Mutation rate variation in multicellular eukaryotes: causes and consequences (original) (raw)

• Morgan, T. H. Evolution and Adaptation (Macmillan, New York, 1903).
  Book Google Scholar
• Sturtevant, A. H. Essays on evolution. I. On the effects of selection on mutation rate. Q. Rev. Biol. 12, 467–477 (1937). A seminal paper in which the problematic nature of non-zero mutation rate was first posed.
  Article Google Scholar
• Timofeeff-Ressovsky, N. W. Qualitativer Vergleich der Mutabilität von Drosophila funebris und D. melanogaster. Zeits. Ind. Abst. Vererb. 71, 276–280 (1936) (in German).
  Google Scholar
• Demerec, M. Frequency of spontaneous mutations in certain stocks of Drosophila melanogaster. Genetics 22, 469–478 (1937).
  CAS PubMed PubMed Central Google Scholar
• Leigh, E. G. The evolution of mutation rates. Genetics 73, 1–18 (1973).
  Google Scholar
• McVean, G. T. & L. D. Hurst . Evidence for a selectively favourable reduction in the mutation rate of the X chromosome. Nature 386, 388–392 (1997).
  Article CAS PubMed Google Scholar
• Drake, J. W. Chaos and order in spontaneous mutation. Genetics 173, 1–8 (2006).
  CAS PubMed PubMed Central Google Scholar
• Fisher, R. A. The Genetical Theory of Natural Selection (Oxford Univ. Press, Oxford, 1930).
  Book Google Scholar
• Kimura, M. Optimum mutation rate and degree of dominance as determined by the principle of minimum genetic load. J. Genet. 57, 21–34 (1960).
  Article Google Scholar
• Kimura, M. On evolutionary adjustment of spontaneous mutation rates. Genet. Res. 9, 23–27 (1967). One of the first theoretical treatments of the evolution of mutation rate; the author introduced the idea of the 'cost of fidelity'.
  Article Google Scholar
• Leigh, E. G. Natural selection and mutability. Am. Nat. 104, 301–305 (1970). Demonstrated that natural selection (almost) always favours a reduced mutation rate in sexual populations but not necessarily among asexuals.
  Article Google Scholar
• Karlin, S. & McGregor, J. Towards a theory of evolution of modifier genes. Theor. Pop. Biol. 5, 59–103 (1974).
  Article CAS Google Scholar
• Kondrashov, A. S. Modifiers of mutation-selection balance — general approach and the evolution of mutation rates. Genet. Res. 66, 53–69 (1995). A very general treatment of the evolution of mutation rate, in which the connection between the strength of selection on a modifier of mutation rate and the average effect of a mutation is made explicit.
  Article Google Scholar
• Kondrashov, A. S. Dynamics of unconditionally deleterious mutations — Gaussian approximation and soft selection. Genet. Res. 65, 113–121 (1995).
  Article CAS PubMed Google Scholar
• Dawson, K. J. Evolutionarily stable mutation rates. J. Theor. Biol. 194, 143–157 (1998).
  Article CAS PubMed Google Scholar
• Johnson, T. Beneficial mutations, hitchhiking and the evolution of mutation rates in sexual populations. Genetics 151, 1621–1631 (1999).
  CAS PubMed PubMed Central Google Scholar
• Andre, J. B. & Godelle, B. The evolution of mutation rate in finite asexual populations. Genetics 172, 611–626 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Sniegowski, P. D., Gerrish, P. J., Johnson, T. & Shaver, A. The evolution of mutation rates: separating causes from consequences. Bioessays 22, 1057–1066 (2000).
  Article CAS PubMed Google Scholar
• Gerrish, P. J., Colato, A., Perelson, A. S. & Sniegowski, P. D. Complete genetic linkage can subvert natural selection. Proc. Natl Acad. Sci. USA 104, 6266–6271 (2007). A theoretical demonstration that fluctuating selection in an asexual organism can cause the population to 'adapt itself to death' by hitchhiking deleterious mutations with beneficial alleles.
  Article CAS PubMed PubMed Central Google Scholar
• Drake, J. W., Charlesworth, B., Charlesworth, D. & Crow, J. F. Rates of spontaneous mutation. Genetics 148, 1667–1686 (1998). Still the most comprehensive review from an evolutionary perspective of the broad field of spontaneous mutation.
  CAS PubMed PubMed Central Google Scholar
• Schaaper, R. M. Antimutator mutants in bacteriophage T4 and Escherichia coli. Genetics 148, 1579–1585 (1998).
  CAS PubMed PubMed Central Google Scholar
• Haldane, J. B. S. The effect of variation on fitness. Am. Nat. 71, 337–349 (1937).
  Article Google Scholar
• Hill, W. G. & Robertson, A. The effects of linkage on limits to artificial selection. Genet. Res. 8, 269–294 (1966).
  Article CAS PubMed Google Scholar
• Charlesworth, B., Morgan, M. T. & Charlesworth, D. The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289–1303 (1993).
  CAS PubMed PubMed Central Google Scholar
• Campbell, N. A. Biology 6th edn (Benjamin Cummings, Menlo Park, California, 2004).
  Google Scholar
• Alberts, B. et al. Molecular Biology of the Cell 4th edn (Garland, New York, 2002).
  Google Scholar
• Jeffreys, A. J., Royle, N. J., Wilson, V. & Wong, Z. Spontaneous mutation rates to new length alleles at tandem-repetitive hypervariable loci in human DNA. Nature 332, 278–281 (1988).
  Article CAS PubMed Google Scholar
• Fileé, J., Forterre, P., Sen-Lin, T. & Laurent, J. Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J. Mol. Evol. 54, 763–773 (2002).
  Article PubMed CAS Google Scholar
• Johnson, R. E., Washington, M. T., Prakash, S. & Prakash, L. Fidelity of human DNA polymerase-η. J. Biol. Chem. 275, 7447–7450 (2000).
  Article CAS PubMed Google Scholar
• Landis, G. N. & Tower, J. Superoxide dismutase evolution and lifespan regulation. Mech. Ageing Dev. 126, 365–379 (2005).
  Article CAS PubMed Google Scholar
• Hebert, P. D. N. & Emery, C. J. The adaptive significance of cuticular pigmentation in Daphnia. Funct. Ecol. 4, 703–710 (1990).
  Article Google Scholar
• Saul, R. L. & Ames, B. N. Background levels of DNA damage in the population. Basic Life Sci. 38, 529–535 (1986).
  CAS PubMed Google Scholar
• Lindahl, T. Instability and decay of the primary DNA structure. Nature 362, 709–715 (1993). A broad-based review that covers all the ways in which the DNA molecule can suffer chemical damage to lead to mutation.
  Article CAS PubMed Google Scholar
• Beckman, R. B. & Ames, B. N. Oxidative decay of DNA. J. Biol. Chem. 272, 19633–19636 (1997).
  Article CAS PubMed Google Scholar
• Eisen, J. A. & Hanawalt, P. C. A phylogenomic study of DNA repair genes, proteins, and processes. Mutat. Res. 435, 171–213 (2000).
  Article Google Scholar
• Taylor, E. M. & Lehmann A. R. Conservation of eukaryotic DNA repair mechanisms. Int. J. Radiat. Biol. 74, 277–286 (1998).
  Article CAS PubMed Google Scholar
• Harfe, B. D. & Jinks-Robertson, S. DNA mismatch repair and genomic instability. Annu. Rev. Genet. 34, 359–399 (2000).
  Article CAS PubMed Google Scholar
• Denver, D. R., Swenson, S. L. & Lynch, M. An evolutionary analysis of the helix–hairpin–helix superfamily of DNA repair glycosylases. Mol. Biol. Evol. 20, 1603–1611 (2003).
  Article CAS PubMed Google Scholar
• Kurowski, M. A., Bhagwat, A. S., Papaj G. & Bujnicki, J. M. Phylogenomic identification of five new human homologs of the DNA repair enzyme AlkB. BMC Genomics 4, 48 (2003).
  Article PubMed PubMed Central Google Scholar
• Weischenfeldt, J., Lykke-Andersen, J. & Porse, B. Messenger RNA surveillance: neutralizing natural nonsense. Curr. Biol. 15, R559–R562 (2005).
  Article CAS PubMed Google Scholar
• Rutherford, S. L. & Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 396, 336–342 (1998). The first report of a protein's ability to buffer the phenotypic effects of mutations.
  Article CAS PubMed Google Scholar
• Rutherford, S. L. Between genotype and phenotype: protein chaperones and evolvability. Nature Rev. Genet. 4, 263–274 (2003).
  Article CAS PubMed Google Scholar
• Selker, E. U. Premeiotic instability of repeated sequences in Neurospora crassa. Annu. Rev. Genet. 24, 579–613 (1990).
  Article CAS PubMed Google Scholar
• Freitag, M., Williams, R. L., Kothe, G. O. & Selker, E. U. A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc. Natl Acad. Sci. USA 99, 8802–8807 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Mukai, T. & Cockerham, C. C. Spontaneous mutation rates at enzyme loci in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 74, 2514–2517 (1977).
  Article CAS PubMed PubMed Central Google Scholar
• Russell, L. B. & Russell, W. L. Spontaneous mutations recovered as mosaics in the mouse specific-locus test. Proc. Natl Acad. Sci. USA 93, 13072–13077 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Kondrashov, A. S. Direct estimates of human per nucleotide mutation rates at 20 loci causing Mendelian diseases. Hum. Mutat. 21, 12–27 (2003).
  Article CAS PubMed Google Scholar
• Nachman, M. W. & Crowell, S. L. Estimate of the mutation rate per nucleotide in humans. Genetics 156, 297–304 (2000).
  CAS PubMed PubMed Central Google Scholar
• Denver, D. R., Morris, K., Lynch, M. & Thomas, W. K. High mutation rate and predominance of insertions in the Caenorhabditis elegans nuclear genome. Nature 430, 679–682 (2004).
  Article CAS PubMed Google Scholar
• Haag-Liautard, C. et al. Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature 445, 82–85 (2007). The authors report significant mutation rate variation among three distinct Drosophila mutation-accumulation line lineages.
  Article CAS PubMed Google Scholar
• Howell, N. et al. The pedigree rate of sequence divergence in the human mitochondrial genome: there is a difference between phylogenetic and pedigree rates. Am. J. Hum. Genet. 72, 659–670 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Denver, D. R., Morris, K., Lynch, M., Vassilieva, L. L. & Thomas, W. K. High direct estimate of the mutation rate in the mitochondrial genome of Caenorhabditis elegans. Science 289, 2342–2344 (2000).
  Article CAS PubMed Google Scholar
• Lynch, M., Koskella, B. & Schaack, S. Mutation pressure and the evolution of organelle genomic architecture. Science 311, 1727–1730 (2006). The authors propose that the features of genomic architecture are largely determined by the non-adaptive forces of genetic drift and mutation pressure.
  Article CAS PubMed Google Scholar
• Palmer, J. D. & Herbon, L. A. Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J. Mol. Evol. 28, 87–97 (1988). A demonstration that plant mitochondrial genomes experience high rates of structural rearrangement and low rates of nucleotide substitution, unlike animal mitochondrial genomes that generally evolve with low rearrangement rates and high substitution rates.
  Article CAS PubMed Google Scholar
• Filipski, J. Why the rate of silent codon substitutions is variable within a vertebrate genome. J. Theor. Biol. 134, 159–164 (1988).
  Article CAS PubMed Google Scholar
• Wolfe, K. H., Sharp, P. M. & Li, W.-H. Mutation rates differ among regions of the mammalian genome. Nature 337, 283–285 (1989).
  Article CAS PubMed Google Scholar
• Lercher, M. J. & Hurst, L. D. Human SNP variability and mutation rate are higher in regions of high recombination. Trends Genet. 18, 337–340 (2002).
  Article CAS PubMed Google Scholar
• Gaffney, D. J. & Keightley, P. D. The scale of mutational variation in the murid genome. Genome Res. 15, 1086–1094 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Hardison, R. C. et al. Covariation in frequencies of substitution, deletion, transposition, and recombination during eutherian evolution. Genome Res. 13, 13–26 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Matassi, G., Sharp, P. M. & Gautier C. Chromosomal location effects on gene sequence evolution in mammals. Curr. Biol. 9, 786–791 (1999).
  Article CAS PubMed Google Scholar
• Williams, E. J. B. & Hurst, L. D. Clustering of tissue-specific genes underlies much of the similarity in rates of protein evolution of linked genes. J. Mol. Evol. 54, 511–518 (2002).
  Article CAS PubMed Google Scholar
• Lercher, M. J., Chamary, J. V. & Hurst, L. D. Genomic regionality in rates of evolution is not explained by clustering of genes of comparable expression profile. Genome Res. 14, 1002–1013 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Webster, M. T., Smith, N. G. C., Lercher, M. J. & Ellegren, H. Gene expression, synteny, and local similarity in human noncoding mutation rates. Mol. Biol. Evol. 21, 1820–1830 (2004).
  Article CAS PubMed Google Scholar
• Boulikas, T. Evolutionary consequences of nonrandom damage and repair of chromatin domains. J. Mol. Evol. 35, 156–180 (1992).
  Article CAS PubMed Google Scholar
• Denver, D. R., Feinberg, S., Steding, C., Durbin, M. & Lynch, M. The relative roles of three DNA repair pathways in preventing Caenorhabditis elegans mutation accumulation. Genetics 174, 57–65 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Prendergast, J. G. D. et al. Chromatin structure and evolution in the human genome. BMC Evol. Biol. 7, 72 (2007). The authors show that the mutational milieu varies predictably with chromatin structure, and that groups of functional genes are nonrandomly associated with different mutational domains.
  Article PubMed CAS PubMed Central Google Scholar
• Lichtenauer-Kaligis, E. G. R., van der Velde-van Dijke, T., Dendulk, H., van de Putte, P., Giphart-Gassler, M. & Tasseron-de Jong, J. G. Genomic position influences spontaneous mutagenesis of an integrated retroviral vector containing the hprt cDNA as target for mutagenesis. Hum. Mol. Genet. 2, 173–182 (1993).
  Article CAS PubMed Google Scholar
• Chuang, J. H. & Li, H. Functional bias and spatial organization of genes in mutational hot and cold regions in the human genome. PLoS Biol. 2, 253–263 (2004).
  Article CAS Google Scholar
• Kondrashov, A. S. Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440 (1988).
  Article CAS PubMed Google Scholar
• Keightley, P. D. & Otto S. P. Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443, 89–92 (2006).
  Article CAS PubMed Google Scholar
• Bateman, A. J. The viability of near-normal irradiated chromosomes. Int. J. Radiat. Biol. 1, 170–180 (1959).
  Google Scholar
• Mukai, T. The genetic structure of natural populations of Drosophila melanogaster. I. Spontaneous mutation rate of polygenes controlling viability. Genetics 50, 1–19 (1964).
  CAS PubMed PubMed Central Google Scholar
• Keightley, P. D. The distribution of mutation effects on viability in Drosophila melanogaster. Genetics 138, 1315–1322 (1994).
  CAS PubMed PubMed Central Google Scholar
• Shaw, F. H., Geyer, C. J. & Shaw, R. G. A comprehensive model of mutations affecting fitness and inferences for Arabidopsis thaliana. Evolution 56, 453–463 (2002).
  Article PubMed Google Scholar
• Kondrashov, A. S. & Crow, J. F. A molecular approach to estimating the human deleterious mutation rate. Hum. Mutat. 2, 229–234 (1993).
  Article CAS PubMed Google Scholar
• Funchain, P. et al. The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics 154, 959–970 (2000).
  CAS PubMed PubMed Central Google Scholar
• Degtyareva, N. P. et al. Caenorhabditis elegans DNA mismatch repair gene msh-2 is required for microsatellite stability and maintenance of genome integrity. Proc. Natl Acad. Sci. USA 99, 2158–2163 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Bégin, M. & Schoen, D. J. Low impact of germline transposition on the rate of mildly deleterious mutation in Caenorhabditis elegans. Genetics 174, 2129–2136 (2006).
  Article PubMed CAS PubMed Central Google Scholar
• Woodruff, R. C., Thompson, J. N., Seeger, M. A. & Spivey, W. E. Variation in spontaneous mutation and repair in natural population lines of Drosophila melanogaster. Heredity 53, 223–234 (1984).
  Article Google Scholar
• Cooper, T. F., Lenski, R. E. & Elena, S. F. Parasites and mutational load: an experimental test of a pluralistic theory for the evolution of sex. Proc. Biol. Sci. 272, 311–317 (2005).
  Article PubMed PubMed Central Google Scholar
• Ohta, T. & Ina, Y. Variation in synonymous substitution rates among mammalian genes and the correlation between synonymous and nonsynonymous divergences. J. Mol. Evol. 41, 717–720 (1995).
  CAS PubMed Google Scholar
• Comeron, J. M. & Kreitman, M. The correlation between synonymous and nonsynonymous substutitions in Drosophila: mutation, selection, or relaxed constraints? Genetics 150, 767–775 (1998).
  CAS PubMed PubMed Central Google Scholar
• Houle, D. & Kondrashov, A. in Evolutionary Genetics: Concepts and Case Studies (eds Fox, C. W. & Wolf, J. B.) 32–48 (Oxford Univ. Press, New York, 2006).
  Google Scholar
• Wayne, M. & Miyamoto, M. M. in Evolutionary Genetics: Concepts and Case Studies (eds Fox, C. W. & Wolf, J. B.) 14–31 (Oxford Univ. Press, New York, 2006).
  Google Scholar
• Gillespie, J. H. The Causes of Molecular Evolution (Oxford Univ. Press, New York, 1991).
  Google Scholar
• Li, W.-H. Molecular Evolution (Sinauer, Sunderland, Massachusetts, 1997). A valuable general text for the study of molecular evolution, particularly of the patterns and processes of sequence change that are due to mutation, drift and selection.
  Google Scholar
• Page, R. D. M. & Holmes, E. C. Molecular Evolution: A Phylogenetic Approach (Blackwell, Malden, Massachusetts, 1998).
  Google Scholar
• Laird, C. D., McConaughy, B. L. & McCarthy, B. J. Rate of fixation of nucleotide substitution in evolution. Nature 224, 149–154 (1969).
  Article CAS PubMed Google Scholar
• Li, W.-H., Tanimura, M. & Sharp, P. M. An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J. Mol. Evol. 25, 330–342 (1987).
  Article CAS PubMed Google Scholar
• Haldane, J. B. S. The mutation rate of the gene for hemophilia, and its segregation ratios in males and females. Ann. Eugen. 13, 262–271 (1947).
  Article CAS PubMed Google Scholar
• Ellegren, H. & Fridolfsson, A. K. Male-driven evolution of DNA sequences in birds. Nature Genet. 17, 182–184 (1997).
  Article CAS PubMed Google Scholar
• Goetting-Minesky, M. P. & Makova, K. D. Mammalian male mutation bias: impacts of generation time and regional variation in substitution rate. J. Mol. Evol. 63, 537–544 (2006).
  Article CAS PubMed Google Scholar
• Taylor, J., Tyekucheva, S., Zody, M., Chiaromonte, F. & Makova, K. D. Strong and weak male mutation bias at different sites in the primate genomes: insights from the human–chimpanzee comparison. Mol. Biol. Evol. 23, 565–573 (2006).
  Article CAS PubMed Google Scholar
• Lercher, M. J., Williams, E. J. & Hurst, L. D. Local similarity in evolutionary rates extends over whole chromosomes in human–rodent and mouse–rat comparisons: implications for understanding the mechanistic basis of the male mutation bias. Mol. Biol. Evol. 18, 2032–2039 (2001).
  Article CAS PubMed Google Scholar
• Martin, A. P. & Palumbi, S. R. Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl Acad. Sci. USA 90, 4087–4091 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Britten, R. J. Rates of DNA sequence evolution differ between taxonomic groups. Science 231, 1393–1398 (1986).
  Article CAS PubMed Google Scholar
• Saparbaev, M. & Laval, J. Excision of hypoxanthine from DNA containing dIMP residues by the Escherichia coli, yeast, rat, and human alkylpurine DNA glycosylases. Proc. Natl Acad. Sci. USA 91, 5873–5877 (1994).
  Article CAS PubMed PubMed Central Google Scholar
• Ohta, T. Slightly deleterious mutant substitutions in evolution. Nature 246, 96–98 (1973).
  Article CAS PubMed Google Scholar
• Keightley, P. D. & Caballero, A. Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 94, 3823–3827 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Kondrashov, F. A., Ogurtsov, A. Y. & Kondrashov, A. S. Selection in favor of nucleotides G and C diversifies evolution rates and levels of polymorphism in mammalian synonymous sites. J. Theor. Biol. 240, 616–626 (2006). This paper provides a basis for the use of | s | < 1 / 4 N e as the cut off between effectively neutral and effectively selected mutations.
  Article CAS PubMed Google Scholar
• Gillooly, J. F., Allen, A. P., West, G. B. & Brown, J. H. The rate of DNA evolution: effects of body size and temperature on the molecular clock. Proc. Natl Acad. Sci. USA 102, 140–145 (2005).
  Article CAS PubMed Google Scholar
• Halligan, D. L. & Keightley, P. D. Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison. Genome Res. 16, 875–884 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Nöthel, H. Adaptation of Drosophila melanogaster populations to high mutation pressure: evolutionary adjustment of mutation rates. Proc. Natl Acad. Sci. USA 84, 1045–1049 (1987).
  Article PubMed PubMed Central Google Scholar
• Baer, C. F. et al. Comparative evolutionary genetics of spontaneous mutations affecting fitness in rhabditid nematodes. Proc. Natl Acad. Sci. USA 102, 5785–5790 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Mardis, E. R. Anticipating the 1,000 dollar genome. Genome Biol. 7, 112 (2006). A review of the ongoing race for highly parallel and inexpensive new DNA sequencing methods that have already resulted in breakthrough technologies, enabling a new scale of mutational analysis.
  Article PubMed CAS PubMed Central Google Scholar
• Gibson, G. Mutation accumulation of the transcriptome. Nature Genet. 37, 458–460 (2005).
  Article CAS PubMed Google Scholar
• Lynch, M. & Conery, J. S. The origins of genome complexity. Science 302, 401–404 (2003).
  Article CAS Google Scholar
• Dacks, J. & Roger, A. J. The first sexual lineage and the relevance of facultative sex. J. Mol. Evol. 48, 779–783 (1999).
  Article CAS PubMed Google Scholar
• Butterfield, N. J. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26, 386–404 (2000).
  Article Google Scholar
• Taddei, F. et al. Role of mutator alleles in adaptive evolution. Nature 387, 700–702 (1997).
  Article CAS PubMed Google Scholar
• Tenaillon, O., Toupance, B., Le Nagard, H., Taddei, F. & Godelle, B. Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics 152, 485–493 (1999).
  CAS PubMed PubMed Central Google Scholar
• Chao, L. & Cox, E. C. Competition between high and low mutating strains of Escherichia coli. Evolution 37, 125–134 (1983).
  Article PubMed Google Scholar
• Matic, I. et al. Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277, 1833–1834 (1997).
  Article CAS PubMed Google Scholar
• Sniegowski, P. D., Gerrish, P. J. & Lenski, R. E. Evolution of high mutation rates in experimental populations of E. coli. Nature 387, 703–705 (1997).
  Article CAS PubMed Google Scholar
• Bjedov, I. et al. Stress-induced mutagenesis in bacteria. Science 300, 1404–1409 (2003).
  Article CAS PubMed Google Scholar
• Denamur, E. & Matic, I. Evolution of mutation rates in bacteria. Mol. Microbiol. 60, 820–827 (2006).
  Article CAS PubMed Google Scholar
• Keightley, P. D. & Caballero, A. Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 94, 3823–3827 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Kimura, M. On probability of fixation of mutant genes in a population. Genetics 47, 713–719 (1962).
  CAS PubMed PubMed Central Google Scholar
• Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer, Sunderland, Massachusetts, 1998).
  Google Scholar
• Garcia-Dorado, A. & Gallego, A. Comparing analysis methods for mutation-accumulation data: a simulation study. Genetics 164, 807–819 (2003).
  PubMed PubMed Central Google Scholar
• Keightley, P. D. & Bataillon, T. M. Multigeneration maximum-likelihood analysis applied to mutation accumulation experiments in Caenorhabditis elegans. Genetics 154, 1193–1201 (2000).
  CAS PubMed PubMed Central Google Scholar
• García-Dorado, A. The rate and effects distribution of viability mutation in Drosophila: minimum distance estimation. Evolution 51, 1130–1139 (1997).
  PubMed Google Scholar
• Deng, H-W. & Lynch, M. Estimation of deleterious mutation parameters in natural populations. Genetics 144, 349–360 (1996).
  CAS PubMed PubMed Central Google Scholar
• Kimura, M. Evolutionary rate at the molecular level. Nature 217, 624–626 (1968).
  Article CAS PubMed Google Scholar
• Schmalhausen, I. I. Factors of Evolution: the Theory of Stabilizing Selection (Univ. Chicago Press, Chicago, 1949).
  Google Scholar
• Waddington, C. H. Genetic assimilation of an acquired character. Evolution 7, 118–126 (1953).
  Article Google Scholar
• de Visser, J. A. et al. Perspective: Evolution and detection of genetic robustness. Evolution 57, 1959–1972 (2003).
  PubMed Google Scholar
• Flatt, T. The evolutionary genetics of canalization. Q. Rev. Biol. 80, 287–316 (2005).
  Article PubMed Google Scholar
• Wagner, G. P., Booth, G. & Bagheri-Chaichian, H. A population genetic theory of canalization. Evolution 51, 329–347 (1997).
  Article PubMed Google Scholar
• Force, A. et al. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531–1545 (1999).
  CAS PubMed PubMed Central Google Scholar
• Lynch, M. & Force, A. The probability of duplicate gene preservation by subfunctionalization. Genetics 154, 459–473 (2000).
  CAS PubMed PubMed Central Google Scholar
• Kimura, M. 1983. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, UK, 1983).
  Book Google Scholar
• Keightley, P. D. & Eyre-Walker, A. Terumi Mukai and the riddle of deleterious mutation rates. Genetics 153, 515–523 (1999).
  CAS PubMed PubMed Central Google Scholar
• Keightley, P. D. & Eyre-Walker, A. Deleterious mutations and the evolution of sex. Science 290, 331–333 (2000).
  Article CAS PubMed Google Scholar
• Harada, K., Kusakabe, S., Yamazaki, T. & Mukai, T. Spontaneous mutation rates in null and band-morph mutations of enzyme loci in Drosophila melanogaster. Jpn. J. Genet. 68, 605–616 (1993).
  Article CAS PubMed Google Scholar
• Downie, D. A. Effects of short-term spontaneous mutation accumulation for life history traits in grape phylloera, Daktulosphaira vitifoliae. Genetica 119, 237–251 (2003).
  Article CAS PubMed Google Scholar
• Vassilieva, L. L., Hook, A. M. & Lynch M. The rate of spontaneous mutation for life-history traits in Caenorhabditis elegans. Evolution 151, 119–129 (2000).
  Google Scholar
• Baer, C. F. et al. Cumulative effects of spontaneous mutations for fitness in Caenorhabditis: role of genotype, environment and stress. Genetics 174, 1387–1395 (2006).
  Article PubMed PubMed Central Google Scholar
• Cutter, A. D. & Payseur, B. A. Rates of deleterious mutation and the evolution of sex in Caenorhabditis. J. Evol. Biol. 16, 812–822 (2003).
  Article CAS PubMed Google Scholar
• Lynch, M., Latta, L., Hicks, J. & Giorgianni, M. Mutation, selection, and the maintenance of life-history variation in a natural population. Evolution 52, 727–733 (1988).
  Article Google Scholar
• Deng, H.-W., Li, J., Pfrender, M. E., Li, J.-L. & Deng, H. Upper limit of the rate and per generation effects of deleterious genomic mutations. Genet. Res. 88, 57–65 (2006).
  Article CAS PubMed Google Scholar
• Schultz, S. T., Lynch, M. & Willis, J. H. Spontaneous deleterious mutation in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 96, 11393–11398 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Wright, S. I., Lauga, B. & Charlesworth, D. Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol. Biol. Evol. 19, 1407–1420 (2002).
  Article CAS PubMed Google Scholar
• Schoen, D. J. Deleterious mutation in related species of the plant genus Amsinckia with contrasting mating systems. Evolution 59, 2370–2377 (2005).
  Article PubMed Google Scholar
• Gaffney, D. J. & Keightley, P. D. Genomic selective constraints in murid noncoding DNA. PLoS Genet. 2, 1912–1923 (2006).
  Article CAS Google Scholar