Asynchronous abundance fluctuations can drive giant genotype frequency fluctuations

Large stochastic population abundance fluctuations are ubiquitous across the tree of life, impacting the predictability and outcomes of population dynamics. It is generally thought that abundance fluctuations with a Taylor’s law exponent of two do not strongly impact evolution. However, we argue that such abundance fluctuations can lead to substantial genotype frequency fluctuations if different genotypes in a population experience these fluctuations asynchronously. By serially diluting mixtures of two closely related Escherichia coli strains, we show that such asynchrony can occur, leading to giant frequency fluctuations that far exceed expectations from genetic drift. We develop an effective model explaining that the abundance fluctuations arise from correlated offspring numbers between individuals, and the large frequency fluctuations result from (even slight) decoupling in offspring number correlations between genotypes. The model quantitatively predicts the observed abundance and frequency fluctuation scaling. Initially close trajectories diverge exponentially, suggesting that chaotic dynamics may underpin the excess frequency fluctuations. Our findings suggest that decoupling noise is also present in mixed-genotype Saccharomyces cerevisiae populations. Theoretical analyses demonstrate that decoupling noise can strongly influence evolutionary outcomes, in a manner distinct from genetic drift. Given the generic nature of these frequency fluctuations, we expect them to be widespread across biological populations.