Proceedings of the Royal Society B: Biological Sciences
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Robustness and evolvability: a paradox resolved

Andreas Wagner

*Author and address for correspondence: Department of Biochemistry, University of Zurich, Building Y27-J-54, Winterthurerstrasse 190, 8057 Zurich, Switzerland (

E-mail Address: [email protected]

)

Andreas Wagner

Department of Biochemistry, University of Zurich8057 Zurich, Switzerland

The Santa Fe InstituteSanta Fe, NM 87501, USA

Swiss Institute of Bioinformatics4056 Basel, Switzerland

[email protected]

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    Understanding the relationship between robustness and evolvability is key to understand how living things can withstand mutations, while producing ample variation that leads to evolutionary innovations. Mutational robustness and evolvability, a system's ability to produce heritable variation, harbour a paradoxical tension. On one hand, high robustness implies low production of heritable phenotypic variation. On the other hand, both experimental and computational analyses of neutral networks indicate that robustness enhances evolvability. I here resolve this tension using RNA genotypes and their secondary structure phenotypes as a study system. To resolve the tension, one must distinguish between robustness of a genotype and a phenotype. I confirm that genotype (sequence) robustness and evolvability share an antagonistic relationship. In stark contrast, phenotype (structure) robustness promotes structure evolvability. A consequence is that finite populations of sequences with a robust phenotype can access large amounts of phenotypic variation while spreading through a neutral network. Population-level processes and phenotypes rather than individual sequences are key to understand the relationship between robustness and evolvability. My observations may apply to other genetic systems where many connected genotypes produce the same phenotypes.

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