de Vos, MarjonIST Austria; Dawid, Alexandre; Šunderlíková, Vanda; Tans, Sander
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 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.
This work is part of the research program of the Foundation for Fundamental Research on Matter, which is part of the Netherlands Organization for Scientific Research (NWO). M.G.J.d.V. was (partially) funded by NWO Earth and Life Sciences (ALW), project 863.14.015. We thank D. M. Weinreich, J. A. G. M. de Visser, T. Paixão, J. Polechová, T. Friedlander, and A. E. Mayo for reading and commenting on earlier versions of the manuscript and B. Houchmandzadeh, O. Rivoire, and M. Hemery for discussions and suggestions on the Markov computation. Furthermore, we thank F. J. Poelwijk for sharing plasmid pCascade5 and pRD007 and Y. Yokobayashi for sharing plasmid pINV-110. We also thank the anonymous reviewers for remarks on the initial version of the manuscript.
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de Vos M, Dawid A, Šunderlíková V, Tans S. Breaking evolutionary constraint with a tradeoff ratchet. PNAS. 2015;112(48):14906-14911. doi:10.1073/pnas.1510282112
de Vos, M., Dawid, A., Šunderlíková, V., & Tans, S. (2015). Breaking evolutionary constraint with a tradeoff ratchet. PNAS. National Academy of Sciences. https://doi.org/10.1073/pnas.1510282112
Vos, Marjon de, Alexandre Dawid, Vanda Šunderlíková, and Sander Tans. “Breaking Evolutionary Constraint with a Tradeoff Ratchet.” PNAS. National Academy of Sciences, 2015. https://doi.org/10.1073/pnas.1510282112.
M. de Vos, A. Dawid, V. Šunderlíková, and S. Tans, “Breaking evolutionary constraint with a tradeoff ratchet,” PNAS, vol. 112, no. 48. National Academy of Sciences, pp. 14906–14911, 2015.
de Vos M, Dawid A, Šunderlíková V, Tans S. 2015. Breaking evolutionary constraint with a tradeoff ratchet. PNAS. 112(48), 14906–14911.
de Vos, Marjon, et al. “Breaking Evolutionary Constraint with a Tradeoff Ratchet.” PNAS, vol. 112, no. 48, National Academy of Sciences, 2015, pp. 14906–11, doi:10.1073/pnas.1510282112.