Chaotic Red Queen coevolution in three-species food chains

Abstract

Coevolution between two antagonistic species follows the so-called 'Red Queen dynamics' when reciprocal selection results in an endless series of adaptation by one species and counteradaptation 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 time scale. 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.

The Red Queen theory of recombination hotspots

“…The result is a Red Queen dynamic (van Valen, 1973) somewhat analogous to what has been described in predator–prey (Dieckmann et al. , 1995; Dercole et al. , 2010) or host–parasite systems (Decaestecker et al.…”

Antagonistic coevolution between quantitative and Mendelian traits

“…Our findings suggest that in-phase and chaotic cycles might also occur as a result of eco-evolutionary feedbacks in experimental studies. The possibility of in-phase cycles [59] and chaotic cycles [24,45] of (co)evolving predator -prey systems has been theoretically suggested, but our study illustrates another possible mechanism.…”

“…[10][11][12][13][14][15][16][17]), mutation-limited asexual clonal models (Adaptive Dynamics) (e.g. [18][19][20][21][22][23][24]) and models for evolutionarily stable strategies (ESS) that cannot be invaded by other strategies (e.g. [25]).…”

Chaos and the (un)predictability of evolution in a changing environment

“…A much less explored source of unpredictability in evolution is deterministic chaos (but see Hamilton ; Altenberg ; Gavrilets and Hastings ; Abrams and Matsuda ; Dercole and Rinaldi ; Dercole et al. ; Doebeli and Ispolatov ), which occurs when the dynamics of a system, despite being completely predictable from the initial conditions, are strongly sensitive to them. Under chaotic dynamics, any measurement error, regardless how small, will be amplified over time to the point that it becomes impossible to make accurate predictions beyond a certain time scale (Ott ; Petchey et al.…”