Skip to main content
SpringerLink
Log in

Patterns of nucleotide change in mitochondrial ribosomal RNA genes and the phylogeny of piranhas

  • Articles
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The patterns and rates of nucleotide substitution in mitochondrial ribosomal RNA genes are described and applied in a phylogenetic analysis of fishes of the subfamily Serrasalminae (Teleostei, Characiformes, Characidae). Fragments of 345 bp of the 12S and 535 bp of the 16S genes were sequenced for 37 taxa representing all but three genera in the subfamily. Secondary-structure models based on comparative sequence analysis were derived to characterize the pattern of change among paired and unpaired nucleotides, forming stem and loop regions, respectively. Base compositional biases were in the direction of A-rich loops and G-rich stems. Ninety-five percent of substitutions in stem regions were compensatory mutations, suggesting that selection for maintenance of base pairing is strong and that independence among characters cannot be assumed in phylogenetic analyses of stem characters. The relative rate of nucleotide substitution was similar in both fragments sequenced but higher in loop than in stem regions. In both genes, C-T transitions were the most common type of change, and overall transitions outnumbered transversions by a factor of two in 16S and four in 12S. Phylogenetic analysis of the mitochondrial DNA sequences suggests that a clade formed by the generaPiaractus, Colossoma, andMylossoma is the sister group to all other serrasalmins and that the generaMyleus, Serrasalmus, andPristobrycon are paraphyletic. A previous hypothesis concerning relationships for the serrasalmins, based on morphological evidence, is not supported by the molecular data. However, phylogenetic analysis of host-specific helminth parasites and cytogenetic data support the phylogeny of the Serrasalminae obtained in this study and provide evidence for coevolution between helminth parasites and their fish hosts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adachi J, Hasegawa M (1994) MOLPHY: a program package for molecular phylogenetics, version 2.2. The Institute of Statistical Mathematics, Tokyo

    Google Scholar 

  • Alves-Gomes JA, Ortí G, Haygood M, Heiligenberg W, Meyer A (1995) Phylogenetic analysis of the South American electric fishes (Order Gymnotiformes) and the evolution of their electrogenic system: a synthesis based on morphology, electrophysiology, and mitochondrial sequence data. Mol Biol Evol 12:298–318

    Google Scholar 

  • Anderson S, Bankier AT, Barrell BG, de Brujin 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 

  • Aquadro CF, Greenberg BD (1983) Human mitochondrial DNA variation and evolution: analysis of nucleotide sequences from seven individuals. Genetics 103:287–312

    Google Scholar 

  • Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239

    Google Scholar 

  • Cestari MM, Galetti Jr PM (1992) Chromosome evolution in the genusSerrasalmus and cytotaxonomic considerations about Serrasalminae (Characidae, Pisces). Rev Brasil Genet 15:555–567

    Google Scholar 

  • Collins TM, Wimberger PH, Naylor GJP (1994) Compositional bias, character-state bias, and character-state reconstruction using parsimony. Syst Biol 43:482–496

    Google Scholar 

  • Dams E, Hendriks L, Van de Peer Y, Neefs JM, Smits G, Vandenbempt I, De Wachter R (1988) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 16s:r87-r173

    Google Scholar 

  • Dixon MT, Hillis DM (1993) Ribosomal RNA secondary structure: compensatory mutations and implications for phylogenetic analysis. Mol Biol Evol 10:256–267

    Google Scholar 

  • Eigenmann C (1915) The Serrasalminae and Mylinae. Ann Carnegie Museum, Pittsburgh 9:266–272

    Google Scholar 

  • Farris JS (1969) A successive approximations approach to character weighting. Syst Zool 18:374–385

    Google Scholar 

  • Felsenstein J (1969) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Google Scholar 

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

    Google Scholar 

  • Fink WL (1993) Revision of the piranha genusPygocentrus (Teleostei, Characiformes). Copeia 1993:665–687

    Google Scholar 

  • Fitch WM, Markowitz E (1970) An improved method for determining codon variability in a gene and its application to the rate of fixation of mutations in evolution. Biochem Genet 4:579–593

    Google Scholar 

  • Géry J (1972) Poissons characoides des Guyanes II. Famille des Serrasalmidae. Zoologische Verhandelingen Leiden 122:134–248

    Google Scholar 

  • Géry J (1977) Characoids of the World. Tropical Fish Hobbyist Publications, Neptune City, NJ, pp 672

    Google Scholar 

  • Gosline W (1951) Notes on the characoid fishes of the Subfamily Serrasalminae. Proc Cal Acad Sci, ser 4 27:17–64

    Google Scholar 

  • Goulding M (1980) The fishes and the forest. Explorations in Amazonian natural history. University of California Press, Berkeley, p 280

    Google Scholar 

  • Gray MW, Cedergren R (1993) The new age of RNA. FASEB J 7:4–6

    Google Scholar 

  • Guttel RR, Fox GE (1988) A compilation of large subunit rRNA sequences presented in a structural format. Nucleic Acids Res 16s:r175-r269

    Google Scholar 

  • Guttel RR, Gray MW, Schare MN (1993) A compilation of large subunit 23S and 23S-like) ribosomal RNA structures: 1993. Nucleic Acids Res 21:3055–3074

    Google Scholar 

  • Guttel RR, Weiser B, Woese CR, Noller HF (1985) Comparative anatomy of 16-S-like ribosomal RNA. Prog Nucleic Acid Res Mol Biol 32:155–216

    Google Scholar 

  • Gyllensten UB, Erlich HA (1988) Generation of single-stranded DNA by the polymerase chain reaction and its application to direct sequencing of the HLA-DQa locus. Proc Natl Acad Sci USA 85:7652–7655

    Google Scholar 

  • Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453

    Google Scholar 

  • 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 3:1–18

    Google Scholar 

  • Jégu M, Tito de Morais L, Mendes dos Santos G (1992) Redescription des types d′Utiaritichthys sennaebragai Miranda Ribeiro, 1937 et description d'une nouvelle espéce du bassin Amazonien, (Characiformes, Serrasalmidae). Cybium 16:105–120

    Google Scholar 

  • Junk WJ (1984) Ecology, fisheries and fish culture in Amazonia. In: Sioli H (ed) The Amazon, limnology and landscape ecology of a mighty tropical river and its basin. Dr. W. Junk Publishers, Dordrecht, pp 443–476

    Google Scholar 

  • Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci USA 78:454–458

    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

    Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals. Proc Natl Acad Sci USA 86:6196–6200

    Google Scholar 

  • Kumar S, Tamura K, Nei M (1993) MEGA: molecular evolutionary genetics analysis, version 1.0. The Pennsylvania State University, University Park, PA

    Google Scholar 

  • Larson A, Wilson AC (1989) Patterns of ribosomal RNA evolution in salamanders. Mol Biol Evol 6:131–154

    Google Scholar 

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

    Google Scholar 

  • Leite RG, Jégu M (1990) Food habits of two species ofAcnodon (Characiformes, Serrasalmidae) and scale-eating habits ofAcnodon normani. Cybium 14:353–360

    Google Scholar 

  • Lundberg JG (1993) African-South American freshwater fish clades and continental drift: problems with a paradigm. In: Goldblatt P (ed) Biological relationships between African and South America. Yale University Press, New Haven, pp 156–199

    Google Scholar 

  • Lundberg JG, Machado-Allison A, Kay RF (1986) Miocene characid fishes from Colombia: evolutionary stasis and extirpation. Science 234:208–209

    Google Scholar 

  • Machado-Allison A (1982) Studies on the systematics of the subfamily Serrasalminae (Pisces-Characidae). Unpublished PhD thesis, The George Washington University, Washington DC

    Google Scholar 

  • Machado-Allison A (1983) Estudios sobre la sistemática de la subfamilia Serrasalminae (Teleostei, Characidae), parte II. Discusión sobre la condición monofilética de la subfamilia. Acta Biol Venez 11:145–195

    Google Scholar 

  • Machado-Allison A, Fink WL, Antonio ME (1989) Revisión del géneroSerrasalmus Lacepede, 1803 y géneros relacionados en Venezuela: I. Notas sobre la morfología y sistemática dePristobrycon striolatus (Steindachner, 1908). Acta Biol Venez 12:140–171

    Google Scholar 

  • Maddison WP, Maddison DR (1992) MacCLADE: analysis of phylogeny and character evolution, version 3.0. Sinauer, Sunderland, MA

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Publications, Cold Spring Harbor, NY

    Google Scholar 

  • Marshall E (1995) Homely fish draws attention to Amazon deforestation. Science 267:814

    Google Scholar 

  • Meyer A (1993) Evolution of mitochondrial DNA of fishes. In: Hochachka PW, Mommsen P (eds) The biochemistry and molecular biology of fishes, vol 2. Elsevier Press, Amsterdam, pp 1–38

    Google Scholar 

  • Meyer A (1994) DNA technology and phylogeny of fish. In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman and Hall, London pp. 219–249

    Google Scholar 

  • Mindell DP, Honeycutt RL (1990) Ribosomal RNA in vertebrates: evolution and phylogenetic implications. Annu Rev Ecol Syst 21:541–566

    Google Scholar 

  • Neefs JM, Van de Peer Y, De Rijk P, Goris A, De Wachter R (1991) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 19s:1987–2015

    Google Scholar 

  • Nelson EM (1961) The swim bladder in the Serrasalminae, with notes on additional morphological features. Fieldiana Zool 39:603–624

    Google Scholar 

  • Nico L, Taphorn DC (1988) Food habits of piranhas in the low Ilanos of Venezuela. Biotropica 20:311–321

    Google Scholar 

  • Noller HF (1984) Structure of ribosomal RNA. Annu Rev Biochem 53:119–162

    Google Scholar 

  • Norman JR (1929) The South American Characid fishes of the subfamily Serrasalmoninae with a revision of the genusSerrasalmus Lacepede. Proc Zool Soc London 52:661–1044

    Google Scholar 

  • Oliveira C, Almeida-Toledo LF, Foresti F, Britski H, Toledo-Filho SA (1988) Chromosome formulae of Neotropical freshwater fishes. Rev Bras Genet 11:577–624

    Google Scholar 

  • Olsen GJ, Matsuda H, Hagstrom R, Overbeek R (1994) fast DNAml: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Appl Biosci 10:41–48

    Google Scholar 

  • Olsen GJ, Woese CR (1993) Ribosomal RNA: a key to phylogeny. FASEB J 7:113–123

    Google Scholar 

  • Ortí G (1995) Molecular systematics of characiform fishes. Unpublished PhD thesis, State University of New York at Stony Brook

  • Ortí G, Meyer A (1996) The radiation of characiform fishes and the limits of resolution of mitochondrial ribosomal DNA sequences. Syst Biol 45(in press)

  • Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool's guide to PCR. Dept of Zoology and Kewalo Marine Laboratory, University of Hawaii, Honolulu

    Google Scholar 

  • Porto JIR, Feldberg E, Nakayama C, Falcao JN (1992) A checklist of chromosome numbers and karyotypes of Amazonian freshwater fishes. Rev Hydrobiol Trop 25:287–299

    Google Scholar 

  • Porto JIR, Feldberg E, Nakayama CM, Jégu M (1989) Análise cariotípica na familia Serrasalmidae (Ostariophysi, Characiformes): aspectos evolutivos. Ciencia é Cultura (Suppl) 41:714

    Google Scholar 

  • Porto JIR, Feldberg E, Nakayama CM, Maia RO, Jégu M (1991) Cytotaxonomic analysis in the Serrasalmidae (Ostariophysi, Characiformnes). VIII Congress of Ichthylogy. Bull Zool Mus Univ, Amsterdam, The Hague

    Google Scholar 

  • Saiki RK, Gelfand DH, Stoffel S, Scharf S, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–525

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminator inhibitors. Proc Natl Acad Sci USA 74:5436–5437

    Google Scholar 

  • Schimmel PR, Soll D, Abelson JN (1979) Transfer RNA: structure, properties and recognition. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  • Swofford DL (1993) PAUP: Phylogenetic Analysis Using Parsimony, ver 3.1.1. Smithsonian Institution, Washington, DC

    Google Scholar 

  • Swofford DL, Maddison WP (1992) Parsimony, character-state reconstructions, and evolutionary inferences. In: Mayden RL (ed) Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, Stanford, pp 186–223

    Google Scholar 

  • Swofford DL, Olsen GJ (1990) Phylogeny reconstruction. In: Hillis DM, Moritz C (eds) Molecular systematics. Sinauer, Sunderland MA, pp 411–501

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Google Scholar 

  • Turner DH, Sugimoto N, Freier SM (1988) RNA structure prediction. Annu Rev Biophys Chem 17:167–192

    Google Scholar 

  • Tzeng CS, Hui CF, Shen SC, Huang PC (1992) The complete nucleotide sequence of theCrossostoma lacustre mitochondrial genome: conservation and variations among vertebrates. Nucleic Acids Res 20:4853–4858

    Google Scholar 

  • Van Every LR, Kritsky DC (1992) Neotropical Monogenoida. 18.Anacanthorus Mizelle and Price, 1965 (Dactylogyridae, Anacanthorinae) of piranha (Characoidea, Serrasalmidae) from the central Amazon, their phylogeny, and aspects of host-parasite coevolution. J Helminthol Soc Wash 59:52–75

    Google Scholar 

  • Vawter L, Brown WM (1993) Rates and patterns of base change in the small subunit ribosomal RNA gene. Genetics 134:597–608

    Google Scholar 

  • Wheeler WC, Honeycutt RL (1988) Paired sequence difference in ribosomal RNAs: evolutionary and phylogenetic implications. Mol Biol Evol 5:90–96

    Google Scholar 

  • Winemiller KO (1989) Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan Llanos. Environ Biol Fishes 26:177–199

    Google Scholar 

  • Wolstenholme DR, Clary DO (1985) Sequence evolution ofDrosophila mitochondrial DNA. Genetics 109:725–744

    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:(in press)

Download references

Author information

Author notes

  1. Guillermo Ortí

    Present address: Department of Genetics, University of Georgia, 30602, Athens, GA, USA

Authors and Affiliations

  1. Department of Ecology and Evolution, State University of New York at Stony Brook, 11794-5245, Stony Brook, NY, USA

    Guillermo Ortí & Axel Meyer

  2. Instituto Nacional de Pesquisas da Amazonia (INPA/CPBA), CxP 478, CEP 69, 083-000, Manaus, AM, Brazil

    Paulo Petry, Jorge I. R. Porto & Michel Jégu

  3. Départment Des Eaux Continentales, ORSTOM, 213 Rue La Fayette, 75480, Paris Cedex 10, France

    Michel Jégu

  4. Program in Genetics, State University of New York at Stony Brook, 11794, Stony Brook, NY, USA

    Axel Meyer

Authors
  1. Guillermo Ortí
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paulo Petry
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jorge I. R. Porto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michel Jégu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Axel Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ortí, G., Petry, P., Porto, J.I.R. et al. Patterns of nucleotide change in mitochondrial ribosomal RNA genes and the phylogeny of piranhas. J Mol Evol 42, 169–182 (1996). https://doi.org/10.1007/BF02198843

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02198843

Key words

Search

Navigation