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

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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.

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References

  • Adachi J (1995) Modeling of molecular evolution and maximum likelihood inference of molecular phylogeny. PhD thesis, The Graduate University for Advanced Studies, Tokyo

    Google Scholar 

  • Adachi J, Hasegawa M (1996a) MOLPHY: programs for molecular phylogenetics based on maximum likelihood. Comput Sci Monographs Inst Stat Math Tokyo 28:1–150

    Google Scholar 

  • Adachi J, Hasegawa M (1996b) Model of amino acid substitution in proteins encoded by mitochondrial DNA. J Mol Evol 42:459–468

    Article  PubMed  CAS  Google Scholar 

  • Ahlberg PE, Milner AR (1994) The origin and early diversification of tetrapods. Nature 368:507–513

    Article  Google Scholar 

  • 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 156:683–717

    Article  PubMed  CAS  Google Scholar 

  • Arnason U, Johnsson E. (1992) The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina. J Mol Evol 34:493–505

    Article  PubMed  CAS  Google Scholar 

  • Arnason U, Gullberg A, Widegren B (1991) The complete nucleotide sequence of the mitochondrial DNA of the fin whale, Balenoptera physalus. J Mol Evol 33:556–568

    Article  PubMed  CAS  Google Scholar 

  • Asakawa S, Himeno H, Miura K, Watanabe K (1995) Nucleotide sequence and gene organization of the starfish Asterina pectinifera mitochondrial genome. Genetics 140:1047–1060

    PubMed  CAS  Google Scholar 

  • 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 31–57

    Google Scholar 

  • Bjerring HC (1989) Apertures of craniate olfactory organs. Acta Zool 70:71–85

    Article  Google Scholar 

  • Brodai A, Fänge R (1963) The biology of Myxine. Universitetsforlaget, Oslo

    Google Scholar 

  • Cabot EL, Beckenbach AT (1988) Simultaneous editing of multiple nucleic and protein sequences with ESEE. Comput Appl Biosci 5:233–234

    Google Scholar 

  • 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 39:519–527

    Article  PubMed  CAS  Google Scholar 

  • 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 445–480

    Chapter  Google Scholar 

  • 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 5:323–332

    Article  PubMed  Google Scholar 

  • Desjardins P, Morais R (1990) Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol 212:599–634

    Article  PubMed  CAS  Google Scholar 

  • Duméril AMC (1806) Zoologie analytique, ou méthode naturelle de classification des aimaux. Didot, Paris

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1991) Phylogenetic inference programs (PHYLIP). University of Washington, Seattle

  • Fitch WM (1971) Toward defining the course of evolution, minimum change from a specific tree topology. Syst Zool 20:406–415

    Article  Google Scholar 

  • Forey PL (1987) Relationships of lungfishes. In: Bemis WE, Burggren WW, Kemp NE (eds) Biology and evolution of lungfishes. J Morphol Suppl 1:75–91

    Google Scholar 

  • Forey PL (1995) Agnathans recent and fossil, and the origin of jawed vertebrates. Revs Fish Biol Fisheries 5:267–303

    Article  Google Scholar 

  • Forey PL, Janvier P (1993) Agnathans and the origin of jawed vertebrates. Nature 361:129–134

    Article  Google Scholar 

  • Forey PL, Janvier P (1994) Evolution of the early vertebrates. Am Sci 82:554–565

    Google Scholar 

  • Gee H (1996) Before the backbone. Chapman, Hall, London

    Google Scholar 

  • Genetics Computer Group (1994) Program manual for the Wisconsin package, version 8

  • 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 141–176

  • Gorr T, Kleinschmidt T (1993) Evolutionary relationships of the coelacanth. Am Sci 81:72–82

    Google Scholar 

  • 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 165–259

    Google Scholar 

  • Härlid A, Janke A, Arnason U (1997) The mtDNA sequence of the ostrich and the divergence between paleognathous and neognathous birds. Mol Biol Evol 14:754–761

    PubMed  Google Scholar 

  • Jacobs HT, Elliott DJ, Math VB, Farquharson A (1988) Nucleotide sequence and gene organization of seaurchin mitochondrial DNA. J Mol Biol 202:185–217

    Article  PubMed  CAS  Google Scholar 

  • Janke A, Feldmaier-Fuchs G, Thomas WK, von Haeseler A, Pääbo S (1994) The marsuipial mitochondrial genome and the evolution of placental mammals. Genetics 137:243–256

    PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Janvier P (1978) Les nageoires paires des Ostéostracés et al position systématique des Céphalaspidomorphes. Ann Paléontol (Vertébrés) 64:113–142

    Google Scholar 

  • Janvier P (181) The phylogeny of the Craniata, with particular reference to the significance of the fossil agnathans. J Vert Paleontol 1:121–159

    Google Scholar 

  • Janvier P (1996) Early vertebrates. Oxford University Press, Oxford

    Google Scholar 

  • Jarvik E (1980) Basic structures and evolution of vertebrates, vols 1 and 2. Academic Press, London

    Google Scholar 

  • Jarvik E (1981) Lungfishes, tetrapods, paleontology, and plesiomorphy. Syst Zool 30:378–384

    Article  Google Scholar 

  • 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 5:203–214

    CAS  Google Scholar 

  • 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 29:170–179

    Article  PubMed  CAS  Google Scholar 

  • Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 31:151–160

    Article  CAS  Google Scholar 

  • 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 2:31–51

    Article  PubMed  CAS  Google Scholar 

  • Lee WJ, Kocher TD (1995) Complete sequence of a sea lamprey (Petromyzon marinas) mitochondrial genome: early establishment of the vertebrate genome organization. Genetics 139:873–887

    PubMed  CAS  Google Scholar 

  • Løvtrup S (1977) The phylogeny of the vertebrata. Wiley, London

    Google Scholar 

  • Meyer A (1995) Molecular evidence on the origin of tetrapods and the relationship of the coelacanth. TREE 10:111–116

    Google Scholar 

  • Meyer A, Wilson AC (1990) Origin of tetrapods inferred from their mitochondrial DNA affiliation to lungfish. J Mol Evol 31:359–364

    Article  PubMed  CAS  Google Scholar 

  • Naylor GJP, Brown WM (1997) Structural biology and phylogenetic estimation. Nature 388:527–528

    Article  PubMed  CAS  Google Scholar 

  • 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 144:1165–1180

    PubMed  CAS  Google Scholar 

  • Philippe H, Chenuil A, Adoutte A (1994) Can the cambrial explosion be inferred through molecular phylogeny? Development Suppl 11: 15–25

    Google Scholar 

  • Reisz RR (1997) The origin and early evolutionary history of amniotes. TREE 12:218–222

    Google Scholar 

  • Retzius G (1893) Das Gehirn und das Auge von Myxine. Biol Unters 5:55–70

    Google Scholar 

  • Roe RA, Ma D-P, Wilson RK, Wong JF-H (1985) The complete nucleotide sequence of the Xenopus laevis mitochondrial genome. J Biol Chem 260:9759–9774

    PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sänger F (1981) Determination of nucleotide sequences in DNA. Science 214:1205–1210

    Article  PubMed  Google Scholar 

  • 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 29–67

    Google Scholar 

  • Schultze HP (1994) Comparison of hypotheses on the relationships of sarcopterygians. Syst Zool 43:155–173

    Google Scholar 

  • Stock DW, Whitt GS (1992) Evidence from 18S ribosomal RNA sequences that lampreys and hagfishs form a natural group. Science 257:787–789

    Article  PubMed  CAS  Google Scholar 

  • Strimmer K, von Haeseler A (1996) Quartet puzzling: a maximum- likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969

    CAS  Google Scholar 

  • Yalden DW (1985) Feeding mechanisms as evidence for cyclostome monophyly. Zool J Linnean Soc 84:291–300

    Article  Google Scholar 

  • 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 142:1249–1263

    PubMed  CAS  Google Scholar 

  • Zardoya R, Meyer A (1997) The complete DNA sequence of the mitochondrial genome of a “living fossil”, the coelacanth (Latimeria chalumnae). Genetics 146:995–1010

    PubMed  CAS  Google Scholar 

  • 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 41:942–951

    PubMed  CAS  Google Scholar 

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Correspondence to Ulfur Arnason.

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Rasmussen, AS., Janke, A. & Arnason, U. The mitochondrial DNA molecule of the hagfish (myxine glutinosa) and vertebrate phylogeny. J Mol Evol 46, 382–388 (1998). https://doi.org/10.1007/PL00006317

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  • DOI: https://doi.org/10.1007/PL00006317

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