Tests of parallel molecular evolution in a long-term experiment with Escherichia coli

doi:10.1073/pnas.0602917103

Tests of parallel molecular evolution in a long-term experiment with Escherichia coli

Departments of *Zoology and
^¶Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824;
^†Laboratoire Adaptation et Pathogénie des Microorganismes, Université Joseph Fourier, Institut Jean Roget, F-38041 Grenoble, France;
^‡Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520; and
^§Department of Biology, University of Massachusetts, Amherst, MA 01003

Communicated by John R. Roth, University of California, Davis, CA, April 10, 2006 (received for review January 22, 2006)

Abstract

The repeatability of evolutionary change is difficult to quantify because only a single outcome can usually be observed for any precise set of circumstances. In this study, however, we have quantified the frequency of parallel and divergent genetic changes in 12 initially identical populations of Escherichia coli that evolved in identical environments for 20,000 cell generations. Unlike previous analyses in which candidate genes were identified based on parallel phenotypic changes, here we sequenced four loci (pykF, nadR, pbpA-rodA, and hokB/sokB) in which mutations of unknown effect had been discovered in one population, and then we compared the substitution pattern in these “blind” candidate genes with the pattern found in 36 randomly chosen genes. Two candidate genes, pykF and nadR, had substitutions in all 11 other populations, and the other 2 in several populations. There were very few cases, however, in which the exact same mutations were substituted, in contrast to the findings from conceptually related work performed with evolving virus populations. No random genes had any substitutions except in four populations that evolved defects in DNA repair. Tests of four different statistical aspects of the pattern of molecular evolution all indicate that adaptation by natural selection drove the parallel changes in these candidate genes.

Footnotes

^‖To whom correspondence should be addressed. E-mail: lenski{at}msu.edu
Author contributions: R.W., D.S., M.A.R., and R.E.L. designed research; R.W., D.S., and C.L.W. performed research; R.W. and R.E.L. analyzed data; and R.W., D.S., and R.E.L. wrote the paper.
Conflict of interest statement: No conflicts declared.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AY849930–AY849933 and AY625099–AY625134).