Resource availability and dimensionality result in ecology-dependent selection in bacteriophage spatial expansions

In microbial populations, fitness, which is essential to understand and predict evolution, is often defined and measured as the net growth rate of a population in isolation. Applying the same definition to viruses is challenging, both because viral replication involves a host infection process, which is determined by several parameters that are context-dependent, and because viruses compete heavily for resources (susceptible cells). These challenges are particularly exacerbated in spatial range expansions, where multiplicity of infection is often high and resource availability varies in time and space. To assess different fitness definitions and their generalizability, we investigate a model of coupled partial differential equations for phage plaque expansion in one and two dimensions. We find that two commonly used metrics for phage fitness in plaque expansions, i.e., steady state phage densities and front expansion speed in isolation, are unable to reliably predict the winner in one- and two-dimensional direct competitions. More generally, we find that optimal phage traits depend on the dimensionality of the system and the make-up of the phage population, leading to unexpected behaviours, e.g., rock-paper-scissor dynamics and, in high dimensions, enhanced phage density due to the nearby presence of a competitor. We show that the phenomenon stems from the interplay between resource consumption and replication and thus may apply more broadly to any population competing for shared resources.