Quantifying the capacity for contemporary trait changes to drive intermittent predator–prey cycles

A large and growing body of theory has demonstrated how the presence of trait variation in prey or predator populations may affect the amplitude and phase of predator–prey cycles. Less attention has been given to so-called intermittent cycles, in which predator–prey oscillations recurrently disappear and re-appear, despite such dynamics being observed in empirical systems and modeling studies. A comprehensive understanding of the conditions under which trait changes may drive intermittent predator–prey dynamics, as well as their potential ecological implications, is therefore missing. Here we provide a first systematic analysis of the eco-evolutionary conditions that may give rise to intermittent predator–prey cycles, investigating 16 models that incorporate different types of trait variation within prey, predators, or both. Our results show that intermittent dynamics often arise through predator–prey coevolution, but only very rarely when only one trophic level can adapt. Additionally, the frequency of intermittent cycles depends on the source of trait variation (genetic variation or phenotypic plasticity) and the genetic architecture (Mendelian or quantitative traits), with intermittency occurring most commonly through Mendelian evolution, and very rarely through phenotypic plasticity. Further analysis identified three necessary conditions for when trait variation can drive intermittent cycles. First, the intrinsic stability of the predator–prey system must depend on the traits of prey, predators, or both. Second, there must be a mechanism causing the recurrent alternation between stable and unstable states, leading to a “trait” cycle superimposed on the population dynamics. Finally, these trait dynamics must be significantly slower than the predator–prey cycles. We show how these conditions explain all the abovementioned patterns. We further show an important unexpected consequence of these necessary conditions: they are most easily met when intraspecific trait variation is at high risk of being lost. As trait diversity is positively associated with ecosystem functioning, this can have potentially severe negative consequences. This novel result highlights the importance of identifying and understanding intermittent cycles in theoretical studies and natural systems. The new approach for detecting and quantifying intermittency we develop here will be instrumental in enabling future study.