Skip to main content
SpringerLink
Log in

Rates of molecular evolution and the fraction of nucleotide positions free to vary

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

Summary

Selective constraints on DNA sequence change were incorporated into a model of DNA divergence by restricting substitutions to a subset of nucleotide positions. A simple model showed that both mutation rate and the fraction of nucleotide positions free to vary are strong determinants of DNA divergence over time.

When divergence between two species approaches the fraction of positions free to vary, standard methods that correct for multiple mutations yield severe underestimates of the number of substitutions per site. A modified method appropriate for use with DNA sequence, restriction site, or thermal renaturation data is derived taking this fraction into account. The model also showed that the ratio of divergence in two gene classes (e.g., nuclear and mitochondrial) may vary widely over time even if the ratio of mutation rates remains constant.

DNA sequence divergence data are used increasingly to detect differences in rates of molecular evolution. Often, variation in divergence rate is assumed to represent variation in mutation rate. The present model suggests that differing divergence rates among comparisons (either among gene classes or taxa) should be interpreted cautiously. Differences in the fraction of nucleotide positions free to vary can serve as an important alternative hypothesis to explain differences in DNA divergence 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

Similar content being viewed by others

References

  • Attardi G (1985) Animal mitochondrial DNA: an extreme example of genetic economy. Int Rev Cytol 93:1

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Brown WM (1985) The mitochondrial genome of animals. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum Press, New York, p 95

    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

    PubMed  Google Scholar 

  • Clary DO, Wolstenhme DR (1985) The mitochondrial DNA molecule ofDrosophila yakuba: nucleotide sequence, gene organization and genetic code. J Mol Evol 22:251–271

    Google Scholar 

  • Cloud P, Glaessner MF (1982) The Ediacarian period and system: Metazoa inherit the Earth. Science 217:783–792

    Google Scholar 

  • Coates M, Stone S (1983) Simulation of the evolution of macromolecular sequences by random fixation of allowed codons In: Goodman M (ed) Macromolecular sequences in systematic and evolutionary biology. Plenum Press, New York, pp 243–280

    Google Scholar 

  • DeSalle R, Hunt J (1987) Molecular evolution in Hawaiian drosophilids. Trends Ecol Evol 2:212–216

    Article  Google Scholar 

  • DeSalle R, Giddings LV, Templeton AR (1986) Mitochondrial DNA variability in natural populations of HawaiianDrosophila. I. Methods and levels of variability inD. silvestris andD. heteroneura populations. Heredity 56:75–85

    PubMed  Google Scholar 

  • DeSalle R, Freedman F, Prager EM, Wilson AC (1987) Tempo and mode of sequence evolution in mitochondrial DNA of HawaiianDrosophila. J Mol Evol 26:157–164

    PubMed  Google Scholar 

  • Dickerson RF (1971) The structure of cytochrome c and the rates of molecular evolution. J Mol Evol 1:26–45

    Article  PubMed  Google Scholar 

  • Fitch WM (1971) The non-identity of variable positions in the cytochrome c of different species. Biochem Genet 5:231–241

    Article  PubMed  Google Scholar 

  • Fitch WM (1980) Estimating the total number of nucleotide substitutions since the common ancestor of a pair of homologous genes: comparison of several methods and three beta hemoglobin messenger RNA's. J Mol Evol 16:153–209

    Article  PubMed  Google Scholar 

  • Fitch WM (1986) The estimate of total nucleotide substitutions from pairwise substitutions is biased. Phil Trans R Soc (Lond) Ser B 312:317–324

    Google Scholar 

  • Fitch WM, Margoliash E (1967) A method for estimating the number of invariant amino acid coding positions in a gene using cytochrome c as a model case. Biochem Genet 1:65–71

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gillespie JH (1984) The molecular clock may be an episodic clock. Proc Natl Acad Sci USA 81:8009–8013

    PubMed  Google Scholar 

  • Gillespie JH (1986a) Variability of evolutionary rates of DNA. Genetics 113:1077–1091

    PubMed  Google Scholar 

  • Gillespie JH (1986b) Natural selection and the molecular clock. Mol Biol Evol 3:138–155

    PubMed  Google Scholar 

  • Gillespie JH (1986c) Rates of molecular evolution. Annu Rev Ecol Syst 17:637–665

    Article  Google Scholar 

  • Golding GB (1987) Non-random patterns of mutation are reflected in evolutionary divergence and may cause some of the unusual patterns observed in sequences. In: Loeschcke V (ed) Genetic constraints on adptive evolution. Springer-Verlag, New York, pp 151–172

    Google Scholar 

  • Goodman M (1976) Protein sequences in phylogeny. In: Ayala FJ (ed) Molecular evolution. Sinauer, Sunderland MA, pp 141–159

    Google Scholar 

  • Hasegawa M, Kishino H, Yano T-a (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    PubMed  Google Scholar 

  • Heindell HC, Liu A, Paddock GV, Studnicka GM, Salser WA (1978) The primary sequences of rabbit α-globin mRNA. Cell 15:43–54

    Article  PubMed  Google Scholar 

  • Helm-Bychowski KM, Wilson AC (1985) Rates of nuclear DNA evolution in pheasant-like birds: evidence from restriction maps. Proc Natl Acad Sci USA 83:688–692

    Google Scholar 

  • Holmquist R, Pearl D (1980) Theoretical foundations for quantitative paleogenetics. Part III. The molecular divergence of nucleic acids and proteins for the case of genetic events of unequal probability. J Mol Evol 16:211–287

    Article  PubMed  Google Scholar 

  • Holmquist R, Cantor CR, Jukes TH (1972) Improved procedures for comparing homologous sequences in molecules of proteins and nucleic acids. J Mol Biol 64:145–161

    Article  PubMed  Google Scholar 

  • Holmquist R, Pearl D, Jukes TH (1983) Non-uniform molecular divergence: the quantitative evolutionary analysis of genes and messenger RNAs under selective structural constraints. In: Goodman M (ed) Macromolecular sequences in systematic and evolutionary biology. Plenum Press, New York, pp 281–315

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. III. Academic Press, New York, pp 21–123

    Google Scholar 

  • Jukes TH, Holmquist R (1972) Estimation of certain evolutionary changes in certain homologous polypeptide chains. J Mol Biol 64:163–179

    Article  PubMed  Google Scholar 

  • Kimura M (1979) Model of selectively neutral mutations in which selective constraint is incorporated. Proc Natl Acad Sci USA 76:3440–3444

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Konkel DA, Tilghman SM, Leder P (1978) The sequences of the chromosomal mouse β-globin major gene: homologies in capping, splicing and poly(A) sites. Cell 15:1125–1132

    Article  PubMed  Google Scholar 

  • Kunkel TA, Loeb LA (1982) Fidelity of mammalian DNA polymerases. Science 213:765–767

    Google Scholar 

  • Lewin B (1987) Genes III. Wiley and Sons, New York

    Google Scholar 

  • Li W-H (1986) Evolutionary change of restriction cleavage sites and phylogenetic inference. Genetics 113:187–213

    PubMed  Google Scholar 

  • Li W-H, Luo C-C, Wu C-I (1985) Evolution of DNA sequences. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum Press, New York, pp 1–94

    Google Scholar 

  • Manske CL, Chapman DJ (1987) Nonuniformity of nucleotide substitution rates in molecular evolution: computer simulation and analysis of 5S ribosomal RNA sequences. J Mol Evol 26:226–251

    PubMed  Google Scholar 

  • Natvig DA, Jackson DA, Taylor JW (1987) Random fragment hybridization analysis of evolution in the genusNeurospora: the status of four-spored strains. Evolution 41:1003–1021

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nicoghosian K, Brigas M, Sankoff D, Cedergren R (1987) Archetypical features of tRNA families. J Mol Evol 26:341–346

    PubMed  Google Scholar 

  • Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes J Mol Evol 26:76–86

    Google Scholar 

  • Palumbi SR, Wilson AC (1989) Mitochondrial DNA diversity in the sea urchinsStrongylocentrotus droebacchiensis andS. pupuratus. Evolution (in press)

  • Perrin P, Bernardi G (1987) Directional fixation of mutations in vertebrate evolution. J Mol Evol 26:301–310

    PubMed  Google Scholar 

  • Powell JR, Caccone A, Amato GD, Yoon C (1986) Rates of nucleotide substitution inDrosophila mitochondrial DNA and nuclear DNA are similar. Proc Natl Acad Sci USA 83:9090–9093

    PubMed  Google Scholar 

  • Quinn TW, White BN (1987) Identification of restriction fragment length polymorphisms in genomic DNA of the lesser snow goose (Anser caerulescens caerulescens). Mol Biol Evol 4:126–143

    PubMed  Google Scholar 

  • Saccone C, Attimonelli M, Sbisa E (1987) Structural elements highly preserved during the evolution of the D-loop containing region of vertebrate mitochondrial DNA. J Mol Evol 26:205–211

    PubMed  Google Scholar 

  • Takahata N (1987) On the overdispersed molecular clock. Genetics 116:169–179

    PubMed  Google Scholar 

  • Topal MD, Fresco JR (1976) Complementary base pairing and the origin of substitution mutations. Nature 263:285–289

    Article  PubMed  Google Scholar 

  • Vawter L, Brown WM (1986) Nuclear and mitochondrial DNA comparisons reveal extreme rate variation in the molecular clock. Science 234:194–196

    PubMed  Google Scholar 

  • Vogel F, Kopun M, Rathenberg R (1976) Mutations and molecular evolution. In: Goodman M, Tashian R, Tashian JH (eds) Molecular anthropology. Plenum Press, New York, p 222

    Google Scholar 

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

    Google Scholar 

  • Wu C-I, Li W-H (1985) Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82:1741–1745

    PubMed  Google Scholar 

  • Zuckerkandl E, Pauling L (1962) Molecular disease, evolution, and genic heterogeneity in proteins. In: Kasha M, Pullman B (eds) Horizons in biochemistry. Academic Press, New York, pp 189–225

    Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Hawaii, 96822, Honolulu, Hawaii, USA

    Stephen R. Palumbi

Authors
  1. Stephen R. Palumbi
    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

Palumbi, S.R. Rates of molecular evolution and the fraction of nucleotide positions free to vary. J Mol Evol 29, 180–187 (1989). https://doi.org/10.1007/BF02100116

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02100116

Key words

Search

Navigation