Predators and parasites have different selective pressures on a population. We use a model organism, threespine stickleback (Gasterosteus aculeatus), to ask whether variation in traits that defend individuals against predators affects their response to parasites, and whether such effects are transmitted across generations via the differential effects of different host phenotypes on the density of parasites in the environment. Defenses against parasites include resistance (avoiding infection) and tolerance (minimizing negative fitness consequences of infection). We tested whether variation in predator defense covaries with resistance and tolerance. Using an in-situ enclosure experiment, we assayed tolerance and resistance of stickleback to a copepod parasite (Ergasilus). We examined differences among stickleback plate morphs (low, partial, and complete-plated), which vary in amount of body armor. In phase one, we introduced ten stickleback of the same morph into each mesocosm, with four replicates for each morph and four fishless controls. After six weeks, we removed all fish and determined survival and infection rate of stickleback, and density of pre-infective parasites in the plankton. In phase two, we introduced four stickleback of each morph into all mesocosms. After two weeks, we determined survival and infection rate of stickleback, and density of pre-infective parasites in the plankton.
During phase one, complete-plated stickleback survived best and left more Ergasilus in the plankton, suggesting higher tolerance. Partial- and low-plated stickleback had lower survival and Ergasilus densities at the end of phase one. Ergasilus densities in fishless treatments were lowest. During phase two, survival was similar between plate morphs, but higher in enclosures that did not have fish during phase one, presumably due to lower parasite densities in the environment. Parasite load on individuals at the end of phase two was shaped by a significant interaction between that individual’s plate morph and the morph of the fish inhabiting its mesocosm in phase one. Low-plated individuals that followed low-plated treatments in phase one and complete-plated individuals who followed partial-plated treatments in phase one had significantly higher parasite loads than did fish in enclosures that had complete-plated or no fish treatments in phase one. We found parasite exposure level was influenced by the phenotypic composition of the stickleback population, which influences the relative infection rates across host phenotypes in the next generation. Our results suggest phenotypic variation in predator defense may also affect host-parasite dynamics. It appears that survival is influenced by differential investment in resistance and tolerance across stickleback plate morphs.