Mutational robustness can facilitate adaptation

Abstract

The role of mutational robustness in evolution has been a topic of much debate and controversy. On the one hand, it would seem to impede adaptation by making it less easy for a new phenotype to develop in the event of environmental changes; on the other it is surely advantageous for an organism to buffer its phenotype against possibly unhelpful mutations. How can an organism handle this paradox, and be both robust and adaptable? A quantitative population genetics model gives a possible resolution to this problem, by showing that mutational robustness can either impede or facilitate adaptation, depending on the population size, the mutation rate and the structure of the fitness landscape. If robustness is the opposite of evolvability, we might expect that a robust population would have difficulty adapting to environmental change; however, some studies have suggested that genetic robustness facilitates adaptation. Here, using a general population genetics model, mutational robustness is found to either impede or facilitate adaptation depending on the population size, the mutation rate and the structure of the fitness landscape. Robustness seems to be the opposite of evolvability. If phenotypes are robust against mutation, we might expect that a population will have difficulty adapting to an environmental change, as several studies have suggested1,2,3,4. However, other studies contend that robust organisms are more adaptable5,6,7,8. A quantitative understanding of the relationship between robustness and evolvability will help resolve these conflicting reports and will clarify outstanding problems in molecular and experimental evolution, evolutionary developmental biology and protein engineering. Here we demonstrate, using a general population genetics model, that mutational robustness can either impede or facilitate adaptation, depending on the population size, the mutation rate and the structure of the fitness landscape. In particular, neutral diversity in a robust population can accelerate adaptation as long as the number of phenotypes accessible to an individual by mutation is smaller than the total number of phenotypes in the fitness landscape. These results provide a quantitative resolution to a significant ambiguity in evolutionary theory.