Journal of Molecular Evolution

, Volume 43, Issue 6, pp 641–649 | Cite as

Phylogenetic relationships within caniform carnivores based on analyses of the mitochondrial 12S rRNA gene

  • Christina Ledje
  • Ulfur Arnason


The complete 12S rRNA gene of 32 carnivore species, including four feliforms and 28 caniforms, was sequenced. The sequences were aligned on the basis of their secondary structures and used in phylogenetic analyses that addressed several evolutionary relationships within the Caniformia. The analyses showed an unresolved polytomy of the basic caniform clades; pinnipeds, mustelids, procyonids, skunks,Ailurus (lesser panda), ursids, and canids. The polytomy indicates a major diversification of caniforms during a relatively short period of time. The lesser panda was distinct from other caniforms, suggesting its inclusion in a monotypic family, Ailuridae. The giant panda and the bears were joined on the same branch. The skunks are traditionally included in the family Mustelidae. The present analysis, however, showed a less close molecular relationship between the skunks and the remaining Mustelidae (sensu stricto) than between Mustelidae (sensu stricto) and Procyonidae, making Mustelidae (sensu lato) paraphyletic. The results suggest that the skunks should be included in a separate family, Mephitidae. Within the Pinnipedia, the grouping of walrus, sea lions, and fur seals was strongly supported. Analyses of a combined set of 12S rRNA and cytochromeb data were generally consistent with the findings based on each gene.

Key words

Carnivora Caniformia Feliformia Canidae Ailuridae Musteloidea Ursidae Pinnipedia Mitochondrial DNA 12S rRNA Secondary structure Phylogeny 


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  1. Allard MW, Honeycutt RL (1992) Nucleotide sequence variation in the mitochondrial 12S rRNA gene and the phylogeny of African mole-rats (Rodentia: Bathyergidae). Mol Biol Evol 9:27–40Google Scholar
  2. Allard MW, Miyamoto MM, Jarecki L, Kraus F, Tennant MR (1992) DNA systematics and evolution of the artiodactyl family Bovidae. Proc Natl Acad Sci 89:3972–3976Google Scholar
  3. Arnason U, Gullberg A (1996) Sequence analyses of the mitochondrial cytochrome b gene identify five primary evolutionary lineages of extant cetaceans. Mol Biol Evol 13:407–417Google Scholar
  4. Arnason U, Johnsson E (1992) The complete mitochondrial DNA sequence of the harbor seal,Phoca vitulina. J Mol Evol 34:493–505Google Scholar
  5. Arnason U, Ledje C (1993) The use of highly repetitive DNA for resolving cetacean and pinniped phylogenies. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal phylogeny, Placentals, vol 2. Springer-Verlag, New York, pp 74–80Google Scholar
  6. Arnason U, Widegren B (1986) Pinniped phylogeny enlightened by molecular hybridizations using highly repetitive DNA. Mol Biol Evol 3:356–365Google Scholar
  7. Arnason U, Gretardsdottir S, Gullberg A (1993a) Comparisons between the 12S rRNA, 16S rRNA, NADH1 and COI genes of sperm and fin whale mitochondrial DNA. Biochem Syst Ecol 21:115–122Google Scholar
  8. Arnason U, Gullberg A, Johnsson E, Ledje C (1993b) The nucleotide sequence of the mitochondrial DNA molecule of the grey seal, Halichoerus grypus, and a comparison with mitochondrial sequences of other true seals. J Mol Evol 37:323–330Google Scholar
  9. Arnason U, Bodin K, Gullberg A, Ledje C, Mouchaty S (1995) A molecular view of pinniped relationships with particular emphasis on the true seals. J Mol Evol 40:78–85Google Scholar
  10. Barnes LG (1979) Fossil enaliarctine pinnipeds (Mammalia: Otariidae) from Pyramid Hill, Kern county, California. Contrib Sci Nat History Mus LA 318:1–41Google Scholar
  11. Berta A, Ray CE, Wyss AR (1989) Skeleton of the oldest known pinniped Enaliarctos mealsi. Science 244:60–62Google Scholar
  12. Bryant HN, Russell Fls AP, Fitch WD (1993) Phylogenetic relationships within the extant Mustelidae (Carnivora): appraisal of the cladistic status of the Simpsonian subfamilies. Zool J Linnean Soc 108:301–334Google Scholar
  13. Cao Y, Adachi J, Janke A, Pääbo S, Hasegawa M (1994) Phylogenetic relationships among eutherian orders estimated from inferred sequences of mitochondrial proteins: instability of a tree based on a single gene. J Mol Evol 39:519–527Google Scholar
  14. Cummings MP, Otto SP, Wakeley J (1995) Sampling properties of DNA sequence data in phylogenetic analysis. Mol Biol Evol 12:814–822Google Scholar
  15. Czelusniak J, Goodman M, Koop BF, Tagle DA, Shoshani J, Braunitzer G, Kleinschmidt TK, de Jong WW, Matsuda G (1990) Perspectives from amino acid and nucleotide sequences on cladistic relationships among higher taxa of Eutheria. In: Genoways HH (ed) Current mammalogy, vol 2. Plenum, pp 545–572Google Scholar
  16. de Jong WW, Leunissen JAM, Wistow GJ (1993) Eye lens crystallins and the phylogeny of placental orders: evidence for a macroscelidpaenungulate clade? In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal phylogeny, placentals, vol 2. Springer-Verlag, New York, pp 5–12Google Scholar
  17. Douzery E (1993) Evolutionary relationships among Cetacea based on the sequence of the mitochondrial 12S rRNA gene: possible paraphyly of toothed-whales (Odontocetes) and long separate evolution of sperm whales (Physeteridae). CR Acad Sci Paris Sci vie 316:1511–1518Google Scholar
  18. Douzery E, Catzeflis FM (1995) Molecular evolution of the mitochondrial 12S rRNA in Ungulata (Mammalia). J Mol Evol 41:622–636Google Scholar
  19. Felsenstein J (1993) PHYLIP, 3.5c edn, Department of Genetics SK-50, University of Washington, SeattleGoogle Scholar
  20. Flynn JJ, Neff NA, Tedford RH (1988) Phylogeny of the Carnivora. In: Benton MJ (ed) The phylogeny and classification of the tetrapods, Mammals, vol 2. Clarendon Press, Oxford, pp 73–115Google Scholar
  21. Gatesy J, Yelon D, DeSalle R, Vrba ES (1992) Phylogeny of the Bovidae (Artiodactyla, Mammalia) based on mitochondrial ribosomal DNA sequences. Mol Biol Evol 9:433–446Google Scholar
  22. Gutell RR (1994) Collection of small subunit (16S and 16S-like) ribosomal RNA structures: 1994. Nucleic Acids Res 22:3502–3507Google Scholar
  23. Gutell RR, Woese CR (1990) Higher order structural elements in ribosomal RNAs: pseudo-knots and the use of noncanonical pairs. Proc Natl Acad Sci 87:663–667Google Scholar
  24. Gutell RR, Weiser B, Woese CR, Noller HF (1985) Comparative anatomy of 16-S-like ribosomal RNA. Prog Nucleic Acid Res Mol Biol 32:155–215Google Scholar
  25. Gutell RR, Larsen N, Woese CR (1994) Lessons from an evolving ribosomal RNA: 16S and 23S rRNA structure from a comparative perspective. Microbiol Rev 58:10–26Google Scholar
  26. Hänni C, Laudet V, Barriel V, Catzeflis FM (1995) Evolutionary relationships of Acomys and other murids (rodentia, mammalia) based on complete 12S rRNA mitochondrial gene sequences. Israel J Zool 41:131–146Google Scholar
  27. Hickson RE, Simon C, Cooper A, Spicer GS, Sullivan J, Penny D (1996) Conserved sequence motifs, alignment, and secondary structure for the third domain of animal 12S rRNA. Mol Biol Evol 13:150–169Google Scholar
  28. Hixon JE, Brown WM (1986) A comparison of the small ribosomal RNA genes from the mitochondrial DNA of the great apes and humans: sequence, structure, evolution, and phylogenetic implications. Mol Biol Evol 3:1–18Google Scholar
  29. Janczewski DN, Modi WS, Stephens JC, O'Brien SJ (1995) Molecular evolution of mitochondrial 12S RNA and cytochrome b sequences in the pantherine lineage of Felidae. Mol Biol Evol 12:690–707Google Scholar
  30. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New YorkGoogle Scholar
  31. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120Google Scholar
  32. Kjer KM (1995) Use of rRNA secondary structure in phylogenetic studies to identify homologous positions: an example of alignment and data presentation from the frogs. Mol Phylogenet Evol 4:314–330Google Scholar
  33. Kraus F, Miyamoto MM (1991) Rapid cladogenesis among the pecoran ruminants: evidence from mitochondrial DNA sequences. Syst Zool 40:117–130Google Scholar
  34. Krettek A, Gullberg A, Arnason U (1995) Sequence analysis of the complete mitochondrial DNA molecule of the hedgehog, Erinaceus europaeus, and the phylogenetic position of the Erinaceidae. J Mol Evol 41:952–957Google Scholar
  35. Ledje C, Arnason U (1996) Phylogenetic analyses of complete cytochrome b genes of the order Carnivora with particular emphasis on the Caniformia. J Mol Evol 42:135–144Google Scholar
  36. Lento GM, Hickson RE, Chambers GK, Penny D (1995) Use of spectral analysis to test hypotheses on the origin of pinniped. Mol Biol Evol 12:28–52Google Scholar
  37. Maddison WP, Maddison DR (1992) MacClade, analysis of phylogeny and character evolution, 3.02 edn. Sinauer, Sunderland, MA, pp 398Google Scholar
  38. Miyamoto MM, Boyle SM (1989) The potential importance of mitochondrial DNA sequence data to eutherian mammal phylogeny. In: Fernholm B, Bremer K, Jörnvall H (eds) The hierarchy of life. Excerpta Medica, Amsterdam, pp 437–450Google Scholar
  39. Miyamoto MM, Kraus F, Ryder OA (1990) Phylogeny and evolution of antlered deer determined from mitochondrial DNA sequences. Proc Natl Acad Sci 87:6127–6131Google Scholar
  40. Neefs J-M, Van de Peer Y, De Rijk P, Chapelle S, De Wachter R (1993) Compilation of small ribosomal subunit RNA structures. Nucleic Acids Res 21:3025–3049Google Scholar
  41. O'Brien SJ, Nash WG, Wildt DE, Bush ME, Benveniste RE (1985) A molecular solution to the riddle of the giant panda's phylogeny. Nature 317:140–144Google Scholar
  42. Repenning CA, Tedford RH (1977) Otarioid seals of the Neogene. US Government Printing Office, Washington, DCGoogle Scholar
  43. Repenning CA, Ray CE, Grigorescu D (1979) Pinniped biogeography. In: Gray J, Boucot AJ (eds) Historical biogeography, plate tectonics, and the changing environment. Oregon State University Press, Corvallis, pp 357–369Google Scholar
  44. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  45. Sarich VM (1969) Pinniped origins and the rate of evolution of carnivore albumins. Syst Zool 18:186–295Google Scholar
  46. Sarich VM (1973) The giant panda is a bear. Nature 245:218–220Google Scholar
  47. Slattery JP, O'Brien SJ (1995) Molecular phylogeny of the red panda (Ailurus fulgens). J Heredity 86:413–422Google Scholar
  48. Sourrouille P, Hänni C, Ruedi M, Catzeflis FM (1995) Molecular systematics of Mus crociduroides, an endemic mouse of Sumatra (Muridae: Rodentia). Mammalia 59:91–102Google Scholar
  49. Springer MS, Hollar LJ, Burk A (1995) Compensatory substitutions and the evolution of the mitochondrial 12S rRNA gene in mammals. Mol Biol Evol 12:1138–1150Google Scholar
  50. Swofford DL (1993) PAUP, phylogenetic analysis using parsimony, 3.1.1 edn, Computer program distributed by the Illinois Natural History Survey, Champaign, ILGoogle Scholar
  51. Tedford RH (1976) Relationship of pinnipeds to other carnivores (Mammalia). Syst Zool 25:363–374Google Scholar
  52. Van der Peer Y, Van den Broeck I, De Rijk P, De Wachter R (1994) Database on the structure of small ribosomal subunit RNA. Nucleic Acids Res 22:3488–3494Google Scholar
  53. Vrana PB, Milinkovitch MC, Powell JR, Wheeler WC (1994) Higher level relationships of the arctoid carnivora based on seuqnece data and “total evidence”. Mol Phylogenet Evol 3:47–58Google Scholar
  54. Wayne RK (1993) Molecular evolution of the dog family. Trends Genet 9:218–224Google Scholar
  55. Wayne RK, Benveniste RE, Janczewski DN, O'Brien SJ (1989) Molecular and biochemical evolution of the Carnivora. In: Gittleman JL (ed) Carnivore behavior, ecology, and evolution. Cornell University Press, Ithaca, NY, pp 465–494Google Scholar
  56. Wilson DE, Reeder DM (eds) (1993) Mammal species of the world. A taxonomic and geographic reference. Smithsonian Institution Press, Washington, 1207 ppGoogle Scholar
  57. Wozencraft WC (1989) The phylogeny of the recent carnivora. In: Gittleman JL (ed) Carnivore behavior, ecology, and evolution. Chapman and Hall, London, pp 495–535Google Scholar
  58. Wyss AR (1987) The walrus auditory region and the monophyly of pinnipeds. Am Mus Novit 2871:1–13Google Scholar
  59. Wyss AR (1988) Evidence from flipper structure for a single origin of pinnipeds. Nature 334:427–428Google Scholar
  60. Wyss AR, Flynn JJ (1993) A phylogenetic analysis and definition of the Carnivora. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal phylogeny, placentals, vol 2. Springer-Verlag, New York, pp 32–52Google Scholar
  61. Xu X, Arnason U (1994) The complete mitochondrial DNA sequence of the horse, Equus caballus: extensive heteroplasmy of the control region. Gene 148:357–362Google Scholar
  62. Xu X, Arnason U (1996) The complete mitochondrial DNA sequence of the white rhinoceros,Ceratotherium simum, and comparison with the mtDNA of Indian rhinoceros,Rhinoceros unicornis. Mol Phyl Evol (in press)Google Scholar
  63. Xu X, Janke A, Arnason U (1996) The complete mitochondrial DNA sequence of the greater Indian rhinoceros,Rhinoceros unicornis, and the phylogenetic relationship among Carnivora, Perissodactyla and Artiodactyla (+Cetacea). Mol Biol Evol (in press)Google Scholar
  64. Zhang Y-P, Ryder OA (1993) Mitochondrial DNA sequence evolution in the Arctoidea. Proc Natl Acad Sci 90:9557–9561Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1996

Authors and Affiliations

  • Christina Ledje
    • 1
  • Ulfur Arnason
    • 1
  1. 1.Division of Evolutionary Molecular Systematics, Department of GeneticsUniversity of LundLundSweden

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