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      Many human RNA viruses show extraordinarily stringent selective constraints on protein evolution

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          Significance

          The nonsynonymous substitutions ( d N)-to-synonymous substitutions ( d S) ratio in protein-coding genes is commonly used to study the mechanisms of gene evolution. To understand why RNA viruses show large variations in d N/ d S, we studied the d N/ d S ratios in 21 human RNA viruses, 8 human DNA viruses, and 17 mammals. Eighteen RNA viruses, but only 2 DNA viruses and no mammals, showed a genome-average d N/ d S < 0.10. Thus, many human RNA viruses exhibited extraordinarily stringent selective constraints on protein evolution. Our among-gene and among-species comparisons revealed that both positive selection and population size play significant roles in the d N/ d S variation among genes and species. This study clarified several controversial issues and increased our understanding of the mechanisms of RNA virus evolution.

          Abstract

          How negative selection, positive selection, and population size contribute to the large variation in nucleotide substitution rates among RNA viruses remains unclear. Here, we studied the ratios of nonsynonymous-to-synonymous substitution rates ( d N/ d S) in protein-coding genes of human RNA and DNA viruses and mammals. Among the 21 RNA viruses studied, 18 showed a genome-average d N/ d S from 0.01 to 0.10, indicating that over 90% of nonsynonymous mutations are eliminated by negative selection. Only HIV-1 showed a d N/ d S (0.31) higher than that (0.22) in mammalian genes. By comparing the d N/ d S values among genes in the same genome and among species or strains, we found that both positive selection and population size play significant roles in the d N/ d S variation among genes and species. Indeed, even in flaviviruses and picornaviruses, which showed the lowest ratios among the 21 species studied, positive selection appears to have contributed significantly to d N/ d S. We found the view that positive selection occurs much more frequently in influenza A subtype H3N2 than subtype H1N1 holds only for the hemagglutinin and neuraminidase genes, but not for other genes. Moreover, we found no support for the view that vector-borne RNA viruses have lower d N/ d S ratios than non–vector-borne viruses. In addition, we found a correlation between d N and d S, implying a correlation between d N and the mutation rate. Interestingly, only 2 of the 8 DNA viruses studied showed a d N/ d S < 0.10, while 4 showed a d N/ d S > 0.22. These observations increase our understanding of the mechanisms of RNA virus evolution.

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          Author and article information

          Journal
          Proc Natl Acad Sci U S A
          Proc. Natl. Acad. Sci. U.S.A
          pnas
          pnas
          PNAS
          Proceedings of the National Academy of Sciences of the United States of America
          National Academy of Sciences
          0027-8424
          1091-6490
          17 September 2019
          4 September 2019
          : 116
          : 38
          : 19009-19018
          Affiliations
          [1] aBiodiversity Research Center, Academia Sinica , 11529 Taipei, Taiwan
          [2] bCenter for Molecular Medicine and Genetics, School of Medicine, Wayne State University , Detroit, MI 48201;
          [3] cDepartment of Ecology and Evolution, University of Chicago , Chicago, IL 60637
          Author notes
          1To whom correspondence may be addressed. Email: ytseng@ 123456wayne.edu or whli@ 123456uchicago.edu .

          Contributed by Wen-Hsiung Li, August 6, 2019 (sent for review May 2, 2019; reviewed by Helen Piontkivska and Jianzhi Zhang)

          Author contributions: J.-J.L., Y.Y.T., and W.-H.L. designed research; J.-J.L., M.J.B., C.-P.Y., Y.Y.T., and W.-H.L. performed research; J.-J.L., M.J.B., C.-P.Y., Y.Y.T., and W.-H.L. analyzed data; and J.-J.L., Y.Y.T., and W.-H.L. wrote the paper.

          Reviewers: H.P., Kent State University; and J.Z., University of Michigan–Ann Arbor.

          Author information
          http://orcid.org/0000-0002-6806-9157
          Article
          PMC6754614 PMC6754614 6754614 201907626
          10.1073/pnas.1907626116
          6754614
          31484772
          dca0b6a2-596c-43b2-a255-8ef02954d4af
          Copyright @ 2019

          Published under the PNAS license.

          History
          Page count
          Pages: 10
          Categories
          Biological Sciences
          Evolution

          flaviviruses,picornaviruses,selective constraints,positive selection,influenza A viruses

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