Ecological and evolutionary consequences of viral plasticity

Viruses can infect any organism. Because viruses use the host machinery to replicate, their performance depends on the host physiological state. For bacteriophages, this host-viral performance link has been characterized empirically and with intracellular theories. Such theories are too detailed to be included in models that study host-phage interactions in the long term, which hinders our understanding of systems that range from pathogens infecting gut bacteria to marine phage shaping present and future oceans. Here, we combined data and models to study the short- and long-term consequences that host physiology has on bacteriophage performance. We compiled data showing the dependence of lytic-phage traits on host growth rate (viral phenotypic “plasticity”) to deduce simple expressions representing such plasticity. We included these expressions in a standard host-phage model, to understand how viral plasticity can break the expected evolutionary trade-off between infection time and viral offspring number. Furthermore, viral plasticity influences dramatically dynamic scenarios (e.g. sudden nutrient pulses or host starvation). We show that the effect of plasticity on offspring number, not generation time, drives the phage ecological and evolutionary dynamics. Standard models do not account for this plasticity, which handicaps their predictability in realistic environments. Our results highlight the importance of viral plasticity to unravel host-phage interactions, and the need of laboratory and field experiments to characterize viral plastic responses across systems.