Skip to main content
SpringerLink
Log in

Phylogenomics of the dog and fox family (Canidae, Carnivora) revealed by chromosome painting

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Canid species (dogs and foxes) have highly rearranged karyotypes and thus represent a challenge for conventional comparative cytogenetic studies. Among them, the domestic dog is one of the best-mapped species in mammals, constituting an ideal reference genome for comparative genomic study. Here we report the results of genome-wide comparative mapping of dog chromosome-specific probes onto chromosomes of the dhole, fennec fox, and gray fox, as well as the mapping of red fox chromosome-specific probes onto chromosomes of the corsac fox. We also present an integrated comparative chromosome map between the species studied here and all canids studied previously. The integrated map demonstrates an extensive conservation of whole chromosome arms across different canid species. In addition, we have generated a comprehensive genome phylogeny for the Canidae on the basis of the chromosome rearrangements revealed by comparative painting. This genome phylogeny has provided new insights into the karyotypic relationships among the canids. Our results, together with published data, allow the formulation of a likely Canidae ancestral karyotype (CAK, 2n = 82), and reveal that at least 6–24 chromosomal fission/fusion events are needed to convert the CAK karyotype to that of the modern canids.

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

Similar content being viewed by others

References

  • Bardeleben C, Moore RL, Wayne RK (2005) A molecular phylogeny of the Canidae based on six nuclear loci. Mol Phylogenet Evol 37: 815–831.

    Article  PubMed  CAS  Google Scholar 

  • Biltueva L, Yang F, Vorobieva NV, Graphodatsky AS (2004) Comparative map between the domestic pig and dog. Mamm Genome 15: 809–818.

    Article  PubMed  CAS  Google Scholar 

  • Bininda-Emonds ORP, Gittleman J, Purvis A (1999) Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol Rev 74: 143–173.

    Article  PubMed  CAS  Google Scholar 

  • Bininda-Emonds ORB, Cardillo M, Jones KE et al. (2007) The delayed rise of present-day mammals. Nature 446: 507–512.

    Article  PubMed  CAS  Google Scholar 

  • Breen M, Thomas R, Binns MM, Carter NP, Langford CF (1999) Reciprocal chromosome painting revealed detailed regions of conserved synteny between the karyotypes of the domestic dog (Canis familiaris) and human. Genomics 61: 145–155.

    Article  PubMed  CAS  Google Scholar 

  • Breen M, Hitte C, Lorentzen TD et al. (2004) An integrated 4249 marker FISH/RH map of the canine genome. BMC Genomics 5: 65.

    Article  PubMed  CAS  Google Scholar 

  • Cavagna P, Menotti A, Stanyon R (2000) Genomic homology of the domestic ferret with cats and humans. Mamm Genome 11: 866–870.

    Article  PubMed  CAS  Google Scholar 

  • Dobigny G, Ducroz JF, Robinson TJ, Volobouev V (2004) Cytogenetics and cladistics. Syst Biol 53: 470–484.

    Article  PubMed  Google Scholar 

  • Froenicke L, Muller-Navia K, Romanakis K, Scherthan H (1997) Zoo-FISH maps of the harbor seal (Phoca vitulina) and the putative ancestral carnivore karyotype. Chromosoma 106: 108–113.

    Article  CAS  Google Scholar 

  • Graphodatsky AS (2007) Comparative chromosomics. Mol Biol (Russ) 41: 408–422.

    Google Scholar 

  • Graphodatsky AS, Radjabli SI (1981) Comparative cytogenetics of three canids species. Genetica (Russ) 17: 1498–1504.

    Google Scholar 

  • Graphodatsky AS, Beklemisheva VR, Dolf G (1995) High resolution GTG-banding patterns of dog and silver fox chromosomes description and comparative analysis. Cytogenet Cell Genet 69: 226–231.

    PubMed  CAS  Google Scholar 

  • Graphodatsky AS, Yang F, O’Brien PC et al. (2000a) A comparative chromosome map of the Arctic fox, red fox and dog defined by chromosome painting and high resolution G-banding. Chromosome Res 8: 253–263.

    Article  PubMed  CAS  Google Scholar 

  • Graphodatsky AS, Yang F, Serdukova N, Perelman P, Zhdanova N, Ferguson-Smith MA (2000b) Dog chromosome-specific paints reveal evolutionary inter- and intrachromosomal rearrangements in the American mink and human. Cytogenet Cell Genet 90: 275–278.

    Article  PubMed  CAS  Google Scholar 

  • Graphodatsky AS, Yang F, O’Brien PCM et al. (2001) Phylogenetic implications of the 38 putative ancestral chromosome segments for four canid species. Cytogenet Cell Genet 92: 243–247.

    Article  PubMed  CAS  Google Scholar 

  • Graphodatsky AS, Yang F, Perelman P et al. (2002) Comparative molecular cytogenetic studies in the order Carnivora: mapping chromosomal rearrangements onto the phylogenetic tree. Cytogenet Genome Res 96: 137–145.

    Article  PubMed  CAS  Google Scholar 

  • Gustavsson I, Sundt CO (1967) Chromosome elimination in the evolution of the silver fox. J Hered 58: 75–78.

    PubMed  CAS  Google Scholar 

  • Hameister H, Klett C, Bruch J, Dixkens C, Vogel W, Christensen K (1997) Zoo-FISH analysis: the American mink (Mustela vison) closely resembles the cat karyotype. Chromosome Res 5: 5–11.

    Article  PubMed  CAS  Google Scholar 

  • Kukekova AV, Trut LN, Oskina IN et al. (2007) A meiotic linkage map of the silver fox. Genome Res 17: 387–399.

    Article  PubMed  CAS  Google Scholar 

  • Lindblad-Toh K, Wade CM, Mikkelsen TS et al. (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438: 803–819.

    Article  PubMed  CAS  Google Scholar 

  • Mäkinen A, Gustavsson I (1982) A comparative chromosome-banding study in the silver fox, the blue fox, and their hybrids. Hereditas 97: 289–297.

    Article  Google Scholar 

  • Murphy WJ, Stanyon R, O’Brien SJ (2001) Evolution of mammalian genome organization inferred from comparative gene mapping. Genome Biol 2: 0005.1–0005.8.

    Article  Google Scholar 

  • Nash WG, Wienberg J, Ferguson-Smith MA, Menninger JC, O’Brien SJ (1998) Comparative genomics: tracking chromosome evolution in the family Ursidae using reciprocal chromosome painting. Cytogenet Cell Genet 83: 182–192.

    Article  PubMed  CAS  Google Scholar 

  • Nash WG, Menninger JC, Wienberg J, Padilla-Nash HM, O’Brien SJ (2001) The pattern of phylogenomic evolution of the Canidae. Cytogenet Cell Genet 95: 210–224.

    Article  PubMed  CAS  Google Scholar 

  • Nie W, Wang J, O’Brien PCM et al. (2002) The genome phylogeny of domestic cat, red panda and five mustelid species revealed by comparative chromosome painting and G-banding. Chromosome Res 10: 209–222.

    Article  PubMed  CAS  Google Scholar 

  • Nie W, Wang J, Perelman P, Graphodatsky AS, Yang F (2003) Comparative chromosome painting defines the karyotypic relationships among the domestic dog, Chinese raccoon dog and Japanese raccoon dog. Chromosome Res 11: 735–740.

    Article  PubMed  CAS  Google Scholar 

  • Perelman PL, Graphodatsky AS, Serdukova NA et al. (2005) Karyotypic conservatism in the Suborder Feliformia (Order Carnivora). Cytogenet Genome Res 108: 348–354.

    Article  PubMed  CAS  Google Scholar 

  • Rettenberger G, Klett Ch, Zechner U et al. (1995) Zoo-FISH analysis: cat and human karyotypes closely resemble the putative ancestral mammalian karyotype. Chromosome Res 3: 479–486.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (1998) PAUP (1998). Phylogenetic Analysis Using Parsimony, version 4.0. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Tian Y, Nie W, Wang J, Yang F, Ferguson-Smith MA (2004) Chromosome evolution in bears: reconstructing phylogenetic relationships by cross-species chromosome painting. Chromosome Res 12: 55–63.

    Article  PubMed  CAS  Google Scholar 

  • Trifonov VA, Perelman PL, Kawada SI, Iwasa MA, Oda SI, Graphodatsky AS (2002) Complex structure of B-chromosomes in two mammalian species: Apodemus peninsulae (Rodentia) and Nyctereutes procyonoides (Carnivora). Chromosome Res 10: 109–116.

    Article  PubMed  CAS  Google Scholar 

  • Vila C, Maldonado JE, Wayne RK (1999) Phylogenetic relationships, evolution, and genetic diversity of the domestic dog. J Hered 90: 71–77.

    Article  PubMed  CAS  Google Scholar 

  • Wayne RK, Nash WG, O’Brien SJ (1987a) Chromosome evolution of the Canidae I: species with high diploid numbers. Cytogenet Cell Genet 44: 123–133.

    PubMed  CAS  Google Scholar 

  • Wayne RK, Nash WG, O’Brien SJ (1987b) Chromosome evolution of the Canidae II: divergence from the primitive carnivore karyotype. Cytogenet Cell Genet 44: 134–141.

    PubMed  CAS  Google Scholar 

  • Wayne RK, Geffen E, Girman DJ, Koepfli KP, Lau LM, Marshall CR (1997) Molecular systematics of the Canidae. Syst Biol 46: 622–653.

    Article  PubMed  CAS  Google Scholar 

  • Wienberg J, Stanyon R, Nash WG et al. (1997) Conservation of human vs. feline genome organization revealed by reciprocal chromosome painting. Cytogenet Cell Genet 77: 211–217.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Graphodatsky AS (2004) Integrated comparative genome maps and their implications for karyotype evolution of carnivores. In: Schmid M, Nanda I, eds. Chromosomes Today, Vol. 14. Dordrecht: Kluwer Academic Publishers, pp. 215–224.

    Google Scholar 

  • 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: 189–202.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Graphodatsky AS, O’Brien PCM et al. (2000) Reciprocal chromosome painting illuminates the history of genome evolution of the domestic cat, dog and human. Chromosome Res 8: 393–404.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Cytology and Genetics, SB RAS, Novosibirsk, 630090, Russia

    Alexander S. Graphodatsky, Polina L. Perelman, Natalya V. Sokolovskaya, Violetta R. Beklemisheva & Natalya A. Serdukova

  2. Laboratory of Genomic Diversity, National Cancer Institute, Frederick, MD, 21702, USA

    Polina L. Perelman & Stephen J. O’Brien

  3. Institut de Recherche pour le Développement, Centre de Biologie et Gestion des Populations, Campus International de Baillarguet, CS30016, 34988, Montferrier-sur-Lez, France

    Gauthier Dobigny

  4. Cambridge Resource Centre for Comparative Genomics, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge, CB3 0ES, UK

    Malcolm A. Ferguson-Smith

  5. The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, CB10 1SA, UK

    Fengtang Yang

Authors
  1. Alexander S. Graphodatsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Polina L. Perelman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalya V. Sokolovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Violetta R. Beklemisheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Natalya A. Serdukova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gauthier Dobigny
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Stephen J. O’Brien
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Malcolm A. Ferguson-Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fengtang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander S. Graphodatsky.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Figure S1

Diploid G-banded karyotype of fennec fox and gray fox. Summary of hybridization pattern of domestic dog probes onto G-banded fennec fox and gray fox chromosomes (JPEG 501 kb)

Supplementary Figure S2

A single tree retrieved from PAUP analysis of 88 characters rooted on bears, with changes mapped onto the topology. Bootstrap values are provided above branches (JPEG 769 kb)

Supplementary Table S1

Matrix of chromosomal characters corresponding to presence (1) or absence (0) of segmental associations of dog chromosomal fragments (XLS 96 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Graphodatsky, A.S., Perelman, P.L., Sokolovskaya, N.V. et al. Phylogenomics of the dog and fox family (Canidae, Carnivora) revealed by chromosome painting. Chromosome Res 16, 129–143 (2008). https://doi.org/10.1007/s10577-007-1203-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-007-1203-5

Key words

Search

Navigation