ABSTRACT
Understanding the occurrence and spatial spread of infectious disease is a major challenge to epidemiologists and evolutionary biologists. Current theory predicts the spread of highly exploitative parasites at the front of spreading epidemics. However, many parasites rely on the dispersal of their hosts to spread to new habitats. This may lead to a conflict between local transmission and spatial spread, counteracting selection for highly virulent parasites. Yet, there are no experimental tests of these hypotheses. Here we investigate parasite evolution in an experiment creating conditions in cores and at fronts of spreading host-parasite populations, using the freshwater host Paramecium caudatum and its bacterial parasite Holospora undulata. We find that parasites from experimental range fronts induce higher rates of host dispersal than parasites from the core. This divergence is accompanied by lower levels of virulence and delayed development of infectious stages of front parasites. We validate these experimental results by fitting an epidemiological model to time-series data independently obtained from the experiment. This combined evidence suggests an evolutionary trade-off between host exploitation (virulence) and host-mediated dispersal, resulting in a shift of the investment in horizontal transmission. In conclusion, our results show that different segments of an epidemic wave may be under divergent selection pressures, shaping the evolution of parasite life history. These findings have important implications for our understanding of the interaction between demography and rapid evolutionary change in spreading populations, which is crucial for the management of emerging diseases, biological invasions and other non-equilibrium scenarios.