Izutsu, M. | bioRxiv Science

bioRxiv2022

Experimental Test of the Contributions of Initial Variation and New Mutations to Adaptive Evolution in a Novel Environment

Experimental evolution is an approach that allows researchers to study organisms as they evolve in controlled environments. Despite the growing popularity of this approach, there are conceptual gaps among projects that use different experimental designs. One such gap concerns the contributions to adaptation of genetic variation present at the start of an experiment and that of new mutations that arise during an experiment. The primary source of genetic variation has historically depended largely on the study organisms. In the long-term evolution experiment (LTEE) using Escherichia coli, for example, each population started from a single haploid cell, and therefore adaptation depended entirely on new mutations. Most other microbial evolution experiments have followed the same strategy. By contrast, evolution experiments using multicellular, sexually-reproducing organisms typically start with pre-existing variation that fuels the response to selection. New mutations may also come into play in later generations of these experiments, but it is generally difficult to quantify their contribution in these studies. Here, we performed an experiment using E. coli to compare the contributions of initial genetic variation and new mutations to adaptation in a new environment. Our experiment had four treatments that varied in their starting diversity, with 18 populations in each treatment. One treatment depended entirely on new mutations, while the other three began with mixtures of clones, whole-population samples, or mixtures of whole-population samples from the LTEE. By tracking genetic markers associated with particular founders in two of our treatments, we could document the impact of the initial variation during the early generations of our experiment. However, there were no differences in fitness among the treatments after 500 or 2000 generations in the new environment, despite the variation in fitness among the founders. These results indicate that new mutations quickly overcame, and eventually contributed more to adaptation, than did the initial variation. Our study thus shows that pre-existing genetic variation can have a strong impact on early evolution in a new environment, but new beneficial mutations may contribute more to later evolution and can even drive some initially beneficial variants to extinction.

evolutionary biology↗

bioRxiv2021

Effects of periodic bottlenecks on the dynamics of adaptive evolution in microbial populations

Population bottlenecks are common in nature, and they can impact the rate of adaptation in evolving populations. On the one hand, each bottleneck reduces the genetic variation that fuels adaptation. On the other hand, each founder that survives a bottleneck can undergo more generations and leave more descendants in a resource-limited environment, which allows surviving beneficial mutations to spread more quickly. A theoretical model predicted that the rate of fitness gains should be maximized using [~]8-fold dilutions. Here we investigate the impact of repeated bottlenecks on the dynamics of adaptation using numerical simulations and experimental populations of Escherichia coli. Our simulations confirm the models prediction when populations evolve in a regime where beneficial mutations are rare and waiting times between successful mutations are long. However, more extreme dilutions maximize fitness gains in simulations when beneficial mutations are common and clonal interference prevents most of them from fixing. To examine the simulations predictions, we propagated 48 E. coli populations with 2-, 8-, 100-, and 1000-fold dilutions for 150 days. Adaptation began earlier and fitness gains were greater with 100- and 1000-fold dilutions than with 8-fold dilutions, consistent with the simulations when beneficial mutations are common. However, the selection pressures in the 2-fold treatment were qualitatively different from the other treatments, violating a critical assumption of the model and simulations. Thus, varying the dilution factor during periodic bottlenecks can have multiple effects on the dynamics of adaptation caused by differential losses of diversity, different numbers of generations, and altered selection. SignificanceMany microorganisms experience population bottlenecks during transmission between hosts or when propagated in the laboratory. These bottlenecks reduce genetic diversity, potentially impeding natural selection. However, bottlenecks can also increase the number of generations over which selection acts, potentially accelerating adaptation. We explored this tension by performing simulations that reflect these opposing factors, and by evolving bacterial populations under several dilution treatments. The simulations show that the dilution factor that maximizes the rate of adaptation depends critically on the rate of beneficial mutations. On balance, the simulations agree well with our experimental results, which imply a high rate of beneficial mutation that generates intense competition between mutant lineages.

evolutionary biology↗