Temporally Autocorrelated Environmental Fluctuations Inhibit the Evolution of Stress Tolerance

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 trade-off between stress tolerance and reproductive ability. The degree to which environmental autocorrelation influences evolutionary trajectories depends on the shape of this trade-off 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.