Sick of Eating: Eco-evo-immuno Dynamics of Predators and Their Trophically Acquired Parasites

When predators consume prey, they risk becoming infected with their prey's parasites, which can then establish the predator as a secondary host. A predator population's diet therefore influences what parasites it is exposed to, as has been repeatedly shown in many species such as threespine stickleback (Gasterosteus aculeatus) (more benthic-feeding individuals obtain nematodes from oligocheate prey, whereas limnetic-feeding individuals catch cestodes from copepod prey). These differing parasite encounters, in turn, determine how natural selection acts on the predator's immune system. We might therefore expect that ecoevolutionary dynamics of a predator's diet (as determined by its ecomorphology) should drive correlated evolution of its immune traits. Conversely, the predator's immunity to certain parasites might alter the relative costs and benefits of different prey, driving evolution of its ecomorphology. To evaluate the potential for ecological morphology to drive evolution of immunity, and vice versa, we use a quantitative genetics framework coupled with an ecological model of a predator and two prey species (the diet options). Our analysis reveals fundamental asymmetries in the evolution of ecomorphology and immunity. When ecomorphology rapidly evolves, it determines how immunity evolves, but not vice versa. Weak trade-offs in ecological morphology select for diet generalists despite strong immunological trade-offs, but not vice versa. Only weak immunological trade-offs can explain negative diet-infection correlations across populations. The analysis also reveals that eco-evo-immuno feedbacks destabilize population dynamics when trade-offs are sufficiently weak and heritability is sufficiently high. Collectively, these results highlight the delicate interplay between multivariate trait evolution and the dynamics of ecological communities.