Antagonistic coevolution accelerates molecular evolution

Abstract

The Red Queen hypothesis proposes that coevolution of interacting species (such as hosts and parasites) should drive molecular evolution through continual natural selection for adaptation and counter-adaptation. Although the divergence observed at some host-resistance and parasite-infectivity genes is consistent with this, the long time periods typically required to study coevolution have so far prevented any direct empirical test. Here we show, using experimental populations of the bacterium Pseudomonas fluorescens SBW25 and its viral parasite, phage Phi2 (refs 10, 11), that the rate of molecular evolution in the phage was far higher when both bacterium and phage coevolved with each other than when phage evolved against a constant host genotype. Coevolution also resulted in far greater genetic divergence between replicate populations, which was correlated with the range of hosts that coevolved phage were able to infect. Consistent with this, the most rapidly evolving phage genes under coevolution were those involved in host infection. These results demonstrate, at both the genomic and phenotypic level, that antagonistic coevolution is a cause of rapid and divergent evolution, and is likely to be a major driver of evolutionary change within species.

Figure 1. Genetic and phenotypic responses to selection

a, Phylogenetic tree for evolved (E1–6) and coevolved (C1, C3–6) phage populations and ancestral reference genotype (ref) based on Euclidean distances calculated from the frequency and identity of mutations in each population. Scale bar indicates a Euclidean distance of one. b, The phage-infectivity range based on the ability of each coevolved population to infect 20 bacterial clones from each host population. Infection by phage is shown in red, and resistance by hosts is shown in grey. The dendrogram indicates phenotypic similarity between phage populations.

Figure 2. Patterns of molecular evolution in the Φ2 genome

a, b, Pairwise genetic distance between each phage population and the ancestral genotype (a), and genetic diversity within each phage population (b). Symbols denote means ± s.e.m. of replicate populations within the coevolved (magenta; n = 5) and the evolved (blue; n = 6) treatments. The locations of mutations within each population are shown as bars underneath each coding sequence, with the colour of each bar indicating the frequency of each mutation within each population (white, rare; red, common). c, Magnified view of identity and frequency of mutations in each population for SBWP25_0027 (gp40) and SBWP25_0036 (gp49). bp, base pairs.