Evolution at experimental epidemic fronts speeds up parasite spread

Abstract

Spreading epidemics can foster the rapid emergence of novel parasite variants. Similar to range expansions, parasites at the front of an epidemic wave may evolve traits facilitating their spatial spread. Typically, higher transmissibility and virulence are expected to evolve at the epidemic front, but predictions change if virulence reduces dispersal of infected hosts. We investigated the feedbacks between epidemiology and evolution in interconnected microcosms of the ciliate Paramecium caudatum and its bacterial parasite Holospora undulata. First, two long-term treatments mimicked the moving front of epidemic waves, with and without the natural dispersal of infected hosts. Phenotypic trait assays revealed an eco-to-evo feedback: front parasites (i.e., travelling with infected hosts) were less virulent and interfered less with host dispersal, but also showed higher infectivity, compared to parasites from the control treatment. Whole-genome resequencing and analyses of functional genomic diversity corroborated such phenotypic divergence. Second, measurement of the spread of evolved parasites in linear landscapes demonstrated an evo-to-eco feedback: front parasites produced stronger infection outbreaks and faster spreading epidemic waves than did control parasites. A simulation model assessed the relative importance of the different parasite traits in determining infectious spread over a broad parameter range. It suggests that, if dispersal is generally low, higher infectivity alone can produce the observed differences in epidemic spread speed. Our study illustrates how the need to travel with the host shapes eco-evolutionary feedbacks at parasite invasion fronts, and it highlights the importance of considering concomitant evolutionary change when predicting epidemic speed. Significance StatementWhen predicting disease spread across spatial scales it is fundamental to consider host dispersal, but also the concomitant evolution of parasite traits such as infectivity and virulence. We tested how dispersal constraints affect parasite evolution and epidemic spread in an aquatic model system, by combining experimental evolution, genetic analysis and mathematical modelling. Our results suggest that epidemics can be accelerated by the evolution of highly infectious, but not necessarily more virulent parasites, in contrast to conventional views. This illustrates the important role of eco-evolutionary feedback loops can play in shaping the spread of emerging or geographically expanding parasites.