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, fewer founders can undergo more generations and leave more descendants in a resource-limited environment, which allows surviving beneficial mutations to spread more quickly. Here we investigate the impact of repeated bottlenecks on the dynamics of adaptation in experimental populations of Escherichia coli. We propagated 48 populations under four dilution regimes (2-, 8-, 100-, and 1000-fold), all reaching the same final size each day, for 150 days. A simple model in which adaptation is limited by the supply rate of beneficial mutations predicts that fitness gains should be maximized with ∼8-fold dilutions. The model also assumes that selection acts only on the overall growth rate and is otherwise identical across dilution regimes. However, we found that selection in the 2-fold regime was qualitatively different from the other treatments. Moreover, we observed earlier and greater fitness gains in the populations subjected to 100- and 1000-fold dilutions than in those that evolved in the 8-fold regime. We also ran simulations using parameters estimated independently from a long-term experiment using the same ancestral strain and environment. The simulations produced dynamics similar to our empirical results under these regimes, and they indicate that the simple model fails owing to the assumption that the supply of beneficial mutations limits adaptation.
Significance Many microorganisms experience population “bottlenecks” during transmission between hosts or when propagated in the laboratory. These bottlenecks reduce genetic variation, 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 propagating 48 bacterial populations for 150 days under regimes in which they were diluted 2-, 8-, 100-, or 1000-fold each day. On balance, the bacteria evolved earlier and adapted faster at the higher dilutions. These results contradict theory that accounts for the loss of genetic variation at higher dilutions, but not for the increased number of generations. We also performed simulations that reflect these opposing factors, and the simulations agree well with our experimental results.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
Data deposition: All of the data and analysis scripts used in this study will be deposited in the Dryad Digital Repository upon acceptance (doi: TO BE ADDED).
Author contributions: M.I., D.M.L., and R.E.L. designed research; M.I. and J.P.D. performed experiments; D.M.L., Z.W.D.M., and R.E.L. performed simulations; M.I., D.M.L., and R.E.L. analyzed data; and M.I., D.M.L., and R.E.L. wrote the paper.
This article contains supporting information online at TO BE ADDED.
