Predicting population genetic change in an autocorrelated random environment: Insights from a large automated experiment

Most natural environments exhibit a substantial component of random variation, with a degree of temporal autocorrelation that defines the color of environmental noise. Such environmental fluctuations cause random fluctuations in natural selection, affecting the predictability of evolution. But despite long-standing theoretical interest in population genetics in stochastic environments, there is a dearth of empirical estimation of underlying parameters of this theory. More importantly, it is still an open question whether evolution in fluctuating environments can be predicted indirectly using simpler measures, which combine environmental time series with population estimates in constant environments. Here we address these questions by using an automated experimental evolution approach. We used a liquid-handling robot to expose over a hundred lines of the micro-alga Dunaliella salina to randomly fluctuating salinity over a continuous range, with controlled mean, variance, and autocorrelation. We then tracked the frequencies of two competing strains through amplicon sequencing of nuclear and choloroplastic barcode sequences. We show that the magnitude of environmental fluctuations (determined by their variance), but also their predictability (determined by their autocorrelation), had large impacts on the average selection coefficient. The variance in frequency change, which quantifies randomness in population genetics, was substantially higher in a fluctuating environment. The reaction norm of selection coefficients against constant salinity yielded accurate predictions for the mean selection coefficient in a fluctuating environment. This selection reaction norm was in turn well predicted by environmental tolerance curves, with population growth rate against salinity. However, both the selection reaction norm and tolerance curves underestimated the variance in selection caused by random environmental fluctuations. Overall, our results provide exceptional insights into the prospects for understanding and predicting genetic evolution in randomly fluctuating environments.Author summary: Being able to predict evolution under natural selection is important for many applied fields of biology, ranging from agriculture to medicine or conservation. However, this endeavor is complicated by factors that inherently limit our ability to predict the future, such as random fluctuations in the environment. Population genetic theory indicates that probabilistic predictions can still be made in this context, but the extent to which this holds empirically, and whether these predictions can be based on simple measurements, are still open questions. Making progress on answering these questions can be achieved by capitalizing on experiments where the environment is precisely controlled over many generations. Here, we used a pipetting robot to generate random time series of salinities with controlled patterns of fluctuations, which we imposed on a microalga, Dunaliella salina. Tracking the frequencies of two genotypes in a mixture by sequencing a short barcode sequence, we were able to show how patterns of fluctuating selection relate to the fluctuating environment. Interestingly, parts of these responses, but not all, could be predicted by simpler measurements in constant environments, allowing precise characterization the limits and prospects for predicting evolution in fluctuating environments.