Fitness Evolution and the Rise of Mutator Alleles in Experimental Escherichia coli Populations

Corresponding author: Paul D. Sniegowski, 415 S. University Ave., University of Pennsylvania, Philadelphia, PA 19104., paulsnie{at}sas.upenn.edu (E-mail)

Communicating editor: P. D. KEIGHTLEY

We studied the evolution of high mutation rates and the evolution of fitness in three experimental populations of Escherichia coli adapting to a glucose-limited environment. We identified the mutations responsible for the high mutation rates and show that their rate of substitution in all three populations was too rapid to be accounted for simply by genetic drift. In two of the populations, large gains in fitness relative to the ancestor occurred as the mutator alleles rose to fixation, strongly supporting the conclusion that mutator alleles fixed by hitchhiking with beneficial mutations at other loci. In one population, no significant gain in fitness relative to the ancestor occurred in the population as a whole while the mutator allele rose to fixation, but a substantial and significant gain in fitness occurred in the mutator subpopulation as the mutator neared fixation. The spread of the mutator allele from rarity to fixation took >1000 generations in each population. We show that simultaneous adaptive gains in both the mutator and wild-type subpopulations (clonal interference) retarded the mutator fixation in at least one of the populations. We found little evidence that the evolution of high mutation rates accelerated adaptation in these populations.

This article has been cited by other articles:

				J. J. Bull and C. O. Wilke Lethal Mutagenesis of Bacteria Genetics, October 1, 2008; 180(2): 1061 - 1070. [Abstract] [Full Text] [PDF]

				Q. Hua, A. R. Joyce, B. O. Palsson, and S. S. Fong Metabolic Characterization of Escherichia coli Strains Adapted to Growth on Lactate Appl. Envir. Microbiol., July 15, 2007; 73(14): 4639 - 4647. [Abstract] [Full Text] [PDF]

				P. J. Gerrish, A. Colato, A. S. Perelson, and P. D. Sniegowski Complete genetic linkage can subvert natural selection PNAS, April 10, 2007; 104(15): 6266 - 6271. [Abstract] [Full Text] [PDF]

				S. Huang, J. Kang, and M. J. Blaser Antimutator Role of the DNA Glycosylase mutY Gene in Helicobacter pylori. J. Bacteriol., September 1, 2006; 188(17): 6224 - 6234. [Abstract] [Full Text] [PDF]

				L. M. C. Hall and S. K. Henderson-Begg Hypermutable bacteria isolated from humans - a critical analysis. Microbiology, September 1, 2006; 152(Pt 9): 2505 - 2514. [Abstract] [Full Text] [PDF]

				L. Pelosi, L. Kuhn, D. Guetta, J. Garin, J. Geiselmann, R. E. Lenski, and D. Schneider Parallel Changes in Global Protein Profiles During Long-Term Experimental Evolution in Escherichia coli Genetics, August 1, 2006; 173(4): 1851 - 1869. [Abstract] [Full Text] [PDF]

				J. Fletcher, C. Bender, B. Budowle, W. T. Cobb, S. E. Gold, C. A. Ishimaru, D. Luster, U. Melcher, R. Murch, H. Scherm, et al. Plant Pathogen Forensics: Capabilities, Needs, and Recommendations Microbiol. Mol. Biol. Rev., June 1, 2006; 70(2): 450 - 471. [Abstract] [Full Text] [PDF]

				J. A. G. M. de Visser and D. E. Rozen Clonal Interference and the Periodic Selection of New Beneficial Mutations in Escherichia coli Genetics, April 1, 2006; 172(4): 2093 - 2100. [Abstract] [Full Text] [PDF]

				J.-B. Andre and B. Godelle The Evolution of Mutation Rate in Finite Asexual Populations Genetics, January 1, 2006; 172(1): 611 - 626. [Abstract] [Full Text] [PDF]

				S. S. Fong, A. R. Joyce, and B. O. Palsson Parallel adaptive evolution cultures of Escherichia coli lead to convergent growth phenotypes with different gene expression states Genome Res., October 1, 2005; 15(10): 1365 - 1372. [Abstract] [Full Text] [PDF]

				M.-R. Baquero, A. I. Nilsson, M. del Carmen Turrientes, D. Sandvang, J. C. Galan, J. L. Martinez, N. Frimodt-Moller, F. Baquero, and D. I. Andersson Polymorphic Mutation Frequencies in Escherichia coli: Emergence of Weak Mutators in Clinical Isolates J. Bacteriol., August 15, 2004; 186(16): 5538 - 5542. [Abstract] [Full Text] [PDF]

				A. C. Shaver and P. D. Sniegowski Spontaneously Arising mutL Mutators in Evolving Escherichia coli Populations Are the Result of Changes in Repeat Length J. Bacteriol., October 15, 2003; 185(20): 6076 - 6082. [Abstract] [Full Text] [PDF]

				B. Li, H.-C. T. Tsui, J. E. LeClerc, M. Dey, M. E. Winkler, and T. A. Cebula Molecular analysis of mutS expression and mutation in natural isolates of pathogenic Escherichia coli Microbiology, May 1, 2003; 149(5): 1323 - 1331. [Abstract] [Full Text] [PDF]