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.

Microbial Speciation

“…However, it is unclear whether "kill-the-winner" dynamics are sufficient to push a bacterial population into the r/s .1 regime , and other factors might also contribute. For example, social interactions and clonal interference could significantly reduce the rates of selective sweeps, and recombination can accelerate the rate of adaptation (Cooper 2007). Further work will be needed to fully understand the factors that maintain diversity within populations and delay selective sweeps.…”

Predicting evolution from genomics: experimental evolution of bacteriophage T7

“…For example, adaptations can involve changes in expression levels of thousands of genes (Fong et al, 2005b), and even single-base changes with profound phenotypic effects can be inexplicable in terms of known biology (Fiegna et al, 2006). Furthermore, the course of evolution in bacteria lacking mechanisms for the exchange of DNA is subject to extensive clonal interference, whereby most beneficial changes are lost in competition with the few genomes that happened to get the best mutation (Cooper, 2007;Perfeito et al, 2007). Interpreting the molecular bases of experimental adaptations done in the absence of recombination thus faces the problem that mutations may have evolved and been lost, not just because of their intrinsic effects, but because of other mutations in the same genome.…”

“…Interpreting the molecular bases of experimental adaptations done in the absence of recombination thus faces the problem that mutations may have evolved and been lost, not just because of their intrinsic effects, but because of other mutations in the same genome. (An interesting irony regarding clonal interference is that, despite the apparent evolutionary advantage of recombination in avoiding clonal interference (Cooper, 2007), the benefit of bacterial transformation-a major mechanism for bacterial recombination-remains elusive in experimental settings (Mongold, 1992;Bacher et al, 2006).) Thus, the ability to predict most of the evolution in an adaptation still eludes us, but the start is encouraging, and this step is a necessary one toward a better theory.…”

Adjusting to alien genes

“…As we recently said, 'Bacteria may not have sex often, but when they do it can be really good, evolutionarily' (Johnsen et al, 2009). The reason is not solely because the rate of evolution can be increased by recombination-mediated shuffling of homologous genes among members of the same species (Cooper, 2007;Baltrus et al, 2008;Levin and Cornejo, 2009), but more because HGT enables bacteria to acquire genes and clusters of genes (pathogenicity and nicer islands) from phylogenetically quite distant species. By exploiting these genetic aliens, evolution in bacteria need not proceed by the slow pace of mutation, selection and occasional recombination within a 'species'.…”