Pleiotropic costs of niche expansion in the RNA bacteriophage phi 6

Abstract

Natural and experimental systems have failed to universally demonstrate a trade-off between generalism and specialism. When a trade-off does occur it is difficult to attribute its cause to antagonistic pleiotropy without dissecting the genetic basis of adaptation, and few previous experiments provide these genetic data. Here we investigate the evolution of expanded host range (generalism) in the RNA virus phi6, an experimental model system allowing adaptive mutations to be readily identified. We isolated 10 spontaneous host range mutants on each of three novel Pseudomonas hosts and determined whether these mutations imposed fitness costs on the standard laboratory host. Sequencing revealed that each mutant had one of nine nonsynonymous mutations in the phi6 gene P3, important in host attachment. Seven of these nine mutations were costly on the original host, confirming the existence of antagonistic pleiotropy. In addition to this genetically imposed cost, we identified an epigenetic cost of generalism that occurs when phage transition between host types. Our results confirm the existence in phi6 of two costs of generalism, genetic and environmental, but they also indicate that the cost is not always large. The possibility for cost-free niche expansion implies that varied ecological conditions may favor host shifts in RNA viruses.

Figure 1.

Frequent antagonistic pleiotropy of expanded host range mutation. The relative fitness of the 30 host range mutants of Φ6 on the original host, grouped by their mutations in P3. The fitness of the common ancestor ATCC Φ6 is shown by the dashed line. Each point represents the grand mean fitness (±95% confidence interval) of the collected mutants bearing the indicated mutation. The killing spectrum of each mutation across the novel hosts is indicated as follows: solid circles, P. syringae pv. atrofaciens and P. pseudoalcaligenes ERA; shaded circles, P. syringae pv. tomato and P. pseudoalcaligenes ERA; open circle, P. pseudoalcaligenes ERA.