Skip to main content
SpringerLink
Log in

Molecular cytogenetic insights to the phylogenetic affinities of the giraffe (Giraffa camelopardalis) and pronghorn (Antilocapra americana)

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Five families are traditionally recognized within higher ruminants (Pecora): Bovidae, Moschidae, Cervidae, Giraffidae and Antilocapridae. The phylogenetic relationships of Antilocapridae and Giraffidae within Pecora are, however, uncertain. While numerous fusions (mostly Robertsonian) have accumulated in the giraffe’s karyotype (Giraffa camelopardalis, Giraffidae, 2n = 30), that of the pronghorn (Antilocapra americana, Antilocapridae, 2n = 58) is very similar to the hypothesised pecoran ancestral state (2n = 58). We examined the chromosomal rearrangements of two species, the giraffe and pronghorn, using a combination of fluorescence in situ hybridization painting probes and BAC clones derived from cattle (Bos taurus, Bovidae). Our data place Moschus (Moschidae) closer to Bovidae than Cervidae. Although the alternative (i.e., Moschidae + Cervidae as sister groups) could not be discounted in recent sequence-based analyses, cytogenetics bolsters conclusions that the former is more likely. Additionally, DNA sequences were isolated from the centromeric regions of both species and compared. Analysis of cenDNA show that unlike the pronghorn, the centromeres of the giraffe are probably organized in a more complex fashion comprising different repetitive sequences specific to single chromosomal pairs or groups of chromosomes. The distribution of nucleolar organiser region (NOR) sites, often an effective phylogenetic marker, were also examined in the two species. In the giraffe, the position of NORs seems to be autapomorphic since similar localizations have not been found in other species within Pecora.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

AAM:

Antilocapra americana

BAC:

Bacterial artificial chromosome

BAK:

Bovidae ancestral karyotype

BTA:

Bos taurus

cenDNA:

Centromeric DNA

CDR:

Camelus dromedarius

CHI:

Capra hircus

CR:

Centromeric region

DOP-PCR:

Degenerate oligonucleotide primed polymerase chain reaction

EDA:

Elaphurus davidianus

FISH:

Fluorescence in situ hybridization

GCA:

Giraffa camelopardalis

HSA:

Homo sapiens

LINE:

Long interspersed nucleotide elements

MMO:

Moschus moschiferus

NOR:

Nucleolar organiser region

OJO:

Okapia johnstoni

PAK:

Pecoran ancestral karyotype

pter:

Terminus of p arm

qter:

Terminus of q arm

SINE:

Short interspersed nucleotide elements

References

  • Bonnet A, Thévenon S, Claro F, Gautier M, Hayes H (2001) Cytogenetic comparison between Vietnamese sika deer and cattle: R-banded karyotypes and FISH mapping. Chromosom Res 9:673–687

    Article  CAS  Google Scholar 

  • Bonnet-Garnier A, Claro F, Thévenon S, Gautier M, Hayes H (2003) Identification by R-banding and FISH of chromosome arms involved in Robertsonian translocations in several deer species. Chromosom Res 11:649–663

    Article  CAS  Google Scholar 

  • Brown JD, O’Neill RJ (2010) Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. Annu Rev Genom Hum Genet 11:291–316

    Article  CAS  Google Scholar 

  • Buckland RA, Evans HJ (1978) Cytogenetic aspects of phylogeny in the Bovidae. Cytogenet Cell Genet 21:64–71

    Article  PubMed  CAS  Google Scholar 

  • Cabelova K, Kubickova S, Cernohorska H, Rubes J (2012) Male-specific repeats in wild Bovidae. J Appl Genet 53:423–433

    Article  PubMed  Google Scholar 

  • Cernohorska H, Kubickova S, Vahala J, Robinson TJ, Rubes J (2011) Cytotypes of Kirk’s dik-dik (Madoqua kirkii, Bovidae) show multiple tandem fusions. Cytogenet Genome Res 132:255–263

    Article  PubMed  CAS  Google Scholar 

  • Cernohorska H, Kubickova S, Vahala J, Rubes J (2012) Molecular insights into X;BTA5 chromosome rearrangements in the tribe Antilopini (Bovidae). Cytogenet Genome Res 136:188–198

    Article  PubMed  CAS  Google Scholar 

  • Chaves R, Guedes-Pinto H, Heslop-Harrison JS, Schwarzacher T (2000) The species and chromosomal distribution of the centromeric α-satellite I sequence from sheep in the tribe Caprini and other Bovidae. Cytogenet Cell Genet 91:62–66

    Article  PubMed  CAS  Google Scholar 

  • 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. Cromosom Res 11:641–648

    Article  CAS  Google Scholar 

  • Chaves R, Santos S, Guedes-Pinto H (2004) Comparative analysis (Hippotragini versus Caprini, Bovidae) of X-chromosome’s constitutive heterochromatin by in situ restriction endonuclease digestion: X-chromosome constitutive heterochromatin evolution. Genetica 121:315–325

    Article  PubMed  CAS  Google Scholar 

  • Chaves R, Guedes-Pinto H, Heslop-Harrison JS (2005) Phylogenetic relationships and the primitive X chromosome inferred from chromosomal and satellite DNA analysis in Bovidae. Proc Biol Sci 272:2009–2016

    Article  PubMed  CAS  Google Scholar 

  • Chi J, Fu B, Nie W, Wang J, Graphodatsky A, Yang F (2005) New insights into the karyotypic ralationships of Chinese muntjac (Muntiacus reevesi), forest musk deer (Moschus berezovskii) and gayal (Bos frontalis). Cytogenet Genome Res 108:310–316

    Article  PubMed  CAS  Google Scholar 

  • 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 106:18644–18649

    Article  PubMed  CAS  Google Scholar 

  • Di Meo G, Perucatti A, Chaves R et al (2006) Cattle rob(1;29) originating from complex chromosome rearrangements as revealed by both banding and FISH-mapping techniques. Chromosom Res 14:649–655

    Article  CAS  Google Scholar 

  • Ferguson-Smith MA, Trifonov V (2007) Mammalian karyotype evolution. Nat Rev Genet 8:950–962

    Article  PubMed  CAS  Google Scholar 

  • Gallagher DS Jr, Derr JN, Womack JE (1994) Chromosome conservation among the advanced Pecorans and determination of the primitive bovid karyotype. J Hered 85:204–210

    PubMed  Google Scholar 

  • Gallagher DS Jr, Davis SK, De Donato M et al (1999) A molecular cytogenetic analysis of the tribe Bovini (Artiodactyla: Bovidae: Bovinae) with an emphasis on sex chromosome morphology and NOR distribution. Chromosom Res 7:481–492

    Article  CAS  Google Scholar 

  • Goldammer T, Brunner RM, Rebl A et al (2009a) Cytogenetic anchoring of radiation hybrid and virtual maps of sheep chromosome X and comparison of X chromosomes in sheep, cattle, and human. Chromosom Res 17:497–506

    Article  CAS  Google Scholar 

  • Goldammer T, Brunner RM, Rebl A (2009b) A high-resolution radiation hybrid map of sheep chromosome X and comparison with human and cattle. Cytogenet Genome Res 125:40–45

    Article  PubMed  CAS  Google Scholar 

  • Goodpasture C, Bloom SE (1975) Visualization of nucleolar organizer in mammalian chromosomes using silver staining. Chromosoma 53:37–50

    Article  PubMed  CAS  Google Scholar 

  • Hassanin A, Douzery EJP (2003) Molecular and morphological phylogenies of Ruminantia and the alternative position of the Moschidae. Syst Biol 52:206–228

    Article  PubMed  Google Scholar 

  • 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 335:32–50

    Article  PubMed  Google Scholar 

  • Huang L, Chi J, Nie W, Wang J, Yang F (2006) Phylogenomics of several deer species revealed by comparative chromosome painting with Chinese muntjac paints. Genetica 127:25–33

    Article  PubMed  Google Scholar 

  • Huang L, Nesterenko A, Nie W et al (2008) Karyotypic evolution of giraffes (Giraffa camelopardalis) revealed by cross-species chromosome painting with Chinese muntjac (Muntiacus reevesi) and human (Homo sapiens) paints. Cytogenet Genome Res 122:132–138

    Article  PubMed  CAS  Google Scholar 

  • 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 106:73–81

    Article  PubMed  CAS  Google Scholar 

  • Iannuzzi L, Di Meo GP, Perucatti A, Incarnato D, Schibler L et al (2000) Comparative FISH-mapping of bovid X chromosomes reveals homologies and divergences between the subfamilies Bovinae and Caprinae. Cytogenet Cell Genet 89:171–176

    Article  PubMed  CAS  Google Scholar 

  • Iannuzzi L, King WA, Di Berardino D (2009) Chromosome evolution in domestic Bovids as revealed by chromosome banding and FISH-mapping techniques. Cytogenet Genom Res 126:49–62

    Article  CAS  Google Scholar 

  • ISCNDB 2000 (2001) International system for chromosome nomenclature of domestic bovids. Cytogenet Cell Genet 92:283–299

    Article  Google Scholar 

  • Jobse C, Buntjer JB, Haagsma N, Breukelman HJ, Beintema JJ, Lenstra JA (1995) Evolution and recombination of bovine DNA repeats. J Mol Evol 41:277–283

    Article  PubMed  CAS  Google Scholar 

  • 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. Chromosom Res 10:571–577

    Article  CAS  Google Scholar 

  • Kulemzina AI, Trifonov VA, Perelman PL et al (2009) Cross-species chromosome painting in Cetartiodactyla: reconstructing the karyotype evolution in key phylogenetic lineages. Chromosom Res 17:419–436

    Article  CAS  Google Scholar 

  • Marcot JD (2007) Molecular phylogeny of terrestrial artiodactyls: Conflicts and resolution. In: Prothero DR, Foss SE (eds) The evolution of artiodactyls (pp 367). The John Hopkins University Press, Baltimore (MD), pp 4–18

    Google Scholar 

  • Miyamoto MM, Goodman M (1986) Biomolecular systematics of eutherian mammals. Phylogenetic patterns and classification. Syst Zool 35:230–240

    Article  Google Scholar 

  • Nguyen TT, Aniskin VM, Gerbault-Seureau M et al (2008) Phylogenetic position of the saola (Pseudoryx nghetinhensis) inferred from cytogenetic analysis of eleven species of Bovidae. Cytogenet Genome Res 122:41–54

    Article  PubMed  CAS  Google Scholar 

  • Pauciullo A, Kubickova S, Cernohorska H (2006) Isolation and physical localization of new chromosome-specific centromeric repeats in farm animals. Vet Med Czech 51:224–231

    CAS  Google Scholar 

  • Perucatti A, Genualdo V, Iannuzzi A et al (2012) Advanced comparative cytogenetic analysis of X chromosomes in river buffalo, cattle, sheep, and human. Chromosom Res 20:413–425

    Article  CAS  Google Scholar 

  • Petit P, de Meurichy W (1986) On the chromosomes of the okapi. Okapia johnstoni. Ann Genet 29:232–234

    PubMed  CAS  Google Scholar 

  • Piumi F, Schibler L, Vaiman D, Oustry A, Cribiu EP (1998) Comparative cytogenetic mapping reveals chromosome rearrangements between the X chromosomes of two closely related mammalian species (cattle and goats). Cytogenet Cell Genet 81:36–41

    Article  PubMed  CAS  Google Scholar 

  • Rens W, O'Brien PCM, Yang F et al (2001) Karyotype relationships between distantly related marsupials from South America and Australia. Chromosom Res 9:301–308

    Article  CAS  Google Scholar 

  • Robinson TJ, Ropiquet A (2011) Examination of Hemiplasy, homoplasy and phylogenetic discordance in chromosomal evolution of the Bovidae. Syst Biol 60:439–450

    Article  PubMed  Google Scholar 

  • Robinson TJ, Ruiz-Herrera A (2008) Defining the ancestral eutherian karyotype: a cladistic interpretation of chromosome painting and genome sequence assembly data. Chromosom Res 16:1133–1141

    Article  CAS  Google Scholar 

  • Robinson TJ, Wilson V, Gallagher DS Jr et al (1996) Chromosomal evolution in duiker antelope (Cephalophinae: Bovidae): Karyotype comparisons, fluorescence in situ hybridization, and rampant X chromosome variation. Cytogenet Cell Genet 73:116–122

    Article  PubMed  CAS  Google Scholar 

  • Robinson TJ, Harrison WR, Ponce de León FA, Davis SK, Elder FF (1998) A molecular cytogenetic analysis of X chromosome repatterning in the Bovidae: transpositions, inversions, and phylogenetic inference. Cytogenet Cell Genet 80:179–184

    Article  PubMed  CAS  Google Scholar 

  • Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R (2012) Centromere repositioning in mammals. Heredity 108:59–67

    Article  PubMed  CAS  Google Scholar 

  • Ropiquet A, Gerbault-Seureau M, Deuve JL et al (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. Chromosom Res 16:1107–1118

    Article  CAS  Google Scholar 

  • Ropiquet A, Hassanin A, Pagacova E et al (2010) A paradox revealed: karyotype evolution in the four horned antelope occurs by tandem fusion (Mammalia, Bovidae, Tetracerus quadricornis). Chromosom Res 18:277–286

    Article  CAS  Google Scholar 

  • Rubes J, Kubickova S, Musilova P et al (2005) Assignment of chromosome rearrangements between X chromosomes of human and cattle by laser microdissection and Zoo-FISH. Chromosom Res 13:569–574

    Article  CAS  Google Scholar 

  • Rubes J, Kubickova S, Pagacova E et al (2008) Phylogenomic study of spiral-horned antelope by cross-species chromosome painting. Chromosom Res 16:935–947

    Article  CAS  Google Scholar 

  • Rubes J, Musilova P, Kopecna O, Kubickova S, Cernohorska H, Kulemsina AI (2012) Comparative molecular cytogenetics in Cetartiodactyla. Cytogenet Genome Res 137:194–207

    Article  PubMed  CAS  Google Scholar 

  • Saffery R, Earle E, Irvine DV, Kalitsis P, Choo KH (1999) Conservation of centromere protein in vertebrates. Chromosom Res 7:261–265

    Article  CAS  Google Scholar 

  • Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2:971–972

    Article  PubMed  CAS  Google Scholar 

  • Slate J, Van Stijn TC, Anderson RM et al (2002) A deer (subfamily Cervinae) genetic linkage map and the evolution of ruminant genomes. Genetics 160:1587–1597

    PubMed  CAS  Google Scholar 

  • Ugarković D, Plohl M (2002) Variation in satellite DNA profiles—causes and effects. EMBO J 21:5955–5959

    Article  PubMed  Google Scholar 

  • Wilson DE, Reeder DM (2005) Mammal species of the world. Johns Hopkins University Press, Baltimore

    Google Scholar 

Download references

Acknowledgements

This work was supported by grants GA CR P506/10/0421, MZE 0002716202 and by the project “CEITEC”- Central European Institute of Technology (ED1.1.00/02.0068) from European regional Development Funds (HC, SK, OK, JR). Research grants of the Russian Fund for Basic Research, programs of the Russian Academy of Science MCB and Integration program of the SB RAS (AIK, PLP, ASG) and the South African National Research Foundation (TJR) are acknowledged. We thank Mitch Bush, David Wildt (Brookfield Zoo, IL, USA) and S. O’Brien for Okapia johnstoni material and A. A. Sharshov for Moschus moschiferus which was collected in the Altai region, Russia.

Author information

Authors and Affiliations

  1. Veterinary Research Institute, Hudcova 70, 621 00, Brno, Czech Republic

    Halina Cernohorska, Svatava Kubickova, Olga Kopecna & Jiri Rubes

  2. Institute of Molecular and Cellular Biology, SB RAS, Novosibirsk, Russia

    Anastasia I. Kulemzina, Polina L. Perelman & Alexander S. Graphodatsky

  3. Department of Pathology, UNM School of Medicine, University of New Mexico Albuquerque, Albuquerque, NM, USA

    Frederick F. B. Elder

  4. Evolutionary Genomics Group, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa

    Terence J. Robinson

Authors
  1. Halina Cernohorska
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Svatava Kubickova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Olga Kopecna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anastasia I. Kulemzina
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Polina L. Perelman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Frederick F. B. Elder
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Terence J. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alexander S. Graphodatsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jiri Rubes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Halina Cernohorska.

Additional information

Responsible Editor: Walther Traut

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM Table S1

(DOC 31 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cernohorska, H., Kubickova, S., Kopecna, O. et al. Molecular cytogenetic insights to the phylogenetic affinities of the giraffe (Giraffa camelopardalis) and pronghorn (Antilocapra americana). Chromosome Res 21, 447–460 (2013). https://doi.org/10.1007/s10577-013-9361-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-013-9361-0

Keywords

Search

Navigation