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.

Rapid contemporary evolution and clonal food web dynamics

“…When the cost of defence is extremely low, a surprising phenomenon occurs, which we have called 'cryptic dynamics': the predator cycles in abundance, but the total prey population remains effectively constant through time (figure 1e). We know that the cost of defence is quite low for some genotypes in our algal study species (Meyer et al 2006), and the cryptic dynamics predicted by the model have been observed in our experimental system ( Yoshida et al 2007; figure 1f ). The constancy of total prey abundance occurs in the model due to near exact compensation between the defended and undefended genotypes.…”

“…Investigations using simple laboratory microcosms of real consumer and resource species combined with mathematical models that incorporate observed interactions and predict resulting dynamics have proven to be particularly fruitful for uncovering some of the potential and diversity of eco-evolutionary dynamics (e.g. Yoshida et al 2003Yoshida et al , 2007Meyer et al 2006;.…”

Temporal dynamics of a simple community with intraguild predation: an experimental test

“…Rapid evolution of algal traits conferring defense against predation has been observed to occur and to substantially change predator-prey cycling in rotiferalgal chemostats, though with different species than used here (Yoshida et al 2003, 2007, Becks et al 2010. In the present system, controlling prey evolution proved to be difficult.…”

Challenges and opportunities for integrating lake ecosystem modelling approaches

“…Allowing for such potential to adapt strongly alters the dynamic behaviour of laboratory food webs and their model representations (Yoshida et al 2007). Hence, neglecting the naturally existing functional diversity and potential to adapt in lake models may strongly reduce their realism and predictive power.…”