Chromosome Homologies Between Tsessebe (Damaliscus Lunatus

Original Article

Cytogenet Genome Res 322821 Accepted: September 15, 2010 DOI: 10.1159/000322821 b y M . S c h m i d Published online: $ $ $

Chromosome Homologies between Tsessebe (Damaliscus lunatus) and Chinese muntjac (Muntiacus reevesi) Facilitate Tracing the Evolutionary History of Damaliscus (Bovidae, Antilopinae, Alcelaphini)

a a b c d L. Huang M. Jing W. Nie T.J. Robinson F. Yang

a b College of Life Sciences, Ludong University, Yantai , and State Key Laboratory of Genetic Resources and Evolution, c Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming , PR China; Evolutionary Genomics Group, d Department of Botany and Zoology, University of Stellenbosch, Stellenbosch, South Africa; Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton , UK

Key Words relationships of 3 species reflected by specific chromosomal -Chromosome painting ؒ Damaliscus lunatus ؒ Karyotype rearrangements were consistent with published phyloge evolution ؒ Rb fusion nies based on morphology, suggesting that chromosomal rearrangements have played an important role in speciation within the Alcelaphini, and that karyotype characters are Abstract valuable phylogenetic markers in this group. Genome-wide homologies between the tsessebe ( Damalis- Copyright © 2011 S. Karger AG, Basel cus lunatus, 2n = 36) and Chinese muntjac ( Muntiacus reevesi , 2n = 46) have been established by cross-species painting with Chinese muntjac chromosome paints. Twenty-two au- The Bovidae is the largest family in suborder Pecora tosomal painting probes detected 35 orthologous segments [Nowak, 1999]. Extensive cytogenetic investigations, of- in the tsessebe. Hybridization results confirmed that: (i) D. ten involving species of economic value where material is

lunatus carries the (9; 14) reciprocal translocation that has relatively easy to obtain (Bovini and Caprini) [e.g. Hayes, been proposed to be a derived chromosomal landmark 1995; Iannuzzi and Di Meo, 1995; Barendse et al., 1997; shared by all species of the Antilopinae; (ii) the karyotype of ISCNDB, 2000; Iannuzzi et al., 2001; Maddox et al., 2001; D. lunatus can be derived almost exclusively from the bovid Di Meo et al., 2003; Chi et al., 2005; Huang et al., 2005], ancestral karyotype through 12 Robertsonian translocations have shown that chromosomal evolution has primarily involving 24 ancestral acrocentric autosomes; (iii) in addition involved Robertsonian translocations (Rb fusions) [see to the Rb fusions, pericentric heterochromatic amplification Ropiquet et al., 2010 for an exception]. This has led to has shaped the morphology of several of the D. lunatus chro- variation in diploid numbers within the family from mosomes. Integrated analysis of these and published cyto- 2n = 30 to 2n = 60 [e.g. Wurster and Benirschke, 1968; genetic data on pecorans has allowed us to accurately dis- Buckland and Evans, 1978; Gallagher and Womack, 1992; cern the karyotype history of Damaliscus (D. lunatus; D. pyg- Gallagher et al., 1994; Vassart et al., 1995; Kumamoto et argus, 2n = 38; D. hunteri , 2n = 44). The phylogenomic al., 1996; Kingswood et al., 1998, 2000; Nguyen et al.,

© 2011 S. Karger AG, Basel Dr. Ling Huang 1424–8581/11/0000–0000$38.00/0 College of Life Sciences, Ludong University Fax +41 61 306 12 34 Yantai 264025 (PR China) E-Mail [email protected] Accessible online at: Tel. +86 535 666 3053, Fax +86 535 669 7636

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CCGR322821.inddGR322821.indd 1 008.12.20108.12.2010 15:44:1115:44:11 2008; Ropiquet et al., 2008; Rubes et al., 2008; Iannuzzi et Banded metaphases were captured using the Genus System (Ap- al., 2009], and to suggestions that the ancestral bovid au- plied Imaging Corp.) and a Cohu CCD camera mounted on a Zeiss microscope (Axioplan 2). tosomal karyotype comprised 58 acrocentric elements. In contrast to the autosomes, the sex chromosomes have un- Fluorescence in situ Hybridization dergone inversions, transpositions, loss or gain of hetero- A set of chromosome-specific painting probes prepared previ- chromatin and infrequently, translocation to autosomes ously from flow-sorted Chinese muntjac chromosomes [Yang et [Gallagher and Womack, 1992; Gallagher et al., 1994; al., 1997a] was used in this study. Hybridization and detection followed Yang et al. [1997b] with modification. Biotin-labelled chro- Ponce de Leon et al., 1996; Piumi et al., 1998; Robinson et mosome-specific paint (50 ng) was made up to 15 ␮ l with hybrid- al., 1997, 1998; Iannuzzi et al., 2000; Di Meo et al., 2005; ization buffer (50% deionized formamide, 10% dextran sulphate, ! Rubes et al., 2007, 2008; Amaral et al., 2008]. 2 SSC, 0.5 M phosphate buffer, pH 7.3), denatured at 75 ° C for 10 Although not endangered, all 3 species of Damaliscus min, and preannealed by incubation at 37 ° C for 30 min. Slides ! (tsessebe; D. lunatus; blesbok, D. pygargus; Hirola ante- were denatured in 70% formamide, 2 SSC solution at 65 ° C for 2 min, quenched in ice-cold 70% ethanol, and dehydrated through lop, D. hunteri), have undergone range modification and a 70, 90 and 100% ethanol series. The preannealed paints were ap-

population declines due to hunting, agricultural en- plied to slides and allowed to hybridize for 24 h at 37 ° C. Post- croachment, competition with domestic livestock and hybridization washes consisted of two 5-min incubations in 50% ! drought [Nowak, 1999]. The G-banded karyotypes of D. formamide, 2 SSC at 42 ° C followed by two 5-min incubations ! lunatus (2n = 36) and D. pygargys (2n = 38) have previ- in 2 SSC at 42 ° C. Biotin-labeled probes were detected with a layer of Cy3-avidin (1: 1,000, Amersham). After detection, slides ,ously been published [van der Veen and Penzhorn, 1987; were counterstained with 4؅,6-diamidino-2-phenylindole (DAPI Robinson et al., 1991; Gallagher and Womack, 1992; 0.24 mg/ml), mounted with antifade AF1 (Citifuor Ltd.) and cov- Claro et al., 1995]. These initial findings were extended ered with 22 ! 32 mm2 coverslips. by Kumamoto et al. [1996] who showed that D. lunatus and D. pygargus differ from each other by a single Rb fu- M i c r o s c o p y Hybridization signals were assigned to specific chromosomes sion, while D. hunteri (2n = 44) was significantly more or chromosome regions defined by enhanced DAPI-banding or rearranged. More recently, Chaves et al. [2004] estab- G-banding patterns. Following the previously published nomen- lished the chromosomal homologies between D. hunter clature [Chi et al., 2005; Huang et al., 2006], we used ‘a’, ‘b’, ‘c’, ‘d’, (DHU) , sheep and human by multi-directional chromo- ‘e’, together with the corresponding Chinese muntjac chromosome painting. some number, to differentiate among the orthologous segments in tsessebe. Chromosome-specific paints from Chinese muntjac (Muntiacus reevesi , MRE, 2n = 46) have been used to Karyotype Phylogeny of Damaliscus great effect in comparative cytogenetic studies of pecor- The D. lunatus karyotype was arranged following the format ans including Moschidae, Bovidae, Cervidae and Giraf- introduced by Kumamoto et al. [1996]. Chromosomal rearrange- fidae, permitting inferences on aspects of the ancestral ments in Damaliscus were examined (using Bos taurus and Chi- nese muntjac chromosomes as reference) with respect to pub- pecoran, bovid and cervid karyotypes [Chi et al., 2005; lished painting results in pecorans [Chaves et al., 2004; Huang et Huang et al., 2005, 2006, 2008]. Here we establish the al., 2005, 2006; this paper] and banding studies in Damaliscus chromosomal homologies between D . lunatus and the [Kumamoto et al., 1996]. The presence/absence of chromosomal Chinese muntjac, M. reevesi, using Chinese muntjac rearrangements were analysed with respect to the bovid ancestral chromosome paints, and analyse these data to accurately karyotype. Given the small number of ingroup taxa, a cladistic analysis could be completed manually and the characters mapped track the karyotype history of this genus. to resulting topology.

Materials and Methods R e s u l t s Cell Culture, Chromosome Preparation and G-banding A fibrobalst cell line derived from a male D . lunatus was cul-

tured at 37 ° C in Dulbecco’s Modified Eagle Medium (DMEM) The Karyotype of D. lunatus enriched with 15% new-born bovine serum. Before harvest, the The male D. lunatus specimen analysed herein had cells were treated with 10 ␮g/ml of BrdU (final concentration) 2n = 36 (fig. 1 ). The G-banding patterns allowed the un- ␮ overnight and then treated with 0.05 g/ml colcemid (final con- ambiguous identification of 18 chromosome pairs that centration) for 1 h. Chromosome preparations were made according to standard procedures that included a 20 min hypotonic included 12 biarmed and 5 acrocentric autosomal pairs,

treatment in 0.4% KCl, fixation in 3: 1 methanol:glacial acetic acid and an acrocentric X and Y chromosome. and air drying. Trypsin G-banding followed Seabright (1972).

2 Cytogenet Genome Res 322821 Huang /Jing /Nie /Robinson /Yang

CCGR322821.inddGR322821.indd 2 008.12.20108.12.2010 15:44:2915:44:29 Fig. 1. A comparative map of D. lunatus chromosomes (DLU, middle) and their correspondence to Chinese muntjac (MRE, right) based on FISH results and G-banding comparison. The orthologous regions in cattle (BTA – nomenclature follows the ISCNDB 2000 cattle standard) are presented to the left. Chromosome numbers are indicated below or beside the chromosomes. Homologous segments are linked by lines. The banded MRE chromosomes were numbered according to Chi et al. [2005].

Comparative Cytogenetic Studies of Cytogenet Genome Res 322821 3 Damaliscus

CCGR322821.inddGR322821.indd 3 008.12.20108.12.2010 15:44:2915:44:29 detected 2 segments each (fig. 2 h), and 3 paints (MRE1, 3, 4) detected 3 segments each (fig. 2 c, d, g). MRE2 is present in 5 discrete segments in the D. lunatus genome. The Chinese muntjac X hybridized to the entire D. lunatus X chromosome; the Y chromosome probe gave no hybridization signal.

a b Discussion

Genome-wide chromosomal homologies between D. lunatus, a member of the Antilopinae, and a cervid, M. reevesi , have been established using Chinese muntjac chromosome painting probes ( fig. 1 , 2). Twenty-two autosomal paints detected 35 orthologous segments in the c d D. lunatus genome and the comparative chromosome map demonstrates that almost all interspecific homologous segments show a high degree of conservation in G- banding patterns ( fig. 1 , 2). Consistent with previous banding studies [Kumamoto et al., 1996], our painting results confirmed that all 29 conserved autosomal segments that have been proposed in the 2n = 60 ancestral bovid karyotype have been retained in the D. lunatus ge- e f nome which can be derived almost exclusively from the bovid ancestral karyotype through 12 centric fusions involving 24 ancestral acrocentric autosomes (fig. 1 ). Inves- tigations based on conventional banding, linkage maps and FISH techniques [e.g. Buckland and Evans, 1978; Gallagher and Womack, 1992; de Gortari et al., 1998; Huang et al., 2005, Iannuzzi et al., 2009] indicated that the autosomal translocation involving chromosomal seg-

g h ments homologous to BTA9 and 14 (rcp t(9; 14)) was the predominant karyotype difference between Bovinae and Fig. 2. FISH examples showing the hybridization patterns ob- Antilopinae. Gallagher and Womack [1992] identified tained with Chinese muntjac (MRE) chromosome-specific probes onto metaphases of D. lunatus (DLU). a , b MRE21 gave signals on this rearrangement in D. lunatus using banding compar- p-ter arm of DLU5; c , d MRE1 gave signals on q-ter arms of DLU3, ison while Kumamoto et al. [1996] did not mention this DLU5 and DLU6; e , f MRE6 painted to the whole qter arm of character in their investigation, and Chaves et al. [2004] DLU4; g MRE4 gave signals on q-ter arms of DLU5, DLU11 and failed to detect this rearrangement in the congener, D. p-ter arm of DLU12; ‘H’ means heterochromatin; h MRE14 gave hunteri, with sheep and human paints. The Rb fusion of signals on p-ter arms of DLU4 and DLU6. BTA14 and BTA4 gave rise to DLU4 in D. lunatus and the Rb fusion of BTA9 and BTA7 to DLU6. The hybridization pattern of Chinese muntjac paint MRE14 (homologous to Hybridization of Chinese muntjac (M. reevesi) BTA9) on DLU4 and DLU6 clearly shows the reciprocal Chromosome-Specific Paints on D. lunatus nature of this translocation in D. lunatus ( fig. 2 h) which, Metaphases with the reanalysis of D. hunteri and other Antilopinae

The 22 autosomal paints from Chinese muntjac were for which data are not available, may show that rcp t(9; 14) hybridized to D. lunatus chromosomes. The paints de- is a synapomorphy (shared derived character) defining tected 35 orthologous segments ( fig. 1 , 2). Fifteen paints the subfamily thus confirming and extending earlier re- (MRE6–10, 12, 13, 15–22) each hybridized to a single or- ports to this effect [Gallagher and Womack, 1992]. The thologous segment ( fig. 2 a, b, e, f), 3 paints (MRE5, 11, 14) presence of MRE4 signal on DLU11q-ter (corresponding

4 Cytogenet Genome Res 322821 Huang /Jing /Nie /Robinson /Yang

CCGR322821.inddGR322821.indd 4 008.12.20108.12.2010 15:44:2915:44:29 Fig. 3. Evolutionary tree based on chromosomal rearrangements defined by chromosome painting [Chaves et al., 2004; this paper] and banding comparison [Kumamoto et al.,1996] using the B. taurus karyotype to polar- i z e c h a r a c t e r s .

Table 1. Correspondence between orthologous segments in BTA and MRE

BTA homologs MRE homologs D. hunteri D. pygargus D. lunatus

9;14 14;12 1 1 1 25+2 2d+3a/3c 1 1 1 19+3 17+1b 1 1 1 Inversion in 20 Inversion in 20 1 ? ? 18+1 2e+18/7 1 0 0 7+4 1c+6 1 0 0 14+5 12+4c/1a 1 0 0 16+6 5b+16/21 1 0 0 11+8 3d+19/11a 1 0 0 10+12 8+9 1 0 0 10+1 8+18/7 0 1 1 14+4 12+6 0 1 1 6+5 16/21+4c/1a 0 1 1 7+9 1c+14/3b 0 1 1 17+8 20+19/11a 0 1 1 23+11 22+3d 0 1 1 16+12 5b+9 0 1 1 15+13 10+2a 0 1 1 22+20 4b+13 0 1 1 18+24 2e+4a 0 0 1 Heterochromatic Heterochromatic amplification of 24 amplification of 4a 0 0 1

BTA = Bos taurus; MRE = Muntiacus reevesi; 1 = presence/0 = absence in the three Damaliscus species as determined by our investigation and those of Kumamoto et al. [1996] and Chaves et al. [2004]; ? = presence or absence of this character has not been confirmed in the present investigations.

to MRE4a and to BTA24) drew our attention to the het- inversion in D. hunteri’s DHU12 (homologous to MRE20, erochromatic amplification of proximal DLU11q ( fig. 2 g, BTA17), but we could not unambiguously determine if proximal region brighter in DAPI f luorescence represent- this inversion is present in the sister species, D. lunatus . ed by ‘H’) which had not been reported previously. Inter- Previous work on the Alcelaphini was based on con- estingly, Chaves et al. [2004] documented a paracentric ventional banding [Buckland and Evans, 1978; Gallagher

Comparative Cytogenetic Studies of Cytogenet Genome Res 322821 5 Damaliscus

CCGR322821.inddGR322821.indd 5 008.12.20108.12.2010 15:44:3015:44:30 and Womack, 1992; Kumamoto et al., 1996] making phy- ments have occurred in the lineage leading to D. pygargus logenetic assessments somewhat tenuous in some in- and D. lunatus indicating that these are karyotypically stances. However, the molecular cytogenetic approaches the most derived species within Damaliscus ; (iv) one Rb

followed in the present investigation, and by Chaves et al. fusion (BTA8; 24 that corresponds to MRE2e and 4a) and [2004] on D. lunatus, and other pecorans [Chi et al., 2005; the heterochromatic amplification of DLU11qprox (ho- Huang et al., 2005, 2006, 2008], provide comparative data mologous to MRE4a) are unique to the D. lunatus karyo- that permit a more detailed assessment of the evolution- type; (v) finally, the evolutionary relationships suggested ary relationships among Damaliscus species. The chro- by the chromosomal characters are consistent with those mosomal rearrangements that have occurred during the in the supertree phylogenies of Hernández Fernández karyotype evolution of Damaliscus from the presumed and Vrba [2005] and Price et al. [2005], suggesting that ancestral state are presented in table 1 and summarized chromosomal changes have earmarked speciation events in a phylogenetic tree ( fig. 3 ). within Damaliscus . The data support: (i) an earlier observation of a reciprocal translocation between BTA9 and BTA14 in D. lunatus [Gallagher and Womack, 1992] and extend this find- Acknowledgements ing to the conspecifics D. hunteri and D. pygargus rein- forcing the idea that it is probably a synapomorphy for all This work was supported by the National Natural Science species within Antilopinae; (ii) that the Rb fusions in- Foundation of China (No. 30700473), Shandong Province Natu- ral Science Foundation (No. ZR2009DZ003) and a start-up fund volving BTA2; 25 and BTA19; 3 (which correspond to or- from the Ludong University (LY20063305). Financial support to thologous segments MRE2d and 3a/3c, 1b and 17) mark T.J.R. by the South African National Research Foundation is the divergence of Damaliscus ; (iii) multiple rearrange- gratefully acknowledged.

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