Primeval populations replicating at high error rates required a mechanism to overcome the accumulation of mutations and information deterioration. Known strategies to overcome mutation pressures include RNA processivity, epistasis, selection, and quasispecies. We investigated the mechanism by which small molecular ribozyme populations can survive under high error rates by propagating several lineages under different mutagen concentrations. We found that every population that evolved without mutagen went extinct, while those subjected to mutagenic evolution survived. To understand how they survived, we characterized the evolved genotypic diversity, the formation of genotype-genotype interaction networks, the fitness of the most common mutants for each enzymatic step, and changes in population size along the course of evolution. We found that the elevated mutation rate was necessary for the populations to survive in the novel environment, in which all the steps of the metabolism worked to promote the survival of even less catalytically efficient ligases. Besides, an increase in population size and the mutational coupling of genotypes in close-knit networks, which helped maintain or recover lost genotypes making their disappearance transient, prevented Muller's ratchet and extinction.
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This work was supported by the Nucleic Acid Chemistry and Engineering, the Ecology and Evolution, and the Physics and Biology Units of the Okinawa Institute of Science and Technology Graduate University (OIST); the Japanese Society for the Promotion of Science KAKENHI Grant-in-Aid for Challenging Exploratory Research (grant number 16K14790) awarded to CDA; the Engineering and Physical Sciences Research Council, and the Medical Research Council (grant number EP/L016044/1) awarded to AA. We thank Robert Sinclair; and Jotun Hein (University of Oxford) for helpful discussions.
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Diaz Arenas, C., Ardaševa, A., Miller, J. et al. Ribozyme Mutagenic Evolution: Mechanisms of Survival. Orig Life Evol Biosph 51, 321–339 (2021). https://doi.org/10.1007/s11084-021-09617-0
- Mutagenic evolution
- Genotypic diversity