Ecological and evolutionary dynamics can occur on similar timescales. However, theoretical predictions of how rapid evolution can affect ecological dynamics are inconclusive and often depend on untested model assumptions. Here we report that rapid prey evolution in response to oscillating predator density affects predator-prey (rotifer-algal) cycles in laboratory microcosms. Our experiments tested explicit predictions from a model for our system that allows prey evolution. We verified the predicted existence of an evolutionary tradeoff between algal competitive ability and defence against consumption, and examined its effects on cycle dynamics by manipulating the evolutionary potential of the prey population. Single-clone algal cultures (lacking genetic variability) produced short cycle periods and typical quarter-period phase lags between prey and predator densities, whereas multi-clonal (genetically variable) algal cultures produced long cycles with prey and predator densities nearly out of phase, exactly as predicted. These results confirm that prey evolution can substantially alter predator-prey dynamics, and therefore that attempts to understand population oscillations in nature cannot neglect potential effects from ongoing rapid evolution.

SignificanceDecades of research have fostered the now-prevalent assumption that noncrop habitat facilitates better pest suppression by providing shelter and food resources to the predators and parasitoids of crop pests. Based on our analysis of the largest pest-control database of its kind, noncrop habitat surrounding farm fields does affect multiple dimensions of pest control, but the actual responses of pests and enemies are highly variable across geographies and cropping systems. Because noncrop habitat often does not enhance biological control, more information about local farming contexts is needed before habitat conservation can be recommended as a viable pest-suppression strategy. Consequently, when pest control does not benefit from noncrop vegetation, farms will need to be carefully comanaged for competing conservation and production objectives.

Adaptive variation in the traits determining ecological interactions can lead to evolution so rapid that ecological dynamics change course while in progress (i.e., 'eco-evolutionary dynamics'). However, little is known about how the qualitative properties of eco-evolutionary dynamics (e.g., cycling, equilibrium, etc.) are affected by the amount of heritable variation present. Here, we show that a change in the range of variation in a heritable prey defense trait determines what dynamics are observed in an experimental predator-prey system. We combine modelling and laboratory experiments to show that initial defense trait variation determines whether populations exhibit eco-evolutionary cycles in which heritable variation is maintained, or converge to an equilibrium at which the prey population becomes monomorphic. Our results show how small changes in the amount of adaptive genetic variance initially present can radically alter eco-evolutionary dynamics, and can ultimately determine whether heritable variation is maintained or lost.

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.

Feedbacks between ecological and evolutionary change may play important roles in community and ecosystem functioning, but a complete eco-evolutionary feedback loop has not been demonstrated at the community level, and we know little about molecular mechanisms underlying this kind of eco-evolutionary dynamics. In predator-prey (rotifer-alga) microcosms, cyclical changes in predator abundance generated fluctuating selection for a heritable prey defence trait, cell clumping. Predator population growth was affected more by prey evolution than by changes in prey abundance, and changes in predator abundance drove further prey evolution, completing the feedback loop. Within a predator-prey cycle, genes up-regulated as clumping declined were down-regulated as clumping increased, and vice-versa. Genes changing most in expression tended to be associated with defence or its cost. Expression patterns of individual genes differed greatly between consecutive cycles (often reversing direction), suggesting that a particular phenotype may be produced by several (perhaps many) different gene transcription pathways.