Infect, replicate, and diffuse on: how bacteriophage grows and evolves during a spatial range expansion

Spatially growing populations are ubiquitous across scales, ranging from the human migration out of Africa to the spreading of diseases. In contrast to well-mixed populations where an individual’s chance of survival is only determined by its fitness, in spatially growing populations the physical location of an individual plays a crucial role: the individuals at the edge of the expanding front benefit from having access to virgin territory and giving their offspring the same advantage. The emerging population dynamic results in an evolutionary dynamic dominated by noise, with extreme consequences such as the accumulation of deleterious mutations at the population’s front.

To investigate how spatial range expansion affects the evolutionary dynamic of a population, we employ the bacteriophage T7-E. coli system. In an evolutionary experiment lasting only 7 days, we were able to evolve a T7 strain that more than doubled its spreading speed on a bacterial lawn compared to its ancestor. The seeming lack of accumulation of deleterious mutations at the front raised questions regarding the physical nature of the traveling wave describing the expansion front of T7, which was traditionally assumed to behave like a pulled wave at long time scales. In contrast to the assumptions used in the FKPP reaction-diffusion equation generating pulled waves, diffusion rate measurements show that phage dispersal is non-uniform along the range expansion since it depends on the local bacterial density. Using stochastic simulations, we find that this effect can have dramatic consequences on the phage genetic diversity at the front and on the adaptation potential of the population. The underlying physical origin of the effect broadens the relevance of our findings to a wide range of host-pathogen systems that share this feature.