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      From Molecular Genetics to Phylodynamics: Evolutionary Relevance of Mutation Rates Across Viruses

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      PLoS Pathogens

      Public Library of Science

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Although evolution is a multifactorial process, theory posits that the speed of molecular evolution should be directly determined by the rate at which spontaneous mutations appear. To what extent these two biochemical and population-scale processes are related in nature, however, is largely unknown. Viruses are an ideal system for addressing this question because their evolution is fast enough to be observed in real time, and experimentally-determined mutation rates are abundant. This article provides statistically supported evidence that the mutation rate determines molecular evolution across all types of viruses. Properties of the viral genome such as its size and chemical composition are identified as major determinants of these rates. Furthermore, a quantitative analysis reveals that, as expected, evolution rates increase linearly with mutation rates for slowly mutating viruses. However, this relationship plateaus for fast mutating viruses. A model is proposed in which deleterious mutations impose an evolutionary speed limit and set an extinction threshold in nature. The model is consistent with data from replication kinetics, selection strength and chemical mutagenesis studies.

          Author Summary

          Viruses are an excellent system for addressing the evolutionary implications of mutation because their mutation rates vary by orders of magnitude, and their evolution takes place within the time frame of human observation. Theory posits a direct relationship between these two processes, but this has rarely been tested empirically. This work shows that evolution rates in nature correlate with experimentally-determined mutation rates for the major viral groups, and identifies key genome properties determining these rates. Current theory allows us to predict evolution rates accurately for slowly-mutating viruses but fails for the fastest mutating viruses. To solve this limitation, a model in which deleterious mutations play a key evolutionary role is proposed.

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          Most cited references 28

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          The neutral theory of molecular evolution.

           M. Kimura (1979)
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            Time-dependent rates of molecular evolution.

            For over half a century, it has been known that the rate of morphological evolution appears to vary with the time frame of measurement. Rates of microevolutionary change, measured between successive generations, were found to be far higher than rates of macroevolutionary change inferred from the fossil record. More recently, it has been suggested that rates of molecular evolution are also time dependent, with the estimated rate depending on the timescale of measurement. This followed surprising observations that estimates of mutation rates, obtained in studies of pedigrees and laboratory mutation-accumulation lines, exceeded long-term substitution rates by an order of magnitude or more. Although a range of studies have provided evidence for such a pattern, the hypothesis remains relatively contentious. Furthermore, there is ongoing discussion about the factors that can cause molecular rate estimates to be dependent on time. Here we present an overview of our current understanding of time-dependent rates. We provide a summary of the evidence for time-dependent rates in animals, bacteria and viruses. We review the various biological and methodological factors that can cause rates to be time dependent, including the effects of natural selection, calibration errors, model misspecification and other artefacts. We also describe the challenges in calibrating estimates of molecular rates, particularly on the intermediate timescales that are critical for an accurate characterization of time-dependent rates. This has important consequences for the use of molecular-clock methods to estimate timescales of recent evolutionary events. © 2011 Blackwell Publishing Ltd.
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              A constant rate of spontaneous mutation in DNA-based microbes.

               W Drake (1991)
              In terms of evolution and fitness, the most significant spontaneous mutation rate is likely to be that for the entire genome (or its nonfrivolous fraction). Information is now available to calculate this rate for several DNA-based haploid microbes, including bacteriophages with single- or double-stranded DNA, a bacterium, a yeast, and a filamentous fungus. Their genome sizes vary by approximately 6500-fold. Their average mutation rates per base pair vary by approximately 16,000-fold, whereas their mutation rates per genome vary by only approximately 2.5-fold, apparently randomly, around a mean value of 0.0033 per DNA replication. The average mutation rate per base pair is inversely proportional to genome size. Therefore, a nearly invariant microbial mutation rate appears to have evolved. Because this rate is uniform in such diverse organisms, it is likely to be determined by deep general forces, perhaps by a balance between the usually deleterious effects of mutation and the physiological costs of further reducing mutation rates.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Pathog
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                May 2012
                May 2012
                3 May 2012
                : 8
                : 5
                Affiliations
                Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, Paterna, Valencia, Spain
                North Carolina State University, United States of America
                Author notes

                Conceived and designed the experiments: RS. Performed the experiments: RS. Analyzed the data: RS. Contributed reagents/materials/analysis tools: RS. Wrote the paper: RS.

                Article
                PPATHOGENS-D-12-00282
                10.1371/journal.ppat.1002685
                3342999
                22570614
                Rafael Sanjuán. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 5
                Categories
                Research Article
                Biology
                Evolutionary Biology
                Evolutionary Genetics
                Population Genetics
                Microbiology
                Microbial Mutation
                Virology

                Infectious disease & Microbiology

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