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Proc Biol Sci. 2000 March 7; 267(1442): 515–522.
PMCID: PMC1690552

Pervasive compensatory adaptation in Escherichia coli.

Abstract

To investigate compensatory adaptation (CA), we used genotypes of Escherichia coli which were identical except for one or two deleterious mutations. We compared CA for (i) deleterious mutations with large versus small effects, (ii) genotypes carrying one versus two mutations, and (iii) pairs of deleterious mutations which interact in a multiplicative versus synergistic fashion. In all, we studied 14 different genotypes, plus a control strain which was not mutated. Most genotypes showed CA during 200 generations of experimental evolution, where we define CA as a fitness increase which is disproportionately large relative to that in evolving control lines, coupled with retention of the original deleterious mutation(s). We observed greater CA for mutations of large effect than for those of small effect, which can be explained by the greater benefit to recovery in severely handicapped genotypes given the dynamics of selection. The rates of CA were similar for double and single mutants whose initial fitnesses were approximately equal. CA was faster for synergistic than for multiplicative pairs, presumably because the marginal gain which results from CA for one of the component mutations is greater in that case. The most surprising result in our view, is that compensation should be so readily achieved in an organism which is haploid and has little genetic redundancy This finding suggests a degree of versatility in the E. coil genome which demands further study from both genetic and physiological perspectives.

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Selected References

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  • Björkman J, Hughes D, Andersson DI. Virulence of antibiotic-resistant Salmonella typhimurium. Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3949–3953. [PubMed]
  • Bouma JE, Lenski RE. Evolution of a bacteria/plasmid association. Nature. 1988 Sep 22;335(6188):351–352. [PubMed]
  • Burch CL, Chao L. Evolution by small steps and rugged landscapes in the RNA virus phi6. Genetics. 1999 Mar;151(3):921–927. [PubMed]
  • Elena SF, Lenski RE. Test of synergistic interactions among deleterious mutations in bacteria. Nature. 1997 Nov 27;390(6658):395–398. [PubMed]
  • Elena SF, Ekunwe L, Hajela N, Oden SA, Lenski RE. Distribution of fitness effects caused by random insertion mutations in Escherichia coli. Genetica. 1998;102-103(1-6):349–358. [PubMed]
  • Gerrish PJ, Lenski RE. The fate of competing beneficial mutations in an asexual population. Genetica. 1998;102-103(1-6):127–144. [PubMed]
  • Gould SJ, Lewontin RC. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci. 1979 Sep 21;205(1161):581–598. [PubMed]
  • Kimura M. Some models of neutral evolution, compensatory evolution, and the shifting balance process. Theor Popul Biol. 1990 Feb;37(1):150–158. [PubMed]
  • Kirby DA, Muse SV, Stephan W. Maintenance of pre-mRNA secondary structure by epistatic selection. Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9047–9051. [PubMed]
  • Kleckner N, Bender J, Gottesman S. Uses of transposons with emphasis on Tn10. Methods Enzymol. 1991;204:139–180. [PubMed]
  • Kondrashov AS. Deleterious mutations and the evolution of sexual reproduction. Nature. 1988 Dec 1;336(6198):435–440. [PubMed]
  • Labedan B, Riley M. Gene products of Escherichia coli: sequence comparisons and common ancestries. Mol Biol Evol. 1995 Nov;12(6):980–987. [PubMed]
  • Lande R. Risk of population extinction from fixation of deleterious and reverse mutations. Genetica. 1998;102-103(1-6):21–27. [PubMed]
  • Lenski RE. Bacterial evolution and the cost of antibiotic resistance. Int Microbiol. 1998 Dec;1(4):265–270. [PubMed]
  • Lenski RE, Travisano M. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6808–6814. [PubMed]
  • Lenski RE, Simpson SC, Nguyen TT. Genetic analysis of a plasmid-encoded, host genotype-specific enhancement of bacterial fitness. J Bacteriol. 1994 Jun;176(11):3140–3147. [PMC free article] [PubMed]
  • Schrag SJ, Perrot V. Reducing antibiotic resistance. Nature. 1996 May 9;381(6578):120–121. [PubMed]
  • Schrag SJ, Perrot V, Levin BR. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc Biol Sci. 1997 Sep 22;264(1386):1287–1291. [PMC free article] [PubMed]
  • Stephan W. The rate of compensatory evolution. Genetics. 1996 Sep;144(1):419–426. [PubMed]
  • Travisano M, Mongold JA, Bennett AF, Lenski RE. Experimental tests of the roles of adaptation, chance, and history in evolution. Science. 1995 Jan 6;267(5194):87–90. [PubMed]
  • Whitlock MC, Otto SP. The panda and the phage: compensatory mutations and the persistence of small populations. Trends Ecol Evol. 1999 Aug;14(8):295–296. [PubMed]

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