Shifts from cooperative to individual-based predation defense determine microbial predator-prey dynamics

Predation defense is an important feature of predator-prey interactions adding complexity to ecosystem dynamics. Prey organisms have developed various strategies to escape predation which differ in mode (elude vs. attack), reversibility (inducible vs. permanent), and scope (individual vs. cooperative defenses). While the mechanisms and controls of many singular defenses are well understood, important ecological and evolutionary facets impacting long-term predator-prey dynamics remain underexplored. This pertains especially to trade-offs and interactions between alternative defenses occurring in prey populations evolving under predation pressure. Here, we explored the dynamics of a microbial predator-prey system consisting of bacterivorous flagellates (Poteriospumella lacustris) feeding on Pseudomonas putida. Within five weeks of co-cultivation corresponding to about 35 predator generations, we observed a consistent succession of bacterial defenses in all replicates (n = 16). Initially, bacteria expressed a highly effective cooperative defense based on toxic metabolites, which brought predators close to extinction. This initial strategy, however, was consistently superseded by a second mechanism of predation defense emerging via de novo mutations. Combining experiments with mathematical modeling, we demonstrate how this succession of defenses is driven by the maximization of individual rather than population benefits, highlighting the role of rapid evolution in the breakdown of social cooperation.