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      Genome dynamics during experimental evolution

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      Nature Reviews Genetics
      Springer Science and Business Media LLC

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          Abstract

          Evolutionary changes in organismal traits may occur either gradually or suddenly. However, until recently, there has been little direct information about how phenotypic changes are related to the rate and the nature of the underlying genotypic changes. Technological advances that facilitate whole-genome and whole-population sequencing, coupled with experiments that 'watch' evolution in action, have brought new precision to and insights into studies of mutation rates and genome evolution. In this Review, we discuss the evolutionary forces and ecological processes that govern genome dynamics in various laboratory systems in the context of relevant population genetic theory, and we relate these findings to evolution in natural populations.

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          Most cited references82

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          The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana.

          To take complete advantage of information on within-species polymorphism and divergence from close relatives, one needs to know the rate and the molecular spectrum of spontaneous mutations. To this end, we have searched for de novo spontaneous mutations in the complete nuclear genomes of five Arabidopsis thaliana mutation accumulation lines that had been maintained by single-seed descent for 30 generations. We identified and validated 99 base substitutions and 17 small and large insertions and deletions. Our results imply a spontaneous mutation rate of 7 x 10(-9) base substitutions per site per generation, the majority of which are G:C-->A:T transitions. We explain this very biased spectrum of base substitution mutations as a result of two main processes: deamination of methylated cytosines and ultraviolet light-induced mutagenesis.
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            The molecular diversity of adaptive convergence.

            To estimate the number and diversity of beneficial mutations, we experimentally evolved 115 populations of Escherichia coli to 42.2°C for 2000 generations and sequenced one genome from each population. We identified 1331 total mutations, affecting more than 600 different sites. Few mutations were shared among replicates, but a strong pattern of convergence emerged at the level of genes, operons, and functional complexes. Our experiment uncovered a set of primary functional targets of high temperature, but we estimate that many other beneficial mutations could contribute to similar adaptive outcomes. We inferred the pervasive presence of epistasis among beneficial mutations, which shaped adaptive trajectories into at least two distinct pathways involving mutations either in the RNA polymerase complex or the termination factor rho.
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              Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli.

              The role of historical contingency in evolution has been much debated, but rarely tested. Twelve initially identical populations of Escherichia coli were founded in 1988 to investigate this issue. They have since evolved in a glucose-limited medium that also contains citrate, which E. coli cannot use as a carbon source under oxic conditions. No population evolved the capacity to exploit citrate for >30,000 generations, although each population tested billions of mutations. A citrate-using (Cit+) variant finally evolved in one population by 31,500 generations, causing an increase in population size and diversity. The long-delayed and unique evolution of this function might indicate the involvement of some extremely rare mutation. Alternately, it may involve an ordinary mutation, but one whose physical occurrence or phenotypic expression is contingent on prior mutations in that population. We tested these hypotheses in experiments that "replayed" evolution from different points in that population's history. We observed no Cit+ mutants among 8.4 x 10(12) ancestral cells, nor among 9 x 10(12) cells from 60 clones sampled in the first 15,000 generations. However, we observed a significantly greater tendency for later clones to evolve Cit+, indicating that some potentiating mutation arose by 20,000 generations. This potentiating change increased the mutation rate to Cit+ but did not cause generalized hypermutability. Thus, the evolution of this phenotype was contingent on the particular history of that population. More generally, we suggest that historical contingency is especially important when it facilitates the evolution of key innovations that are not easily evolved by gradual, cumulative selection.
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                Author and article information

                Journal
                Nature Reviews Genetics
                Nat Rev Genet
                Springer Science and Business Media LLC
                1471-0056
                1471-0064
                December 2013
                October 29 2013
                December 2013
                : 14
                : 12
                : 827-839
                Article
                10.1038/nrg3564
                4239992
                24166031
                a53b9a33-77c3-47f2-ab8f-91c1f4c171fb
                © 2013

                http://www.springer.com/tdm

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