Spatial structure, transmission modes and the evolution of viral exploitation strategies.

Sylvain Gandon,Sébastien Lion,Thomas W Berngruber,Sam Paul Brown

doi:10.1371/journal.ppat.1004810

Abstract

Spatial structure and local migration are predicted to promote the evolution of less aggressive host exploitation strategies in horizontally transmitted pathogens. Here we explore the effect of spatial structure on the evolution of pathogens that can use both horizontal and vertical routes of transmission. First, we analyse theoretically how vertical transmission can alter evolutionary trajectories and confirm that space can impede the spread of virulent pathogens. Second, we test this prediction using the latent phage λ which transmits horizontally and vertically in Escherichia coli populations. We show that the latent phage λ wins competition against the virulent mutant λcI857 in spatially structured epidemics, but loses when spatial structure is eroded. The vertical transmission of phage λ immunizes its local host pool against superinfection and prevents the spread of the virulent λcI857. This effect breaks down when mixing facilitates horizontal transmission to uninfected hosts. We thus confirm the importance of spatial structure for the evolutionary maintenance of prudent infection strategies in latent viruses.

Highlights

When individuals compete for a common resource natural selection often favours more aggressive exploitation strategies
Why do some viruses use latent infection strategies and in which environments can such prudent host exploitation strategies evolve? Theory of mathematical epidemiology and social evolution predicts that prudent pathogens can evolve when they cluster in space and share the mutual benefits of prudent exploitation of the host population
We explore these effects experimentally by competing the latent bacteriophage λ and the virulent mutant λcI857 in spatially structured epidemics and gradually erode spatial structure

Summary

Introduction

When individuals compete for a common resource natural selection often favours more aggressive exploitation strategies. This may lead to resource exhaustion and, to population extinction, a process known as the 'tragedy of the commons'[1]. Decreased availability of susceptible hosts weakens selection for higher transmission rates [6,7,8] This may select for intermediate evolutionarily stable strategies, balancing the benefit (transmission) and the cost (virulence: induced host mortality) of host exploitation. We recently tested this idea using the bacteriophage λ in experimental epidemics spreading through well-mixed environments [9]. We confirmed that more virulent strains are selected for during early epidemics, when uninfected hosts are abundant, and that natural selection favours latent strains of the virus as disease prevalence increases

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Conclusion