Host and parasite functional morphology jointly explain parasite specificity

Host–parasite coevolution is a major diversifying force. However, while the genetic determinants of host–parasite coevolution have received substantial attention, it remains unresolved how morphological adaptations contribute to host–parasite coevolutionary dynamics. We used a well-studied and ecologically important host–parasite system to explore morphological adaptation in host–parasite interactions. In this daphniid-fungal parasite system, infection occurs when fungal spores puncture the host gut and enter the body cavity. Prior work found genetic differences in the parasite associated with spore size. We studied how host gut traits, parasite spore size and host immune responses influenced the infection process. We collected parasite spores from two host species, the larger Daphnia dentifera and the smaller Ceriodaphnia dubia, and exposed both host species to spores sourced from each host. The ability of a spore to embed in the host gut and to penetrate into the body cavity was influenced by the host species that was exposed to the parasite (‘exposure host species’) and the species from which the spores were sourced (‘source host species’). Spores sourced from D. dentifera were better able to attack both hosts, but were especially good at attacking D. dentifera. These differences likely resulted from morphological differences, with a striking correspondence between the diameter of host guts and the size of the parasite spores. Immune responses were influenced by both exposure and source host, with D. dentifera-sourced spores triggering a larger immune response in D. dentifera than in C. dubia. In addition, in C. dubia exposure hosts, D. dentifera-sourced spores triggered a greater immune response than did C. dubia-sourced spores. Only 13.5% of hosts that had at least one parasite spore penetrate ended up with terminal infections; all but one of these infections occurred in D. dentifera hosts exposed to D. dentifera-sourced spores. Overall, infection was influenced by morphological traits of both hosts and parasites, with the outcome at each step of the infection process—and the likelihood of terminal infection—being determined by both the exposure host and the source host. Read the free Plain Language Summary for this article on the Journal blog.