Journal of Molecular Evolution

, Volume 38, Issue 6, pp 602–609 | Cite as

Relationship among coelacanths, lungfishes, and tetrapods: A phylogenetic analysis based on mitochondrial cytochrome oxidase I gene sequences

  • Shin-ichi Yokobori
  • Masami Hasegawa
  • Takuya Ueda
  • Norihiro Okada
  • Kazuya Nishikawa
  • Kimitsuna Watanabe
Article

Abstract

To clarify the relationship among coelacanths, lungfishes, and tetrapods, the amino acid sequences deduced from the nucleotide sequences of mitochondrial cytochrome oxidase subunit I (COI) genes were compared. The phylogenetic tree of these animals, including the coelacanth Latimeria chalumnae and the lungfish Lepidosiren paradoxa, was inferred by several methods. These analyses consistently indicate a coelacanth/lungfish clade, to which little attention has been paid by previous authors with the exception of some morphologists. Overall evidence of other mitochondrial genes reported previously and the results of this study equally support the coelacanth/lungfish and lungfish/tetrapod clades, ruling out the coelacanth/tetrapod clade.

Key words

Origin of tetrapods Coelacanth Latimeria chalumnae Lungfish Lepidosiren paradoxa Cytochrome oxidase subunit I (COI) Maximum likelihood inference of protein phylogeny 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adachi J, Hasegawa M (1992) Computer science monographs no. 27, MOLPHY: Programs for molecular phylogenetics I — PROTML: Maximum likelihood inference of protein phylogeny. Institute of Statistical Mathematics, TokyoGoogle Scholar
  2. Adachi J, Cao Y, Hasegawa M (1993) Tempo and mode of mitochondrial DNA evolution in vertebrates at the amino acid sequence level: rapid evolution in warm-blooded vertebrates. J Mol Evol 36:270–281CrossRefPubMedGoogle Scholar
  3. Anderson S, Bankier AT, Barrell BG, de 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 290:457–465PubMedGoogle Scholar
  4. Anderson S, de Bruijn MHL, Coulson AR, Eperon IC, Sanger F, Young IG (1982) The complete sequence of bovine mitochondrial DNA: conserved features of the mammalian mitochondrial genome. J Mol Biol 156:683–717Google Scholar
  5. Bibb MJ, van Etten RA, Wright CT, Walberg MW, Clayton DA (1981) Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167–180Google Scholar
  6. Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239Google Scholar
  7. Cantatore P, Roberti M, Rainaldi G, Gadaleta MN, Saccone C (1989) The complete nucleotide sequence, gene organization and genetic code of mitochondrial genome of Paracentroutus lividus. J Biol Chem 264:10695–10975Google Scholar
  8. Chang M-M (1991) “Rhipidistians”, dipnoans, and tetrapods. In: Schultze H-P, Trueb L (eds) Origins of the higher groups of tetrapods. Controversy and consensus. Cornell University Press, Ithaca, NY, pp 3–28Google Scholar
  9. Chang YS, Huang FL (1991) EMBL accession number X61010Google Scholar
  10. Clary DO, Wolstenholme DR (1985) The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–271Google Scholar
  11. Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in proteins. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation, Washington, DC, pp 345–352Google Scholar
  12. Desjardins P, Morais R (1990) Sequence and organization of the chicken mitochondrial genome: a novel gene order in higher vertebrates. J Mol Biol 212:599–634PubMedGoogle Scholar
  13. Felsenstein J (1978) Cases in which parsimony and compatibility methods will be positively misleading. Syst Zool 27:401–410Google Scholar
  14. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376PubMedGoogle Scholar
  15. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791Google Scholar
  16. Felsenstein J (1989) PHYLIP, Version 3.2. University of Washington, SeattleGoogle Scholar
  17. Forey PL (1987) Relationships of lungfishes. J Morphol [suppl] 1:75–91Google Scholar
  18. Forey PL (1988) Golden jubilee for the coelacanth Latimeria chalumnae. Nature 336:727–732Google Scholar
  19. Forey PL (1991) Blood lines of the coelacanth. Nature 351:347–348Google Scholar
  20. Fritsch B (1987) Inner ear of the coelacanth fish Latimeria has tetrapod affinities. Nature 327:153–154Google Scholar
  21. Gadaleta G, Pepe G, Decandia G, Quagliariello C, Sbisa E, Saccone C (1989) The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: cryptic signals revealed by comparative analysis between vertebrates. J Mol Evol 28:497–516Google Scholar
  22. Gorr T, Kleinschmidt T, Fricke H (1991) Close tetrapod relationships of the coelacanth Latimeria indicated by haemoglobin sequences. Nature 351:394–397Google Scholar
  23. Hasegawa M, Cao Y, Adachi J, Yano T (1992a) Rodent polyphyly? Nature 355:595Google Scholar
  24. Hasegawa M, Fujiwara M (1993) Relative efficiencies of the maximum likelihood, maximum parsimony, and neighbor-joining methods for estimating protein phylogeny. Mol Phylogenet Evol 2:1–5Google Scholar
  25. Hasegawa M, Hashimoto T (1993) Ribosomal RNA trees misleading? Nature 361:23Google Scholar
  26. Hasegawa M, Hashimoto T, Adachi J (1992b) Origin and evolution of eukaryotes as inferred from protein sequence data. In: Hartman H, Matsumoto K (eds) The origin and evolution of the cell. World Scientific, Singapore, pp 107–130Google Scholar
  27. Hasegawa M, Hashimoto T, Adachi J, Iwabe N, Miyata T (1993) Early branchings in the evolution of eukaryotes: ancient divergence of Entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Biol 36:380–388Google Scholar
  28. Hasegawa M, Kishino H (1994) Accuracies of the simple methods for estimating the bootstrap probability of a maximum-likelihood tree. Mol Biol Evol (in press)Google Scholar
  29. Hasegawa M, Kishino H, Saitou N (1991) On the maximum likelihood method in molecular phylogenetics. J Mol Evol 32:443–445Google Scholar
  30. Hedges SB, Hass CA, Maxon LR (1993) Relations of fish and tetrapods. Nature 363:501–502Google Scholar
  31. Hennig W (1983) Stammesgeschichte der Chordaten. P Parey, HamburgGoogle Scholar
  32. Hillis DM, Dixon MT, Ammerman LK (1991) The relationships of the coelacanth Latimeria chalumnae: evidence from sequences of vertebrate 28S ribosomal RNA genes. Environ Biol Fishes 32:119–130Google Scholar
  33. Irwin DM, Kocher KD, Wilson AC (1990) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144Google Scholar
  34. Jacobs HT, Elliot DJ, Math VB, Farquharson A (1988a) Nucleotide sequence and gene organization of sea urchin mitochondrial DNA. J Mol Biol 202:185–217Google Scholar
  35. Jacobs HT, Balfe P, Cohen BL, Farquharson A, Comito L (1988b) Phylogenetic implications of genome rearrangement and sequence evolution in echinoderm mitochondrial DNA. In: Paul CRC, Smith AB (eds) Echinoderm phylogeny and evolutionary biology. Clarendon Press, Oxford, pp 121–137Google Scholar
  36. 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 29:170–179PubMedGoogle Scholar
  37. Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood of protein phylogeny and the origin of chloroplasts. J Mol Evol 31: 151–160Google Scholar
  38. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A 86:6196–6200PubMedGoogle Scholar
  39. Kumazawa Y, Nishida M (1993) Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. J Mol Evol 37:380–398PubMedGoogle Scholar
  40. Maeda N, Zhu D, Fitch WM (1984) Amino acid sequence of lower vertebrate parvalbumins and their evolution. Mol Biol Evol 1:473–488Google Scholar
  41. Marshall C, Schultze H-P (1992) Relative importance of molecular, neontological, and paleontological data in understanding the biology of the vertebrate invasion of land. J Mol Evol 35:93–101Google Scholar
  42. Meyer A, Wilson AC (1990) Origins of tetrapods inferred from their mitochondrial DNA affiliation to lungfish. J Mol Evol 31:359–364Google Scholar
  43. Meyer A, Wilson AC (1991) Coelacanth's relationships. Nature 353: 219Google Scholar
  44. Meyer A, Dolven SI (1992) Molecules, fossils, and the origin of tetrapods. J Mol Evol 35:102–113Google Scholar
  45. Miles R (1975) The relationships of the Dipnoi. Collq Int CNRS 218:133–148Google Scholar
  46. Miles R (1977) Dipnoan (lungfish) skulls and the relationships of the group: a study based on new species from the Devonian of Australia. Zool J Linn Soc 61:1–328Google Scholar
  47. 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. Elsevier, Amsterdam, pp 437–450Google Scholar
  48. Normark BB, McCane AR, Harrison RG (1991) Phylogenetic relationships of neopterygian fishes, inferred from mitochondrial DNA sequences. Mol Biol Evol 8:819–834Google Scholar
  49. Northcutt RG (1987) Lungfish neural characters and their bearing on sarcopterygian phylogeny. J Morphol [Suppl]1:277–297Google Scholar
  50. Osawa S, Jukes TH, Watanabe K, Muto A (1992) Recent evidence for evolution of the genetic code. J Microbiol Rev 56:229–264Google Scholar
  51. Roe BA, MA DP, Wilson RK, Wong JF-H (1985) The complete sequence of the Xenopus laevis mitochondrial genome. J Biol Chem 260:9759–9774Google Scholar
  52. Romer AS (1966) Vertebrate paleontology, 3rd ed. University of Chicago Press, ChicagoGoogle Scholar
  53. Rosen DE, Forey PL, Gardiner BG, Patterson C (1981) Lungfishes, tetrapods, paleontology and plesiomorphy, Bull Am Mus Nat Hist 167:159–276Google Scholar
  54. Saiki RK, Gelfand DH, Stoffel S, Schorf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491PubMedGoogle Scholar
  55. Saiki RK (1989) The design and optimization of the PCR. In: Erlich HA (ed) PCR technology, Stockton Press, NY, pp 7–16Google Scholar
  56. Saito N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  57. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  58. Schultze H-P (1987) Dipnoans as Sarcopterygians. J Morphol [Suppl]3:39–74Google Scholar
  59. Schultze H-P, Campbell KSW (1987) Characterization of the Dipnoi, a monophyletic group. J Morphol [Suppl]1:25–37Google Scholar
  60. Sharp PM, Lloyd AT, Higgins DG (1991) Coelacanth's relationship. Nature 353:218–219Google Scholar
  61. Stock DW, Moberg KD, Maxson LR, Whitt GS (1991) A phylogenetic analysis of the 18S ribosomal RNA sequence of the coelacanth Latimeria chalumnae. Environ Biol Fishes 32:99–117Google Scholar
  62. Stock DW, Swofford DL (1991) Coelacanth's relationships. Nature 353:217–218Google Scholar
  63. Tzeng C-S, Hui C-F, Shen S-C, Huang PC (1992) The complete nucleotide sequence of the Crossostoma lacustre mitochondrial genome: conservation and variations among vertebrates. Nucleic Acids Res 20:4853–4858Google Scholar
  64. Yokobori S, Ueda T, Watanabe K (1993) Codons AGA and AGG are read as glycine in ascidian mitochondria. J Mol Evol 36:1–8Google Scholar

Copyright information

© Springer-Verlag New York Inc 1994

Authors and Affiliations

  • Shin-ichi Yokobori
    • 1
    • 3
  • Masami Hasegawa
    • 2
  • Takuya Ueda
    • 3
  • Norihiro Okada
    • 1
  • Kazuya Nishikawa
    • 1
  • Kimitsuna Watanabe
    • 3
  1. 1.Department of Biological Sciences, Faculty of Bioscience and BiotechnologyTokyo Institute of TechnologyYokohamaJapan
  2. 2.The Institute of Statistical MathematicsMinato-ku, TokyoJapan
  3. 3.Department of Industrial Chemistry, Faculty of EngineeringUniversity of TokyoTokyoJapan

Personalised recommendations