Journal of Molecular Evolution

, Volume 46, Issue 4, pp 382–388

The mitochondrial DNA molecule of the hagfish (myxine glutinosa) and vertebrate phylogeny

Article

Abstract

The vertebrates are traditionally classified into two distinct groups, Agnatha (jawless vertebrates) and Gnathostomata (jawed vertebrates). Extant agnathans are represented by hagfishes (Myxiniformes) and lampreys (Petromyzontiformes), frequently grouped together within the Cyclostomata. Whereas the recognition of the Gnathostomata as a clade is commonly acknowledged, a consensus has not been reached regarding whether or not Cyclostomata represents a clade. In the present study we have used newly established sequences of the protein-coding genes of the mitochondrial DNA molecule of the hagfish to explore agnathan and gnathostome relationships. The phylogenetic analysis of Pisces, using echinoderms as outgroup, placed the hagfish as a sister group of Vertebrata sensu stricto, i.e., the lamprey and the gnathostomes. The phylogenetic analysis of the Gnathostomata identified a basal divergence between gnathostome fishes and a branch leading to birds and mammals, i.e., between “Anamnia” and Amniota. The lungfish has a basal position among gnathostome fishes with the teleosts as the most recently evolving lineage. The findings portray a hitherto unrecognized polarity in the evolution of bony fishes. The presently established relationships are incompatible with previous molecular studies.

Key words

Molecular phylogeny Vertebrate evolution Cyclostomata Gnathostomata Pisces “Anamnia” Amniota 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adachi J (1995) Modeling of molecular evolution and maximum likelihood inference of molecular phylogeny. PhD thesis, The Graduate University for Advanced Studies, TokyoGoogle Scholar
  2. Adachi J, Hasegawa M (1996a) MOLPHY: programs for molecular phylogenetics based on maximum likelihood. Comput Sci Monographs Inst Stat Math Tokyo 28:1–150Google Scholar
  3. Adachi J, Hasegawa M (1996b) Model of amino acid substitution in proteins encoded by mitochondrial DNA. J Mol Evol 42:459–468PubMedCrossRefGoogle Scholar
  4. Ahlberg PE, Milner AR (1994) The origin and early diversification of tetrapods. Nature 368:507–513CrossRefGoogle Scholar
  5. Anderson S, de Brujin MHL, Coulson AR, Eperon IC, Sanger F, Young G (1982) Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717PubMedCrossRefGoogle Scholar
  6. Arnason U, Johnsson E. (1992) The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina. J Mol Evol 34:493–505PubMedCrossRefGoogle Scholar
  7. Arnason U, Gullberg A, Widegren B (1991) The complete nucleotide sequence of the mitochondrial DNA of the fin whale, Balenoptera physalus. J Mol Evol 33:556–568PubMedCrossRefGoogle Scholar
  8. Asakawa S, Himeno H, Miura K, Watanabe K (1995) Nucleotide sequence and gene organization of the starfish Asterina pectinifera mitochondrial genome. Genetics 140:1047–1060PubMedGoogle Scholar
  9. Bjerring HC (1985) Facts and thoughts on piscine phylogeny. In: Foreman RE, Gorbman A, Dodd JM, Olsson R (eds) Evolutionary biology of primitive fishes. Plenum Press, New York, pp 31–57Google Scholar
  10. Bjerring HC (1989) Apertures of craniate olfactory organs. Acta Zool 70:71–85CrossRefGoogle Scholar
  11. Brodai A, Fänge R (1963) The biology of Myxine. Universitetsforlaget, OsloGoogle Scholar
  12. Cabot EL, Beckenbach AT (1988) Simultaneous editing of multiple nucleic and protein sequences with ESEE. Comput Appl Biosci 5:233–234Google Scholar
  13. Cao Y, Adachi J, Janke A, Pääbo S, Hasegawea 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 39:519–527PubMedCrossRefGoogle Scholar
  14. Cloutier R, Ahlberg PE (1996) Interrelationships of basal sarcopterygians. In: Stiassny MLJ, Parenti LR, Johnson GD (eds) Interrelationships of fishes. Academic Press, New York, pp 445–480CrossRefGoogle Scholar
  15. de Giorgi C, Martiradonna A, Lanave C, Saccone C (1996) Complete sequence of the mitochondrial DNA in the sea urchin Arbacia lixula: conserved features of the echinoid mitochondrial genome. Mol Phylogenet Evol 5:323–332PubMedCrossRefGoogle Scholar
  16. Desjardins P, Morais R (1990) Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol 212:599–634PubMedCrossRefGoogle Scholar
  17. Duméril AMC (1806) Zoologie analytique, ou méthode naturelle de classification des aimaux. Didot, ParisGoogle Scholar
  18. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376PubMedCrossRefGoogle Scholar
  19. Felsenstein J (1991) Phylogenetic inference programs (PHYLIP). University of Washington, SeattleGoogle Scholar
  20. Fitch WM (1971) Toward defining the course of evolution, minimum change from a specific tree topology. Syst Zool 20:406–415CrossRefGoogle Scholar
  21. Forey PL (1987) Relationships of lungfishes. In: Bemis WE, Burggren WW, Kemp NE (eds) Biology and evolution of lungfishes. J Morphol Suppl 1:75–91Google Scholar
  22. Forey PL (1995) Agnathans recent and fossil, and the origin of jawed vertebrates. Revs Fish Biol Fisheries 5:267–303CrossRefGoogle Scholar
  23. Forey PL, Janvier P (1993) Agnathans and the origin of jawed vertebrates. Nature 361:129–134CrossRefGoogle Scholar
  24. Forey PL, Janvier P (1994) Evolution of the early vertebrates. Am Sci 82:554–565Google Scholar
  25. Gee H (1996) Before the backbone. Chapman, Hall, LondonGoogle Scholar
  26. Genetics Computer Group (1994) Program manual for the Wisconsin package, version 8Google Scholar
  27. Goodman M, Miyamoto MM, Czelusniak J (1987) Pattern and process in vertebrate phylogeny revealed by coevolution of molecules and morphologies. In: Patterson C (ed) Molecules and morphology in evolution: conflict or compromise? Cambridge University Press, pp 141–176Google Scholar
  28. Gorr T, Kleinschmidt T (1993) Evolutionary relationships of the coelacanth. Am Sci 81:72–82Google Scholar
  29. Hardisty MW (1982) Lampreys and hagfishes: analysis of cyclostome relationships. In: Hardisty MW, Potter JC (eds) The biology of Lampreys, vol 4B. Academic Press, London, pp 165–259Google Scholar
  30. Härlid A, Janke A, Arnason U (1997) The mtDNA sequence of the ostrich and the divergence between paleognathous and neognathous birds. Mol Biol Evol 14:754–761PubMedGoogle Scholar
  31. Jacobs HT, Elliott DJ, Math VB, Farquharson A (1988) Nucleotide sequence and gene organization of seaurchin mitochondrial DNA. J Mol Biol 202:185–217PubMedCrossRefGoogle Scholar
  32. Janke A, Feldmaier-Fuchs G, Thomas WK, von Haeseler A, Pääbo S (1994) The marsuipial mitochondrial genome and the evolution of placental mammals. Genetics 137:243–256PubMedGoogle Scholar
  33. 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 94:1276–1281PubMedCrossRefGoogle Scholar
  34. Janvier P (1978) Les nageoires paires des Ostéostracés et al position systématique des Céphalaspidomorphes. Ann Paléontol (Vertébrés) 64:113–142Google Scholar
  35. Janvier P (181) The phylogeny of the Craniata, with particular reference to the significance of the fossil agnathans. J Vert Paleontol 1:121–159Google Scholar
  36. Janvier P (1996) Early vertebrates. Oxford University Press, OxfordGoogle Scholar
  37. Jarvik E (1980) Basic structures and evolution of vertebrates, vols 1 and 2. Academic Press, LondonGoogle Scholar
  38. Jarvik E (1981) Lungfishes, tetrapods, paleontology, and plesiomorphy. Syst Zool 30:378–384CrossRefGoogle Scholar
  39. Johansen S, Bakke I (1996) The complete mitochondrial DNA sequence of Atlantic cod (Gadus morhua): relevance to taxonomic studies among codfishes. Mol Marine Biol Biotech 5:203–214Google Scholar
  40. Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data and the branching order in Hominoidea. J Mol Evol 29:170–179PubMedCrossRefGoogle Scholar
  41. Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 31:151–160CrossRefGoogle Scholar
  42. Le HLV, Lecointre G, Perasso R (1993) A 28S rRNA-based phylogeny of the gnathostomes: first steps in the analysis of conflict and congruence with morphologically based cladograms. Mol Phylogenet Evol 2:31–51PubMedCrossRefGoogle Scholar
  43. Lee WJ, Kocher TD (1995) Complete sequence of a sea lamprey (Petromyzon marinas) mitochondrial genome: early establishment of the vertebrate genome organization. Genetics 139:873–887PubMedGoogle Scholar
  44. Løvtrup S (1977) The phylogeny of the vertebrata. Wiley, LondonGoogle Scholar
  45. Meyer A (1995) Molecular evidence on the origin of tetrapods and the relationship of the coelacanth. TREE 10:111–116Google Scholar
  46. Meyer A, Wilson AC (1990) Origin of tetrapods inferred from their mitochondrial DNA affiliation to lungfish. J Mol Evol 31:359–364PubMedCrossRefGoogle Scholar
  47. Naylor GJP, Brown WM (1997) Structural biology and phylogenetic estimation. Nature 388:527–528PubMedCrossRefGoogle Scholar
  48. Noack K, Zardoya R, Meyer A (1996) The complete mitochondrial DNA sequence of the bichir (Polypterus ornatipinnis), a basal rayfinned fish: ancient establishment of the consensus vertebrate gene order. Genetics 144:1165–1180PubMedGoogle Scholar
  49. Philippe H, Chenuil A, Adoutte A (1994) Can the cambrial explosion be inferred through molecular phylogeny? Development Suppl 11: 15–25Google Scholar
  50. Reisz RR (1997) The origin and early evolutionary history of amniotes. TREE 12:218–222Google Scholar
  51. Retzius G (1893) Das Gehirn und das Auge von Myxine. Biol Unters 5:55–70Google Scholar
  52. Roe RA, Ma D-P, Wilson RK, Wong JF-H (1985) The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem 260:9759–9774PubMedGoogle Scholar
  53. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  54. Sänger F (1981) Determination of nucleotide sequences in DNA. Science 214:1205–1210PubMedCrossRefGoogle Scholar
  55. Schultze HP (1991) A comparison of controversial hypotheses on the origin of tetrapods. In: Schultze H-P, Trueb L (eds) Origin of the higher groups of tetrapods. Comstock, Ithaca, pp 29–67Google Scholar
  56. Schultze HP (1994) Comparison of hypotheses on the relationships of sarcopterygians. Syst Zool 43:155–173Google Scholar
  57. Stock DW, Whitt GS (1992) Evidence from 18S ribosomal RNA sequences that lampreys and hagfishs form a natural group. Science 257:787–789PubMedCrossRefGoogle Scholar
  58. Strimmer K, von Haeseler A (1996) Quartet puzzling: a maximum- likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969Google Scholar
  59. Yalden DW (1985) Feeding mechanisms as evidence for cyclostome monophyly. Zool J Linnean Soc 84:291–300CrossRefGoogle Scholar
  60. Zardoya R, Meyer A (1996) The complete nucleotide sequence of the mitochondrial genome of the lungfish (Protopterus dolloi) supports its phylogenetic position as a close relative of land vertebrates. Genetics 142:1249–1263PubMedGoogle Scholar
  61. Zardoya R, Meyer A (1997) The complete DNA sequence of the mitochondrial genome of a “living fossil”, the coelacanth (Latimeria chalumnae). Genetics 146:995–1010PubMedGoogle Scholar
  62. Zardoya R, Garrido-Pertierra A, Bautista JM (1995) The complete nucleotide sequence of the mitochondrial DNA genome of the rainbow trout, Oncorhynchus mykiss. J Mol Evol 41:942–951PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1998

Authors and Affiliations

  • Ann-Sofie Rasmussen
    • 1
  • Axel Janke
    • 1
  • Ulfur Arnason
    • 1
  1. 1.Division of Evolutionary Molecular Systematics, Department of GeneticsUniversity of LundLundSweden

Personalised recommendations