Host-parasite coevolutionary arms races give way to fluctuating selection

Abstract

Host-parasite coevolution is a key driver of biological diversity and parasite virulence, but its effects depend on the nature of coevolutionary dynamics over time. We used phenotypic data from coevolving populations of the bacterium Pseudomonas fluorescens SBW25 and parasitic phage SBW25Φ2, and genetic data from the phage tail fibre gene (implicated in infectivity evolution) to show that arms race dynamics, typical of short-term studies, decelerate over time. We attribute this effect to increasing costs of generalism for phages and bacteria with increasing infectivity and resistance. By contrast, fluctuating selection on individual host and parasite genotypes was maintained over time, becoming increasingly important for the phenotypic properties of parasite and host populations. Given that costs of generalism are reported for many other systems, arms races may generally give way to fluctuating selection in antagonistically coevolving populations.

Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

“…2). These observations are consistent with previous work reporting ARD-like coevolution in the well-studied interaction between P. fluorescens SBW25 and its phage ϕ2 (12,15).…”

“…Results from the P. fluorescens-ϕ2 system suggest that ARD may predominate in the coevolutionary process for more than 100 bacterial generations and give way to FSD only subsequently, when the accumulation of resistance or infectivity genes becomes costly (12). In contrast, we detected a strong signature of FSD early in coevolution, during the first 60 generations.…”

“…For example, the FSD systems may involve reciprocal selection of matching-allele type of infectivity and resistance, whereas ARD dynamics have an underlying gene-for-gene type of interaction (9). Evidence from the P. fluorescens-ϕ2 system indicates that genotypic change is consistent with ARD or FSD, depending on the observation period in the coevolutionary process (12). For example, declining gene diversity in experimentally coevolving populations of Caenorhabditis elegans and Bacillus thuringiensis may have resulted from ARD dynamics or from FSD dynamics with large amplitudes (54).…”

“…In contrast, fluctuating selection dynamics (FSD), in which there is no directional change in the evolution of the host resistance range, is governed by negative frequencydependent selection, favoring hosts that resist the most frequently encountered parasite genotypes and parasites that infect the most common host genotypes (9)(10)(11). It has been suggested that ARD predominates during the initial stages of coevolution, when adaptations to the coevolving opponent are largely cost-free, whereas FDS is more significant at later stages, when attack/ defense alleles accumulate in the genome and impose costs (12). Thus, when systems shift from ARD to FSD, dynamic coevolutionary equilibria may arise, with constant numbers of attack/defense alleles at the individual level (13) and the continuous frequencydependent (re)cycling of alleles at the population level (14).…”

“…Some of the prime experimental models are bacteria and their lytic phages, which exhibit rapid evolution and are amenable to time-shift tests. Recent study indicates that coevolving populations may exhibit either ARD or FSD (12,(21)(22)(23)(24), and there is some evidence for the genetic mechanism involved [e.g., mutations at tail fiber genes (12,25)] and for the expansion of the phage host range as coevolution proceeds (6). Most studies of bacteria-phage coevolution involve the model system Pseudomonas fluorescens SBW25 and its lytic phage ϕ2 (15).…”