Migration enhances adaptation in bacteriophage populations evolving in ecological sinks.

Migration between populations can be a major evolutionary force. However, some disagreement exists as to precisely how migration affects population adaptation. Some theories emphasize the inhibitory effects of gene flow between locally adapted populations, whereas others propose that migration can enhance adaptation. Migration has also been theorized to rescue sink populations from extinction. In our experiments, we serially passaged bacteriophage Φ6 host range mutants under sink conditions on a novel host while manipulating the source and number of migrants into these experimental populations. Migrants from two sources were used: mutant Φ6 phage able to infect a novel host (treatment) and wild-type Φ6 phage unable to infect a novel host (control). We used quadratic regressions to determine the relationship between the number of migrants per passage and the absolute fitnesses of experimental populations following 30 passages. Our results showed that migration from a control population had no effect on absolute fitnesses of our serially passaged populations following 30 passages. By contrast, the relationship between migrants per passage and absolute fitnesses for populations receiving migrants able to infect the novel host was best described by an upwardly concave curve. These results suggest that intermediate levels of migration can have favorable impacts on evolutionary adaptation.

Pleiotropic costs of niche expansion in the RNA bacteriophage phi 6.

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.

Co-infection weakens selection against epistatic mutations in RNA viruses.

Co-infection may be beneficial in large populations of viruses because it permits sexual exchange between viruses that is useful in combating the mutational load. This advantage of sex should be especially substantial when mutations interact through negative epistasis. In contrast, co-infection may be detrimental because it allows virus complementation, where inferior genotypes profit from superior virus products available within the cell. The RNA bacteriophage phi6 features a genome divided into three segments. Co-infection by multiple phi6 genotypes produces hybrids containing reassorted mixtures of the parental segments. We imposed a mutational load on phi6 populations by mixing the wild-type virus with three single mutants, each harboring a deleterious mutation on a different one of the three virus segments. We then contrasted the speed at which these epistatic mutations were removed from virus populations in the presence and absence of co-infection. If sex is a stronger force, we predicted that the load should be purged faster in the presence of co-infection. In contrast, if complementation is more important we hypothesized that mutations would be eliminated faster in the absence of co-infection. We found that the load was purged faster in the absence of co-infection, which suggests that the disadvantages of complementation can outweigh the benefits of sex, even in the presence of negative epistasis. We discuss our results in light of virus disease management and the evolutionary advantage of haploidy in biological populations.