Cryptic Population Dynamics: Rapid Evolution Masks Trophic Interactions

Abstract

Trophic relationships, such as those between predator and prey or between pathogen and host, are key interactions linking species in ecological food webs. The structure of these links and their strengths have major consequences for the dynamics and stability of food webs. The existence and strength of particular trophic links has often been assessed using observational data on changes in species abundance through time. Here we show that very strong links can be completely missed by these kinds of analyses when changes in population abundance are accompanied by contemporaneous rapid evolution in the prey or host species. Experimental observations, in rotifer-alga and phage-bacteria chemostats, show that the predator or pathogen can exhibit large-amplitude cycles while the abundance of the prey or host remains essentially constant. We know that the species are tightly linked in these experimental microcosms, but without this knowledge, we would infer from observed patterns in abundance that the species are weakly or not at all linked. Mathematical modeling shows that this kind of cryptic dynamics occurs when there is rapid prey or host evolution for traits conferring defense against attack, and the cost of defense (in terms of tradeoffs with other fitness components) is low. Several predictions of the theory that we developed to explain the rotifer-alga experiments are confirmed in the phage-bacteria experiments, where bacterial evolution could be tracked. Modeling suggests that rapid evolution may also confound experimental approaches to measuring interaction strength, but it identifies certain experimental designs as being more robust against potential confounding by rapid evolution. The presence and strength of interactions between species has frequently been inferred from observational data on changes in species abundance. For example, correlated cycles in potential predator and prey species may be interpreted as evidence that the species interact, while the absence of such coupled oscillations might be interpreted as evidence for lack of interaction. Here we show that prey abundance can be decoupled from changes in predator abundance when there is genetic variability in the prey for antipredator defense traits, allowing rapid evolutionary changes in prey defense levels. It then appears that the two species are not interacting, when in fact they are. We deduce this from studies of two laboratory microcosm systems, one with algae consumed by rotifers and the other with bacteria attacked by phage. In each, when the prey vary genetically for defense traits and undefended genotypes are superior competitors, defended and undefended prey frequencies evolve in a cyclical way that is almost exactly counterbalancing, so that total prey density remains nearly constant. We show mathematically that these “cryptic cycles” occur whenever conditions are right for predator-prey cycles, when prey vary genetically for defense traits, and when prey defense against predation is effective but inexpensive to produce. Under these conditions, observations of predator and prey population dynamics cannot be trusted to be informative about the strength or even the existence of interspecific trophic links.