, Volume 124, Issue 2, pp 235–247 | Cite as

Nanger, Eudorcas, Gazella, and Antilope form a well-supported chromosomal clade within Antilopini (Bovidae, Cetartiodactyla)

  • Halina CernohorskaEmail author
  • Svatava Kubickova
  • Olga Kopecna
  • Miluse Vozdova
  • Conrad A. Matthee
  • Terence J. Robinson
  • Jiri Rubes
Research Article


The evolutionary clade comprising Nanger, Eudorcas, Gazella, and Antilope, defined by an X;BTA5 translocation, is noteworthy for the many autosomal Robertsonian fusions that have driven the chromosome number variation from 2n = 30 observed in Antilope cervicapra, to the 2n = 58 in present Eudorcas thomsoni and Eudorcas rufifrons. This work reports the phylogenetic relationships within the Antilopini using comprehensive cytogenetic data from A. cervicapra, Gazella leptoceros, Nanger dama ruficollis, and E. thomsoni together with corrected karyotypic data from an additional nine species previously reported in the literature. Fluorescence in situ hybridization using BAC and microdissected cattle painting probes, in conjunction with differential staining techniques, provide the following: (i) a detailed analysis of the E. thomsoni chromosomes, (ii) the identification and fine-scale analysis the BTA3 orthologue in species of Antilopini, and (iii) the location of the pseudoautosomal regions on sex chromosomes of the four species. Our phylogenetic analysis of the chromosomal data supports monophyly of Nanger and Eudorcas and suggests an affiliation between A. cervicapra and some of the Gazella species. This renders Gazella paraphyletic and emphasizes a closer relationship between Antilope and Gazella than what has previously been considered.


Phylogeny Painting probes BAC Repetitive sequences Nucleolus organizer region Antilopini 



This work was supported by the project “CEITEC” Central European Institute of Technology (ED1.1.00/02.0068) from European Regional Development Funds, partly by Grant No. P502/11/0719 from the Grant Agency of the Czech Republic (HC, SK, OK, MV, JR) and by grants from the South African National Research Foundation (TJR, CAM).

Supplementary material

412_2014_494_Fig8_ESM.gif (89 kb)
Fig. S1

(a) Gel showing satellite DNA patterns after PCR analysis with SI (detection of satI DNA) and SII (detection of satII DNA) primers and dissected X;BTA5 fusion sites as templates. The PCR amplicons derived from NDR, GLE and ACE were prepared in Cernohorska et al. (2012) study. (b) Gel showing satellite DNA patterns after PCR analysis with SI and SII primers and dissected NDRX functional centromeres as template. PK = positive control, NK = negative control; molecular weights are represented on the first line (GIF 89 kb)

412_2014_494_MOESM1_ESM.tif (553 kb)
High resolution image (TIFF 553 kb)
412_2014_494_MOESM2_ESM.pdf (40 kb)
Table S1 List of chromosome fusions identified within Antilopini of the X;BTA5 clade by G- banding and comparative painting with whole-chromosome and region-specific probes derived from cattle. Classification of Antilopini was carried out following Groves and Grubb (2011). The highlighted characters were modified with regard to the FISH results published in Cernohorska et al. (2012) (see the text). R = References: 1 = Cernohorska et al. (2012); 2 = O´Brien et al. (2006); 3 = Vassart et al. (1995); 4 = Kumamoto et al. (1995). (PDF 40 kb)
412_2014_494_MOESM3_ESM.pdf (38 kb)
Table S2 Presence and absence matrix of the chromosomal rearrangement included in this study. Taxon names are abbreviated to represent the genus and first two letters of the species in each instance. BTA, MKI and AMA represent outgroup taxa (see text for details). (PDF 38 kb)


  1. Ashley T (2002) X-Autosome translocations, meiotic synapsis, chromosome evolution and speciation. Cytogenet Genome Res 96:33–39CrossRefPubMedGoogle Scholar
  2. Avise JC, Robinson TJ (2008) Hemiplasy: a new term in the lexicon of phylogenetics. Syst Biol 57:503–507CrossRefPubMedGoogle Scholar
  3. Bärmann EV, Rössner GE, Wörheide G (2013) A revised phylogeny of Antilopini (Bovidae, Artiodactyla) using combined mitochondrial and nuclear genes. Mol Phylogen Evol 67:484–493CrossRefGoogle Scholar
  4. Bibi F (2013) A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics. BMC Evol Biol 13:166CrossRefPubMedCentralPubMedGoogle Scholar
  5. Biémont C, Vieira C (2006) Junk DNA as an evolutionary force. Nature 443(7111):521–524CrossRefPubMedGoogle Scholar
  6. Brown JD, O’Neill RJ (2010) Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. Annu Rev Genomics Hum Genet 11:291–316CrossRefPubMedGoogle Scholar
  7. Buckland RA, Evans HJ (1978) Cytogenetic aspects of phylogeny in the Bovidae. I. G-banding. Cytogenet. Cell Genet 78:42–63CrossRefGoogle Scholar
  8. Cernohorska H, Kubickova S, Vahala J, Rubes J (2012) Molecular insights into X; BTA5 chromosome rearrangements in the tribe Antilopini (Bovidae). Cytogenet Genome Res 136:188–198CrossRefPubMedGoogle Scholar
  9. Cernohorska H, Kubickova S, Kopecna O, Kulemzina AI, Perelman PL, Elder FF, Robinson TJ, Graphodatsky AS, Rubes J (2013) Molecular cytogenetic insights to the phylogenetic affinities of the giraffe (Giraffa camelopardalis) and pronghorn (Antilocapra americana). Chromosome Res 21:447–460CrossRefPubMedGoogle Scholar
  10. Chaves R, Adega F, Heslop-Harrison JS, Guedes-Pinto H, Wienberg J (2003) Complex satellite DNA reshuffling in the polymorphic t(1;29) Robertsonian translocation and evolutionarily derived chromosomes in cattle. Cromosome Res 11:641–648CrossRefGoogle Scholar
  11. Decker JE, Pires JC, Conant GC et al (2009) Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics. Proc Natl Acad Sci U S A 106:18644–18649CrossRefPubMedCentralPubMedGoogle Scholar
  12. Dobigny G, Ozouf-Costaz C, Bonillo C, Volobouev V (2004) Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study. Chromosoma 113:34–41CrossRefPubMedGoogle Scholar
  13. Elder FFB; Hsu TC (1988) Tandem fusion in the evolution of mammalian chromosomes. The Cytogenetics of Mammalian Autosomal Rearrangements, pages 481–501, Alan R. Liss, Inc.Google Scholar
  14. Fernández MH, Vrba ES (2005) A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biol Rev 80:269–302CrossRefGoogle Scholar
  15. Gallagher DS Jr, Womack JE (1992) Chromosome conservation in the Bovidae. J Hered 83:287–298PubMedGoogle Scholar
  16. Gallagher DS Jr, Davis SK, De Donato M, Burzlaff JD, Womack JE, Taylor JF, Kumamoto AT (1999) A molecular cytogenetic analysis of the tribe Bovini (Artiodactyla: Bovidae: Bovinae) with an emphasis on sex chromosome morphology and NOR distribution. Chromosome Res 7:481–492CrossRefPubMedGoogle Scholar
  17. Gatesy J, Yelon D, DeSalle R, Vrba ES (1992) Phylogeny of the Bovidae (Artiodactyla, Mammalia), based on mitochondrial ribosomal DNA sequences. J Mol Biol Evol 9:433–446Google Scholar
  18. Goodpasture C, Bloom SE (1975) Visualization of nucleolar organizer in mammalian chromosomes using silver staining. Chromosoma 53:37–50CrossRefPubMedGoogle Scholar
  19. Groves C, Grubb P (2011) Ungulate taxonomy. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  20. Hassanin A, Douzery EJP (1999) The tribal radiation of the family Bovidae (Artiodactyla) and the evolution of the mitochondrial cytochrome b gene. Mol Phylogenet Evol 13:227–243CrossRefPubMedGoogle Scholar
  21. Hassanin A, Delsuc F, Ropiquet A et al (2012) Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C R Biol 335:32–50CrossRefPubMedGoogle Scholar
  22. Iannuzzi L, Di Berardino D, Gustavsson I, Ferrara L, Di Meo GP (1987) Centromeric loss in translocations of centric fusion type in cattle and water buffalo. Hereditas 106:73–81CrossRefPubMedGoogle Scholar
  23. ISCNDB 2000 (2001) International system for chromosome nomenclature of domestic bovids. Cytogenet Cell Genet 92:283–299CrossRefGoogle Scholar
  24. Kejnovsky E, Hobza R, Cermak T, Kubat Z, Vyskot B (2009) The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity 102:533–541CrossRefPubMedGoogle Scholar
  25. Kidwell MG, Lisch DR (2001) Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55:1–24CrossRefPubMedGoogle Scholar
  26. King M (1993) Species evolution: the role of chromosome change. Cambridge University Press, CambridgeGoogle Scholar
  27. Kopecna O, Kubickova S, Cernohorska H, Cabelova K, Vahala J, Martinkova N, Rubes J (2014) Tribe-specific satellite DNA in non-domestic Bovidae. Chromosome Res 22:277–291CrossRefPubMedGoogle Scholar
  28. Kubickova S, Cernohorska H, Musilova P, Rubes J (2002) The use of laser microdissection for the preparation of chromosome-specific painting probes in farm animals. Chromosome Res 10:571–577CrossRefPubMedGoogle Scholar
  29. Kumamoto AT, Kingswood OA, Rebholz WER, Houck ML (1995) The chromosomes of Gazella bennetti and Gazella saudiya. Int J Mammal Biol 60:159–169Google Scholar
  30. Louzada S, Paço A, Kubickova S, Adega F, Guedes-Pinto H, Rubes J, Chaves R (2008) Different evolutionary trails in the related genomes Cricetus cricetus and Peromyscus eremicus (Rodentia, Cricetidae) uncovered by orthologous satellite DNA repositioning. Micron 39:1149–1155CrossRefPubMedGoogle Scholar
  31. Marcot JD (2007) Molecular phylogeny of terrestrial artiodactyls. In: Prothero DR, Foss SE (eds) The evolution of Artiodactyls. The John Hopkins University Press, Baltimore, pp 4–18Google Scholar
  32. Marshall OJ, Chueh AC, Wong LH, Choo KH (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82:261–282CrossRefPubMedCentralPubMedGoogle Scholar
  33. Matthee CA, Davis SK (2001) Molecular insights into the evolution of the family Bovidae: a nuclear DNA perspective. Mol Biol Evol 18:1220–1230CrossRefPubMedGoogle Scholar
  34. Nguyen TT, Aniskin VM, Gerbault-Seureau M, Planton H, Renard JP, Nguyen BX, Hassanin A, Volobouev VT (2008) Phylogenetic position of the saola (Pseudoryx nghetinhensis) inferred from cytogenetic analysis of 11 species of Bovidae. Cytogenet Genome Res 122:41–54CrossRefPubMedGoogle Scholar
  35. O´Brien SJ, Menninger JC, Nash WG (2006) Atlas of mammalian chromosomes. Wiley, HobokenCrossRefGoogle Scholar
  36. Rebholz W, Harley E (1999) Phylogenetic relationships in the bovid subfamily Antilopinae based on mitochondrial DNA sequences. Mol Phylogenet Evol 12:87–94CrossRefPubMedGoogle Scholar
  37. Robinson TJ, Ruiz-Herrera A, Avise JC (2008) Hemiplasy and homoplasy in the karyotypic phylogenies of mammals. Proc Natl Acad Sci U S A 105:14477–81CrossRefPubMedCentralPubMedGoogle Scholar
  38. Robinson TJ, Ropiquet A (2011) Examination of hemiplasy, homoplasy and phylogenetic discordance in chromosomal evolution of the Bovidae. Syst Biol 60:439–450CrossRefPubMedGoogle Scholar
  39. Robinson TJ, Cernohorska H, Diedericks G, Cabelova K, Duran A, Matthee CA (2014) Phylogeny and vicariant speciation of the Grey Rhebok, Pelea capreolus. Heredity 112:325–332CrossRefPubMedCentralPubMedGoogle Scholar
  40. Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R (2012) Centromere repositioning in mammals. Heredity 108:59–67CrossRefPubMedCentralPubMedGoogle Scholar
  41. Rokas A, Holland PW (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15:454–459CrossRefPubMedGoogle Scholar
  42. Ropiquet A, Gerbault-Seureau M, Deuve JL, Gilbert C, Pagacova E, Chai N, Rubes J, Hassanin A (2008) Chromosome evolution in the subtribe Bovina (Mammalia, Bovidae): the karyotype of the Cambodian banteng (Bos javanicus birmanicus) suggests that Robertsonian translocations are related to interspecific hybridization. Chromosome Res 16:1107–1118CrossRefPubMedGoogle Scholar
  43. Ropiquet A, Li B, Hassanin A (2009) SuperTRI: a new approach based on branch support analyses of multiple independent data sets for assessing reliability of phylogenetic inferences. C R Biol 332:832–847CrossRefPubMedGoogle Scholar
  44. Rubes J, Kubickova S, Pagacova E et al (2008) Phylogenomic study of spiral-horned antelope by cross-species chromosome painting. Chromosome Res 16:935–947CrossRefPubMedGoogle Scholar
  45. Rubes J, Musilova P, Kopecna O, Kubickova S, Cernohorska H, Kulemsina AI (2012) Comparative molecular cytogenetics in Cetartiodactyla. Cytogenet Genome Res 137:194–207CrossRefPubMedGoogle Scholar
  46. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–25PubMedGoogle Scholar
  47. Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2:971–972CrossRefPubMedGoogle Scholar
  48. Stimpson KM, Sullivan BA (2010) Epigenomics of centromere assembly and function. Curr Opin Cell Biol 22:772–80CrossRefPubMedGoogle Scholar
  49. Swofford DL (2002) PAUP: phylogenetic analysis using parsimony. Version 4.0b10. Champaign (IL): National History SurveyGoogle Scholar
  50. Vassart M, Seguela A, Hayes H (1995) Chromosomal evolution in gazelles. J Hered 86:216–266PubMedGoogle Scholar
  51. Veyrunes F, Catalan J, Sicard B, Robinson TJ, Duplantier JM, Granjon L, Dobigny G, Britton-Davidian J (2004) Autosome and sex chromosome diversity among the African pygmy mice, subgenus Nannomys (Murinae; Mus). Chromosome Res 12:369–382CrossRefPubMedGoogle Scholar
  52. White MJD (1978) Modes of speciation. WH Freeman, San FranciscoGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Halina Cernohorska
    • 1
    Email author
  • Svatava Kubickova
    • 1
  • Olga Kopecna
    • 1
  • Miluse Vozdova
    • 1
  • Conrad A. Matthee
    • 2
  • Terence J. Robinson
    • 2
  • Jiri Rubes
    • 1
  1. 1.CEITEC - Veterinary Research InstituteBrnoCzech Republic
  2. 2.Evolutionary Genomics Group, Department of Botany and ZoologyStellenbosch UniversityStellenboschSouth Africa

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