Hosts are exposed to a suite of microbes over the course of their lives. These microbes may or may not occupy the host at the same time, but they can leave an imprint on the within-host environment through their influence on immunity or stored energetic resources that modulates the fitness of other within-host community members. An open question in the study of multiple infections is whether top-down (immune-driven) or bottom-up (resource-driven) feedbacks among parasite populations are more important in structuring parasite infracommunity dynamics, infection outcomes, and disease transmission. In this study, we manipulated the exposure of flour beetles (Tribolium castaneum) to two parasites: a benign protozoan parasite (Gregarina spp.) and a virulent entomopathogenic bacterium (Bacillus thuringiensis, Bt). We quantified the impact of larval gregarine exposure on host survival against Bt as well as host immunological dynamics using qPCR. We then manipulated the quality and quantity of host resource acquisition using nutritional geometry methods to quantify the interaction of macronutrient ratios and gregarine infection on host survival, resistance, and tolerance to Bt infection.
Results/Conclusions
Gregarine-infected individuals were less likely to survive Bt infection than those who were not exposed to the protozoa as larvae. Gregarine exposure resulted in the down-regulation of antibacterial immune genes in the gut. Furthermore, protein supplementation exacerbated bacteria-induced mortality in gregarine-infected individuals but enhanced survival in larvae who were not coinfected with gregarines, indicating an interaction between coinfection and bottom-up regulation of bacterial growth dynamics. Taken together, our results suggest that top-down mechanisms are more important for determining the outcome of single infections in this system, while co-infection shifts the system toward the dominance of bottom-up regulation. Our study therefore sheds new light on the regulation of within-host parasite communities and the impact of multiple infections on the evolution of host life history and immune systems.