Chromosome Research

, 15:499 | Cite as

Cross-species chromosome painting among camel, cattle, pig and human: further insights into the putative Cetartiodactyla ancestral karyotype

  • Gabriel Balmus
  • Vladimir A. Trifonov
  • Larisa S. Biltueva
  • Patricia C.M. O’Brien
  • Elena S. Alkalaeva
  • Beiyuan Fu
  • Julian A. Skidmore
  • Twink Allen
  • Alexander S. Graphodatsky
  • Fengtang YangEmail author
  • Malcolm A. Ferguson-SmithEmail author


The great karyotypic differences between camel, cattle and pig, three important domestic animals, have been a challenge for comparative cytogenetic studies based on conventional cytogenetic approaches. To construct a genome-wide comparative chromosome map among these artiodactyls, we made a set of chromosome painting probes from the dromedary camel (Camelus dromedarius) by flow sorting and degenerate oligonucleotide primed-PCR. The painting probes were first used to characterize the karyotypes of the dromedary camel (C. dromedarius), the Bactrian camel (C. bactrianus), the guanaco (Lama guanicoe), the alpaca (L. pacos) and dromedary × guanaco hybrid karyotypes (all with 2n = 74). These FISH experiments enabled the establishment of a high-resolution GTG-banded karyotype, together with chromosome nomenclature and idiogram for C. dromedarius, and revealed that these camelid species have almost identical karyotypes, with only slight variations in the amount and distribution patterns of heterochromatin. Further cross-species chromosome painting between camel, cattle, pig and human with painting probes from the camel and human led to the establishment of genome-wide comparative maps. Between human and camel, pig and camel, and cattle and camel 47, 53 and 53 autosomal conserved segments were detected, respectively. Integrated analysis with previously published comparative maps of human/pig/cattle enabled us to propose a Cetartiodactyla ancestral karyotype and to discuss the early karyotype evolution of Cetartiodactyla. Furthermore, these maps will facilitate the positional cloning of genes by aiding the cross-species transfer of mapping information.

Key words

camel Camelus Cetartiodactyla chromosome painting cytogenetics evolution karyotype Lama 


  1. Arnason U, Adegoke JA, Bodin K et al. (2002) Mammalian mitogenomic relationships and the root of the eutherian tree. Proc Natl Acad Sci USA 99: 8151-156.CrossRefPubMedGoogle Scholar
  2. Arnason U, Gullberg A (1996) Cytochrome b nucleotide sequences and the identification of five primary lineages of extant cetaceans. Mol Biol Evol 13: 407-17.PubMedGoogle Scholar
  3. Bajpai S, Gingerich PD (1998) A new Eocene archaeocete (Mammalia, Cetacea) from India and the time of origin of whales. Proc Natl Acad Sci USA 95: 15464-5468.CrossRefPubMedGoogle Scholar
  4. Bianchi NO, Larramendy ML, Bianchi MS, Cortes L (1986) Karyological conservatism in South American camelids. Experientia 42: 622-24.CrossRefGoogle Scholar
  5. Bielec PE, Gallagher DS, Womack JE, Busbee DL (1998) Homologies between human and dolphin chromosomes detected by heterologous chromosome painting. Cytogenet Cell Genet 81: 18-6.CrossRefPubMedGoogle Scholar
  6. Biltueva LS, Yang F, Vorobieva NV, Graphodatsky AS (2004) Comparative map between the domestic pig and dog. Mamm Genome 15: 809-18.CrossRefPubMedGoogle Scholar
  7. Bininda-Emonds ORP, Cardillo M, Jones KE et al. (2007) The delayed rise of present-day mammals. Nature 446: 507-12.CrossRefPubMedGoogle Scholar
  8. Bosma AA, de Haan NA, Arkesteijn GJ, Yang F, Yerle M, Zijlstra C (2004) Comparative chromosome painting between the domestic pig (Sus scrofa) and two species of peccary, the collared peccary (Tayassu tajacu) and the white-lipped peccary (T. pecari): a phylogenetic perspective. Cytogenet Genome Res 105: 115-21.CrossRefPubMedGoogle Scholar
  9. Bosma AA, de Haan NA, Mellink CHM, Yerle M, Zijlstra C (1996) Chromosome homology between the domestic pig and the babirusa (family Suidae) elucidated with the use of porcine painting probes. Cytogenet Cell Genet 75: 32-5.CrossRefPubMedGoogle Scholar
  10. Buckland RA, Evans HJ (1978) Cytogenetic aspects of phylogeny in the Bovidae, G-banding. Cytogenet Cell Genet 32: 64-1.CrossRefGoogle Scholar
  11. Bunch TD, Foote WC, Maciulis A (1985) Chromosome banding pattern homologies and NORs for the Bactrian camel, guanaco and llama. J Hered 76: 115-18.Google Scholar
  12. Chi J, Fu B, Nie W, Wang J, Graphodatsky AS, Yang F (2005) New insights into the karyotypic relationships of Chinese muntjac (Muntiacus reevesi), forest musk deer (Moschus berezovskii) and gayal (Bos frontalis). Cytogenet Genome Res 108: 310-16.CrossRefPubMedGoogle Scholar
  13. Di Berardino D, Lioi MB, Iannuzzi L (1985) Identification of nucleolus organizer chromosome in cattle (Bos taurus L.) by sequential silver staining-+  RBA banding. Caryologia 38: 95-02.Google Scholar
  14. Di Berardino D, Nicodemo D, Coppola G et al. (2006) Cytogenetic characterization of alpaca (Lama pacos, fam. Camelidae) prometaphase chromosomes. Cytogenet Genome Res 115: 138-44.CrossRefPubMedGoogle Scholar
  15. Everts-van der Wind A, Kata SR, Band MR et al. (2004) A 1463 gene cattle–human comparative map with anchor points defined by human genome sequence coordinates. Genome Res 14: 1424-437.CrossRefPubMedGoogle Scholar
  16. Frönicke L, Wienberg J (2001) Comparative chromosome painting defines the high rate of karyotype changes between pigs and bovids. Mamm Genome 12: 442-49.CrossRefPubMedGoogle Scholar
  17. Frönicke L, Caldés MG, Graphodatsky A et al. (2006) Are molecular cytogenetics and bioinformatics suggesting diverging models of ancestral mammalian genomes? Genome Res 16: 311-13.CrossRefGoogle Scholar
  18. 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. Chromosome Res 7: 481-92.CrossRefPubMedGoogle Scholar
  19. Gatesy J, Matthee C, DeSalle R, Hayashi C (2002) Resolution of a supertree/supermatrix paradox. Syst Biol 51: 652-64.CrossRefPubMedGoogle Scholar
  20. Gatesy J, Milinkovitch M, Waddell V, Stanhope M (1999) Stability of cladistic relationships between Cetacea and higher-level artiodactyl taxa. Syst Biol 48: 6-0.CrossRefPubMedGoogle Scholar
  21. Graphodatsky AS (2006) Camelus bactrianus. In O’Brien SJ, Menninger JC, Nash WG, eds. Atlas of Mammalian Chromosomes. New York: Wiley-Liss p. 547.Google Scholar
  22. Graphodatsky AS, Yang F, O’Brien PC et al. (2000) A comparative chromosome map of the Arctic fox, red fox and dog defined by chromosome painting and high resolution G-banding. Chromosome Res 8: 253-63.CrossRefPubMedGoogle Scholar
  23. Gray AP (1972) Mammalian Hybrids. Technical Communication Number 10 (Revised) of the Commonwealth Bureau of Animal Breeding and Genetics, Edinburgh.Google Scholar
  24. Hassanin A, Douzery EJP (2003) Molecular and morphological phylogenies of Ruminantia and the alternative position of the Moschidae. Syst Biol 52: 206-28.CrossRefPubMedGoogle Scholar
  25. Hsu TC, Benirschke K (1967) An Atlas of Mammalian Chromosomes 1: 40. New York: Springer.Google Scholar
  26. Huang L, Wang J, Nie W, Su W, Yang F (2006) Tandem chromosome fusions in karyotypic evolution of Muntiacus: evidence from M. feae and M. gongshanensis. Chromosome Res 14: 637-47.CrossRefPubMedGoogle Scholar
  27. Itoh T, Watanabe T, Ihara N et al. (2005) A comprehensive radiation hybrid map of the bovine genome comprising 5593 loci. Genomics 85: 413-24.CrossRefPubMedGoogle Scholar
  28. Janis CM, Scott KM, Jacobs LL et al. (1998) Evolution of Tertiary Mammals of North America, Vol. 1: Terrestrial Carnivores, Ungulates, and Ungulatelike Mammals. Cambridge, UK: Cambridge University Press.Google Scholar
  29. Koulischer L, Tijskens J, Mortelmans J (1971) Mammalian cytogenetics. IV. The chromosomes of two male Camelidae: Camelus bactrianus and Lama vicugna. Acta Zool Pathol Antverp 52: 89-2.PubMedGoogle Scholar
  30. Lahbib-Mansais Y, Karlskov-Mortensen P, Mompart F et al. (2005) A high-resolution comparative map between pig chromosome 17 and human chromosomes 4, 8, and 20: identification of synteny breakpoints. Genomics 86: 405-13.CrossRefPubMedGoogle Scholar
  31. Matthee C, Burzlaff JD, Taylor JF, Davis SK (2001) Mining the mammalian genome for artiodactyl systematics. Syst Biol 50: 367-90.CrossRefPubMedGoogle Scholar
  32. Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O’Brien SJ (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409: 614-18.CrossRefPubMedGoogle Scholar
  33. Nikaido M, Rooney AP, Okada N (1999) Phylogenetic relationships among cetartiodactyls based on insertions of short and long interpersed elements: hippopotamuses are the closest extant relatives of whales. Proc Natl Acad Sci USA 96: 10261-0266.CrossRefPubMedGoogle Scholar
  34. Pinton A, Ducos A, Yerle M (2003) Chromosomal rearrangements in cattle and pigs revealed by chromosome microdissection and chromosome painting. Genet Sel Evol 35: 685-96.CrossRefPubMedGoogle Scholar
  35. Price SA, Bininda-Emonds OR, Gittleman JL (2005) A complete phylogeny of the whales, dolphins and even-toed hoofed mammals (Cetartiodactyla). Biol Rev Camb Phil Soc 80: 445-73.CrossRefGoogle Scholar
  36. Schibler L, Vaiman D, Oustry A, Giraud-Delville C, Cribiu EP (1998) Comparative gene mapping: a fine-scale survey of chromosome rearrangements between ruminants and humans. Genome Res 8: 901-15.PubMedGoogle Scholar
  37. Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2: 971-72.CrossRefPubMedGoogle Scholar
  38. Skidmore JA, Billah M, Binns M, Short RV, Allen WR (1999) Hybridizing Old and New World camelids: Camelus dromedarius × Lama guanicoe. Proc Biol Sci 266: 649-56.CrossRefPubMedGoogle Scholar
  39. 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: 1587-597.PubMedGoogle Scholar
  40. Stanley HF, Kadwell M, Wheeler JC (1994) Molecular evolution of the family Camelidae: a mitochondrial study. Proc R Soc Lond B 256: 1-.CrossRefGoogle Scholar
  41. Taylor KM, Hungerford DA, Snyder RC, Ulmer FA (1968) Uniformity of karyotypes in the Camelidae. Cytogenetics 7: 8-5.CrossRefPubMedGoogle Scholar
  42. Telenius H, Pelmear AH, Tunnacliffe A et al. (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosomes Cancer 4: 257-63.CrossRefPubMedGoogle Scholar
  43. Theodor JM (2004) Molecular clock divergence estimates and the fossil record of Cetartiodactyla. J Paleontol 78: 39-4.CrossRefGoogle Scholar
  44. Wurster DH, Benirschke K (1968) Chromosome studies in the superfamily Bovoidea. Chromosoma 25: 152-71.CrossRefPubMedGoogle Scholar
  45. Yang F, Carter NP, Shi L, Ferguson-Smith MA (1995) A comparative study of karyotypes of muntjacs by chromosome painting. Chromosoma 103: 642-52.CrossRefPubMedGoogle Scholar
  46. Yang F, Fu B, O’Brien PC, Nie W, Ryder OA, Ferguson-Smith MA (2004) Refined genome-wide comparative map of the domestic horse, donkey and human based on cross-species chromosome painting: insight into the occasional fertility of mules. Chromosome Res 12: 65-6.CrossRefPubMedGoogle Scholar
  47. Yang F, Fu B, O’Brien PC, Robinson TJ, Ryder OA, Ferguson-Smith MA (2003) Karyotypic relationships of horses and zebras: results of cross-species chromosome painting. Cytogenet Genome Res 102: 235-43.CrossRefPubMedGoogle Scholar
  48. Yang F, Graphodatsky AS, Li T et al. (2006) Comparative genome maps of the pangolin, hedgehog, sloth, anteater and human revealed by cross-species chromosome painting: further insight into the ancestral karyotype and genome evolution of eutherian mammals. Chromosome Res 14: 283-86.CrossRefPubMedGoogle Scholar
  49. Yang F, Müller S, Just R, Ferguson-Smith MA, Wienberg J (1997a) Comparative chromosome painting in mammals: human and the Indian muntjac (Muntiacus muntjak vaginalis). Genomics 39: 396-01.CrossRefGoogle Scholar
  50. Yang F, O’Brien PC, Milne BS et al. (1999) A complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps. Genomics 62: 189-02.CrossRefPubMedGoogle Scholar
  51. Yang F, O’Brien PCM, Wienberg J, Ferguson-Smith MA (1997b) A reappraisal of the tandem fusion theory of karyotype evolution in the Indian muntjac using chromosome painting. Chromosome Res 5: 109-17.CrossRefGoogle Scholar
  52. Yang F, O’Brien PCM, Wienberg J, Neitzel H, Lin CC, Ferguson-Smith MA (1997c) Chromosomal evolution of the Chinese muntjac (Muntiacus reevesi). Chromosoma 106: 37-3.CrossRefGoogle Scholar
  53. Yousef MK (1991) Biometeorology and animal protein production: the case of arid lands. Int J Biometeorol 35: 176-79.CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Gabriel Balmus
    • 1
    • 4
  • Vladimir A. Trifonov
    • 1
    • 2
  • Larisa S. Biltueva
    • 2
  • Patricia C.M. O’Brien
    • 1
  • Elena S. Alkalaeva
    • 2
  • Beiyuan Fu
    • 1
  • Julian A. Skidmore
    • 5
  • Twink Allen
    • 6
  • Alexander S. Graphodatsky
    • 2
  • Fengtang Yang
    • 1
    • 3
    Email author
  • Malcolm A. Ferguson-Smith
    • 1
    Email author
  1. 1.Cambridge Resource Centre for Comparative Genomics, Department of Veterinary MedicineCambridgeUK
  2. 2.Institute of Cytology and Genetics, Russian Academy of SciencesNovosibirskRussia
  3. 3.Wellcome Trust Sanger InstituteHinxtonUK
  4. 4.University of Agricultural Sciences and Veterinary Medicine–Iasi, Faculty of Veterinary MedicineIasiRomania
  5. 5.Camel Reproduction CentreDubaiUnited Arab Emirates
  6. 6.Department of Clinical Veterinary Medicine, Equine Fertility UnitUniversity of CambridgeNewmarketUK

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