The genetic basis of parallel and divergent phenotypic responses in evolving populations of Escherichia coli

Pleiotropy plays a central role in theories of adaptation, but little is known about the distribution of pleiotropic effects associated with different adaptive mutations. Previously, we described the phenotypic effects of a collection of independently arising beneficial mutations in Escherichia coli. We quantified their fitness effects in the glucose environment in which they evolved and their pleiotropic effects in five novel resource environments. Here we use a candidate gene approach to associate the phenotypic effects of the mutations with the underlying genetic changes. Among our collection of 27 adaptive mutants, we identified a total of 21 mutations (18 of which were unique) encompassing five different loci or gene regions. There was limited resolution to distinguish among loci based on their fitness effects in the glucose environment, demonstrating widespread parallelism in the direct response to selection. However, substantial heterogeneity in mutant effects was revealed when we examined their pleiotropic effects on fitness in the five novel environments. Substitutions in the same locus clustered together phenotypically, indicating concordance between molecular and phenotypic measures of divergence.

[1]  Roy Kishony,et al.  Analysis of genetic systems using experimental evolution and whole-genome sequencing , 2007, Genome Biology.

[2]  D. J. Kiviet,et al.  Empirical fitness landscapes reveal accessible evolutionary paths , 2007, Nature.

[3]  C. Ofria,et al.  Ecological Specialization and Adaptive Decay in Digital Organisms , 2006, The American Naturalist.

[4]  Anu Raghunathan,et al.  Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale , 2006, Nature Genetics.

[5]  Paul B Rainey,et al.  Unraveling adaptive evolution: how a single point mutation affects the protein coregulation network , 2006, Nature Genetics.

[6]  P. Insel,et al.  A Single Amino Acid Mutation Contributes to Adaptive Beach Mouse Color Pattern , 2006, Science.

[7]  Dominique Schneider,et al.  Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Nigel F. Delaney,et al.  Darwinian Evolution Can Follow Only Very Few Mutational Paths to Fitter Proteins , 2006, Science.

[9]  E. Ostrowski,et al.  PLEIOTROPIC EFFECTS OF BENEFICIAL MUTATIONS IN ESCHERICHIA COLI , 2005, Evolution; international journal of organic evolution.

[10]  D. Kwiatkowski.  How malaria has affected the human genome and what human genetics can teach us about malaria. , 2005, American journal of human genetics.

[11]  J. Roth,et al.  Regulation of NAD Synthesis by the Trifunctional NadR Protein of Salmonella enterica , 2005, Journal of bacteriology.

[12]  Jeremy Schmutz,et al.  Widespread Parallel Evolution in Sticklebacks by Repeated Fixation of Ectodysplasin Alleles , 2005, Science.

[13]  Patrick C. Phillips,et al.  Testing hypotheses regarding the genetics of adaptation , 2005, Genetica.

[14]  M. Nachman.  The genetic basis of adaptation: lessons from concealing coloration in pocket mice , 2005, Genetica.

[15]  Loren H. Rieseberg,et al.  Parallel genotypic adaptation: when evolution repeats itself , 2005, Genetica.

[16]  H. A. Orr,et al.  THE PROBABILITY OF PARALLEL EVOLUTION , 2005, Evolution; international journal of organic evolution.

[17]  G. Bell,et al.  The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Dolph Schluter,et al.  Parallel Evolution and Inheritance of Quantitative Traits , 2004, The American Naturalist.

[19]  T. Hart,et al.  Conserved Genetic Basis of a Quantitative Plumage Trait Involved in Mate Choice , 2004, Science.

[20]  D. Schemske,et al.  Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers , 2003, Nature.

[21]  G. Bell,et al.  Divergent evolution during an experimental adaptive radiation , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[23]  M. Nachman,et al.  The genetic basis of adaptive melanism in pocket mice , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  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.

[25]  A. Osterman,et al.  Ribosylnicotinamide Kinase Domain of NadR Protein: Identification and Implications in NAD Biosynthesis , 2002, Journal of bacteriology.

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

[27]  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.

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

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

[30]  Nadia Raffaelli,et al.  The Escherichia coli NadR Regulator Is Endowed with Nicotinamide Mononucleotide Adenylyltransferase Activity , 1999, Journal of bacteriology.

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

[32]  A. F. Bennett,et al.  EVOLUTIONARY ADAPTATION TO TEMPERATURE. VII. EXTENSION OF THE UPPER THERMAL LIMIT OF ESCHERICHIA COLI , 1999, Evolution; international journal of organic evolution.

[33]  Corbin D. Jones,et al.  The genetic basis of Drosophila sechellia's resistance to a host plant toxin. , 1998, Genetics.

[34]  D. Schemske,et al.  Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). , 1998, Genetics.

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

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

[37]  M. Cashel,et al.  Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation , 1996, Molecular microbiology.

[38]  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.

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

[40]  Jessica Gurevitch,et al.  Design and Analysis of Ecological Experiments , 1993 .

[41]  K. R. Clarke,et al.  Non‐parametric multivariate analyses of changes in community structure , 1993 .

[42]  H. A. Orr,et al.  The Genetics of Adaptation: A Reassessment , 1992, The American Naturalist.

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

[44]  G. S. Mani,et al.  Mutational order: a major stochastic process in evolution , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[45]  S. Wright.  Evolution and the Genetics of Populations, Volume 3: Experimental Results and Evolutionary Deductions , 1977 .

[46]  T. Dobzhansky,et al.  Evolution and the Genetics of Populations, Vol. 1, Genetic and Biometric Foundations , 1969 .

[47]  R. Lenski,et al.  Microbial genetics: Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation , 2003, Nature Reviews Genetics.

[48]  J. Hodgkin,et al.  Seven types of pleiotropy. , 1998, The International journal of developmental biology.

[49]  R F Doolittle,et al.  Convergent evolution: the need to be explicit. , 1994, Trends in biochemical sciences.

[50]  S. Tanksley.  Mapping polygenes. , 1993, Annual review of genetics.

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