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Robustness and adaptability in evolving viral populations

Viruses are everywhere. They infect every organism on the planet, including the bacteria that inhabit our gut. Their numbers are unfathomable: a handful of soil contains nearly one billion viral particles, and the majority of DNA from seawater belongs to viruses. Influenza A alone infects one fifth of the human population every year. Even our own genome is littered with the remains of extinct retro-viruses.

Despite their ubiquity, viruses have historically received little attention from evolutionary biologists. In part, this neglect reflects the egocentricism of scientific inquiry. But theorists also eschew viruses because they present highly atypical evolutionary scenarios. Viruses are bound by the same constraints that shape the evolution of higher organisms: the need to replicate with fidelity and adapt to local environments. And viral proteins are governed by the same physical laws that determine folding and functionality in higher organisms. But viruses are often subject to genetic mutations and environmental changes at rates that vastly exceed those of all other living organisms. As a result, the persistence of viruses presents an extraordinary enigma: How can a viral population achieve both sufficient robustness against high mutation rates, as well as sufficient plasticity to adapt to rapidly changing environments? On the one hand, a viral population must purge itself of deleterious mutants; but at the same time it must be prepared to leverage genetic diversity in order to escape a host’s immune system.

We propose that the unique aspects of viral evolution are best studied as emergent prop- erties of a self-organized population of naive agents. After all, the enigmatic questions of robustness and adaptability do not concern individual viral genotypes, but rather the viral population as a whole. Although these questions are fascinating from the perspective of evolu- tionary theory and complex systems, they are not of academic interest alone. The emergence and persistence of some of the world’s most devastating viruses