Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in
            <i>Escherichia coli</i>

Plucain, Jessica; Hindré, Thomas; Gac, Mickaël Le; Tenaillon, Olivier; Cruveiller, Stéphane; Médigue, Claudine; Leiby, Nicholas; Harcombe, William R.; Marx, Christopher J.; Lenski, Richard E.; Schneider, Dominique

doi:10.1126/science.1248688

Cited by 128 publications

(147 citation statements)

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“…Instead, long-term coexistence is likely maintained by negative frequency-dependent selection, as has been demonstrated in Ara–2 27,28 . It is not known whether these additional examples of coexistence revealed by our data involve the same glucose/acetate cross-feeding interaction seen in Ara–2, or whether these populations have exploited other opportunities for ecological diversification.…”

Section: Emergence Of Quasi-stable Coexistencementioning

confidence: 90%

“…Instead, their relative abundance can shift by at least ~10-fold during their coexistence. The timing and magnitudes of these shifts vary from population to population; they could reflect ongoing selection on the mechanism of coexistence or a general coupling between the ecologically divergent phenotypes and ordinary fitness gains 28–30 . Further work is needed to distinguish between these scenarios.…”

Section: Emergence Of Quasi-stable Coexistencementioning

confidence: 99%

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The dynamics of molecular evolution over 60,000 generations

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McDonald

Barrick

et al. 2017

Nature

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The outcomes of evolution are determined by a stochastic dynamical process that governs how mutations arise and spread through a population. Here, we analyze the dynamics of molecular evolution in twelve experimental populations of Escherichia coli, using whole-genome metagenomic sequencing at 500-generation intervals through 60,000 generations. Despite a declining rate of fitness gain, molecular evolution continues to be characterized by signatures of rapid adaptation, 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 new 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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Section: Emergence Of Quasi-stable Coexistencementioning

confidence: 90%

Section: Emergence Of Quasi-stable Coexistencementioning

confidence: 99%

The dynamics of molecular evolution over 60,000 generations

Good

McDonald

Barrick

et al. 2017

Nature

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631

839

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“…Some other populations-such as Ara-4, which became hypermutable, and Ara+2, which did not-are more linear in structure, without deep branches among the sequenced clones. The deepest branches were likely supported by the diversity--promoting effects of negative frequency--dependent interactions, as demonstrated in the Ara-2 population (18,19).…”

Section: Genome--wide Mutations and Hypermutabilitymentioning

confidence: 99%

“…The LTEE is a model system for studying fundamental evolutionary questions (10)(11)(12)(13)(14)(15)(16)(17)(18)(19).…”

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confidence: 99%

Tempo and mode of genome evolution in a 50,000-generation experiment

Tenaillon

Barrick

Ribeck

et al. 2016

Preprint

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*These authors contributed equally to this work.Adaptation depends on the rates, effects, and interactions of many mutations. We analyzed 264 genomes from 12 Escherichia coli populations to characterize their dynamics over 50,000 generations. The trajectories for genome evolution in populations that retained the ancestral mutation rate fit a model where most fixed mutations are beneficial, the fraction of beneficial mutations declines as fitness rises, and neutral mutations accumulate at a constant rate. We also compared these populations to lines evolved under a mutation--accumulation regime that minimizes selection. Nonsynonymous mutations, intergenic mutations, insertions, and deletions are overrepresented in the long--term populations, supporting the inference that most fixed mutations are favored by selection. These results illuminate the shifting balance of forces that govern genome evolution in populations adapting to a new environment.All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

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“…In particular, there are no predators, parasites, or other competing species in the LTEE environment; there is no sexual recombination or horizontal gene transfer; the physical environment is well mixed and lacks spatial structure; and the density-limiting resource, glucose, is provided at a low concentration, which limits the concentration of metabolic byproducts that could support cross-feeding specialists. Nonetheless, frequency-dependent interactions have emerged in at least two LTEE populations (Elena and Lenski 1997;Rozen and Lenski 2000;Blount et al 2008;Rozen et al 2009;Le Gac et al 2012;Plucain et al 2014;Ribeck and Lenski 2015), and it is possible that such interactions have evolved in some or all of the other populations as well.In previous work, we sequenced individual clones and population samples taken at generations 2000, 5000, 10,000, 15,000, 20,000, 30,000, and 40,000 from one LTEE population, designated Ara21, that has served as the focal population for many in-depth analyses (Barrick and Lenski 2009;). Using these genomic data, we designed genotyping assays for many derived alleles present in one or more clones or population samples.…”

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confidence: 99%

Adaptation, Clonal Interference, and Frequency-Dependent Interactions in a Long-Term Evolution Experiment withEscherichia coli

2015

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Twelve replicate populations of Escherichia coli have been evolving in the laboratory for .25 years and 60,000 generations. We analyzed bacteria from whole-population samples frozen every 500 generations through 20,000 generations for one wellstudied population, called Ara21. By tracking 42 known mutations in these samples, we reconstructed the history of this population's genotypic evolution over this period. The evolutionary dynamics of Ara21 show strong evidence of selective sweeps as well as clonal interference between competing lineages bearing different beneficial mutations. In some cases, sets of several mutations approached fixation simultaneously, often conveying no information about their order of origination; we present several possible explanations for the existence of these mutational cohorts. Against a backdrop of rapid selective sweeps both earlier and later, two genetically diverged clades coexisted for .6000 generations before one went extinct. In that time, many additional mutations arose in the clade that eventually prevailed. We show that the clades evolved a frequency-dependent interaction, which prevented the immediate competitive exclusion of either clade, but which collapsed as beneficial mutations accumulated in the clade that prevailed. Clonal interference and frequency dependence can occur even in the simplest microbial populations. Furthermore, frequency dependence may generate dynamics that extend the period of coexistence that would otherwise be sustained by clonal interference alone.KEYWORDS experimental evolution; clonal interference; frequency-dependent selection; beneficial mutations; asexual populations; mutational cohorts T HE long-term evolution experiment (LTEE) spans .25 years and 60,000 generations of bacterial evolution. In this experiment, 12 replicate populations of Escherichia coli have been propagated in a simple environment, and samples of each population have been frozen at 500-generation intervals. This experiment originally focused on whether and to what extent the populations would diverge in their mean fitness and other phenotypic properties as they adapted to identical environments (Lenski et al. 1991;Lenski and Travisano 1994). Over time, this experiment has become a model for exploring many other aspects of evolution, including the emergence of new functions (Blount et al. 2008), the evolution of mutation rates (Sniegowski et al. 1997), the maintenance of genetic diversity (Elena and Lenski 1997;Rozen and Lenski 2000;Le Gac et al. 2012), and the structure of the fitness landscape (Khan et al. 2011;Woods et al. 2011;Wiser et al. 2013). The ability to examine these and other issues has grown tremendously as data that were difficult or impossible to obtain when the LTEE began have yielded to new technologies, particularly genome sequencing Lenski 2009, 2013;Blount et al. 2012;Wielgoss et al. 2013).The LTEE has also inspired theoretical work, especially on the dynamics of adaptation in large asexual populations (Gerrish and Lenski 1998;Hegreness et al....

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Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in Escherichia coli

Cited by 128 publications

References 31 publications

The dynamics of molecular evolution over 60,000 generations

The dynamics of molecular evolution over 60,000 generations

Tempo and mode of genome evolution in a 50,000-generation experiment

Adaptation, Clonal Interference, and Frequency-Dependent Interactions in a Long-Term Evolution Experiment withEscherichia coli

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