Mutators and sex in bacteria: conflict between adaptive strategies.

Bacterial mutation rates can increase and produce genetic novelty, as shown by in vitro and in silico experiments. Despite the cost due to a heavy deleterious mutation load, mutator alleles, which increase the mutation rate, can spread in asexual populations during adaptation because they remain associated with the rare favorable mutations they generate. This indirect selection for a genetic system generating diversity (second-order selection) is expected to be highly sensitive to changes in the dynamics of adaptation. Here we show by a simulation approach that even rare genetic exchanges, such as bacterial conjugation or transformation, can dramatically reduce the selection of mutators. Moreover, drift or competition between the processes of mutation and recombination in the course of adaptation reveal how second-order selection is unable to optimize the rate of generation of novelty.

[1]  R. Lenski,et al.  Diminishing returns from mutation supply rate in asexual populations. , 1999, Science.

[2]  F. Jacob,et al.  Evolution and tinkering. , 1977, Science.

[3]  M. Nowak,et al.  Adaptive evolution of highly mutable loci in pathogenic bacteria , 1994, Current Biology.

[4]  Christopher G. Dowson,et al.  Localized sex in bacteria , 1991, Nature.

[5]  H. Muller Some Genetic Aspects of Sex , 1932, The American Naturalist.

[6]  A. Kondrashov MODIFIERS OF MUTATION-SELECTION BALANCE - GENERAL-APPROACH AND THE EVOLUTION OF MUTATION-RATES , 1995 .

[7]  F. Taddei,et al.  cAMP-dependent SOS induction and mutagenesis in resting bacterial populations. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[8]  F B Christiansen,et al.  Waiting with and without recombination: the time to production of a double mutant. , 1998, Theoretical population biology.

[9]  W. Whitman,et al.  Prokaryotes: the unseen majority. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[10]  P. Reeves,et al.  Nucleotide sequences of the gnd genes from nine natural isolates of Escherichia coli: evidence of intragenic recombination as a contributing factor in the evolution of the polymorphic gnd locus , 1991, Journal of bacteriology.

[11]  T. Johnson The approach to mutation–selection balance in an infinite asexual population, and the evolution of mutation rates , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  Motoo Kimura,et al.  On the evolutionary adjustment of spontaneous mutation rates , 1967 .

[13]  F. Taddei,et al.  Highly variable mutation rates in commensal and pathogenic Escherichia coli. , 1997, Science.

[14]  D. Dykhuizen Experimental Studies of Natural Selection in Bacteria , 1990 .

[15]  Mark M. Tanaka,et al.  Contingency Loci, Mutator Alleles, and Their Interactions: Synergistic Strategies for Microbial Evolution and Adaptation in Pathogenesis a , 1999, Annals of the New York Academy of Sciences.

[16]  R. Redfield Evolution of bacterial transformation: is sex with dead cells ever better than no sex at all? , 1988, Genetics.

[17]  R. Lenski,et al.  Evolution of high mutation rates in experimental populations of E. coli , 1997, Nature.

[18]  Alex van Belkum,et al.  Short-Sequence DNA Repeats in Prokaryotic Genomes , 1998, Microbiology and Molecular Biology Reviews.

[19]  D. Dykhuizen,et al.  Recombination in Escherichia coli and the definition of biological species , 1991, Journal of bacteriology.

[20]  Hervé Le Nagard,et al.  Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. , 1999, Genetics.

[21]  J. Miller,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. , 2000, Genetics.

[22]  H. Berger,et al.  Selective allele loss in mixed infections with T4 bacteriophage. , 1973, Genetics.

[23]  W. L. Payne,et al.  High Mutation Frequencies Among Escherichia coli and Salmonella Pathogens , 1996, Science.

[24]  M W Feldman,et al.  Modifiers of mutation rate: a general reduction principle. , 1986, Theoretical population biology.

[25]  K. Dawson The dynamics of infinitesimally rare alleles, applied to the evolution of mutation rates and the expression of deleterious mutations. , 1999, Theoretical population biology.

[26]  J. Miller,et al.  Proliferation of mutators in A cell population , 1997, Journal of bacteriology.

[27]  T. Whittam,et al.  Nucleotide polymorphism and evolution in the glyceraldehyde-3-phosphate dehydrogenase gene (gapA) in natural populations of Salmonella and Escherichia coli. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[28]  T. Johnson Beneficial mutations, hitchhiking and the evolution of mutation rates in sexual populations. , 1999, Genetics.

[29]  R. A. Fisher,et al.  The Genetical Theory of Natural Selection , 1931 .

[30]  L. V. Valen,et al.  A new evolutionary law , 1973 .

[31]  J. Peden,et al.  Simple sequence repeats in the Helicobacter pylori genome , 1998, Molecular microbiology.

[32]  F. Taddei,et al.  Role of mutator alleles in adaptive evolution , 1997, Nature.

[33]  D. Thaler,et al.  Microbial genetics: The tinkerer's evolving tool-box , 1997, Nature.

[34]  J. M. Smith,et al.  Free recombination within Helicobacter pylori. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Edward C. Cox,et al.  Transposable elements as mutator genes in evolution , 1983, Nature.

[36]  J. Miller,et al.  Spontaneous mutators in bacteria: insights into pathways of mutagenesis and repair. , 1996, Annual review of microbiology.

[37]  E Pennisi,et al.  How the Genome Readies Itself for Evolution , 1998, Science.

[38]  Michael Lynch,et al.  Estimate of the genomic mutation rate deleterious to overall fitness in E. coll , 1996, Nature.

[39]  D. Dykhuizen,et al.  Clonal divergence in Escherichia coli as a result of recombination, not mutation. , 1994, Science.

[40]  J Ninio,et al.  Transient mutators: a semiquantitative analysis of the influence of translation and transcription errors on mutation rates. , 1991, Genetics.