Chaotic Red Queen coevolution in three-species food chains

Coevolution between two antagonistic species follow the so-called `Red Queen dynamics' when reciprocal selection results in an endless series of adaptation by one species and counter-adaptation by the other. Red Queen dynamics are `genetically-driven' when selective sweeps involving new beneficial mutations result in perpetual oscillations of the coevolving traits on the slow evolutionary timescale. Mathematical models have shown that a prey and a predator can coevolve along a genetically-driven Red Queen cycle. We found that embedding the prey-predator interaction into a three-species food chain that includes a coevolving superpredator often turns the genetically-driven Red Queen cycle into chaos. A key condition is that the prey evolves fast enough. Red Queen chaos implies that the direction and strength of selection are intrinsically unpredictable beyond a short evolutionary time, with greatest evolutionary unpredictability in the superpredator. We hypothesize that genetically-driven Red Queen chaos could explain why many natural populations are poised at the edge of ecological chaos. Over space, genetically-driven chaos is expected to cause the evolutionary divergence of local populations, even under homogenizing environmental fluctuations, and thus to promote genetic diversity among ecological communities over long evolutionary time.