Skip to main content
Log in

DNA turnover and the molecular clock

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

Summary

Many detailed studies on the mechanisms by which different components of eukaryotic nuclear genomes have diverged reveal that the majority of sequences are seemingly not passively accumulating base substitutions in a clocklike manner solely determined by laws of diffusion at the population level. It appears that variation in the rates, units, biases, and gradients of several DNA turnover mechanisms are contributing to the course of DNA divergence. Turnover mechanisms have the potential to retard, maintain, or accelerate the rate of DNA differentiation between populations. Furthermore, examples are known of coding and noncoding DNA subject to the simultaneous operation of several turnover mechanisms leading to complex patterns of fine-scale restructuring and divergence, generally uninterpretable using selection and/or neutral drift arguments in isolation. Constancy in the rate of divergence, where observed over defined periods of time, could be a reflection of constancy in the rates and units of turnover. However, a consideration of the generally large disparity between rates of turnover and mutation reveals that DNA clocks, which would be independently driven by turnover in separate genomic components, would tend to be episodic. The utility of any given DNA sequence for measuring time and species relationships, like individual proteins, is proportional to the extent to which all contributing forces to the evolution of the sequence, internal and external, are understood.

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

Access this article

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

  • Arnheim N (1983) Concerted evolution of multigene families. In: Nei M, Koehn RK (eds) Evolution of genes and proteins. Sinauer, Sunderland MA, pp 38–61

    Google Scholar 

  • Baltimore D (1981) Gene conversion: some implications for immunoglobulin genes. Cell 24:592–594

    Article  PubMed  Google Scholar 

  • Bentley DL, Rabbitts TH (1983) Evolution of immunoglobulin VK genes: evidence indicating that recently duplicated human VK sequences have diverged by gene conversion. Cell 32:181–190

    Article  PubMed  Google Scholar 

  • Blaisdell BE (1985) Markov chain analysis finds a significant influence of neighbouring bases on the occurrence of a base in eukaryotic nuclear DNA sequences both protein-coding and noncoding. J Mol Evol 21:278–288

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Burke WD, Eickbush TH (1986) The silkmoth late chorion locus. I. Variation within two paired multigene families. J Mol Biol 190:343–356

    Article  PubMed  Google Scholar 

  • Coen ES, Dover GA (1982) Multiple Pol I initiation sequences in the rDNA of spacers ofDrosophila melanogaster. Nucleic Acids Res 10:7017–7026

    PubMed  Google Scholar 

  • Coen ES, Dover GA (1983) Unequal exchanges and the coevolution of X and Y rDNA arrays inD. melanogaster. Cell 33:849–855

    Article  PubMed  Google Scholar 

  • Coen ES, Strachan T, Dover GA (1982a) The dynamics of concerted evolution of rDNA and histone gene families in themelanogaster species subgroup ofDrosophila. J Mol Biol 158:17–35

    Article  PubMed  Google Scholar 

  • Coen ES, Thoday JM, Dover GA (1982b) Rate of turnover of structural variants in the rDNA gene family ofDrosophila melanogaster. Nature 295:564–568

    Article  PubMed  Google Scholar 

  • Cross NCP, Dover GA (1987) A novel arrangement of sequence elements surrounding the rDNA promoter and its spacer duplications in tsetse species. J Mol Biol 195:63–74

    PubMed  Google Scholar 

  • Davidson EH, Britten RJ (1971) Repetitive and non-repetitive DNA sequences and a speculation on the origins of evolutionary novelty. Q Rev Biol 66:111–138

    Google Scholar 

  • Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603

    Article  PubMed  Google Scholar 

  • Dover GA (1982) Molecular drive: a cohesive mode of species evolution. Nature 299:111–117

    Article  PubMed  Google Scholar 

  • Dover GA (1986a) The spread and success of non-Darwinian novelties. In: Karlin S, Nevo E (eds) Evolutionary processes and theory. Academic Press, New York, pp 199–237

    Google Scholar 

  • Dover GA (1986b) Molecular drive in multigene families: how biological novelties arise, spread and are assimilated. Trends Genet 2:159–165

    Article  Google Scholar 

  • Dover GA (1986c) How to drive an egg. Trends Genet 2:300–301

    Article  Google Scholar 

  • Dover GA, Flavell RB (1984) Molecular coevolution: DNA divergence and the maintenance of function. Cell 38:623–624

    Article  Google Scholar 

  • Dover GA, Strachan T (1987) Molecular drive in the evolution of the immune superfamily of genes: the initiation and spread of novelty. In: Kelsoe G, Schulze DH (eds) Evolution and vertebrate immunity. University of Texas Press, Austin, pp 15–34

    Google Scholar 

  • Dover GA, Tautz D (1986) Conservation and divergence in multigene families: alternative to selection and drift. In: Clarke BC, Robertson A, Jeffreys AJ (eds) Evolution of DNA. Phil Trans R Soc Lond [Biol] 312:275–289

  • Dover GA, Brown SDM, Coen ES, Dallas J, Strachan T, Trick M (1982) The dynamics of genome evolution and species differentiation. In: Dover GA, Flavell RB (eds) Genome evolution. Academic Press, London, pp 343–374

    Google Scholar 

  • Eickbush TH, Burke WD (1986) The silkmoth late chorion locus. II. Gradients of gene conversion in two paired multigene families. J Mol Biol 190:357–366

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Flavell RA, Allen H, Huber B, Wake C, Widera G (1985) Organisation and expression of the MHC of the C57 Black/10 mouse. Immunol Rev 84:29–40

    PubMed  Google Scholar 

  • Flavell RB (1982) Sequence amplification, deletion and rearrangement: major sources of variation during species divergence. In: Dover GA, Flavell RB (eds) Genome evolution. Academic Press, London, pp 301–324

    Google Scholar 

  • Flavell RB (1986) Repetitive DNA and chromosome evolution in plants. Phil Trans R Soc Lond [Biol] 312:227–249

    Google Scholar 

  • Gerbi SA (1985) Evolution of ribosomal DNA. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 419–517

    Google Scholar 

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

    PubMed  Google Scholar 

  • Gillespie JH (1986b) Statistical aspects of the molecular clock. In: Karlin S, Nevo E (eds) Evolutionary processes and theory. Academic Press, New York, pp 255–272

    Google Scholar 

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

    PubMed  Google Scholar 

  • Gojobori T, Nei M (1984) Concerted evolution of the immunoglobulin VH gene family. Mol Biol Evol 1:195–212

    PubMed  Google Scholar 

  • Goldsmith MR, Kafatos FC (1984) Developmentally regulated genes in silkmoths. Annu Rev Genet 18:443–487

    Article  PubMed  Google Scholar 

  • Goodman M, Koop BF, Czelusniak J, Weiss ML, Slightom JL (1984) The eta-globin gene: its long evolutionary history in the beta-globin gene family of mammals. J Mol Biol 180:803–823

    Article  PubMed  Google Scholar 

  • Grummt I Roth E, Paule MR (1982) Ribosomal RNA transcriptionin vitro is species specific. Nature 296:173–176

    Article  PubMed  Google Scholar 

  • Gutz H, Leslie JF (1976) Gene conversion: a hitherto overlooked parameter in population genetics. Genetics 83:861–866

    PubMed  Google Scholar 

  • Hancock J, Dover GA (1987) Molecular coevolution amongst ‘expansion segments’ of eukaryotic 26S/28S RNA gene inDrosophila andXenopus. J Mol Evol (in press)

  • Hess JF, Schmid CW, Shen CKJ (1984) A gradient of sequence divergence in the human adult alpha-globin duplication units. Science 226:67–70

    PubMed  Google Scholar 

  • Hood L, Campbell JH, Elgin SCR (1975) The organization, expression and evolution of antibody genes and other multigene families. Annu Rev Genet 9:305–353

    Article  PubMed  Google Scholar 

  • Jagadeeswaran P, Iorget BG, Weissmann SM (1981) Short interspersed repetitive DNA elements in eukaryotes: transposable DNA elements generated by reverse transcription of RNA Pol III transcripts? Cell 26:141–142

    Article  PubMed  Google Scholar 

  • Jeffreys AJ, Wilson V, Thein SL (1985) Hypervariable ‘minisatellite’ regions in human DNA. Nature 314:67–73

    Article  PubMed  Google Scholar 

  • Jeffreys AJ, Wilson V, Kelly R, Taylor BA, Bulfield G (1987) Mouse DNA ‘fingerprints’: analysis of chromosome localization and germ-line stability of hypervariable loci in recombinant mouse strains. Nucleic Acids Res 15:2823–2836

    PubMed  Google Scholar 

  • Karlin S, Ghandour G (1985) Comparative statistics for DNA and protein sequences: single sequence analysis. Proc Natl Acad Sci USA 82:5800–5804

    PubMed  Google Scholar 

  • Karlin S, Ghandour G, Foulser DE (1985) DNA sequence comparisons of the human, mouse and rabbit immunoglobulin kappa gene. Mol Biol Evol 2:35–45

    PubMed  Google Scholar 

  • Kedes LH (1979) Histone genes and histone messengers. Annu Rev Biochem 48:837–870

    Article  PubMed  Google Scholar 

  • Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275–276

    Article  PubMed  Google Scholar 

  • Kimura M (1983) The neutral theory of evolution. Cambridge University Press, Cambridge, pp 1–367

    Google Scholar 

  • Kreitman ME, Aguadé M (1986) Excess polymorphism at theAdh locus inDrosophila melanogaster. Genetics 114:93–110

    PubMed  Google Scholar 

  • Lamb BC, Helmi S (1982) The extent to which gene conversion can change allelic frequencies in populations. Genet Res 39:199–217

    Google Scholar 

  • Li WH, Gojobori T, Nei M (1981) Pseudogenes as a paradigm of neutral evolution. Nature 292:237–239

    Article  PubMed  Google Scholar 

  • Li WH, Luo CC, Wu CI (1985) Evolution of DNA sequences. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 1–84

    Google Scholar 

  • MacIntyre R (ed) (1985) Molecular evolutionary genetics. Plenum, New York, p 641

    Google Scholar 

  • Miklos GLG (1985) Localized highly repetitive DNA sequences in vertebrate and invertebrate genomes. In: MacIntyre RJ (ed) Molecular evolutionary genetics. Plenum, New York, pp 241–313

    Google Scholar 

  • Moss T, Mitchelson K, de Winter R (1985) The promotion of ribosomal transcription in eukaryotes. Oxford Survey of Eukaryotic Genes 2:207–250

    Google Scholar 

  • Moyzis RK, Bonnet J, Li DW, Ts'o POP (1981) An alternative view of mammalian sequence organization: short repetitive sequences organized into scrambled tandem clusters. J Mol Biol 153:871–896

    Article  PubMed  Google Scholar 

  • Nagylaki T, Petes TD (1982) Intrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes. Genetics 100:315–337

    PubMed  Google Scholar 

  • Ohno S, Epplen JT (1983) The primitive code and repeats of base oligomers as the primordial protein-encoding sequence. Proc Natl Acad Sci USA 80:3391–3395

    PubMed  Google Scholar 

  • Ohta T (1980) Evolution and variation in multigene families. Springer, Berlin

    Google Scholar 

  • Ohta T (1983) On the evolution of multigene families. Theor Popul Biol 23:216–240

    Article  PubMed  Google Scholar 

  • Ohta T, Dover GA (1983) Population genetics of multigene families that are dispersed into two or more chromosomes. Proc Natl Acad Sci USA 89:4079–4083

    Google Scholar 

  • Ohta T, Dover GA (1984) The cohesive population genetics of molecular drive. Genetics 108:501–521

    PubMed  Google Scholar 

  • Ollo R, Rougeon F (1983) Gene conversion and polymorphism: generation of mouse immunoglobulin gamma 2a chain alleles by differential gene conversion by gamma 2b chain gene. Cell 32:515–523

    Article  PubMed  Google Scholar 

  • Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604–606

    Article  PubMed  Google Scholar 

  • Palmer JD (1985) Evolution of chloroplast and mitochondrial DNA in plants and algae. In: MacIntyre R (ed) Molecular evolutionary genetics. Plenum, New York, pp 131–216

    Google Scholar 

  • Reeder RH (1984) Enhancers and ribosomal gene spacers Cell 38:349–351

    Article  PubMed  Google Scholar 

  • Rossignol JL, Nicolas A, Hamza H, Langin T (1984) Origins of gene conversion and reciprocal exchange inAscobolus. Cold Spring Harbor Symp Quant Biol 49:13–21

    PubMed  Google Scholar 

  • Ruvolo M, Smith TF (1986) Phylogeny and DNA-DNA hybridization. Mol Biol Evol 3:285–289

    PubMed  Google Scholar 

  • Sibley CG, Ahlquist JE (1984) The phylogeny of the hominoid primates, as indicated by DNA-DNA hybridisation. J Mol Evol 20:2–15

    PubMed  Google Scholar 

  • Singer MF (1982) Highly repeated sequences in mammalian genomes. Int Rev Cytol 76:67–112

    PubMed  Google Scholar 

  • Smith GP (1973) Unequal crossover and the evolution of multigene families. Cold Spring Harbor Symp Quant Biol 38:507–513

    Google Scholar 

  • Smithies O, Powers PA (1986) Gene conversions and their relation to homologous chromosome pairing. Phil Trans R Soc Lond [Biol] 312:291–302

    Google Scholar 

  • Southern EM (1975) Long range periodicities in mouse satellite DNA. J Mol Biol 94:51–69

    Article  PubMed  Google Scholar 

  • Steinmetz M, Hood L (1983) Genes of the major histocompatibility complex in mouse and man. Science 222:727–734

    PubMed  Google Scholar 

  • Steinmetz M, Malissen M, Hood L, Orn A, Maki RA, Dastournikoo GR, Stephan D, Bibb E, Romaniuk R (1984) Tracts of high and low sequence divergence in the mouse major histocompatibility complex. EMBO J 3:2995–3003

    PubMed  Google Scholar 

  • Strachan T, Sodoyer R, Damotte M, Jordan BR (1984) Complete nucleotide sequence of a functional Class I HLA gene, HLA-3: implications for the evolution of HLA genes. EMBO J 3:887–893

    PubMed  Google Scholar 

  • Strachan T, Webb DA, Dover GA (1985) Transition stages during molecular drive in multiple copy DNA families inDrosophila. EMBO J 4:1701–1708

    Google Scholar 

  • Tartof KD (1975) Redundant genes. Annu Rev Genet 9:355–387

    Article  PubMed  Google Scholar 

  • Tautz D, Dover GA (1986) Transcription of the tandem array of ribosomal DNA inDrosophila does not terminate at any fixed point. EMBO J 5:1267–1273

    Google Scholar 

  • Tautz D, Trick M, Dover GA (1986) Cryptic simplicity in DNA is a major source of genetic variation. Nature 322:652–656

    Article  PubMed  Google Scholar 

  • Tautz D, Tautz C, Webb DA, Dover GA (1987) Evolutionary divergence of promoters and spacers of the rDNA family of fourDrosophila species: implications for molecular coevolution in multigene families. J Mol Biol 195:525–542

    Article  PubMed  Google Scholar 

  • Templeton AR (1985) The phylogeny of the hominoid primates: a statistical analysis of the DNA-DNA hybridization data. Mol Biol Evol 2:420–433

    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 

  • Walsh JB (1985) Interaction of selection and biased gene conversion in a multigene family. Proc Natl Acad Sci USA 82:153–157

    PubMed  Google Scholar 

  • Walsh JB (1986) Selection and biased gene conversion in a multigene family: consequences of interallelic bias and threshold selection. Genetics 112:699–716

    PubMed  Google Scholar 

  • Whitehouse HLK (1982) Genetic recombination. Understanding the mechanisms. Wiley, New York

    Google Scholar 

  • Wilson AC, Carlson SS, White TJ (1977) Biochemical evolution. Annu Rev Biochem 46:573–639

    Article  PubMed  Google Scholar 

  • Wong Z, Wilson V, Jeffreys AJ, Thein SL (1986) Cloning a selected fragment from a human DNA ‘fingerprint’: isolation of an extremely polymorphic minisatellite. Nucleic Acids Res 14:4605–4616

    PubMed  Google Scholar 

  • Zuckerkandl E (1983) Topological and quantitative relationships in evolving genomes. In: Hélène C (ed) Structure, dynamics, interactions and evolution of biological macromolecules. Reidel, Dordrecht, pp 395–412

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dover, G.A. DNA turnover and the molecular clock. J Mol Evol 26, 47–58 (1987). https://doi.org/10.1007/BF02111281

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02111281

Key words

Navigation