The outcomes of evolution are determined by a stochastic dynamical process that governs how mutations arise and spread through a population. However, it is difficult to observe these dynamics directly over long periods and across entire genomes. Here we analyse the dynamics of molecular evolution in twelve experimental populations of Escherichia coli, using whole-genome metagenomic sequencing at five hundred-generation intervals through sixty thousand generations. Although the rate of fitness gain declines over time, molecular evolution is characterized by signatures of rapid adaptation throughout the duration of the experiment, with multiple beneficial variants simultaneously competing for dominance in each population. Interactions between ecological and evolutionary processes play an important role, as long-term quasi-stable coexistence arises spontaneously in most populations, and evolution continues within each clade. We also present evidence that the targets of natural selection change over time, as epistasis and historical contingency alter the strength of selection on different genes. Together, these results show that long-term adaptation to a constant environment can be a more complex and dynamic process than is often assumed.
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We thank N. Hajela, A. N. Nguyen Ba, and E. Jerison for assistance. B.H.G. acknowledges support from the US National Science Foundation (DEB-1501580) and the Miller Institute for Basic Research in Science at the University of California Berkeley. R.E.L. acknowledges support from the US National Science Foundation (DEB-1451740) and BEACON Center for the Study of Evolution in Action (DBI-0939454). M.M.D. acknowledges support from the Simons Foundation (grant 376196), the US National Science Foundation (PHY-1313638), and the US National Institutes of Health (GM104239). Computational work was performed on the Odyssey cluster supported by the Research Computing Group at Harvard University.
Extended data figures
This file contains a comma-separated list of metagenomic samples used in this study.
This file contains a comma-separated list of clonal isolates used in this study.
This file contains a comma-separated list of genes showing significant parallelism in the nonmutator populations.
This file contains a comma-separated list of operons showing significant parallelism in the nonmutator populations.