Recombination Speeds Adaptation by Reducing Competition between Beneficial Mutations in Populations of Escherichia coli

Abstract

Identification of the selective forces contributing to the origin and maintenance of sex is a fundamental problem in biology. The Fisher–Muller model proposes that sex is advantageous because it allows beneficial mutations that arise in different lineages to recombine, thereby reducing clonal interference and speeding adaptation. I used the F plasmid to mediate recombination in the bacterium Escherichia coli and measured its effect on adaptation at high and low mutation rates. Recombination increased the rate of adaptation ∼3-fold more in the high mutation rate treatment, where beneficial mutations had to compete for fixation. Sequencing of candidate loci revealed the presence of a beneficial mutation in six high mutation rate lines. In the absence of recombination, this mutation took longer to fix and, over the course of its substitution, conferred a reduced competitive advantage, indicating interference between competing beneficial mutations. Together, these results provide experimental support for the Fisher–Muller model and demonstrate that plasmid-mediated gene transfer can accelerate bacterial adaptation.

Author Summary

Why have sex? One explanation is that sex is good because it allows beneficial mutations from different lineages to recombine. This reduces competition between mutations in a population and can increase the speed with which the population can adapt to environmental change. This explanation, known as the Fisher–Muller model, has extensive theoretical support; however, it is difficult to test experimentally. Using a simple microbial system I showed that recombination increased the rate of fitness improvement when beneficial mutations were common in the population and had to compete for fixation, but had little effect when mutations occurred rarely. Sequencing of candidate genes revealed the presence of the same beneficial mutation in a number of replicate populations. In the absence of recombination, this mutation took longer to spread and conferred a lower overall competitive advantage, indicating interference between competing beneficial mutations. Together, these results provide direct experimental support for the Fisher–Muller model.

Abstract

Why there is sexual reproduction is an important question. Here the authors show that making bacteria have sex allows faster accumulation and fixation of beneficial mutations.