Eutrophication disturbs many ecosystems. Enrichment could become worrisome if it increases prevalence of virulent parasites, and thus harm to host populations. Many purely ecological models predict this result. However hosts can rapidly evolve higher resistance to infection in response to increased parasite pressure. Such rapid evolution could buffer the effect of enrichment on disease, perhaps reducing harm to host populations. However, this prediction typically stems from models that imagine that parasites castrate hosts. We test these predictions, loosening the castration assumption, using a model of eco-evolutionary disease dynamics along a productivity gradient. Predictions from the model were tested with a zooplankton host-fungal parasite system, experimental mesocosm, and patterns from field epidemics.
Results/Conclusions
The general yet mechanistic mathematical model was parameterized with a tradeoff between fecundity and resistance to infection among host genotypes. Furthermore, the model assumes that the parasite virulently depresses survival, not fecundity. The model predicts that low nutrient supply can allow low resistance-high fecundity genotypes to dominate. At intermediate levels of enrichment, the more resistant (lower fecundity type) dominates. This response buffers the host from large outbreaks. However, once a critical threshold is reached, enrichment can overwhelm evolution of resistance. In this scenario, the least resistant genotype can dominate again, and massive epidemics can ensue. A mesocosm experiment with two genotypes echoes this prediction along a field-relevant gradient of nutrient enrichment: the less resistant host dominates at very low and then again at high nutrient enrichment, undermining the potential buffering effect of evolution of resistance. Field data is consistent with these results, qualitatively demonstrating the low, intermediate, and high productivity regimes and their respective predicted relationships between enrichment and prevalence.
These model and empirical results show how parasite life history, rapid evolution, and fecundity-resistance tradeoffs among hosts can greatly change the expectation that evolution of host resistance can save host populations from the disease-amplifying effects of eutrophication.