Abstract

Mutational (genetic) robustness is phenotypic constancy in the face of mutational changes to the genome. Robustness is critical to the understanding of evolution because phenotypically expressed genetic variation is the fuel of natural selection. Nonetheless, the evidence for adaptive evolution of mutational robustness in biological populations is controversial. Robustness should be selectively favored when mutation rates are high, a common feature of RNA viruses. However, selection for robustness may be relaxed under virus co-infection because complementation between virus genotypes can buffer mutational effects. We therefore hypothesized that selection for genetic robustness in viruses will be weakened with increasing frequency of co-infection. To test this idea, we used populations of RNA phage φ6 that were experimentally evolved at low and high levels of co-infection and subjected lineages of these viruses to mutation accumulation through population bottlenecking. The data demonstrate that viruses evolved under high co-infection show relatively greater mean magnitude and variance in the fitness changes generated by addition of random mutations, confirming our hypothesis that they experience weakened selection for robustness. Our study further suggests that co-infection of host cells may be advantageous to RNA viruses only in the short term. In addition, we observed higher mutation frequencies in the more robust viruses, indicating that evolution of robustness might foster less-accurate genome replication in RNA viruses.

Highlights

  • Mutational robustness can be defined as constancy of phenotype in the face of mutational perturbation [1]

  • Evolution of genetic robustness is hard to observe in most laboratory systems because equilibrium states are difficult to achieve and the benefit of mutational robustness is not experienced until offspring carrying mutations arise [2]

  • The inherently high error rates in genome replication occurring in RNA viruses make them an obvious choice for examining the adaptive evolution of mutational robustness

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Summary

Introduction

Mutational (genetic) robustness can be defined as constancy of phenotype in the face of mutational perturbation [1]. Robustness is crucial to the understanding of evolution because it dictates phenotypic expression of genetic variation [2] It remains unclear whether robustness is merely accidental or a consequence of natural selection. Evolution of genetic robustness is hard to observe in most laboratory systems because equilibrium states are difficult to achieve (or definitively prove) and the benefit of mutational robustness is not experienced until offspring carrying mutations arise [2]. For these reasons, the evidence for adaptive evolution of mutational robustness in biological populations remains controversial [3,4,5]. The vast majority of studies demonstrating the phenomenon have relied on theory [6] or artificial life systems [7]

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