“Temporally autocorrelated environmental fluctuations inhibit the evolution of stress tolerance”

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Daniel J. Wieczynski, Paul E. Turner, and David A. Vasseur (June 2018)

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Adaptive responses to stress are controlled by environmental ‘color’

Evolutionary responses to stress are controlled by the ‘color’ of the environment

Bacteriophage ϕ6 shown attacking its host bacterium Pseudomonas syringae.
(Photo credit: Dennis Bamford; inset © Protein Data Bank Japan (PDBj) licensed under CC-BY-4.0 International)

The biological world is constantly changing, introducing new challenges to which species must adapt. For example, climate change might increase the incidence of extreme events like heat waves or droughts. But will species be able to evolve adaptations to combat these new environmental challenges? In this study, Wieczynski et al. address this question and ask specifically whether the temporal structure of a fluctuating environment, a.k.a. ‘environmental color,’ can direct the course of evolution. The authors subject a model virus (bacteriophage ϕ6) to a range of environmental scenarios in the laboratory and compare these results to a suite of evolutionary models. They find that adaptations to tolerate environmental stress are more likely to occur in ‘whiter’ environments that rapidly fluctuate between harsh and benign conditions than in ‘redder’ environments in which these fluctuations are much slower, even when the total amount of stress stays the same. This result can be explained by a tradeoff – although stress tolerant individuals can withstand harsh conditions, they suffer reduced reproductive ability under benign conditions. Harsh events happen so frequently in ‘white’ environments that the cost of low reproduction during benign conditions is negligible. However, ‘redder’ environments create extended periods of benign conditions in which stress tolerant individuals are outcompeted by less tolerant, fast-growing individuals, meaning that the cost of low reproduction outweighs the advantage of stress tolerance in the long term. This work represents an important advance in understanding how species evolve in fluctuating environments and shows that the temporal structure of the environment can be an important factor controlling adaptation in response to environmental challenges.


Abstract

As global environmental conditions continue to change at an unprecedented rate many species will experience increases in natural and anthropogenic stress. Generally speaking, selection is expected to favor adaptations that reduce the negative impact of environmental stress (i.e., stress tolerance). However, natural environmental variables typically fluctuate, exhibiting various degrees of temporal autocorrelation, known as environmental ‘colors,’ which may complicate evolutionary responses to stress. Here we combine experiments and theory to show that temporal environmental autocorrelation can determine long-term evolutionary responses to stress, without affecting the total amount of stress experienced over time. Experimental evolution of RNA virus lineages in differing environmental autocorrelation treatments agreed closely with predictions from our theoretical models that stress tolerance is favored in less autocorrelated (whiter) environments but disfavored in more autocorrelated (redder) environments. This is explained by an interaction between environmental autocorrelation and a phenotypic tradeoff between stress tolerance and reproductive ability. The degree to which environmental autocorrelation influences evolutionary trajectories depends on the shape of this tradeoff as well as the relative level of tolerance exhibited by novel mutants. These results suggest that long-term evolutionary dynamics depend not only on the overall strength of selection, but also on the way that selection is distributed over time.