Skip to main content
SpringerLink
Log in

The complete mitochondrial genome of dhole Cuon alpinus: phylogenetic analysis and dating evolutionary divergence within canidae

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The dhole (Cuon alpinus) is the only existent species in the genus Cuon (Carnivora: Canidae). In the present study, the complete mitochondrial genome of the dhole was sequenced. The total length is 16672 base pairs which is the shortest in Canidae. Sequence analysis revealed that most mitochondrial genomic functional regions were highly consistent among canid animals except the CSB domain of the control region. The difference in length among the Canidae mitochondrial genome sequences is mainly due to the number of short segments of tandem repeated in the CSB domain. Phylogenetic analysis was progressed based on the concatenated data set of 14 mitochondrial genes of 8 canid animals by using maximum parsimony (MP), maximum likelihood (ML) and Bayesian (BI) inference methods. The genera Vulpes and Nyctereutes formed a sister group and split first within Canidae, followed by that in the Cuon. The divergence in the genus Canis was the latest. The divarication of domestic dogs after that of the Canis lupus laniger is completely supported by all the three topologies. Pairwise sequence divergence data of different mitochondrial genes among canid animals were also determined. Except for the synonymous substitutions in protein-coding genes, the control region exhibits the highest sequence divergences. The synonymous rates are approximately two to six times higher than those of the non-synonymous sites except for a slightly higher rate in the non-synonymous substitution between Cuon alpinus and Vulpes vulpes. 16S rRNA genes have a slightly faster sequence divergence than 12S rRNA and tRNA genes. Based on nucleotide substitutions of tRNA genes and rRNA genes, the times since divergence between dhole and other canid animals, and between domestic dogs and three subspecies of wolves were evaluated. The result indicates that Vulpes and Nyctereutes have a close phylogenetic relationship and the divergence of Nyctereutes is a little earlier. The Tibetan wolf may be an archaic pedigree within wolf subspecies. The genetic distance between wolves and domestic dogs is less than that among different subspecies of wolves. The domestication of dogs was about 1.56–1.92 million years ago or even earlier.

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

Similar content being viewed by others

References

  1. Thenius E (1954) On the origins of the dhole. Osterr Zoological Zeitsch 5:377–388

    Google Scholar 

  2. Cohen JA (1978) Cuon alpinus. Mammal Species 100:1–3

    Article  Google Scholar 

  3. Durbin L, Venkataraman A, Hedges S, Duckworth JW (2004) Dhole (Cuon alpinus). In: IUCN/SSC Canid Specialist Group, Sillero-Zubiri C, Hoffman M, Macdonald DW (eds) Canids: foxes, wolves, jackals and dogs. Information Press, Oxford, pp 210–219

    Google Scholar 

  4. Iyengar A, Babu VN, Hedges S, Venkataraman AB, Maclean N, Morin PA (2005) Phylogeography, genetic structure, diversity in the dhole (Cuon alpinus). Mol Ecol 14:2281–2297

    Article  CAS  PubMed  Google Scholar 

  5. Brown WM (1983) Evolution of animal mitochondrial DNA. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer Association, Sunderland, MA, pp 62–88

    Google Scholar 

  6. Wolstenholme DR (1992) Animal mitochondrial DNA: structure and evolution. In: Wolstenholme DR, Jeon KW (eds) Mitochondrial genomes. Academic Press, New York, pp 173–216

    Google Scholar 

  7. Avis JC (1994) Animal mitochondrial DNA. In: Avis JC (ed) Molecular markers, natural history and evolution. Kluwer Academic Publishers, New York, pp 60–68

    Google Scholar 

  8. Castro JA, Picornell A, Ramon M (1998) Mitochondrial DNA: a tool for population genetics studies. Int Microbiol 1:327–332

    CAS  PubMed  Google Scholar 

  9. Brown WM, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971

    Article  CAS  PubMed  Google Scholar 

  10. Miyata T, Hayashida H, Kikuno R, Hasegawa M, Kobayashi M, Koike K (1982) Molecular clock of silent substitutions: at least a sixfold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J Mol Evol 19:28–35

    Article  CAS  PubMed  Google Scholar 

  11. Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mtDNA: relevance for population biology and systematics. Annu Rev Ecol Syst 18:269–292

    Article  Google Scholar 

  12. Anderson S, Bankier AT, Barrell BG, Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJH, Staden R, Young IG (1981) Sequence and organization of the human mitochondrial genome. Nature 290:457–465

    Article  CAS  PubMed  Google Scholar 

  13. Wu X, Wang L, Chen S, Zan R, Xiao H, Zhang YP (2009) The complete mitochondrial genomes of two species from Sinocyclocheilus (Cypriniformes: Cyprinidae) and a phylogenetic analysis within Cyprininae. Mol Biol Rep. doi:10.1007/s11033-009-9689-x

  14. Ji X, Wu X, Yan P, Amato G (2008) Complete sequence and gene organization of the mitochondrial genome of Siamensis Crocodile (Crocodylus siamensis). Mol Biol Rep 35:133–138

    Article  CAS  PubMed  Google Scholar 

  15. Yang R, Wu X, Yan P, Su X, Yang B (2009) Complete mitochondrial genome of Otis tarda (Gruiformes: Otididae) and phylogeny of Gruiformes inferred from mitochondrial DNA sequences. Mol Biol Rep. doi:10.1007/s11033-009-9878-7

  16. Xu X, Arnason U (1994) The complete mitochondrial DNA sequence of the horse, Equus caballus: extensive heteroplasmy of the control region. Gene 148:357–362

    Article  CAS  PubMed  Google Scholar 

  17. Lopez JV, Cevario S, O’Brien SJ (1996) Complete nucleotide sequences of the domestic cat (Felis catus) mitochondrial genome and a transposed mtDNA tandem repeat (Numt) in the nuclear genome. Genomics 33(2):229–246

    Article  CAS  PubMed  Google Scholar 

  18. Janke A, Xu X, Arnason U (1997) The complete mitochondrial genome of the wallaroo (Macropus robustus) and the phylogenetic relationship among Monotremata, Marsupialia, and Eutheria. Proc Natl Acad Sci USA 94:1276–1281

    Article  CAS  PubMed  Google Scholar 

  19. Ursing BM, Arnason U (1998) The complete mitochondrial DNA sequence of the pig (Sus scrofa). J Mol Evol 47:302–306

    Article  CAS  PubMed  Google Scholar 

  20. Gissi C, Gullberg A, Arnason U (1998) The Complete mitochondrial DNA sequence of the Rabbit (Oryctolagus cuniculus). Genomics 50:161–169

    Article  CAS  PubMed  Google Scholar 

  21. Zhang P, Chen YQ, Liu YF, Zhou H, Qu LH (2003) The complete mitochondrial genome of the Chinese giant salamander, Andrias davidianus (Amphibia: Caudata). Gene 311:93–98

    Article  CAS  PubMed  Google Scholar 

  22. Brinkmann H, Denk A, Zitzler J, Joss JJ, Meyer A (2004) Complete mitochondrial genome sequences of the South American and the Australian lungfish: testing of the phylogenetic performance of mitochondrial data sets for phylogenetic problems in tetrapod relationships. J Mol Evol 59:834–848

    Article  CAS  PubMed  Google Scholar 

  23. Peng R, Zeng B, Meng X, Yue B, Zhang Z, Zou F (2007) The complete mitochondrial genome and phylogenetic analysis of the giant panda (Ailuropoda melanoleuca). Gene 397:76–83

    Article  CAS  PubMed  Google Scholar 

  24. Wada K, Nishibori M, Yokohama M (2007) The complete nucleotide sequence of mitochondrial genome in the Japanese Sika deer (Cervus nippon), and a phylogenetic analysis between Cervidae and Bovidae. Small Rumin Res 69:46–54

    Article  Google Scholar 

  25. Ki J, Hwang D, Park T, Han S, Lee J (2009) A comparative analysis of the complete mitochondrial genome of the Eurasian otter Lutra lutra (Carnivora: Mustelidae). Mol Biol Rep. doi:10.1007/s11033-009-9641-0

  26. Wei L, Wu X, Jiang Z (2009) The complete mitochondrial genome structure of snow leopard Panthera uncia. Mol Biol Rep 36:871–878

    Article  CAS  PubMed  Google Scholar 

  27. Kim KS, Seong EL, Ho WJ, Ha JH (1998) The complete nucleotide sequence of the domestic dog (Canis familiaris) mitochondrial genome. Mol Phylogenet Evol 10:210–220

    Article  CAS  PubMed  Google Scholar 

  28. Inoue T, Nonaka N, Mizuno A, Morishima Y, Sato H, Katakura K, Oku Y (2007) Mitochondrial DNA phylo-geography of the red fox (Vulpes vulpes) in northern Japan. Zool Sci 24:1178–1186

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  30. 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  CAS  PubMed  Google Scholar 

  31. Delisle I, Strobeck C (2005) A phylogeny of the Caniformia (order Carnivora) based on 12 complete protein-coding mitochondrial genes. Mol Phylogenet Evol 37:192–201

    Article  CAS  PubMed  Google Scholar 

  32. Arnason U, Gullberg A, Janke A, Kullberg M (2007) Mitogenomic analyses of caniform relationships. Mol Phylogenet Evol 45:863–874

    Article  CAS  PubMed  Google Scholar 

  33. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, vol 6, 3rd edn. Cold Spring Harbor Laboratory Press, New York, pp 4–58

    Google Scholar 

  34. Tompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DJ (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  Google Scholar 

  35. Lowe TM, Eddy SR (1997) tRNAscan-SE: a programfor improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  PubMed  Google Scholar 

  36. Kumazawa Y, Nishida M (1993) Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. J Mol Evol 37:380–398

    Article  CAS  PubMed  Google Scholar 

  37. Kumar S, Tamura K, Nei M (2004) MEGA: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  Google Scholar 

  38. Farris JS, Kluge AG, Eckardt MJ (1970) A numerical approach to phylogenetic systematics. Syst Zool 19:172–189

    Article  Google Scholar 

  39. Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416

    Article  Google Scholar 

  40. Felsenstein J (1981) Evolutionary trees from DNA sequences—a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  41. Rannala B, Yang ZH (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311

    Article  CAS  PubMed  Google Scholar 

  42. Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov chain Monte Carlo method. Mol Biol Evol 14:717–724

    CAS  PubMed  Google Scholar 

  43. Larget B, Simon D (1999) Markov chains Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759

    CAS  Google Scholar 

  44. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  45. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  46. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808

    Article  PubMed  Google Scholar 

  47. Swofford DL, Olsen GJ, Waddell PJ, Hillis DM (1996) Phylogenetic inference. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer, Sunderland, MA, pp 407–514

    Google Scholar 

  48. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  49. Kimura MA (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  50. Fu YX, Li WH (1997) Estimating the age of the common ancestor of a sample of DNA sequences. Mol Biol Evol 14:195–199

    CAS  PubMed  Google Scholar 

  51. Sbisa E, Tanzariello F, Reyes A, Pesole G, Saccone C (1997) Mammalian mitochondrial D-loop region structural analysis: identification of new conserved sequences and their functional and evolutionary implications. Gene 205:125–140

    Article  CAS  PubMed  Google Scholar 

  52. Pesole G, Gissi C, Chirico AD, Saccone C (1999) Nucleotide substitution rate of mammalian mitochondrial genomes. J Mol Evol 48:427–434

    Article  CAS  PubMed  Google Scholar 

  53. Meng C, Zhang H, Meng Q (2009) Mitochondrial genome of the Tibetan wolf. Mitochondrial DNA 20:61–63

    CAS  PubMed  Google Scholar 

  54. Simpson GG (1945) The principles of classification and a classification of mammals. Bull Am Mus Nat Hist 85:1–350

    Google Scholar 

  55. Ewer RF (1973) The carnivores. Cornell University Press, Now York

    Google Scholar 

  56. Van Valkenburgh B (1991) Iterative evolution of hypercarnivory in canids (Mammalia: Carnivora): evolutionary interactions among sympatric predators. Paleobiology 17:340–362

    Google Scholar 

  57. Kleiman DG, Eisenberg JF (1973) Comparisons of canid and felid social systems from an evolutionary perspective. Anim Behav 21:637–659

    Article  CAS  PubMed  Google Scholar 

  58. Lorenz KZ (1975) Foreword. In: Fox M (ed) The wild canids. Van Nostrand Reinhold, New York, pp vii–xii

    Google Scholar 

  59. Clutton-Brock J, Corbet GB, Hills M (1976) A review of the family Canidae, with a classification by numerical methods. Bull Br Mus 29:119–199

    Google Scholar 

  60. Berta A (1987) Origin, diversification and zoogeography of the South American Canidae. Fieldiana Zool 39:455–471

    Google Scholar 

  61. Lyras GA, Van Der Geer AAE (2003) External brain anatomy in relation to the phylogeny of Caninae (Carnivora: Canidae). Zool J Linn Soc 138:505–522

    Article  Google Scholar 

  62. Tedford RH, Taylor BE, Wang X (1995) Phylogeny of the Caninae (Carnivora: Canidae): the living taxa. Am Mus Novit 0:1–37

    Google Scholar 

  63. Bininda-Emonds ORP, Gittleman JL, Purvis A (1999) Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol Rev 74:143–175

    Article  CAS  PubMed  Google Scholar 

  64. Wayne RK, O’ Brien SJ (1987) Allozyme divergence within the Canidae. Syst Zool 36:339–355

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  67. Wayne RK, Nash WG, O’ Brien SJ (1987) Chromosomal evolution of the Canidae. II. Species with high diploid numbers. Cytogenet Cell Genet 44:123–133

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Natural Science Fund in China (30370218), the Program for New Century Excellent Talents in China (NCET-07-0507), the Natural Science Fund in Shandong Province of China (Z2008D01) and the Project of Science and Technology Development Plan in Shandong Province of China (2007GG2009011).

Author information

Authors and Affiliations

  1. College of Life Science, Qufu Normal University, Qufu, 273165, China

    Honghai Zhang & Lei Chen

  2. College of Wildlife Resource, Northeast Forestry University, Harbin, 150040, China

    Lei Chen

Authors
  1. Honghai Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lei Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Honghai Zhang.

Additional information

Lei Chen and Honghai Zhang contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 163 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, H., Chen, L. The complete mitochondrial genome of dhole Cuon alpinus: phylogenetic analysis and dating evolutionary divergence within canidae. Mol Biol Rep 38, 1651–1660 (2011). https://doi.org/10.1007/s11033-010-0276-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-010-0276-y

Keywords

Search

Navigation