Evolutionary Dynamics of Prey Exploitation in a Metapopulation of Predators

Abstract

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.

Variation in predator foraging behaviour changes predator–prey spatio‐temporal dynamics

“…Temporal dynamics of the predator-prey interaction in a patch are likely to be affected by the initial predator-prey ratio, with subsequent effects on the duration of the predator-prey interaction and production of dispersive propagules (Pels, de Roos & Sabelis 2002). In our study, the initial predator-prey ratio (1 : 10 or 1 : 30) had the expected effect on prey dynamics under the unselected line, but such an effect was absent under any of the selected lines.…”

“…This might make predators with the high conversion efficiency trait more successful at immediately exploiting local prey patches and locating new patches. However, simulations of a large-scale metapopulation model showed that selection for high conversion efficiency leads to the extinction of prey and predators in a patchy environment, while selection for higher consumption or emigration rates allows the predator-prey interaction to persist (Pels, de Roos & Sabelis 2002). Compared with consumption, emigration is a more likely target for selection to achieve persistent exploitation.…”

“…Under that scenario, when predators and prey are homogeneously mixed in the environment, natural selection should favour predators with the highest consumption and population growth rates (Maynard Smith 1982), although in the long run, this may cause predator-prey dynamics to become unstable because prey are overexploited (May 1972). However, when there is spatial structure in both predators and prey distribution, alternatives to a high consumption strategy, such as high conversion efficiency or rate of emigration from a local habitat, might be advantageous (Van Baalen & Sabelis 1995;Pels, de Roos & Sabelis 2002). The best strategy would depend on the degree to which predators exploit local prey populations, which in turn depends on the spatial distribution of prey in the landscape, the number of migrants and the stochastic nature of the colonization process (Pels, de Roos & Sabelis 2002).…”

“…However, when there is spatial structure in both predators and prey distribution, alternatives to a high consumption strategy, such as high conversion efficiency or rate of emigration from a local habitat, might be advantageous (Van Baalen & Sabelis 1995;Pels, de Roos & Sabelis 2002). The best strategy would depend on the degree to which predators exploit local prey populations, which in turn depends on the spatial distribution of prey in the landscape, the number of migrants and the stochastic nature of the colonization process (Pels, de Roos & Sabelis 2002).…”

“…Limited quantitative information is available concerning the interrelations between spatial distribution of predators and prey and population dynamics (Bell et al 2009), and even less is known about how predator foraging traits affect these processes. However, theoretical treatments (Hassell & May 1985;Pels, de Roos & Sabelis 2002) and empirical evidence (e.g. Takafuji 1977;Murdoch, Briggs & Nisbet 1996;Hanski et al 2004) suggest that even small differences in predator efficiency, because of differences in foraging strategy or landscape structure, might greatly alter population dynamics of predator and prey.…”