Biology subjects

Richard E. Lenski

Publications and source records attributed to Richard E. Lenski.

8 recordsLinked to original sources

bioRxiv2016

Competition between continuously evolving lineages in asexual populations

In an asexual population, the fate of a beneficial mutation depends on how its lineage competes against other mutant lineages in the population. With high beneficial mutation rates or large population sizes, competition between contending mutations is strong, and successful lineages can accumulate multiple mutations before any single one achieves fixation. Most current theory about asexual population dynamics either neglects this multiple-mutations regime or introduces simplifying assumptions that may not apply. Here, we develop a theoretical framework that describes the dynamics of adaptation and substitution over all mutation-rate regimes by conceptualizing the population as a collection of continuously adapting lineages. This model of \"lineage interference\" shows that each new mutants advantage over the rest of the population must be above a critical threshold in order to likely achieve fixation, and we derive a simple expression for that threshold. We apply this framework to examine the role of beneficial mutations with different effect sizes across the transition to the multiple-mutations regime.

Evolutionary Biology↗

bioRxiv2016

Core Genes Evolve Rapidly in the Long-term Evolution Experiment with Escherichia coli

Bacteria can evolve rapidly under positive selection owing to their vast numbers, allowing their genes to diversify by adapting to different environments. We asked whether the same genes that are fast evolving in the long-term evolution experiment with Escherichia coli (LTEE) have also diversified extensively in nature. We identified ~2000 core genes shared among 60 E. coli strains. During the LTEE, core genes accumulated significantly more nonsynonymous mutations than flexible (i.e., noncore) genes. Furthermore, core genes under positive selection in the LTEE are more conserved in nature than the average core gene. In some cases, adaptive mutations appear to fine-tune protein functions, rather than merely knocking them out. The LTEE conditions are novel for E. coli, at least in relation to the long sweep of its evolution in nature. The constancy and simplicity of the environment likely favor the complete loss of some unused functions and the fine-tuning of others.\n\nCompeting Interests StatementWe, the authors, declare that we have no conflicts of interest.

Evolutionary Biology↗

bioRxiv2016

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

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 50,0 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.

Evolutionary Biology↗

bioRxiv2015

Replaying Evolution to Test the Cause of Extinction of One Ecotype in an Experimentally Evolved Population

In a long-term evolution experiment with Escherichia coli, bacteria in one of twelve populations evolved the ability to consume citrate, a previously unexploited resource in a glucose-limited medium. This innovation led to the frequency-dependent coexistence of citrate-consuming (Cit+) and non-consuming (Cit-) ecotypes, with Cit- bacteria persisting on the exogenously supplied glucose as well as other carbon molecules released by the Cit+ bacteria. After more than 10,000 generations of coexistence, however, the Cit- lineage went extinct; cells with the Cit- phenotype dropped to levels below detection, and the Cit- clade could not be detected by molecular assays based on its unique genotype. We hypothesized that this extinction event was a deterministic outcome of evolutionary change within the population, specifically the appearance of a more-fit Cit+ ecotype that competitively excluded the Cit- ecotype. We tested this hypothesis by re-evolving the population from one frozen sample taken just prior to the extinction and from another sample taken several thousand generations earlier, in each case for 500 generations and with 20-fold replication. To our surprise, the Cit- type did not go extinct in any of these replays, and Cit- cells also persisted in a single replicate that was propagated for 3,000 generations. Even more unexpectedly, we showed that the Cit- ecotype could reinvade the Cit+ population after its extinction. Taken together, these results indicate that the extinction of the Cit- ecotype was not a deterministic outcome driven by competitive exclusion by the Cit+ ecotype. The extinction also cannot be explained by demographic stochasticity, as the population size of the Cit- ecotype should have been many thousands of cells even during the daily transfer events. Instead, we infer that the extinction must have been caused by a rare chance event in which some aspect of the experimental conditions was inadvertently perturbed.

Evolutionary Biology↗

bioRxiv2015

Evolution of organismal stoichiometry in a 50,000-generation experiment with Escherichia coli

Organismal stoichiometry refers to the relative proportion of chemical elements in the biomass of organisms, and it can have important effects on ecological interactions from population to ecosystem scales. Although stoichiometry has been studied extensively from an ecological perspective, little is known about rates and directions of evolutionary changes in elemental composition in response to nutrient limitation. We measured carbon, nitrogen, and phosphorus content of Escherichia coli evolved under controlled carbon-limited conditions for 50,000 generations. The bacteria evolved higher relative nitrogen and phosphorus content, consistent with selection for increased use of the more abundant elements. Total carbon assimilated also increased, indicating more efficient use of the limiting element. Altogether, our study shows that stoichiometry evolved over a relatively short time-period, and that it did so in a predictable direction given the carbon-limiting environment.

Evolutionary Biology↗

bioRxiv2015

Evolution and coexistence in response to a key innovation in a long-term evolution experiment with Escherichia coli

Evolution of a novel function can greatly alter the effects of an organism on its environment. These environmental changes can, in turn, affect the further evolution of that organism and any coexisting organisms. We examine these effects and feedbacks following evolution of a novel function in the long-term evolution experiment (LTEE) with Escherichia coli. A characteristic feature of E. coli is its inability to consume citrate aerobically. However, that ability evolved in one of the LTEE populations. In this population, citrate-utilizing bacteria (Cit+) coexisted stably with another clade of bacteria that lacked the capacity to utilize citrate (Cit-). This coexistence was shaped by the evolution of a cross-feeding relationship in which Cit+ cells released the dicarboxylic acids succinate, fumarate, and malate into the medium, and Cit- cells evolved improved growth on these carbon sources, as did the Cit+ cells. Thus, the evolution of citrate consumption led to a flask-based ecosystem that went from a single limiting resource, glucose, to one with five resources either shared or partitioned between two coexisting clades. Our findings show how evolutionary novelties can change environmental conditions, thereby facilitating diversity and altering both the structure of an ecosystem and the evolutionary trajectories of coexisting organisms.\n\nEvolution does not produce novelties from scratch. It works on what already exists, either transforming a system to give it new functions or combining several systems to produce a more elaborate one.\n\n-Francois Jacob

Evolutionary Biology↗

bioRxiv2015

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

Twelve replicate populations of Escherichia coli have been evolving in the laboratory for more than 25 years and 60,000 generations. We analyzed bacteria from whole-population samples frozen every 500 generations through 20,000 generations for one well-studied population, called Ara-1. By tracking 42 known mutations in these samples, we reconstructed the history of this populations genotypic evolution over this period. The evolutionary dynamics of Ara-1 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, we found that two clades coexisted for over 6000 generations before one drove the other extinct. In that time, at least nine mutations arose in the clade that prevailed. We found evidence that the clades evolved a frequency-dependent interaction, which prevented the competitive exclusion of either clade, but which eventually 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.

Evolutionary Biology↗

bioRxiv2014

Modeling and quantifying frequency-dependent fitness in microbial populations with cross-feeding interactions

Coexistence of multiple populations by frequency-dependent selection is common in nature, and it often arises even in well-mixed experiments with microbes. If ecology is to be incorporated into models of population genetics, then it is important to represent accurately the functional form of frequency-dependent interactions. However, measuring this functional form is problematic for traditional fitness assays, which assume a constant fitness difference between competitors over the course of an assay. Here, we present a theoretical framework for measuring the functional form of frequency-dependent fitness by accounting for changes in abundance and relative fitness during a competition assay. Using two examples of ecological coexistence that arose in a long-term evolution experiment with Escherichia coli, we illustrate accurate quantification of the functional form of frequency-dependent relative fitness. Using a Monod-type model of growth dynamics, we show that two ecotypes in a typical cross-feeding interaction--such as when one bacterial population uses a byproduct generated by another--yields relative fitness that is linear with relative frequency.

Evolutionary Biology↗