Resource-dependent antagonistic coevolution leads to a new paradox of enrichment

The classical, ecological, paradox of enrichment describes a phenomenon that resource enrichment destabilizes predator-prey systems by exacerbating population oscillations. Here we suggest a new, evolutionary, paradox of enrichment. Resource enrichment can lead to more asymmetrical predator-prey coevolution (i.e., extremely high levels of prey defenses against predators) that decreases predator abundances and increases predator extinction risk. A major reason for this is that high resource availability can reduce fitness costs associated with prey defenses. In our experiments with a bacterium and its lytic phage, nutrient-balanced resource enrichment led to patterns in population demography and coevolutionary dynamics consistent with this coevolution-based paradox of enrichment; in particular, phage population extinction events were observed under nutrient-rich, not nutrient-poor, conditions. Consistent with ecological studies, carbon-biased resource enrichment (with carbon availability disproportionately increased relative to other nutrients) did not destabilize dynamics, and the asymmetry of coevolution was not altered in this context. Our work highlights the importance of integrating ecological and evolutionary thinking for studies of the consequences of nutrient pollution and other types of environmental changes.