Evolutionary dynamics of prey exploitation in a metapopulation of predators

In well-mixed populations of predators and prey, natural selection favors predators with high rates of prey consumption and population growth. When spatial structure prevents the populations from being well mixed, such predators may have a selective disadvantage because they do not make full use of the prey's growth capacity and hence produce fewer propagules. The best strategy then depends on the degree to which predators can monopolize the exploitation of local prey populations, which in turn depends on the spatial structure, the number of migrants, and, in particular, the stochastic nature of the colonization process. To analyze the evolutionary dynamics of predators in a spatially structured predator-prey system, we performed simulations with a metapopulation model that has explicit local dynamics of nonpersistent populations, keeps track of the number of emigrants entering the migration pool, assumes individuals within local populations as well as within the migration pool to be well mixed, and takes stochastic colonization into account. We investigated which of the predator's exploitation strategies are evolutionarily stable and whether these strategies minimize the overall density of prey, as is the case in Lotka-Volterra-type models of competitive exclusion. This was analyzed by pairwise invasibility plots based on short-term simulations and tested by long-term simulation experiments of competition between resident and mutant predator-types that differed in one of the following parameters: the prey-to-predator conversion efficiency, the per capita prey consumption rate, or the per capita emigration rate from local populations. In addition, we asked which of these three strategies are most likely to evolve. Our simulations showed that under selection for conversion efficiency the predator-prey system always goes globally extinct yet persists under selection for consumption or emigration rates and that the evolutionarily stable (ES) exploitation strategies do not maximize local population growth rates. The most successful exploitation strategy minimizes the overall density of prey but does not make it settle exactly at the minimum. The system did not settle at the point where the mean time to co-invasion (i.e., immigration of a second predator in a local prey population) equals the mean local interaction time (an idea borne out from studies on host exploitation strategies in host-pathogen systems) but rather where the mean time to co-invasion was larger. The ES exploitation strategies represent more prudent strategies than the ones that minimize prey density. Finally, we show that-compared to consumption-emigration is a more likely target for selection to achieve prudent exploitation and that prudent exploitation strategies can evolve only provided the prey-to-predator conversion efficiency is subject to constraints.