Microbial genetics: Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation

Microorganisms have been mutating and evolving on Earth for billions of years. Now, a field of research has developed around the idea of using microorganisms to study evolution in action. Controlled and replicated experiments are using viruses, bacteria and yeast to investigate how their genomes and phenotypic properties evolve over hundreds and even thousands of generations. Here, we examine the dynamics of evolutionary adaptation, the genetic bases of adaptation, tradeoffs and the environmental specificity of adaptation, the origin and evolutionary consequences of mutators, and the process of drift decay in very small populations.

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

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

[3]  K. Atwood,et al.  Periodic selection in Escherichia coli. , 1951, Proceedings of the National Academy of Sciences of the United States of America.

[4]  A. Bateman THE VIABILITY OF NEAR-NORMAL IRRADIATED CHROMOSOMES , 1959 .

[5]  A. Gray,et al.  I. THE ORIGIN OF SPECIES BY MEANS OF NATURAL SELECTION , 1963 .

[6]  L. Pauling,et al.  Evolutionary Divergence and Convergence in Proteins , 1965 .

[7]  V. Bryson,et al.  Evolving Genes and Proteins. , 1965, Science.

[8]  R. Levins Evolution in Changing Environments , 1968 .

[9]  T. Mukai The Genetic Structure of Natural Populations of DROSOPHILA MELANOGASTER. VII Synergistic Interaction of Spontaneous Mutant Polygenes Controlling Viability. , 1969, Genetics.

[10]  M. King,et al.  Evolution at two levels in humans and chimpanzees. , 1975, Science.

[11]  C. Woese,et al.  Phylogenetic structure of the prokaryotic domain: The primary kingdoms , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[12]  F. M. Stewart,et al.  A Complex Community in a Simple Habitat: An Experimental Study with Bacteria and Phage , 1977 .

[13]  J. Haigh The accumulation of deleterious genes in a population--Muller's Ratchet. , 1978, Theoretical population biology.

[14]  N. Hairston EVOLUTION UNDER INTERSPECIFIC COMPETITION: FIELD EXPERIMENTS ON TERRESTRIAL SALAMANDERS , 1980, Evolution; international journal of organic evolution.

[15]  Daniel Hartl,et al.  EVOLUTION OF COMPETITIVE ABILITY IN ESCHERICHIA COLI , 1981, Evolution; international journal of organic evolution.

[16]  L. Chao,et al.  COMPETITION BETWEEN HIGH AND LOW MUTATING STRAINS OF ESCHERICHIA COLI , 1983, Evolution; international journal of organic evolution.

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

[18]  Masatoshi Nei,et al.  Evolution of genes and proteins. , 1983 .

[19]  R. Mortlock Microorganisms as Model Systems for Studying Evolution , 1984, Monographs in Evolutionary Biology.

[20]  R. Lenski,et al.  Constraints on the Coevolution of Bacteria and Virulent Phage: A Model, Some Experiments, and Predictions for Natural Communities , 1985, The American Naturalist.

[21]  R. Lenski EXPERIMENTAL STUDIES OF PLEIOTROPY AND EPISTASIS IN ESCHERICHIA COLI. I. VARIATION IN COMPETITIVE FITNESS AMONG MUTANTS RESISTANT TO VIRUS T4 , 1988, Evolution; international journal of organic evolution.

[22]  A. Kondrashov Deleterious mutations and the evolution of sexual reproduction , 1988, Nature.

[23]  S. Gould Wonderful Life: The Burgess Shale and the Nature of History , 1989 .

[24]  Lin Chao,et al.  Fitness of RNA virus decreased by Muller's ratchet , 1990, Nature.

[25]  D. Dykhuizen,et al.  Enzyme activity and fitness: Evolution in solution. , 1990, Trends in ecology & evolution.

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

[27]  M. Lynch,et al.  MUTATION LOAD AND THE SURVIVAL OF SMALL POPULATIONS , 1990, Evolution; international journal of organic evolution.

[28]  M. Pagel,et al.  The comparative method in evolutionary biology , 1991 .

[29]  R. Rosenzweig,et al.  Identification of adaptive changes in an evolving population of Escherichia coli: the role of changes with regulatory and highly pleiotropic effects. , 1991, Molecular biology and evolution.

[30]  R. Lenski,et al.  Long-Term Experimental Evolution in Escherichia coli. I. Adaptation and Divergence During 2,000 Generations , 1991, The American Naturalist.

[31]  J. Holland,et al.  Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses , 1991, Journal of virology.

[32]  R. Lenski,et al.  Long-term experimental evolution in Escherichia coli , 1991 .

[33]  C. Kurland,et al.  Selection of laboratory wild-type phenotype from natural isolates of Escherichia coli in chemostats. , 1992, Molecular biology and evolution.

[34]  L. Chao,et al.  Evolution of sex in RNA viruses. , 1992, Trends in ecology & evolution.

[35]  D. Penny The comparative method in evolutionary biology , 1992 .

[36]  A. Moya,et al.  Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[37]  D A Siegele,et al.  Microbial competition: Escherichia coli mutants that take over stationary phase cultures. , 1993, Science.

[38]  A. Kondrashov,et al.  Classification of hypotheses on the advantage of amphimixis. , 1993, The Journal of heredity.

[39]  A. F. Bennett,et al.  EVOLUTIONARY ADAPTATION TO TEMPERATURE II. THERMAL NICHES OF EXPERIMENTAL LINES OF ESCHERICHIA COLI , 1993, Evolution; international journal of organic evolution.

[40]  R. Rosenzweig,et al.  Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. , 1994, Genetics.

[41]  R. Lenski,et al.  Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[42]  J. Saunders Population Genetics of bacteria. , 1994 .

[43]  Richard E. Lenski,et al.  Long-Term Experimental Evolution in Escherichia coli. II. Changes in Life-History Traits During Adaptation to a Seasonal Environment , 1994, The American Naturalist.

[44]  R. Lenski,et al.  Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[45]  S. Elena,et al.  Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandfly cells , 1995, Journal of virology.

[46]  R. Lenski,et al.  LONG‐TERM EXPERIMENTAL EVOLUTION IN ESCHERICHIA COLI. III. VARIATION AMONG REPLICATE POPULATIONS IN CORRELATED RESPONSES TO NOVEL ENVIRONMENTS , 1995, Evolution; international journal of organic evolution.

[47]  W. Fitch,et al.  Dynamics of IS-related genetic rearrangements in resting Escherichia coli K-12. , 1995, Molecular biology and evolution.

[48]  Population Genetics of Bacteria , 1995 .

[49]  S. Elena,et al.  Exponential increases of RNA virus fitness during large population transmissions. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[50]  R. Lenski,et al.  Mutation and Adaptation: The Directed Mutation Controversy in Evolutionary Perspective , 1995 .

[51]  A. F. Bennett,et al.  Experimental tests of the roles of adaptation, chance, and history in evolution. , 1995, Science.

[52]  A. Moya,et al.  Genetic lesions associated with Muller's ratchet in an RNA virus. , 1996, Journal of molecular biology.

[53]  T Kibota,et al.  Estimate of the genomic mutation rate deleterious to overall fitness in E. coli , 1996 .

[54]  N. Moran Accelerated evolution and Muller's rachet in endosymbiotic bacteria. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[55]  A. F. Bennett,et al.  EVOLUTIONARY ADAPTATION TO TEMPERATURE. IV. ADAPTATION OF ESCHERICHIA COLI AT A NICHE BOUNDARY , 1996, Evolution; international journal of organic evolution.

[56]  R. Lenski,et al.  Punctuated Evolution Caused by Selection of Rare Beneficial Mutations , 1996, Science.

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

[58]  M Travisano,et al.  Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. , 1996, Genetics.

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

[60]  J. Bull,et al.  Exceptional convergent evolution in a virus. , 1997, Genetics.

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

[62]  M. Travisano,et al.  Long-term experimental evolution in Escherichia coli. VI. Environmental constraints on adaptation and divergence. , 1997, Genetics.

[63]  J. Bull,et al.  Parallel molecular evolution of deletions and nonsense mutations in bacteriophage T7. , 1997, Molecular biology and evolution.

[64]  D. Chadwick,et al.  Antibiotic resistance : origins, evolution, selection, and spread , 1997 .

[65]  Graham Bell,et al.  Experimental evolution in Chlamydomonas. III. Evolution of specialist and generalist types in environments that vary in space and time , 1997, Heredity.

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

[67]  D. Ebert Experimental evolution of parasites. , 1998, Science.

[68]  H. A. Orr,et al.  THE POPULATION GENETICS OF ADAPTATION: THE DISTRIBUTION OF FACTORS FIXED DURING ADAPTIVE EVOLUTION , 1998, Evolution; international journal of organic evolution.

[69]  P. Keightley,et al.  Inference of genome-wide mutation rates and distributions of mutation effects for fitness traits: a simulation study. , 1998, Genetics.

[70]  S. Morris Crucible Of Creation , 1998 .

[71]  J. Adams,et al.  Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. , 1998, Molecular biology and evolution.

[72]  S. Elena,et al.  EVOLUTIONARY DYNAMICS OF FITNESS RECOVERY FROM THE DEBILITATING EFFECTS OF MULLER'S RATCHET , 1998, Evolution; international journal of organic evolution.

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

[74]  J. Drake,et al.  Mutation rates among RNA viruses. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Richard E. Lenski,et al.  EVOLUTIONARY TRADE-OFFS UNDER CONDITIONS OF RESOURCE ABUNDANCE AND SCARCITY: EXPERIMENTS WITH BACTERIA , 1999 .

[76]  S. Elena,et al.  Clonal interference and the evolution of RNA viruses. , 1999, Science.

[77]  D. Botstein,et al.  Systematic changes in gene expression patterns following adaptive evolution in yeast. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[78]  T. Ferenci,et al.  Adaptive mgl-regulatory mutations and genetic diversity evolving in glucose-limited Escherichia coli populations. , 1999, Environmental microbiology.

[79]  E. Domingo,et al.  Drastic Fitness Loss in Human Immunodeficiency Virus Type 1 upon Serial Bottleneck Events , 1999, Journal of Virology.

[80]  E. Domingo,et al.  Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. , 1999, Journal of molecular biology.

[81]  T. Ferenci,et al.  The generation of multiple co-existing mal-regulatory mutations through polygenic evolution in glucose-limited populations of Escherichia coli. , 1999, Environmental microbiology.

[82]  Elena,et al.  Rate of deleterious mutation and the distribution of its effects on fitness in vesicular stomatitis virus , 1999 .

[83]  Scott C. Weaver,et al.  Genetic and Fitness Changes Accompanying Adaptation of an Arbovirus to Vertebrate and Invertebrate Cells , 1999, Journal of Virology.

[84]  J. Bull,et al.  Different trajectories of parallel evolution during viral adaptation. , 1999, Science.

[85]  R. Kolter,et al.  Evolution of microbial diversity during prolonged starvation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[86]  L. Chao,et al.  Evolution by small steps and rugged landscapes in the RNA virus phi6. , 1999, Genetics.

[87]  T. Ferenci,et al.  OmpF changes and the complexity of Escherichia coli adaptation to prolonged lactose limitation. , 1999, FEMS microbiology letters.

[88]  W Arber,et al.  Genomic evolution during a 10,000-generation experiment with bacteria. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[89]  J. Bull,et al.  Evolutionary reversals during viral adaptation to alternating hosts. , 2000, Genetics.

[90]  Carl T. Bergstrom,et al.  Bacteria are different: observations, interpretations, speculations, and opinions about the mechanisms of adaptive evolution in prokaryotes. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Geoffrey B. West,et al.  Scaling in Biology , 2000 .

[92]  S. Elena,et al.  Diminishing Returns of Population Size in the Rate of RNA Virus Adaptation , 2000, Journal of Virology.

[93]  G. Bell,et al.  THE ECOLOGY AND GENETICS OF FITNESS IN CHLAMYDOMONAS. IX. THE RATE OF ACCUMULATION OF VARIATION OF FITNESS UNDER SELECTION , 2000, Evolution; international journal of organic evolution.

[94]  D. Endy,et al.  Computation, prediction, and experimental tests of fitness for bacteriophage T7 mutants with permuted genomes. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[95]  J. Bull,et al.  Big-benefit mutations in a bacteriophage inhibited with heat. , 2000, Molecular biology and evolution.

[96]  L. Cowen,et al.  Evolution of Drug Resistance in Experimental Populations of Candida albicans , 2000, Journal of bacteriology.

[97]  Andres Moya,et al.  EFFECT OF DELETERIOUS MUTATION‐ACCUMULATION ON THE FITNESS OF RNA BACTERIOPHAGE MS2 , 2000, Evolution; international journal of organic evolution.

[98]  L. Chao,et al.  Evolvability of an RNA virus is determined by its mutational neighbourhood , 2000, Nature.

[99]  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.

[100]  S. Elena,et al.  Cost of host radiation in an RNA virus. , 2000, Genetics.

[101]  R. Kolter,et al.  Prolonged Stationary-Phase Incubation Selects forlrp Mutations in Escherichia coliK-12 , 2000, Journal of bacteriology.

[102]  D. Schluter,et al.  The Ecology of Adaptive Radiation , 2000 .

[103]  T. Ferenci,et al.  Experimental analysis of molecular events during mutational periodic selections in bacterial evolution. , 2000, Genetics.

[104]  R. Lenski,et al.  Pervasive compensatory adaptation in Escherichia coli , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[105]  J. Bull,et al.  Experimental evolution recapitulates natural evolution. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[106]  R. Lenski,et al.  The population genetics of ecological specialization in evolving Escherichia coli populations , 2000, Nature.

[107]  R. Lenski,et al.  Long-term experimental evolution in Escherichia coli. IX. Characterization of insertion sequence-mediated mutations and rearrangements. , 2000, Genetics.

[108]  A. Oliver,et al.  High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. , 2000, Science.

[109]  Charles R. Brown,et al.  Ecology and Evolution of Darwin’s Finches , 2001, Heredity.

[110]  M Imhof,et al.  Fitness effects of advantageous mutations in evolving Escherichia coli populations. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[111]  C Zeyl,et al.  MUTATIONAL MELTDOWN IN LABORATORY YEAST POPULATIONS , 2001, Evolution; international journal of organic evolution.

[112]  A F Bennett,et al.  Genetic architecture of thermal adaptation in Escherichia coli. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[113]  Richard E. Lenski,et al.  Mechanisms Causing Rapid and Parallel Losses of Ribose Catabolism in Evolving Populations of Escherichia coli B , 2001, Journal of bacteriology.

[114]  F. Taddei,et al.  Costs and Benefits of High Mutation Rates: Adaptive Evolution of Bacteria in the Mouse Gut , 2001, Science.

[115]  T. Scott,et al.  Differential evolution of eastern equine encephalitis virus populations in response to host cell type. , 2001, Genetics.

[116]  R. Lenski,et al.  Rapid phenotypic change and diversification of a soil bacterium during 1000 generations of experimental evolution. , 2001, Microbiology.

[117]  C. Ofria,et al.  Evolution of digital organisms at high mutation rates leads to survival of the flattest , 2001, Nature.

[118]  R H Borts,et al.  Direct estimate of the mutation rate and the distribution of fitness effects in the yeast Saccharomyces cerevisiae. , 2001, Genetics.

[119]  EVOLUTION OF THE SOLUTION , 2001 .

[120]  C. Zeyl,et al.  Estimates of the rate and distribution of fitness effects of spontaneous mutation in Saccharomyces cerevisiae. , 2001, Genetics.

[121]  David Y. Thomas,et al.  Population genomics of drug resistance in Candida albicans , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[122]  R. Lenski,et al.  Long-term experimental evolution in Escherichia coli. XI. Rejection of non-transitive interactions as cause of declining rate of adaptation , 2002, BMC Evolutionary Biology.

[123]  B. Palsson,et al.  Escherichia coli K-12 undergoes adaptive evolution to achieve in silico predicted optimal growth , 2002, Nature.

[124]  Santiago F. Elena,et al.  Endosymbiotic bacteria: GroEL buffers against deleterious mutations , 2002, Nature.

[125]  Lingchong You,et al.  Dependence of epistasis on environment and mutation severity as revealed by in silico mutagenesis of phage t7. , 2002, Genetics.

[126]  P. Gerrish,et al.  Fitness Effects of Fixed Beneficial Mutations in Microbial Populations , 2002, Current Biology.

[127]  P. Sniegowski,et al.  Fitness evolution and the rise of mutator alleles in experimental Escherichia coli populations. , 2002, Genetics.

[128]  S. Elena,et al.  Molecular basis of adaptive convergence in experimental populations of RNA viruses. , 2002, Genetics.

[129]  David Botstein,et al.  Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[130]  R. H.J.MULLE THE RELATION OF RECOMBINATION TO MUTATIONAL ADVANCE , 2002 .

[131]  V. Cooper Long-term experimental evolution in Escherichia coli. X. Quantifying the fundamental and realized niche , 2002, BMC Evolutionary Biology.

[132]  T. Ferenci,et al.  Enrichment and elimination of mutY mutators in Escherichia coli populations. , 2002, Genetics.

[133]  Robert T. Pennock,et al.  The evolutionary origin of complex features , 2003, Nature.

[134]  Anthony D Long,et al.  Evolutionary changes in heat-inducible gene expression in lines of Escherichia coli adapted to high temperature. , 2003, Physiological genomics.

[135]  R. Lenski,et al.  Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[136]  O. Berg,et al.  Regulating general mutation rates: examination of the hypermutable state model for Cairnsian adaptive mutation. , 2003, Genetics.

[137]  Richard E. Lenski,et al.  Rates of DNA Sequence Evolution in Experimental Populations of Escherichia coli During 20,000 Generations , 2003, Journal of Molecular Evolution.

[138]  R. Lenski,et al.  The fate of competing beneficial mutations in an asexual population , 2004, Genetica.

[139]  J. Adams,et al.  The population biology and evolutionary significance of Ty elements in Saccharomyces cerevisiae , 2004, Genetica.

[140]  Explore Configuring,et al.  A Simulation Study to , 2004 .