CI,

The microsatellites d(CGG)10 probe highly accumulated size and type of chromosome in male and female of the at the correspondence sites of NORs (chromosome pair serow are shown in Table 2. The idiogram demonstrates 2, 3 and 4). FISH with the telomeric probe revealed hy- a continuous length gradation of chromosomes. The size bridization signals on each telomere of all chromosomes difference of the largest and the smallest chromosomes (except the Y-chromosome) and interstitial telomeric is approximately 11-fold. The important karyotype fea- 2017 Cytogenetics Study and Characterization of Sumatra Serow, Capricornis sumatraensis (Artiodactyla, Bovidae) by Classical and FISH Techniques 133

Table 2. Mean of length short arm chromosomes (Ls), length long arm chromosomes (Ll), length total arm chromosomes (LT), relative length (RL), centromeric index (CI) and standard deviation (SD) of RL, CI from metaphase chromosomes in 20 cells of male and female Su- matra serow (Capricornis sumatraensis), 2n (diploid)=48.

Chro. pair Ls Ll LT RL±SD CI±SD Chro. size Chro. type

1 77.177 115.587 192.764 0.046±0.003 0.600±0.057 Large Submetacentric 2* 78.019 100.950 178.969 0.043±0.004 0.564±0.066 Large Metacentric 3* 45.472 102.481 147.953 0.035±0.004 0.694±0.106 Large Submetacentric 4* 36.536 91.817 128.353 0.031±0.003 0.716±0.045 Large Acrocentric 5 0.000 98.870 98.870 0.023±0.005 1.000±0.000 Medium Telocentric 6 0.000 91.549 91.549 0.022±0.003 1.000±0.000 Small Telocentric 7 0.000 86.835 86.835 0.021±0.002 1.000±0.000 Small Telocentric 8 34.109 52.230 86.338 0.021±0.004 0.601±0.097 Small Submetacentric 9 0.000 81.342 81.342 0.019±0.002 1.000±0.000 Small Telocentric 10 0.000 75.897 75.897 0.018±0.001 1.000±0.000 Small Telocentric 11 29.628 45.722 75.350 0.018±0.002 0.601±0.119 Small Submetacentric 12 0.000 72.983 72.983 0.017±0.001 1.000±0.000 Small Telocentric 13 0.000 70.068 70.068 0.017±0.001 1.000±0.000 Small Telocentric 14 0.000 67.225 67.225 0.016±0.001 1.000±0.000 Small Telocentric 15 0.000 65.269 65.269 0.016±0.001 1.000±0.000 Small Telocentric 16 0.000 62.487 62.487 0.015±0.001 1.000±0.000 Small Telocentric 17 0.000 59.842 59.842 0.014±0.001 1.000±0.000 Small Telocentric 18 0.000 57.465 57.465 0.014±0.002 1.000±0.000 Small Telocentric 19 0.000 55.249 55.249 0.013±0.002 1.000±0.000 Small Telocentric 20 0.000 53.184 53.184 0.013±0.002 1.000±0.000 Small Telocentric 21 0.000 50.837 50.837 0.012±0.002 1.000±0.000 Small Telocentric 22 0.000 47.389 47.389 0.011±0.002 1.000±0.000 Small Telocentric 23 0.000 42.370 42.370 0.010±0.002 1.000±0.000 Small Telocentric X 0.000 110.729 101.502 0.024±0.010 1.000±0.389 Medium Telocentric Y 0.000 33.100 16.550 0.003±0.003 1.000±0.000 Small Telocentric

Remarks: Chro.=chromosome and *=Nucleolar organizer region/NOR.

Fig. 7. Idiogram showing lengths and shapes of chromosomes of Sumatra serow (Capricornis sumatraensis), 2n=48 by con- Fig. 8. Idiogram of Sumatra serow (Capricornis sumatraensis), ventional staining technique. 2n=48 by GTG-banding technique. ture is the asymmetrical karyotype, which was found in ed and high-resolution GTG-banded with landmarks, four types of chromosomes (metacentric, submetacen- regions, bands and sub-bands. The karyotype formula of tric, acrocentric and telocentric chromosomes). Fig. 7 C. sumatraensis was as follows: m sm a t sm t shows the idiogram of C. sumatraensis from convention- 2n (diploid) 48 = L 2 +L4 +L2+M2+S4 +S32 al, while Figs. 8 and 9 show idiograms from GTG-band- +sex-chromosomes 134 S. Jantarat et al. Cytologia 82(2)

Gallagher, D. S. Jr. and Womack, J. E. 1992. Chromosome conservation in the Bovidae. J. Hered. 83: 287–298. Gomontean, B., Tanomtong, A., Kakampuy, W. and Chaveerach, A. 2009. A novel Robertsonian translocation [57,rob(1/29)(4/28)] and polymorphism of nucleolar organizer regions (NORs) of captive Thai banteng (Bos javanicus birmanicus). Cytologia 74: 427–436. Groves, C. P. and Grubb, P. 1985. Reclassification of the Serows and Gorals (Nemorhaedus: Bovidae). In: Lovari, S. (ed.). The Biology and Management of Mountain Ungulates. Croom Helm, London. pp. 45–50. Hayes, H., Petit, E., Bouniol, C. and Popescu, C. P. 1993. Localiza- tion of the α-S2-casein gene (CASAS2) to the homologous cattle, sheep and goat chromosome 4 by in situ hybridization. Cyto- genet. Cell Genet. 64: 281–285. Hayes, H., Petit, E. and Dutrillaux, B. 1991. Comparison of RBG- banded karyotypes of cattle, sheep, and goats. Cytogenet. Cell Genet. 57: 51–55. Huang, L., Nie, W., Wang, J., Su, W. and Yang, F. 2005. Phylogenomic study of the subfamily Caprinae by cross-species chromosome painting with Chinese muntjac paints. Chromosome Res. 13: 389–399. Iannuzzi, L., Di Meo, G. P., Perucatti, A. and Ferrara, L. 1995. G- and R-banding comparison of sheep (Ovis aries L.) chromosomes. Fig. 9. Idiogram of Sumatra serow (Capricornis sumatraensis), Cytogenet. Cell Genet. 68: 85–90. 2n=48 by high-resolution GTG-banding technique. Iannuzzi, L., Di Meo, G. P., Perucatti, A., Ferrara, L. and Gustavs- son, I. 1991. Sister chromatid exchange in chromosomes of cattle from three different breeds reared under similar conditions. Acknowledgements Hereditas 114: 201–205. Jantarat, S., Tanomtong, A., Kakampuy, W., Kaewsri, S. and Buran- The authors are grateful to thank Toxic Substances arom, K. 2009. Standardized karyotype and idiogram of Thai’s in Livestock and Aquatic Animals Research Group, native cattle, Bos indicus (Artiodactyla, Bovidae) by convention- Khon Kaen University and Faculty of Science and Tech- al staining, G-banding, C-banding and NOR-banding techniques. Thai J. Genet. 2: 164–174. nology, Prince of Songkla University (Pattani) for the Kaftanovskaya, H. M. and Serov, O. L. 1994. High-resolution GTG- financial support. banded chromosomes of cattle, sheep, and goat: A comparative study. J. Hered. 85: 395–400. References Kenthao, A., Tanomtong, A., Supanuam, P., Pinyoteppratan, C., Muangprom, P., Buranarom, K. and Sanoamuang, L. 2012. Stan- dardized karyotype and idiogram of Mehsani buffaloes, Bubalus Benirschke, K., Soma, H. and Ito, T. 1972. The chromosomes of the bubalis by conventional staining, GTG-banding, CBG-banding Japanese serow, Capricornis crispus (Temminck). Proc. Jpn. and Ag-NOR banding techniques. Buffalo Bull. 31: 24–39. Acad., Ser. B, Phys. Biol. Sci. 48: 608–612. Kubat, Z., Hobza, R., Vyskot, B. and Kejnovsky, E. 2008. Microsat- Chaiyasut, K. 1989. Cytogenetics and Cytotaxonomy of the Family ellite accumulation on the Y chromosome of Silene latifolia. Zephyranthes. Department of Botany, Faculty of Science, Chul- Genome 51: 350–356. alongkorn University, Bangkok, Thailand. Lekagul, B. and McNeely, J. A. 1988. Mammals of Thailand. 2nd edi- Chowdhary, B. P., Harbitz, I., Davies, W. and Gustavsson, I. 1991. tion, Association for the Conservation of Wildlife, Bangkok. Chromosomal localization of the glucose phosphate isomerase Liehr, T. 2009. Fluorescence In Situ Hybridization (FISH) Application (GPI) gene in cattle, sheep and goat by in situ hybridization: Guide. Springer, Berlin. Chromosomal banding homology versus molecular conservation Oh, S. H., Yun, Y. M., Lee, J. E., Kim, I. Y., Shin, J. H., Kweon, O. in Bovidae. Hereditas 114: 161–170. K., Lee, H., Yoon, Y. S., Shin, N. S. and Seong, J. K. 2011. G-, Claro, F., Hayes, H. and Cribiu, E. P. 1996. The karyotype of the ad- R- and C-band patterns of goral (Nemorhaedus caudatus) and dax and its comparison with karyotypes of other species of Hip- comparison to goat (Capra hircus). Mol. Cells 31: 351–354. potraginae antelopes. Hereditas 124: 223–227. Pinkel, D., Straume, T. and Gray, J. 1986. Cytogenetic analysis using Cribiu, E. P., Asmonde, J. F., Durand, V., Greth, A. and Anagariyah, quantitative, high-sensitivity, fluorescence hybridization. Proc. S. 1990. Robertsonian chromosome polymorphism in the Ara- Natl. Acad. Sci. U.S.A. 83: 2934–2938. bian oryx (Oryx leucoryx). Cytogenet. Cell Genet. 54: 161–163. Robinson, T. J., Wilson, V., Gallagher, D. S. Jr., Taylor, J. F., Davis, S. Di Berardino, D., Hayes, H., Fries, R. and Long, S. 1990. Internation- K., Harrison, W. R. and Elder, F. F. 1996. Chromosomal evolu- al system for cytogenetic nomenclature of domestic animals. The tion in duiker antelope (Cephalophinae: Bovidae) karyotype Second International Conference on Standardization of Domestic comparisons, fluorescence in situ hybridization, and rampant X Animal Karyotypes, INRA, Jouy-en Josas, France, 22nd–26th chromosome variation. Cytogenet. Cell Genet. 73: 116–122. May, 1989. Cytogenet. Cell Genet. 53: 65–79. Rooney, D. E. 2001. Human Cytogenetics: Constitutional Analysis. Di Berardino, D. and Iannuzzi, L. 1981. Chromosome banding ho- Oxford University Press, Oxford. mologies in swamp and murrah buffalo. J. Hered. 72: 183–188. Soma, H., Kada, H., Matayoshi, K., Suzuki, Y., Meckvichal, C., Ma- Fischer, H. and Höhn, H. 1972. Der karyotype der serau (Capriconis hannop, A. and Vatanaromya, B. 1982. The chromosomes of the sumatraensis Bechstein, 1799). Giess Beitr Erbpath Zuchthyhyg Sumatran serow (Capriconis sumatraensis). Proc. Jpn. Acad., 4: 8–15. 2017 Cytogenetics Study and Characterization of Sumatra Serow, Capricornis sumatraensis (Artiodactyla, Bovidae) by Classical and FISH Techniques 135

Ser. B, Phys. Biol. Sci. 58: 265–269. readei) by conventional, GTG-banding, CBG-banding and Ag- Soma, H., Kada, H., Matayoshi, K., Ysai, M. T., Kiyokawa, T., Ito, T., NOR-banding techniques. Cytologia 76: 99–108. Wang, K. P., Chen, B. P. and Chen, S. C. 1981. Cytogenetic simi- Tantravahi, R., Miller, D. A., Dev, V. G. and Miller, O. J. 1976. Detec- larities between the Formosan serow (Capricornis swinhoei) and tion of nucleolus organizer regions in chromosomes of human, the Japanese serow (Capricornis crispus). Proc. Jpn. Acad., Ser. chimpanzee, gorilla, orangutan and gibbon. Chromosoma 56: B, Phys. Biol. Sci. 57: 254–259. 15–27. Supanuam, P., Tanomtong, A., Jantarat, S., Kakampuy, W., Kaewsri, Warburton, D., Henderson, A. S. and Atwood, K. C. 1975. Localiza- S. and Kenthao, A. 2010. Standardized karyotype and idiogram tion of rDNA and Giemsa-banded chromosome complement of of Thai native swamp buffalo, Bubalus bubalis (Artiodactyla, white-handed gibbon, Hylobates lar. Chromosoma 51: 35–40. Bovidae) by convention staining, G-banding, C-banding and Wilson, D. E. and Reeder, D. M. 2005. Mammal Species of the World. NOR-banding techniques. Thai J. Genet. 3: 83–93. 3rd edition, Johns Hopkins University Press, Baltimore. Tanomtong, A., Kakampuy, W., Suntararak, S., Thammarat, K., Yunis, J. J. and Prakash, O. 1982. The origin of man: A chromosome Kaewsri, S. and Kenthao, A. 2011. Robertsonian translocation pictorial legacy. Science 215: 1525–1530. [56, XX and 57, XY, rob(1; 29)] in captive Thai gaur (Bos gaurus