Resource quality differentially impacts Daphnia interactions with two parasites

Abstract

Resource quality can have conflicting effects on host–parasite interactions; for example, higher resource quality might increase host investment in immune function, or conversely, might permit greater parasite reproduction. Thus, anticipating the impact of changing resource quality on host–parasite interactions is challenging, especially because we often lack a mechanistic understanding of how resource quality influences host physiology and fitness to alter infection outcomes. We investigated whether there are generalizations in how resource quality affects multiple host clones' interactions with different parasites. We used the Daphnia freshwater zooplankton model system to experimentally investigate how a resource quality gradient from high-quality green algae to poor-quality cyanobacteria diets influences host fitness, physiology, and infection by two parasites: a bacterium, Pasteuria ramosa, and a fungus, Metschnikowia bicuspidata. We ran a separate experiment for each parasite using a factorial design with four diets, two Daphnia dentifera host clones, and parasite-inoculated and -uninoculated treatments (16 treatments per experiment). Diet strongly influenced infection by the fungus but not the bacterium. These relationships between diet and infection cannot be explained by changes in feeding rate (and, therefore, parasite exposure). Instead, the impact of diet on fungal infection was associated with impacts of diet on the earliest stage of infection: hosts that fed on poor quality diets had very few attacking spores in their guts. Diet did not significantly influence host immune responses. Diet influenced spore production differently for the two parasites, with reduced resource quality limiting the number of fungal spores and the size (but not number) of bacterial spores. Diet, host clone, and infection all affected host fitness. Interestingly, diet influenced the impact of the bacterium, a parasitic castrator that induces gigantism; for one clone, infected hosts fed high-quality diets still produced a substantial number of offspring, whereas resource limitation hindered gigantism. Finally, there were often costs of resisting infection, though these generally were not affected by diet. Overall, we show that resource quality differentially impacts the exposure, infection, and proliferation processes for different parasites and host clones, which highlights the need to use multi-genotype and multi-parasite studies to better understand these complex interactions.