Greater phage genotypic diversity constrains arms-race coevolution

Antagonistic coevolution between hosts and parasites, the reciprocal evolution of host resistance and parasite infectivity, has important implications in ecology and evolution. Whether the parasite or host has an advantage in coevolution can determine their relative success as one is better adapted than the other. The amount of genetic diversity in a population is thought to determine evolutionary rates with the population of higher genetic variability having an evolutionary advantage over its host/parasite. While studies have manipulated genetic diversity during coevolution, such as by increasing mutation rates, it is unclear how starting genetic diversity affects host-parasite coevolution. Here, we (co)evolved the bacterium Pseudomonas fluorescens SBW25 and two bacteriophage genotypes of its lytic phage SBW25?2 in isolation (one phage genotype) and together (two phage genotypes). Bacterial populations rapidly evolved phage resistance and phage reciprocally increased their infectivity in response. When phage populations were evolved with bacteria in isolation, bacterial resistance and phage infectivity increased through time, indicative of arms-race coevolution. In contrast, when both phage genotypes were together, bacteria did not increase their resistance in response to increasing phage infectivity. This was likely due to bacteria being unable to evolve resistance to both phage via the same mutations. These results suggest that increasing initial parasite genotypic diversity can give parasites an evolutionary advantage that arrests long-term coevolution. This study has important implications for the applied use of phage in phage therapy and in understanding host-parasite dynamics in broader ecological and evolutionary theory.