Abstract

The ability of organisms to adapt and persist in the face of environmental change is accepted as a fundamental feature of natural systems. More contentious is whether the capacity of organisms to adapt (or “evolvability”) can itself evolve and the mechanisms underlying such responses. Using model gene networks, I provide evidence that evolvability emerges more readily when populations experience positively autocorrelated environmental noise (red noise) compared to populations in stable or randomly varying (white noise) environments. Evolvability was correlated with increasing genetic robustness to effects on network viability and decreasing robustness to effects on phenotypic expression; populations whose networks displayed greater viability robustness and lower phenotypic robustness produced more additive genetic variation and adapted more rapidly in novel environments. Patterns of selection for robustness varied antagonistically with epistatic effects of mutations on viability and phenotypic expression, suggesting that trade-offs between these properties may constrain their evolutionary responses. Evolution of evolvability and robustness was stronger in sexual populations compared to asexual populations indicating that enhanced genetic variation under fluctuating selection combined with recombination load is a primary driver of the emergence of evolvability. These results provide insight into the mechanisms potentially underlying rapid adaptation as well as the environmental conditions that drive the evolution of genetic interactions.

Highlights

  • In his classic studies of evolution in heterogeneous environments, Levins proposed that a population’s reduction in mean fitness due to temporal environmental variation can be alleviated if the temporal covariance between its mean phenotype and the changing optimal phenotype is sufficiently large [1,2]

  • When environmental fluctuations exhibit a sufficient degree of autocorrelation and predictability through time will the presence of additive genetic variance and tracking of environmental change be at a selective advantage [1,2]

  • It was assumed that all genes had the potential to interact, increasing the possibility of epistatic interactions

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Summary

Introduction

In his classic studies of evolution in heterogeneous environments, Levins proposed that a population’s reduction in mean fitness due to temporal environmental variation can be alleviated if the temporal covariance between its mean phenotype and the changing optimal phenotype is sufficiently large [1,2]. The ability to track environmental change depends on the presence of additive genetic variance. Genetic variance reduces fitness by introducing non-optimal phenotypes to a population. A genetic response to a changing environment will only be favored if it is rapid and accurate enough such that covariances compensate for any fitness losses due to phenotypic variation. In weakly autocorrelated or randomly varying environments there is little opportunity for populations to accurately track environmental variation and selection for variant phenotypes is weak. When environmental fluctuations exhibit a sufficient degree of autocorrelation and predictability through time (i.e., when fluctuations are ‘‘reddened’’ or ‘‘red shifted’’) will the presence of additive genetic variance and tracking of environmental change be at a selective advantage [1,2]

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