Breaking evolutionary constraint with a tradeoff ratchet

Abstract

Epistatic interactions can frustrate and shape evolutionary change. Indeed, phenotypes may fail to evolve when essential mutations are only accessible through positive selection if they are fixed simultaneously. How environmental variability affects such constraints is poorly understood. Here, we studied genetic constraints in fixed and fluctuating environments using the Escherichia coli lac operon as a model system for genotypeenvironment interactions. We found that, in different fixed environments, all trajectories that were reconstructed by applying point mutations within the transcription factor-operator interface became trapped at suboptima, where no additional improvements were possible. Paradoxically, repeated switching between these same environments allows unconstrained adaptation by continuous improvements. This evolutionary mode is explained by pervasive cross-environmental tradeoffs that reposition the peaks in such a way that trapped genotypes can repeatedly climb ascending slopes and hence, escape adaptive stasis. Using a Markov approach, we developed a mathematical framework to quantify the landscape-crossing rates and show that this ratchet-like adaptive mechanism is robust in a wide spectrum of fluctuating environments. Overall, this study shows that genetic constraints can be overcome by environmental change and that crossenvironmental tradeoffs do not necessarily impede but also, can facilitate adaptive evolution. Because tradeoffs and environmental variability are ubiquitous in nature, we speculate this evolutionary mode to be of general relevance.evolution | environment | epistasis | fitness landscape | constraint I t is widely believed that epistatic interactions can direct evolutionary change (1-7). Epistasis has been implicated in shaping RNA (8) and protein (4, 6, 7, 9) sequences, sensing (5) and translation (10) functions, and developmental programs (11) and speciation (12)(13)(14). Phenotypes may be difficult to evolve not because they are impossible biochemically or physically, but because essential mutations are mutually dependent and must be fixed together to be selected positively (5,(15)(16)(17). How such genetic constraints can be overcome has been considered previously: population expansion or subdivision can limit negative selection and maintain less fit phenotypes (18,19), and large populations and long waiting times can enable the joint fixation of multiple mutations (20), whereas recombination can join mutant alleles (21-23). Other mechanisms include drift (24-26), partial penetrance (27), and nonheritable lifetime plasticity (28, 29). However, how the constraining effects of such genetic interactions are affected by environmental variability remains poorly understood. It has been shown that mutational effects (30-33) and epistasis itself (34, 35) can depend on the environment, that bacterial resistance evolution can be contingent on the rate of antibiotic increase (36), and that adaptation in silico can be accelerated by environmental change (37-40). These observations sugg...

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Beyond the Hypercube: Evolutionary Accessibility of Fitness Landscapes with Realistic Mutational Networks

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