Unifying (simple) models of genetic robustness and evolvability

Abstract

AbstractSimple models, in which genetic robustness is expressed as the probability that a mutation is neutral, appear to offer disparate views of the relationship between robustness and evolvability. If we assume robustness trades off with evolvability, but let environmental and mutational robustness vary across genotypes, we find that evolvability is maximized at intermediate rates of environmental change. On the other hand, if we assume that the robustness of a genotype is fixed, but let the mutational networks connecting such genotypes vary, we find that robustness and evolvability need not trade off, and in fact, evolvability is maximized at intermediate levels of robustness. Here, I reconcile and extend these models. First, I show that even without a hard genotype-level trade-off between robustness and evolvability, selection optimizes phenotypic robustness depending on the rate of environmental change. Moreover, when adaptive landscapes are complex, counter-intuitively, certain increases in environmental stability can increase the frequency of environmentally-robust but mutationally-sensitive genotypes; in other words, some environments favor evolvable generalists. Next, with minor adjustments and re-interpretations, I show that simple models connecting mutational robustness to evolvability can be readily applied to environmental (or developmental) robustness. Then, with further model extensions, I show that even if the probability of neutral mutation is fixed, populations can evolve along the spectrum of robustness and evolvability by evolving the genotype-determined neighborhood of mutationally-accessible phenotypes. Indeed, because it allows for the evolution of increased evolvability without a concomitant increase in genetic load, selection should favor changes in the phenotypic neighborhood over changes in mutational sensitivity.