title: 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 genotype-environment 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 cross-environmental 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.
authors.affiliation: Foundation for Fundamental Research on Matter Institute for Atomic and Molecular Physics (FOM Institute AMOLF), 1098 XG Amsterdam, The Netherlands; Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria; Wageningen University, 6708 PB Wageningen, The Netherlands;
authors.forename: Marjon G J
authors.initials: MG
authors.lastname: de Vos
authors.affiliation: University of Grenoble Alpes, Laboratoire Interdisciplinaire de Physique, F-38402 Grenoble, France; CNRS, Laboratoire Interdisciplinaire de Physique, F-38402 Grenoble, France.
authors.forename: Alexandre
authors.initials: A
authors.lastname: Dawid
authors.affiliation: Foundation for Fundamental Research on Matter Institute for Atomic and Molecular Physics (FOM Institute AMOLF), 1098 XG Amsterdam, The Netherlands;
authors.forename: Vanda
authors.initials: V
authors.lastname: Sunderlikova
authors.affiliation: Foundation for Fundamental Research on Matter Institute for Atomic and Molecular Physics (FOM Institute AMOLF), 1098 XG Amsterdam, The Netherlands; tans@amolf.nl.
authors.forename: Sander J
authors.initials: SJ
authors.lastname: Tans
mesh_terms: D019020:Directed Molecular Evolution; D004926:Escherichia coli / Q000235:genetics*; D029968:Escherichia coli Proteins / Q000235:genetics* / Q000378:metabolism; D059647:Gene-Environment Interaction; D007763:Lac Operon / Q000235:genetics*; D017354:Point Mutation; D014157:Transcription Factors / Q000235:genetics* / Q000378:metabolism
chemical_list: D029968:Escherichia coli Proteins; D014157:Transcription Factors
keywords: constraint; environment; epistasis; evolution; fitness landscape