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

Abstract

Abstract 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 model’s 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. Significance Many 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.