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Evolutionary analysis of cytochrome b sequences in some perciformes: Evidence for a slower rate of evolution than in mammals

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Abstract

To obtain information relative to the phylogenesis and microevolutionary rate of fish mitochondrial DNA, the nucleotide sequence of cytochrome b gene in seven fish species belonging to the order of Perciformes was determined. Sequence analysis showed that fish mitochondrial DNA has a nucleotide compositional bias similar to that of sharks but lower compared to mammals and birds. Quantitative evolutionary analysis, carried out by using a markovian stochastic model, clarifies some phylogenetic relationships within the Perciformes order, particularly in the Scombridae family, and between Perciformes, Gadiformes, Cypriniformes, and Acipenseriformes. The molecular clock of mitochondrial DNA was calibrated with the nucleotide substitution rate of cytochrome b gene in five shark species having divergence times inferred from paleontological estimates. The results of such analysis showed that Acipenseriformes diverged from Perciformes by about 200 MY, that the Perciformes common ancestor dates back to 150 MY, and that fish mitochondrial DNA has a nucleotide substitution rate three to five times lower than that of mammals.

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References

  • Adams SM, Blakesley R (1991) Linear amplification DNA sequencing. Focus-BRL 13: 56–58

    Google Scholar 

  • Adelman R, Saul RL, Ames BN (1988) Oxidative damage to DNA: relation to species metabolic rate and life span. Proc Natl Acad Sci USA 85: 2706–2708

    Google Scholar 

  • Anderson S, Bankier AT, Barrel BG, de Bruijin 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

    Google Scholar 

  • Attardi G (1985) Animal mitochondrial DNA: an extreme example of genetic economy. Int Rev Cytol 93: 93–145

    Google Scholar 

  • Avise JC, Bowen BW, Lamb T, Meylan AB, Bermingham E (1992) Mitochondrial DNA evolution at a turtle pace: evidence for low genetic variability and reduced microevolufionary rate in the testudines. Mol Biol Evol 9: 457–473

    Google Scholar 

  • Bartlett SE, Davidson WS (1991) Identification of Thunnus tuna species by the polymerase chain reaction and direct sequence analysis of their mitochondrial cytochrome by genes. Can J Fish Aquat Sci 48: 309–317

    Google Scholar 

  • Benton MJ (1990) Vertebrate palaeontology. Unwin Hyman Ltd, London

    Google Scholar 

  • Benton MJ (ed) (1993) The fossil record 2. Chapman and Hall, London

    Google Scholar 

  • Bernardi G, D'Onofrio G, Caccio S, Bernardi G (1993) Molecular phylogeny of bony fishes based on the aminoacid sequence of the growth hormone. J Mol Evol 37: 644–649

    Google Scholar 

  • Block BA (1991) Endothermy in fish: thermogenesis, ecology and evolution. In: Hochachka P, Mommsen T (eds) Biochemistry and molecular biology of fishes. Elsevier, New York, pp 269–311

    Google Scholar 

  • Block BA, Finnerty JR, Stewart AFR, Kidd J (1993) Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny. Science 260: 210–213

    Google Scholar 

  • Britten RJ (1986) Rates of DNA sequence evolution differ between taxonomic groups. Science 231: 1393–1398

    Google Scholar 

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

    Google Scholar 

  • Brown JR, Gilbert TL, Kowbel DJ, O'Hara PJ, Buroker NE, Beckenbach AT, Smith MJ (1989) Nucleotide sequence of the apocytochrome b gene in white sturgeon mitochondrial DNA. Nucleic Acids Res 17: 4389

    Google Scholar 

  • Carey FC, Teal JM (1966) Heat conservation in tuna fish muscle. Proc Natl Acad Sci USA 56: 1464–1469

    Google Scholar 

  • Degli Esposti M, Ghelli A, Crimi M, Baracca A, Solaino G, Tron T, Meyer A (1992) Cytochrome b of fish mitochondria is strongly resistant to funicolosin, a powerful inhibitor of respiration. Arch Biochem Biophys 295: 198–204

    Google Scholar 

  • DeSalle R, Templeton AR (1988) Founder effect and rate of mitochondrial DNA evolution of Hawaiian Drosophila. Evolution 42: 157–164

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791

    Google Scholar 

  • Felsenstein J (1993) PHYLIP (phylogeny inference package) v 3.5. Department of Genetics, University of Washington, Seattle

    Google Scholar 

  • GCG, Genetics Computer Group (1993) Program manual for the GCG package, v 7.3. 575 Science Drive, Madison, Wisconsin, USA 53711

    Google Scholar 

  • Gouy M, Gautier C, Attimonelli M, Lanave C, Di Paola G (1985) ACNUC—a portable retrieval system for nucleic acid sequence databases: logical and physical designs and usage. Comput Appl Biosci 1: 167–172

    Google Scholar 

  • Hauswirth WW, Laipis MJ (1985) Transmission genetics of mammalian mitochondria: a molecular model and experimental evidence. In: Quagliariello E et al. (ed) Achievements and perspectives of mitochondrial research. Elsevier, Amsterdam, pp 49–59

    Google Scholar 

  • Hayashi J-I, Walle MJVD, Laipis PJ, Olivo PD (1985) Absence of extensive recombination between inter and intraspecies mitochondrial DNA in mammalian cells. Exp Cell Res 160: 387–395

    Google Scholar 

  • Hillis DM, Moritz C (ed) (1990) Molecular systematics. Sinauer, Sunderland, MA, pp 502–515

    Google Scholar 

  • Howell N (1989) Evolutionary conservation of protein regions in the protonmotive cytochrome b and their possible roles in redox catalysis. J Mol Evol 29: 157–169

    Google Scholar 

  • Irwin DM, Kocher TD, Wilson AC (1991) Evolution of cytochrome b gene of mammals. J Mol Evol 32: 128–144

    Google Scholar 

  • Johansen S, Johansen T (1994) Sequence analysis of 12 structural genes and a novel non coding region from mitochondrial DNA of Atlantic cod Gadus morhua. Biochim Biophys Acta 1218: 213–217

    Google Scholar 

  • Jonje H (1989) Genetic toxicology of oxigen. Murat Res219: 193–208

    Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edward SV, Paabo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86: 6196–6200

    Google Scholar 

  • Lansman RA, Shade RO, Shapira YF, Avise JC (1981) The use of restriction endonuclease to measure mitochondrial DNA sequence relatedness in natural populations. III. Techniques and potential applications. J Mol Evol 17: 214–226

    Google Scholar 

  • Le HLV, Lecointre G, Perasso R (1993) A 28S based phylogeny of Gnathostomes: first steps in the analysis of conflict and congruence with morphologically based cladograms. Mol Phyl Evol 2: 31–51

    Google Scholar 

  • Li W-H, Tanimura M, Sharp PM (1987) An evaluation of the Molecular Clock hypothesis using mammalian DNA sequences. J Mol Evol 25: 330–342

    Google Scholar 

  • Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357: 153–155

    Google Scholar 

  • Martin AP, Palumbi SR (1993) Body size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci USA 90: 4087–4091

    Google Scholar 

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

    Google Scholar 

  • Meyer A, Kocher TD, Basabwaki P, Wilson AC (1990) Monophyletic origin of Victoria cichlid fish suggested by mitochondrial DNA sequence. Nature 347: 550–553

    Google Scholar 

  • Meyer A (1992) Evolution of mitochondrial DNA in fish. In: Hochachka PW, Mommsen TP (ed) Biochemistry and molecular biology of fish, vol 2. Elsevier Press,

  • Normark BB, McCune AR, Harrison RG (1991) Phylogenetic relationships of neopterygian fish inferred from mitochondrial DNA sequence. Mol Biol Evol 8: 819–834

    Google Scholar 

  • Novacek MJ (1982) Information for molecular studies from anatomical and fossil evidence on higher eutherian phylogeny. In: Goodman M (ed) Macromolecular sequences in systematic and evolutionary biology. Plenum Press, New York, pp 3–41

    Google Scholar 

  • Pesole G, Sbisà E, Mignotte F, Saccone C (1991) The branching order of mammals: phylogenetic trees inferred from nuclear and mitochondrial molecular data. J Mol Evol 33: 537–542

    Google Scholar 

  • Pesole G, Attimonelli M, Preparata G, Saccone C (1992) A statistical method for detecting regions with different evolutionary dynamics in multialigned sequences. Mol Phyl Evol 1: 91–96

    Google Scholar 

  • Preparata G, Saccone C (1987) A simple quantitative model of the molecular clock. J Mol Evol 26: 7–15

    Google Scholar 

  • Roe BA, 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

    Google Scholar 

  • Saccone C, Lanave C, Pesole G, Preparata G (1990) Influence of base composition on quantitative estimates of gene evolution. Methods Enzymol 183: 570–583

    Google Scholar 

  • Saccone C, Pesole G, Preparata G (1989) DNA microenvironment and the molecular clock. J Mol Evol 29: 407–411

    Google Scholar 

  • Saccone C, Pesole G, Kadenbach B (1991) Evolutionary analysis of the nucleus encoded subunits of mammalian cytochrome c oxidase. Eur J Biochem 195: 151–156

    Google Scholar 

  • Saccone C, Lanave C, Pesole G (1993a) Time and biosequences. J Mol Evol 37: 154–159

    Google Scholar 

  • Saccone C, Lanave C, Pesole G, Sbisa E (1993b) Peculiar features and evolution of mitochondrial genomes in mammals. In: Di Mauro S, Wallace DC (ed) Mitochondrial DNA in human pathology. Raven Press, New York, pp 27–37

    Google Scholar 

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

    Google Scholar 

  • Sarich VM, Wilson AC (1967) Generation time and genomic evolution in primates. Science 158: 1200–1203

    Google Scholar 

  • Schlotterer C, Amos B, Tautz D (1991) Conservation of polymorphic simple sequence loci in cetacean species. Nature 354: 63–65

    Google Scholar 

  • Shields G, Wilson AC (1987) Calibration of mitochondrial DNA evolution in geese. J Mol Evol 24: 212–217

    Google Scholar 

  • Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci USA 85: 2653–2657

    Google Scholar 

  • Thomas WK, Beckenbach AT (1989) Variation in salmonid mitochondrial DNA: evolutionary constraints and mechanisms of substitution. J Mol Evol 29: 233–245

    Google Scholar 

  • Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, HelmBichowski KM, Higuchi RG, Palumbi SR, Prager EM, Sage RD, Stoneking M (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linnean Soc 26: 375–400

    Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, University of Bari, via Orabona 4, 70126, Bari, Italy

    P. Cantatore, M. Roberti, G. Pesole, F. Milella, M. N. Gadaletal & C. Saccone

  2. Istituto Sperimentale Talassografico “Angelo Cerruti” CNR Taranto, Italy

    A. Ludovico

Authors
  1. P. Cantatore
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  2. M. Roberti
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  3. G. Pesole
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  4. A. Ludovico
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  5. F. Milella
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  6. M. N. Gadaletal
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  7. C. Saccone
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Additional information

Correspondence to: C. Saccone

The nucleotide sequences reported in this paper have been submitted to the GenBank/EMBL Data Library with accession numbers X81562 (Sarda sarda), X81563 (Thunnus thynnus), X81564 (Scomber scombrus), X81565 (Oreochromis mossambicus), X81566 (Dicentrarchus labrax), X81567 (Boops hoops), X81568 (Trachurus trachurus)

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Cantatore, P., Roberti, M., Pesole, G. et al. Evolutionary analysis of cytochrome b sequences in some perciformes: Evidence for a slower rate of evolution than in mammals. J Mol Evol 39, 589–597 (1994). https://doi.org/10.1007/BF00160404

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  • DOI: https://doi.org/10.1007/BF00160404

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