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We take computational and biophysical approaches to study how enzymes catalyze reactions and how allosteric signals are transmitted within and between proteins. We use directed evolution techniques to examine the emergence and resilience of functional protein motions during genetic drift. We investigate the consequences of altering biophysical properties in the context of living systems using high-throughput genetic screens. These approaches are revealing extensive parallels that scale from systems biology to atomic mechanisms in how we understand genetic non-additivity (epistasis), buffering, and robustness.