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The origin of adaptive mutants: Random or nonrandom?

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Abstract

Several recent reports have claimed that adaptive mutants in bacteria and yeast are induced by selective conditions. The results of these reports suggest that mutants can arise nonrandomly with respect to fitness, contrary to what has been widely accepted. In several cases that have received careful experimental reexamination, however, the detection of seemingly nonrandom mutation has been explained as an experimental artifact. In the remaining cases, there is no evidence to suggest that cells have the capacity to direct or choose which genetic variants will arise. Instead, current models propose processes by which genetic variants persist as mutations only if they enable cell growth and DNA replication. Most of these models are apparently contradicted by experimental data. One model, the hypermutable state model, has recently received limited circumstantial support. However, in this model the origin of adaptive mutants is random; the apparent nonrandomness of mutation is merely a consequence of natural selection. The critical distinction between the origin of genetic variation (mutation) and the possible consequence of that variation (selection) has been neglected by proponents of directed mutation.

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References

  • Benson SA (1988) Is bacterial evolution random or selective? Nature 336:21–22

    Google Scholar 

  • Benson SA, Decloux AM, Munro J (1991) Mutant bias in nonlethal selections results from selective recovery of mutants. Genetics 129: 647–658

    Google Scholar 

  • Benson SA, Occi JL, Sampson BA (1988) Mutations that alter the pore function of the OmpF porin of Escherichia coli K12. J Mol Biol 203:961–970

    Google Scholar 

  • Boe L (1990) Mechanism for induction of adaptive mutations in Escherichia coli. Mol Microbiol 4:597–601

    Google Scholar 

  • Cairns J, Foster PL (1991) Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128:695–701

    Google Scholar 

  • Cairns J, Overbaugh J, Miller S (1988) The origin of mutants. Nature 335:142–145

    Google Scholar 

  • Cavalli-Sforza LL, Lederberg J (1956) Isolation of pre-adaptive mutants in bacteria by sib selection. Genetics 41:367–381

    Google Scholar 

  • Chao L, Cox EC (1983) Competition between high and low mutating strains of Escherichia coli. Evolution 37:125–134

    Google Scholar 

  • Chao L, Vargas C, Spear BB, Cox EC (1983) Transposable elements as mutator genes in evolution. Nature 303:633–635

    Google Scholar 

  • Charlesworth D, Charlesworth B, Bull JJ (1988) Origin of mutants disputed. Nature 336:525

    Google Scholar 

  • Cox EC (1976) Bacterial mutator genes and the control of spontaneous mutation. Annu Rev Genet 10:135–156

    Google Scholar 

  • Cox EC, Gibson TC (1974) Selection for high mutation rates in chemostats. Genetics 77:169–184

    Google Scholar 

  • Davis BD (1989) Transcriptional bias: a non-Lamarckian mechanism for substrate-induced mutations. Proc Natl Acad Sci USA 86:5005–5009

    Google Scholar 

  • Demassey B, Fayet O, Kogoma T (1984) Multiple origin usage for DNA replication in sdr (rnh) mutants of Escherichia coli K12: initiation in the absence of oriC. J Mol Biol 128:227–236

    Google Scholar 

  • Dijkmans R, Kreps S, Mergeay M (1994) Poisson-like fluctuation patterns of revertants of leucine auxotrophy (leu-500) in Salmonella typhimurium caused by delay in mutant cell division. Genetics 137: 353–359

    Google Scholar 

  • Drake JW (1991a) A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci USA 88:7160–7164

    Google Scholar 

  • Drake JW (1991b) Spontaneous mutation. Annu Rev Genet 25:125–146

    Google Scholar 

  • Eshel I (1973) Clone selection and the evolution of modifying features. Theor Pop Biol 4:196–208

    Google Scholar 

  • Foster PL (1992) Directed mutation: between unicorns and goats. J Bacteriol 174:1711–1716

    Google Scholar 

  • Foster PL (1993) Adaptive mutation: the uses of adversity. Ann Rev Microbiol 47:467–504

    Google Scholar 

  • Foster PL, Cairns J (1992) Mechanisms of directed mutation. Genetics 131:783–789

    Google Scholar 

  • Foster PL, Cairns J (1995) The occurrence of heritable Mu excisions in starving cells of Escherichia coli. EMBO J (in press)

  • Foster PL, Trimarchi JM (1994) Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science 265:407–409

    Google Scholar 

  • Gillespie JH (1981a) Mutation modification in a random environment. Evolution 35:468–476

    Google Scholar 

  • Gillespie JH (1981b) Evolution of the mutation rate at a heterotic locus. Proc Natl Acad Sci USA 78:2452–2454

    Google Scholar 

  • Hall BG (1988) Adaptive evolution that requires multiple spontaneous mutations. I. Mutations involving an insertion sequence. Genetics 120:887–897

    Google Scholar 

  • Hall BG (1990) Spontaneous point mutations that occur more often when advantageous than when neutral. Genetics 126:5–16

    Google Scholar 

  • Hall BG (1991) Adaptive evolution that requires multiple spontaneous mutations: mutations involving base substitutions. Proc Natl Acad USA 88:5882–5886

    Google Scholar 

  • Hall BG (1992) Selection-induced mutations occur in yeast. Proc Natl Acad Sci USA 89:4300–4303

    Google Scholar 

  • Hall BG (1993) The role of single-mutant intermediates in the generation of trpAB double revertants during prolonged selection. J Bacteriol 175:6411–6414

    Google Scholar 

  • Hall BG (1994) On alternatives to selection-induced mutation in the bgl operon of Escherichia coli. Mol Biol Evol 11:159–168

    Google Scholar 

  • Harris RS, Longerich S, Rosenberg SM (1994) Recombination in adaptive mutation. Science 264:258–260

    Google Scholar 

  • Holsinger K, Feldman MW (1983) Modifiers of mutation rate: evolutionary optimum with complete selfing. Proc Natl Acad Sci USA 80:6772–6784

    Google Scholar 

  • Ishii K, Matsuda H, Iwasa Y, Sasaki A (1989) Evolutionarily stable mutation rate in a periodically changing environment. Genetics 121:163–174

    Google Scholar 

  • Kimura M (1960) Optimum mutation rate and degree of dominance as determined by the principle of minimum genetic load. J Genet 57:21–34

    Google Scholar 

  • Kimura M (1967) On the evolutionary adjustment of spontaneous mutation rates. Genet Res Camb 9:23–34

    Google Scholar 

  • Koch AL (1982) Mutation and growth rates from Luria-Delbrück fluctuation tests. Mutat Res 95:129–143

    Google Scholar 

  • Kondrashov AS (1988) Deleterious mutations and the evolution of sexual reproduction. Nature 336:435–440

    Google Scholar 

  • Lederberg J, Lederberg EM (1952) Replica plating and indirect selection of bacterial mutants. J Bacteriol 63:399–406

    Google Scholar 

  • Leigh EG (1970) Natural selection and mutability. Am Nat 104:301–305

    Google Scholar 

  • Leigh EG (1973) The evolution of mutation rates. Genetics (Suppl)73: 1–18

    Google Scholar 

  • Lenski RE (1989) Are some mutations directed? Trends Ecol Evol 4:148–150

    Google Scholar 

  • Lenski RE, Mittler JE (1993) The directed mutation controversy and neo-darwinism. Science 259:188–194

    Google Scholar 

  • Lenski RE, Slatkin M, Ayala FJ (1989) Mutation and selection in bacterial populations: alternatives to the hypothesis of directed mutation. Proc Natl Acad Sci USA 86:2775–2778

    Google Scholar 

  • Levins R (1967) Theory of fitness in a heterogeneous environment. VI. The adaptive significance of mutation. Genetics 56:163–178

    Google Scholar 

  • Lincoln RJ, Boxshall GA, Clark PF (1982) A dictionary of ecology, evolution and systematics. Cambridge University Press, Cambridge

    Google Scholar 

  • Luria SE, Delbrück M (1943) Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28:491–511

    Google Scholar 

  • MacPhee DG (1993a) Is there evidence for directed mutation in bacteria? Mutagenesis 8:3–5

    Google Scholar 

  • MacPhee DG (1993b) Directed mutation: paradigm postponed. Mutat Res 285:109–116

    Google Scholar 

  • Maenhaut-Michel G, Shapiro JA The roles of starvation and selective substrates in the emergence of araB-lacZ fusion clones. EMBO J (in press)

  • Milder JE, Lenski RE (1990) New data on excisions of Mu from E. coli MCS2 cast doubt on directed mutation hypothesis. Nature 344: 173–175

    Google Scholar 

  • Milder JE, Lenski RE (1992) Experimental evidence for an alternative to directed mutation in the bgl operon. Nature 356:446–448

    Google Scholar 

  • Moxon ER, Rainey PB, Nowak MA, Lenski RE (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4:24–33

    Google Scholar 

  • Painter PR (1975) Clone selection and the mutation rate. Theor Pop Biol 8:74–80

    Google Scholar 

  • Rosenberg SM, Longerich S, Gee P, Harris RS (1994) Adaptive mutation by deletions in small mononucleotide repeats. Science 265: 405–407

    Google Scholar 

  • Shapiro JA (1984) Observations on the formation of clones containing araB-lacZ cistron fusions. Mol Gen Genet 194:79–90

    Google Scholar 

  • Shapiro JA, Leach D (1990) Action of a transposable element in coding sequence fusions. Genetics 126:293–299

    Google Scholar 

  • Smith KG (1992) Spontaneous mutagenesis: experimental, genetic and other factors. Mutat Res 277:139–162

    Google Scholar 

  • Stahl FW (1988) A unicorn in the garden. Nature 355:112–113

    Google Scholar 

  • Stahl FW (1992) Unicorns revisited. Genetics 132:865–867

    Google Scholar 

  • Steele DF, Jinks-Robertson S (1992) An examination of adaptive reversion in Saccharomyces cerevisiae. Genetics 132:9–21

    Google Scholar 

  • Stewart FM, Gordon DM, Levin BR (1990) Fluctuation analysis: the probability distribution of the number of mutants under different conditions. Genetics 124:175–185

    Google Scholar 

  • Stewart FM (1994) Fluctuation tests: how reliable are the estimates of mutation rates? Genetics 137:1139–1146

    Google Scholar 

  • Sturtevant AH (1937) Essays on evolution. I. On the effects of selection on mutation rate. Q Rev Biol 12:467–477

    Google Scholar 

  • Symonds N (1989) Anticipatory mutagenesis? Nature 337:119–120

    Google Scholar 

  • Tessman I (1988) Origin of mutants disputed. Nature 336:527

    Google Scholar 

  • Thaler DS, Stahl FW (1988) DNA double-chain breaks in recombination of phage λ and of yeast. Annu Rev Genet 22:169–197

    Google Scholar 

  • Tröbner W, Piechocki R (1984a) Competition between isogenic mutS and mut + populations of Escherichia coli K12 in continuously growing cultures. Mol Gen Genet 198:175–176

    Google Scholar 

  • Tröbner W, Piechocki R (1984b) Selection against hypermutability in Escherichia coli during long term evolution. Mol Gen Genet 198: 177–178

    Google Scholar 

  • Witkin E, Kogoma T (1984) Involvement of the activated form of RecA protein in SOS mutagenesis and stable DNA replication in Escherichia coli. Proc Natl Acad Sci USA 81:7539–7543

    Google Scholar 

Download references

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  1. Center for Microbial Ecology, Michigan State University, 48824, East Lansing, MI, USA

    Paul D. Sniegowski

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Sniegowski, P.D. The origin of adaptive mutants: Random or nonrandom?. J Mol Evol 40, 94–101 (1995). https://doi.org/10.1007/BF00166600

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