Lotka–Volterra dynamics kills the Red Queen: population size fluctuations and associated stochasticity dramatically change host-parasite coevolution

Abstract

Background

Host-parasite coevolution is generally believed to follow Red Queen dynamics consisting of ongoing oscillations in the frequencies of interacting host and parasite alleles. This belief is founded on previous theoretical work, which assumes infinite or constant population size. To what extent are such sustained oscillations realistic?

Results

Here, we use a related mathematical modeling approach to demonstrate that ongoing Red Queen dynamics is unlikely. In fact, they collapse rapidly when two critical pieces of realism are acknowledged: (i) population size fluctuations, caused by the antagonism of the interaction in concordance with the Lotka-Volterra relationship; and (ii) stochasticity, acting in any finite population. Together, these two factors cause fast allele fixation. Fixation is not restricted to common alleles, as expected from drift, but also seen for originally rare alleles under a wide parameter space, potentially facilitating spread of novel variants.

Conclusion

Our results call for a paradigm shift in our understanding of host-parasite coevolution, strongly suggesting that these are driven by recurrent selective sweeps rather than continuous allele oscillations.