Rapid evolution of virulence leading to host extinction under host-parasite coevolution

Charlotte Rafaluk, Markus Gildenhard, Andreas Mitschke, Arndt Telschow, Hinrich Schulenburg, Gerrit Joop

Host-parasite coevolution is predicted to result in changes in the virulence of the parasite in order to maximise its reproductive success and transmission potential, either via direct host-to-host transfer or through the environment. The majority of coevolution experiments, however, do not allow for environmental transmission or persistence of long lived parasite stages, in spite of the fact that these may be critical for the evolutionary success of spore forming parasites under natural conditions. We carried out a coevolution experiment using the red flour beetle, Tribolium castaneum, and its natural microsporidian parasite, Paranosema whitei. Beetles and their environment, inclusive of spores released into it, were transferred from generation to generation. We additionally took a modelling approach to further assess the importance of transmissive parasite stages on virulence evolution. In all parasite treatments of the experiment, coevolution resulted in extinction of the host population, with a pronounced increase in virulence being seen. Our modelling approach highlighted the presence of environmental transmissive parasite stages as being critical to the trajectory of virulence evolution in this system. The extinction of host populations was unexpected, particularly as parasite virulence is often seen to decrease in host-parasite coevolution. This, in combination with the increase in virulence and results obtained from the model, suggest that the inclusion of transmissive parasite stages is important to improving our understanding of virulence evolution.