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Dramatic rise of mutators has been found to accompany adaptation of bacteriain response to many kinds of stress. Two views on the evolutionary origin ofthis phenomenon emerged: the pleiotropic hypothesis positing that it is abyproduct of environmental stress or other specific stress response mechanismsand the second order selection which states that mutators hitchhike to fixationwith unrelated beneficial alleles. Conventional population genetics modelscould not fully resolve this controversy because they are based on certainassumptions about fitness landscape. Here we address this problem using amicroscopic multiscale model, which couples physically realistic moleculardescriptions of proteins and their interactions with population genetics ofcarrier organisms without assuming any a priori fitness landscape. We foundthat both pleiotropy and second order selection play a crucial role atdifferent stages of adaptation: the supply of mutators is provided throughdestabilization of error correction complexes or fluctuations of productionlevels of prototypic mismatch repair proteins (pleiotropic effects), while riseand fixation of mutators occur when there is a sufficient supply of beneficialmutations in replication-controlling genes. This general mechanism assures arobust and reliable adaptation of organisms to unforeseen challenges. Thisstudy highlights physical principles underlying physical biological mechanismsof stress response and adaptation.

Interplay between pleiotropy and secondary selection determines rise and fall of mutators in stress response