The evolutionary dynamics of hyperparasites

Evolutionary theory has typically focused on pairwise interactions, such as those between hosts and parasites, with relatively little work having been carried out on more complex interactions including hyperparasites: parasites of parasites. Hyperparasites are common in nature, with the chestnut blight fungus virus CHV-1 a well-known natural example, but also notably include the phages of important human bacterial diseases. We build a general modeling framework for the evolution of hyperparasites that highlights the central role that the ability of a hyperparasite to be transmitted with its parasite plays in their evolution. A key result is that hyperparasites which transmit with their parasite hosts (hitchhike) will be selected for lower virulence, trending towards hypermutualism or hypercommensalism. We examine the impact on the evolution of hyperparasite systems of a wide range of host and parasite traits showing, for example, that high parasite virulence selects for higher hyperparasite virulence resulting in reductions in parasite virulence when hyperparasitized. Furthermore, we show that acute parasite infection will also select for increased hyperparasite virulence. Our results have implications for hyperparasite research, both as biocontrol agents and for their role in shaping community ecology and evolution and moreover emphasize the importance of understanding evolution in the context of multitrophic interactions.