The evolution of exploitative specificity can be influenced by environmental variability in space and time and the intensity of tradeoffs. Coevolution, the process of reciprocal adaptation in two or more species, can produce variability in host exploitation and as such potentially drive patterns in host and parasite specificity. We employed the bacterium Pseudomonas fluorescens SBW25 and its DNA phage Φ2 to investigate the role of coevolution in the evolution of phage infectivity range and its relation with phage growth rate. At the phage population level, coevolution led to the evolution of broader infectivity range, but without an associated decrease in phage growth rate relative to the ancestor, whereas phage evolution in the absence of bacterial evolution led to an increased growth rate but no increase in infectivity range. In contrast, both selection regimes led to phage adaptation (in terms of growth rates) to their respective bacterial hosts. At the level of individual phage genotypes, coevolution resulted in within-population diversification in generalist and specialist infectivity range types. This pattern was consistent with a multilocus gene-for-gene interaction, further confirmed by an observed cost of broad infectivity range for individual phage. Moreover, coevolution led to the emergence of bacterial genotype by phage genotype interactions in the reduction of bacterial growth rate by phage. Our study demonstrates that the strong reciprocal selective pressures underlying the process of coevolution lead to the emergence and coexistence of different strategies within populations and to specialization between selective environments.

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Identifying factors that promote host shifts is crucial for understanding the origin and maintenance of biodiversity as well as the emergence of novel infectious diseases. Previous research has demonstrated that the opportunity for cross-species transmission and parasite adaptation can play an important role in determining if and when a host shift occurs. Another possibility is that the genetic basis of infection and resistance, when coupled with the process of coevolution (i.e., coevolutionary genetics), plays a pivotal role in determining when, if ever, a host shift occurs. Here we explore this possibility by developing and analyzing a genetically explicit epidemiological model that allows for coevolution and alternative forms of infection genetics. Approximate analytical solutions to this model demonstrate that infection genetics can influence the likelihood of a host shift. Stochastic simulations confirm the important role of infection genetics but in some cases reveal that coevolutionary dynamics modulate the likelihood of host shifts. Our results demonstrate that predicting host shifts requires a detailed understanding of the underlying genetics of infection and resistance. Thus, identifying the genetic architecture of infection and resistance in real systems is of central importance.