title: Natural selection fails to optimize mutation rates for long-term adaptation on rugged fitness landscapes.
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.
authors.affiliation: Department of Computer Science and Engineering, Michigan State University, East Lansing, Michigan, United States of America. jclune@msu.edu
authors.forename: Jeff
authors.initials: J
authors.lastname: Clune
authors.forename: Dusan
authors.initials: D
authors.lastname: Misevic
authors.forename: Charles
authors.initials: C
authors.lastname: Ofria
authors.forename: Richard E
authors.initials: RE
authors.lastname: Lenski
authors.forename: Santiago F
authors.initials: SF
authors.lastname: Elena
authors.forename: Rafael
authors.initials: R
authors.lastname: Sanjuán
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D005075:Biological Evolution; D019295:Computational Biology; D003198:Computer Simulation; D008957:Models, Genetic; D009154:Mutation; D012641:Selection, Genetic; D013997:Time Factors