Philadelphia, PA, USA. Organisms with an optimal level of robustness against the effects of mutation maintains the phenotype in one environment but also allows adaptation to environmental change. The seemingly contradictory co-existence has posed a conundrum to evolutionary biologists.

"Biologists have long wondered how can organisms be robust and also adaptable," said Joshua B. Plotkin, assistant professor in the Department of Biology at the University of Pennsylvania. "After all, robust things don't change, so how can an organism be robust against mutation but also be prepared to adapt when the environment changes? It has always seemed like an enigma."

Robustness is a measure of how genetic mutations affect an organism's phenotype, or the set of physical traits, behaviors and features shaped by evolution. It would seem to be the opposite of evolvability, preventing a population from adapting to environmental change.

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Using an original mathematical model, researchers demonstrated that mutational robustness can either impede or facilitate adaptation depending on the population size, the mutation rate and a measure of the reproductive capabilities of a variety of genotypes, called the fitness landscape.

The results provide a quantitative understanding of the relationship between robustness and evolvability, clarify a significant ambiguity in evolutionary theory and should help illuminate outstanding problems in molecular and experimental evolution, evolutionary development and protein engineering.

The key insight behind this counterintuitive finding is that neutral mutations can set the stage for future, beneficial adaptation. Specifically, researchers found that more robust populations are faster to adapt when the effects of neutral and beneficial mutations are intertwined. Neutral mutations do not impact the phenotype, but they may influence the effects of subsequent mutations in beneficial ways.

To quantify this idea, the study's authors created a general mathematical model of gene interactions and their effects on an organism's phenotype. When the researchers analyzed the model, they found that populations with intermediate levels of robustness were the fastest to adapt to novel environments. These adaptable populations balanced genetic diversity and the rate of phenotypically penetrant mutations to optimally explore the range of possible phenotypes.

The researchers also used computer simulations to check their result under many alternative versions of the basic model. Although there is not yet sufficient data to test these theoretical results in nature, the authors simulated the evolution of RNA molecules, confirming that their theoretical results could predict the rate of adaptation.

CitationMutational robustness can facilitate adaptation. Jeremy A. Draghi, Todd L. Parsons, Günter P. Wagner and Joshua B. Plotkin. Nature 2010; 463(7279): 353-355. doi:10.1038/nature08694

Abstract

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 suggested. However, other studies contend that robust organisms are more adaptable. 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.

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