Natural Selection Fails to Optimize Mutation Rates for Long-Term Adaptation on Rugged Fitness Landscapes

Santiago F. Elena,Richard E. Lenski,Laurence D. Hurst,Rafael Sanjuán,Jeff Clune,Dusan Misevic,Charles Ofria

doi:10.1371/journal.pcbi.1000187

Abstract

The rate of mutation is central to evolution. Mutations are required for adaptation, yet most mutations with phenotypic effects are deleterious. As a consequence, the mutation rate that maximizes adaptation will be some intermediate value. Here, we used digital organisms to investigate the ability of natural selection to adjust and optimize mutation rates. We assessed the optimal mutation rate by empirically determining what mutation rate produced the highest rate of adaptation. Then, we allowed mutation rates to evolve, and we evaluated the proximity to the optimum. Although we chose conditions favorable for mutation rate optimization, the evolved rates were invariably far below the optimum across a wide range of experimental parameter settings. We hypothesized that the reason that mutation rates evolved to be suboptimal was the ruggedness of fitness landscapes. To test this hypothesis, we created a simplified landscape without any fitness valleys and found that, in such conditions, populations evolved near-optimal mutation rates. In contrast, when fitness valleys were added to this simple landscape, the ability of evolving populations to find the optimal mutation rate was lost. We conclude that rugged fitness landscapes can prevent the evolution of mutation rates that are optimal for long-term adaptation. This finding has important implications for applied evolutionary research in both biological and computational realms.

Highlights

Mutation is the ultimate source of genetic variation, and the rate at which spontaneous mutations appear is a fundamental evolutionary parameter
We use digital organisms to analyze the ability of evolving populations to optimize their mutation rate, a fundamental evolutionary parameter
We show that when the mutation rate is constrained to be high, populations adapt considerably faster over the long term than when the mutation rate is allowed to evolve

Summary

Introduction

Mutation is the ultimate source of genetic variation, and the rate at which spontaneous mutations appear is a fundamental evolutionary parameter. Most mutations with phenotypic effects are deleterious, producing a genetic load that favors organisms with low mutation rates; on the other hand, beneficial mutations are necessary for adaptation. Given this trade-off between genetic load and adaptation, there should exist an intermediate mutation rate—hereafter referred to as the ‘optimal’ rate, or Uopt—that balances these forces and maximizes adaptation over the longterm [6,7,8,9]. The costs of genetic load are continuously paid in the short-term, whereas the payoffs of adaptation come in the long-term [6,7,8,10,11,12]

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Conclusion