Skip to main content
SpringerLink
Log in

Relative Rates of Nucleotide Substitution in Frogs

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

Abstract

Accurate estimation of relative mutation rates of mitochondrial DNA (mtDNA) and single-copy nuclear DNA (scnDNA) within lineages contributes to a general understanding of molecular evolutionary processes and facilitates making demographic inferences from population genetic data. The rate of divergence at synonymous sites (K s) may be used as a surrogate for mutation rate. Such data are available for few organisms and no amphibians. Relative to mammals and birds, amphibian mtDNA is thought to evolve slowly, and the K s ratio of mtDNA to scnDNA would be expected to be low as well. Relative K s was estimated from a mitochondrial gene, ND2, and a nuclear gene, c-myc, using both “approximate” and likelihood methods. Three lineages of congeneric frogs were studied and this ratio was found to be approximately 16, the highest of previously reported ratios. No evidence of a low K s in the nuclear gene was found: c-myc codon usage was not biased, the K s was double the intron divergence rate, and the absolute K s was similar to estimates obtained here for other genes from other frog species. A high K s in mitochondrial vs. nuclear genes was unexpected in light of previous reports of a slow rate of mtDNA evolution in amphibians. These results highlight the need for further investigation of the effects of life history on mutation rates.

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

Figure 1
Figure 2

Similar content being viewed by others

References

  1. WR Atchley WM Fitch (1995) ArticleTitleMyc and Max: molecular evolution of a family of proto-oncogene products and their dimerization partner. Proc Natl Acad Sci USA 92 10217–10221 Occurrence Handle1:CAS:528:DyaK2MXovFalsLs%3D Occurrence Handle7479755

    CAS  PubMed  Google Scholar 

  2. AM Báez (1996) The fossil record of the Pipidae. RC Tinsley HR Kobel (Eds) The biology of Xenopus. Oxford University Press New York 329–347

    Google Scholar 

  3. F Bossuyt MC Milinkovitch (2000) ArticleTitleConvergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proc Nat Acad Sci USA 97 6585–6590 Occurrence Handle10.1073/pnas.97.12.6585 Occurrence Handle1:CAS:528:DC%2BD3cXktFaju74%3D Occurrence Handle10841558

    Article  CAS  PubMed  Google Scholar 

  4. WM Brown M George Jr AC Wilson (1979) ArticleTitleRapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76 1967–1971 Occurrence Handle1:CAS:528:DyaE1MXktVWmsb8%3D Occurrence Handle109836

    CAS  PubMed  Google Scholar 

  5. K Burke (1988) ArticleTitleTectonic evolution of the Caribbean. Annu Rev Earth Planet Sci 16 201–230 Occurrence Handle10.1146/annurev.ea.16.050188.001221

    Article  Google Scholar 

  6. JM Comeron (1995) ArticleTitleA method for estimating the numbers of synonymous and nonsynonymous substitutions per site. J Mol Evol 41 1152–1159 Occurrence Handle1:CAS:528:DyaK28XivFOnsQ%3D%3D Occurrence Handle8587111

    CAS  PubMed  Google Scholar 

  7. JM Comeron (1999) ArticleTitleK-Estimator: Calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15 763–764 Occurrence Handle1:CAS:528:DyaK1MXnt1Cks7g%3D Occurrence Handle10498777

    CAS  PubMed  Google Scholar 

  8. AJ Crawford (2003) ArticleTitleHuge populations and old species of Costa Rican and Panamanian dirt frogs inferred from mitochondrial and nuclear gene sequences. Mol Ecol 12 2525–2540 Occurrence Handle10.1046/j.1365-294X.2003.01910.x Occurrence Handle1:STN:280:DC%2BD3svivFKktg%3D%3D Occurrence Handle12969459

    Article  CAS  PubMed  Google Scholar 

  9. MA Donnelly (1999) ArticleTitleReproductive phenology of Eleutherodactylus bransfordii in northeastern Costa Rica. J Herpetol 33 624–631

    Google Scholar 

  10. WE Duellman JB Pramuk (1999) ArticleTitleFrogs of the genus Eleutherodactylus (Anura: Leptodactylidae) in the Andes of northern Peru. Sci Papers Nat Hist Mus Univ Kans 13 1–78

    Google Scholar 

  11. N Goldman Z Yang (1994) ArticleTitleA codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 11 725–736 Occurrence Handle7968486

    PubMed  Google Scholar 

  12. MA Iturralde-Vinent RDE MacPhee (1999) ArticleTitlePaleogeography of the Caribbean region: Implications for Cenozoic biogeography. Bull Am Mus Nat Hist 238 1–95

    Google Scholar 

  13. KP Johnson DH Clayton (2000) ArticleTitleNuclear and mitochondrial genes contain similar phylogenetic signal for pigeons and doves (Aves: Columbiformes). Mol Phylogenet Evol 14 141–151 Occurrence Handle10.1006/mpev.1999.0682 Occurrence Handle1:CAS:528:DC%2BD3cXisFemsA%3D%3D Occurrence Handle10631048

    Article  CAS  PubMed  Google Scholar 

  14. M Kimura (1983) The neutral theory of molecular evolution. Cambridge University Press Cambridge

    Google Scholar 

  15. JD Lynch (2000) ArticleTitleThe relationships of an ensemble of Guatemalan and Mexican frogs (Eleutherodactylus: Leptodactylidae: Amphibia). Rev Acad Colomb Cienc 24 67–94 Occurrence Handle1:STN:280:BiyC1MrgtlU%3D Occurrence Handle6573657

    CAS  PubMed  Google Scholar 

  16. JD Lynch WE Duellman (1997) ArticleTitleFrogs of the genus Eleutherodactylus in western Ecuador. Univ Kans Nat Hist Mus Spec Pub 23 1–236

    Google Scholar 

  17. JR Macey A Larson NB Ananjeva Z Fang TJ Papenfuss (1997) ArticleTitleTwo novel gene orders and the role of light-stand replication in rearrangement of the vertebrate mitochondrial genome. Mol Biol Evol 14 91–104 Occurrence Handle1:CAS:528:DyaK2sXjvFyisw%3D%3D Occurrence Handle9000757

    CAS  PubMed  Google Scholar 

  18. JR Macey JA Schulte II A Larson Z Fang Y Wang BS Tuniyev TJ Papenfuss (1998) ArticleTitlePhylogenetic relationships of toads in the Bufo bufo species group from the eastern escarpment of the Tibetan Plateau: A case of vicariance and dispersal. Mol Phylogenet Evol 9 80–87 Occurrence Handle10.1006/mpev.1997.0440 Occurrence Handle1:CAS:528:DyaK1cXht1yhurk%3D Occurrence Handle9479697

    Article  CAS  PubMed  Google Scholar 

  19. AP Martin (1999) ArticleTitleSubstitution rates of organelle and nuclear genes in sharks: Implicating metabolic rate (again). Mol Biol Evol 16 996–1002 Occurrence Handle1:CAS:528:DyaK1MXksFOlsLw%3D Occurrence Handle10406116

    CAS  PubMed  Google Scholar 

  20. AP Martin SR Palumbi (1993) ArticleTitleBody size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci USA 90 4087–4091 Occurrence Handle1:CAS:528:DyaK3sXkt1ehs7o%3D

    CAS  Google Scholar 

  21. AP Martin GJP Naylor SR Palumbi (1992) ArticleTitleRate of mitochondrial DNA evolution is slow in sharks compared to mammals. Nature 357 153–155 Occurrence Handle1:CAS:528:DyaK38XktVCmtLg%3D Occurrence Handle1579163

    CAS  PubMed  Google Scholar 

  22. T Miyata H Hayashida R Kikuno M Hasegawa M Kobayashi K Koike (1982) ArticleTitleMolecular clock of silent substitution: at least six-fold preponderance of silent changes in mitochondrial genes over those in nuclear genes. J Mol Evol 19 28–35 Occurrence Handle1:CAS:528:DyaL3sXms1Cmsw%3D%3D Occurrence Handle7161808

    CAS  PubMed  Google Scholar 

  23. EN Moriyama JR Powell (1997) ArticleTitleSynonymous substitution rates in Drosophila: Mitochondrial versus nuclear genes. J Mol Evol 45 378–391 Occurrence Handle1:CAS:528:DyaK2sXms1Wmur4%3D Occurrence Handle9321417

    CAS  PubMed  Google Scholar 

  24. SR Palumbi (1989) ArticleTitleRates of molecular evolution and the fraction of nucleotide positions free to vary. J Mol Evol 29 180–187 Occurrence Handle1:CAS:528:DyaL1MXkvFansL0%3D Occurrence Handle2509718

    CAS  PubMed  Google Scholar 

  25. G Pesole C Gissi A De Chirico C Saccone (1999) ArticleTitleNucleotide substitution rate of mammalian mitochondrial genomes. J Mol Evol 48 427–434 Occurrence Handle1:CAS:528:DyaK1MXhvFyqu7w%3D Occurrence Handle10079281

    CAS  PubMed  Google Scholar 

  26. JR Powell A Caccone GD Amato C Yoon (1986) ArticleTitleRates of nucleotide substitution in Drosophila mitochondrial DNA and nuclear DNA are similar. Proc Natl Acad Sci USA 83 9090–9093 Occurrence Handle1:CAS:528:DyaL2sXjtVeisA%3D%3D Occurrence Handle3097641

    CAS  PubMed  Google Scholar 

  27. TM Prychitko WS Moore (2000) ArticleTitleComparative evolution of the mitochondrial cytochrome b gene and nuclear β-fibrinogen intron 7 in woodpeckers. Mol Biol Evol 17 1101–1111 Occurrence Handle1:CAS:528:DC%2BD3cXksVOlsr0%3D Occurrence Handle10889223

    CAS  PubMed  Google Scholar 

  28. DM Rand (1994) ArticleTitleThermal habit, metabolic rate and the evolution of mitochondrial DNA. Trends Ecol Evol 9 125–131 Occurrence Handle10.1016/0169-5347(94)90176-7

    Article  Google Scholar 

  29. DE Rosen (1976) ArticleTitleA vicariance model of Caribbean biogeography. Syst Zool 24 431–464

    Google Scholar 

  30. J Rozas R Rozas (1999) ArticleTitleDnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15 174–175 Occurrence Handle10.1093/bioinformatics/15.2.174 Occurrence Handle1:CAS:528:DyaK1MXisVOksrY%3D Occurrence Handle10089204

    Article  CAS  PubMed  Google Scholar 

  31. JM Savage (1966) ArticleTitleThe origins and history of the Central American herpetofauna. Copeia 1966 719–766

    Google Scholar 

  32. JM Savage (1982) ArticleTitleThe enigma of the Central American herpetofauna: Dispersals or vicariance? Ann Mo Bot Gard 69 464–547

    Google Scholar 

  33. PM Sharp W-H Li (1989) ArticleTitleOn the rate of DNA sequence evolution in Drosophila. J Mol Evol 28 398–402 Occurrence Handle1:CAS:528:DyaL1MXit1yrs78%3D Occurrence Handle2501501

    CAS  PubMed  Google Scholar 

  34. FH Sheldon CE Jones KG McCracken (2000) ArticleTitleRelative patterns and rates of evolution in heron nuclear and mitochondrial DNA. Mol Biol Evol 17 437–450 Occurrence Handle1:CAS:528:DC%2BD3cXhvVahsL0%3D Occurrence Handle10723744

    CAS  PubMed  Google Scholar 

  35. RW Slade C Moritz A Heideman (1994) ArticleTitleMultiple nuclear-gene phylogenies: Application to pinnipeds and comparison with a mitochondrial DNA gene phylogeny. Mol Biol Evol 11 341–356 Occurrence Handle1:CAS:528:DyaK2cXksl2hu70%3D Occurrence Handle8015430

    CAS  PubMed  Google Scholar 

  36. SM Stigler (1999) Statistics on the table: The history of statistical concepts and methods. Harvard University Press Cambridge, MA

    Google Scholar 

  37. RC Tinsley MJ McCoid (1996) Feral populations of Xenopus outside Africa. RC Tinsley HR Kobel (Eds) The biology of Xenopus. Oxford University Press New York 329–347

    Google Scholar 

  38. L Vawter WM Brown (1986) ArticleTitleNuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science 234 194–196 Occurrence Handle1:CAS:528:DyaL28XlvVGhsr0%3D Occurrence Handle3018931

    CAS  PubMed  Google Scholar 

  39. F Wright (1990) ArticleTitleThe “effective number of codons” used in a gene. Gene 87 23–29

    Google Scholar 

  40. C-I Wu W-H Li (1985) ArticleTitleEvidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82 1741–1745 Occurrence Handle1:CAS:528:DyaL2MXhvVSisro%3D Occurrence Handle3856856

    CAS  PubMed  Google Scholar 

  41. Z Yang (2000) Phylogenetic analysis by maximum likelihood (PAML), version 3.0. University College London London

    Google Scholar 

Download references

Acknowledgements

Thanks go to E.N. Smith for the samples of the “mexicanus” group and A. Carnaval for the Brazilian sample. Collecting permits were kindly provided by MINAE in Costa Rica and ANAM in Panama. E. Stahl got me fixated on silent site variation. I thank J. Comeron and G. Reeves for help with analyses. Comments on earlier incarnations of this paper were provided by M. Kreitman, M. Wade, J. Comeron, T. Duda, N. Lehman, and two anonymous reviewers. This project was supported by an OTS graduate research fellowship, a STRI-OTS Mellon predoctoral fellowship, Sigma Xi, the ASIH, and the SICB.

Author information

Authors and Affiliations

  1. Committee on Evolutionary Biology, University of Chicago, Chicago, IL 60637, USA

    Andrew J. Crawford

Authors
  1. Andrew J. Crawford
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew J. Crawford.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crawford, A.J. Relative Rates of Nucleotide Substitution in Frogs . J Mol Evol 57, 636–641 (2003). https://doi.org/10.1007/s00239-003-2513-7

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-2513-7

Keywords

Search

Navigation