Causes and Consequences of Purifying Selection on SARS-CoV-2
Abstract Owing to a lag between a deleterious mutation’s appearance and its selective removal, gold-standard methods for mutation rate estimation assume no meaningful loss of mutations between parents and offspring. Indeed, from analysis of closely related lineages, in SARS-CoV-2, the Ka/Ks ratio wa...
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Published in | Genome biology and evolution Vol. 13; no. 10 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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England
Oxford University Press
01.10.2021
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Abstract | Abstract
Owing to a lag between a deleterious mutation’s appearance and its selective removal, gold-standard methods for mutation rate estimation assume no meaningful loss of mutations between parents and offspring. Indeed, from analysis of closely related lineages, in SARS-CoV-2, the Ka/Ks ratio was previously estimated as 1.008, suggesting no within-host selection. By contrast, we find a higher number of observed SNPs at 4-fold degenerate sites than elsewhere and, allowing for the virus’s complex mutational and compositional biases, estimate that the mutation rate is at least 49–67% higher than would be estimated based on the rate of appearance of variants in sampled genomes. Given the high Ka/Ks one might assume that the majority of such intrahost selection is the purging of nonsense mutations. However, we estimate that selection against nonsense mutations accounts for only ∼10% of all the “missing” mutations. Instead, classical protein-level selective filters (against chemically disparate amino acids and those predicted to disrupt protein functionality) account for many missing mutations. It is less obvious why for an intracellular parasite, amino acid cost parameters, notably amino acid decay rate, is also significant. Perhaps most surprisingly, we also find evidence for real-time selection against synonymous mutations that move codon usage away from that of humans. We conclude that there is common intrahost selection on SARS-CoV-2 that acts on nonsense, missense, and possibly synonymous mutations. This has implications for methods of mutation rate estimation, for determining times to common ancestry and the potential for intrahost evolution including vaccine escape. |
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AbstractList | Owing to a lag between a deleterious mutation's appearance and its selective removal, gold-standard methods for mutation rate estimation assume no meaningful loss of mutations between parents and offspring. Indeed, from analysis of closely related lineages, in SARS-CoV-2, the Ka/Ks ratio was previously estimated as 1.008, suggesting no within-host selection. By contrast, we find a higher number of observed SNPs at 4-fold degenerate sites than elsewhere and, allowing for the virus's complex mutational and compositional biases, estimate that the mutation rate is at least 49-67% higher than would be estimated based on the rate of appearance of variants in sampled genomes. Given the high Ka/Ks one might assume that the majority of such intrahost selection is the purging of nonsense mutations. However, we estimate that selection against nonsense mutations accounts for only ∼10% of all the "missing" mutations. Instead, classical protein-level selective filters (against chemically disparate amino acids and those predicted to disrupt protein functionality) account for many missing mutations. It is less obvious why for an intracellular parasite, amino acid cost parameters, notably amino acid decay rate, is also significant. Perhaps most surprisingly, we also find evidence for real-time selection against synonymous mutations that move codon usage away from that of humans. We conclude that there is common intrahost selection on SARS-CoV-2 that acts on nonsense, missense, and possibly synonymous mutations. This has implications for methods of mutation rate estimation, for determining times to common ancestry and the potential for intrahost evolution including vaccine escape. Abstract Owing to a lag between a deleterious mutation’s appearance and its selective removal, gold-standard methods for mutation rate estimation assume no meaningful loss of mutations between parents and offspring. Indeed, from analysis of closely related lineages, in SARS-CoV-2, the Ka/Ks ratio was previously estimated as 1.008, suggesting no within-host selection. By contrast, we find a higher number of observed SNPs at 4-fold degenerate sites than elsewhere and, allowing for the virus’s complex mutational and compositional biases, estimate that the mutation rate is at least 49–67% higher than would be estimated based on the rate of appearance of variants in sampled genomes. Given the high Ka/Ks one might assume that the majority of such intrahost selection is the purging of nonsense mutations. However, we estimate that selection against nonsense mutations accounts for only ∼10% of all the “missing” mutations. Instead, classical protein-level selective filters (against chemically disparate amino acids and those predicted to disrupt protein functionality) account for many missing mutations. It is less obvious why for an intracellular parasite, amino acid cost parameters, notably amino acid decay rate, is also significant. Perhaps most surprisingly, we also find evidence for real-time selection against synonymous mutations that move codon usage away from that of humans. We conclude that there is common intrahost selection on SARS-CoV-2 that acts on nonsense, missense, and possibly synonymous mutations. This has implications for methods of mutation rate estimation, for determining times to common ancestry and the potential for intrahost evolution including vaccine escape. |
Author | Mühlhausen, Stefanie Young, Bethan Rice, Alan M Watson, Samir Ho, Alexander T Mordstein, Christine Kudla, Grzegorz Hurst, Laurence D Morales, Atahualpa Castillo Cano, Laura |
AuthorAffiliation | 2 MRC Human Genetics Unit, Institute for Genetics and Molecular Medicine, The University of Edinburgh , United Kingdom 3 Department of Molecular Biology and Genetics, Aarhus University , Denmark 1 The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath , United Kingdom |
AuthorAffiliation_xml | – name: 2 MRC Human Genetics Unit, Institute for Genetics and Molecular Medicine, The University of Edinburgh , United Kingdom – name: 3 Department of Molecular Biology and Genetics, Aarhus University , Denmark – name: 1 The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath , United Kingdom |
Author_xml | – sequence: 1 givenname: Atahualpa Castillo surname: Morales fullname: Morales, Atahualpa Castillo organization: The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, United Kingdom – sequence: 2 givenname: Alan M surname: Rice fullname: Rice, Alan M organization: The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, United Kingdom – sequence: 3 givenname: Alexander T surname: Ho fullname: Ho, Alexander T organization: The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, United Kingdom – sequence: 4 givenname: Christine surname: Mordstein fullname: Mordstein, Christine organization: The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, United Kingdom – sequence: 5 givenname: Stefanie surname: Mühlhausen fullname: Mühlhausen, Stefanie organization: The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, United Kingdom – sequence: 6 givenname: Samir surname: Watson fullname: Watson, Samir organization: Department of Molecular Biology and Genetics, Aarhus University, Denmark – sequence: 7 givenname: Laura surname: Cano fullname: Cano, Laura organization: MRC Human Genetics Unit, Institute for Genetics and Molecular Medicine, The University of Edinburgh, United Kingdom – sequence: 8 givenname: Bethan surname: Young fullname: Young, Bethan organization: The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, United Kingdom – sequence: 9 givenname: Grzegorz surname: Kudla fullname: Kudla, Grzegorz organization: MRC Human Genetics Unit, Institute for Genetics and Molecular Medicine, The University of Edinburgh, United Kingdom – sequence: 10 givenname: Laurence D orcidid: 0000-0002-1002-1054 surname: Hurst fullname: Hurst, Laurence D email: l.d.hurst@bath.ac.uk organization: The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, United Kingdom |
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Cites_doi | 10.1007/PL00006381 10.1007/s00239-006-0206-8 10.1093/molbev/msz203 10.1093/molbev/msr170 10.1016/j.jmb.2019.04.021 10.1093/genetics/159.4.1779 10.1186/1471-2148-4-21 10.1016/j.cels.2020.03.001 10.1073/pnas.062526999 10.1093/molbev/msw048 10.1038/nrg.2016.104 10.18637/jss.v064.i04 10.1186/1471-2148-10-253 10.1073/pnas.1701670114 10.1038/nrg2413 10.7554/eLife.12735 10.5808/GI.2018.16.4.e28 10.1016/j.cell.2020.10.004 10.1093/nar/gku075 10.1128/JVI.01443-15 10.1093/molbev/mst010 10.1186/s12915-020-00870-9 10.1093/molbev/msl029 10.1093/ve/vez038 10.1016/j.jtbi.2005.08.037 10.1016/j.ijid.2020.08.066 10.1128/mSphere.00408-20 10.1038/2251025a0 10.1016/j.cell.2020.08.012 10.1101/2021.02.24.432721 10.1016/j.chaos.2020.110018 10.1093/molbev/msaa247 10.1016/j.cell.2020.04.011 10.1038/s41559-017-0425-y 10.1093/gbe/evab106 10.1016/j.virol.2020.12.018 10.1038/nature05137 10.1016/j.meegid.2011.02.018 10.5281/zenodo.3685264 10.1016/j.celrep.2021.108872 10.2807/1560-7917.ES.2017.22.13.30494 10.1093/nsr/nwaa036 10.1093/molbev/msq132 10.1109/MCSE.2011.37 10.1093/molbev/msaa188 10.1093/cid/ciaa203 10.1186/gb-2001-2-11-research0049 10.1371/journal.pgen.1002283 10.1093/molbev/msaa015 10.1093/bioinformatics/btq228 10.1016/j.meegid.2020.104351 10.1093/gbe/evab087 10.1093/molbev/msz003 10.1016/j.isci.2021.102116 10.1093/nar/gkq291 10.1038/s41559-020-1124-7 10.1093/ve/veaa032 10.1126/science.1155761 10.1038/nature14649 10.1073/pnas.2008281117 10.1007/BF02103132 10.1093/ve/veaa061 10.1126/science.290.5490.331 10.1093/nar/gkh834 10.1126/science.abg0821 10.1093/nar/18.19.5793 10.1128/mBio.01661-20 |
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Keywords | SARS-CoV-2 purifying selection mutation rate codon usage |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Atahualpa Castillo Morales, Alan M Rice and Alexander T Ho contributed equally to this work. Grzegorz Kudla and Laurence D. Hurst Co-senior authors. |
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References | Gu (2021101111442524700_evab196-B26) 2020; 6 Liu (2021101111442524700_evab196-B40) 2011; 11 Nekrutenko (2021101111442524700_evab196-B20) 2020 Genomic Epidemiology of Novel Coronavirus – Global Subsampling (2021101111442524700_evab196-B22) 2020 Graudenzi (2021101111442524700_evab196-B25) 2021; 24 Li (2021101111442524700_evab196-B39) 1985; 2 Long (2021101111442524700_evab196-B41) 2018; 2 Sukumaran (2021101111442524700_evab196-B64) 2010; 26 Bai (2021101111442524700_evab196-B5) 2020; 100 Goldman (2021101111442524700_evab196-B24) 1994; 11 Dunham (2021101111442524700_evab196-B16) 2021 De Maio (2021101111442524700_evab196-B11) 2021; 13 O’Fallon (2021101111442524700_evab196-B49) 2010; 27 Yang (2021101111442524700_evab196-B73) 2015; 523 Mordstein (2021101111442524700_evab196-B47) 2021 Ratcliff (2021101111442524700_evab196-B53) 2021; 556 Simmonds (2021101111442524700_evab196-B61) 2020; 11 Wong (2021101111442524700_evab196-B72) 2010; 10 Schwersensky (2021101111442524700_evab196-B57) 2020; 18 Alexaki (2021101111442524700_evab196-B3) 2019; 431 dos Reis (2021101111442524700_evab196-B14) 2004; 32 Fan (2021101111442524700_evab196-B17) 2015; 89 Hill (2021101111442524700_evab196-B51) 2020 Simmonds (2021101111442524700_evab196-B62) 2020; 5 Katoh (2021101111442524700_evab196-B32) 2013; 30 Kim (2021101111442524700_evab196-B34) 2020; 181 Freeland (2021101111442524700_evab196-B18) 1998; 47 Richmond (2021101111442524700_evab196-B55) 1970; 225 Rice (2021101111442524700_evab196-B54) 2021; 38 Dearlove (2021101111442524700_evab196-B12) 2020; 117 Tang (2021101111442524700_evab196-B66) 2020; 7 van Dorp (2021101111442524700_evab196-B68) 2020; 83 Gu (2021101111442524700_evab196-B27) 2019; 5 Lynch (2021101111442524700_evab196-B42) 2016; 17 Hurst (2021101111442524700_evab196-B31) 2006; 442 Shen (2021101111442524700_evab196-B58) 2020; 71 Kogay (2021101111442524700_evab196-B35) 2020; 11 Chen (2021101111442524700_evab196-B9) 2020; 4 Lanfear (2021101111442524700_evab196-B37) 2020 Shpaer (2021101111442524700_evab196-B59) 1990; 18 Mugal (2021101111442524700_evab196-B48) 2020; 37 Coleman (2021101111442524700_evab196-B10) 2008; 320 Ponting (2021101111442524700_evab196-B52) 2008; 9 Heizer (2021101111442524700_evab196-B29) 2006; 23 Yoon (2021101111442524700_evab196-B74) 2018; 16 Duchene (2021101111442524700_evab196-B15) 2020; 6 Keightley (2021101111442524700_evab196-B33) 2000; 290 Lythgoe (2021101111442524700_evab196-B43) 2021; 372 Haig (2021101111442524700_evab196-B28) 1991; 33 Weber (2021101111442524700_evab196-B70) 2019; 36 Banerjee (2021101111442524700_evab196-B6) 2020; 183 Hernandez-Alias (2021101111442524700_evab196-B30) 2021; 34 Delignette-Muller (2021101111442524700_evab196-B13) 2015; 64 Lapierre (2021101111442524700_evab196-B38) 2016; 33 Atkinson (2021101111442524700_evab196-B4) 2014; 42 Gaunt (2021101111442524700_evab196-B21) 2016; 5 Minh (2021101111442524700_evab196-B45) 2020; 37 Shu (2021101111442524700_evab196-B60) 2017; 22 Abascal (2021101111442524700_evab196-B1) 2010; 38 Wertheim (2021101111442524700_evab196-B71) 2011; 28 Pathan (2021101111442524700_evab196-B50) 2020; 138 Akashi (2021101111442524700_evab196-B2) 2002; 99 Kustin (2021101111442524700_evab196-B36) 2021; 38 Rocha (2021101111442524700_evab196-B56) 2006; 239 Starr (2021101111442524700_evab196-B63) 2020; 182 Tonkin-Hill (2021101111442524700_evab196-B67) 2021 2021101111442524700_evab196-B19 Bustamante (2021101111442524700_evab196-B7) 2001; 159 Mahmoudabadi (2021101111442524700_evab196-B44) 2017; 114 Swire (2021101111442524700_evab196-B65) 2007; 64 Charneski (2021101111442524700_evab196-B8) 2011; 7 Gilis (2021101111442524700_evab196-B23) 2001; 2 Zhao (2021101111442524700_evab196-B75) 2004; 4 Walt (2021101111442524700_evab196-B69) 2011; 13 Mordstein (2021101111442524700_evab196-B46) 2020; 10 |
References_xml | – volume: 47 start-page: 238 issue: 3 year: 1998 ident: 2021101111442524700_evab196-B18 article-title: The genetic code is one in a million publication-title: J Mol Evol doi: 10.1007/PL00006381 contributor: fullname: Freeland – volume: 64 start-page: 558 issue: 5 year: 2007 ident: 2021101111442524700_evab196-B65 article-title: Selection on synthesis cost affects interprotein amino acid usage in all three domains of life publication-title: J Mol Evol doi: 10.1007/s00239-006-0206-8 contributor: fullname: Swire – volume: 37 start-page: 260 issue: 1 year: 2020 ident: 2021101111442524700_evab196-B48 article-title: Polymorphism data assist estimation of the nonsynonymous over synonymous fixation rate ratio ω for closely related species publication-title: Mol Biol Evol doi: 10.1093/molbev/msz203 contributor: fullname: Mugal – volume: 28 start-page: 3355 issue: 12 year: 2011 ident: 2021101111442524700_evab196-B71 article-title: Purifying selection can obscure the ancient age of viral lineages publication-title: Mol Biol Evol doi: 10.1093/molbev/msr170 contributor: fullname: Wertheim – volume: 431 start-page: 2434 issue: 13 year: 2019 ident: 2021101111442524700_evab196-B3 article-title: Codon and codon-pair usage tables (CoCoPUTs): facilitating genetic variation analyses and recombinant gene design publication-title: J Mol Biol doi: 10.1016/j.jmb.2019.04.021 contributor: fullname: Alexaki – volume: 159 start-page: 1779 issue: 4 year: 2001 ident: 2021101111442524700_evab196-B7 article-title: Directional selection and the site-frequency spectrum publication-title: Genetics doi: 10.1093/genetics/159.4.1779 contributor: fullname: Bustamante – volume: 4 start-page: 21 year: 2004 ident: 2021101111442524700_evab196-B75 article-title: Moderate mutation rate in the SARS coronavirus genome and its implications publication-title: BMC Evol Biol doi: 10.1186/1471-2148-4-21 contributor: fullname: Zhao – volume: 10 start-page: 351 issue: 4 year: 2020 ident: 2021101111442524700_evab196-B46 article-title: Codon usage and splicing jointly influence mRNA localization publication-title: Cell Syst doi: 10.1016/j.cels.2020.03.001 contributor: fullname: Mordstein – volume: 99 start-page: 3695 issue: 6 year: 2002 ident: 2021101111442524700_evab196-B2 article-title: Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.062526999 contributor: fullname: Akashi – volume: 33 start-page: 1711 issue: 7 year: 2016 ident: 2021101111442524700_evab196-B38 article-title: The impact of selection, gene conversion, and biased sampling on the assessment of microbial demography publication-title: Mol Biol Evol doi: 10.1093/molbev/msw048 contributor: fullname: Lapierre – volume: 17 start-page: 704 issue: 11 year: 2016 ident: 2021101111442524700_evab196-B42 article-title: Genetic drift, selection and the evolution of the mutation rate publication-title: Nat Rev Genet doi: 10.1038/nrg.2016.104 contributor: fullname: Lynch – volume: 64 start-page: 1 issue: 4 year: 2015 ident: 2021101111442524700_evab196-B13 article-title: fitdistrplus: an R package for fitting distributions publication-title: J Stat Soft doi: 10.18637/jss.v064.i04 contributor: fullname: Delignette-Muller – volume: 10 start-page: 253 year: 2010 ident: 2021101111442524700_evab196-B72 article-title: Codon usage bias and the evolution of influenza A viruses. Codon usage biases of influenza virus publication-title: BMC Evol Biol doi: 10.1186/1471-2148-10-253 contributor: fullname: Wong – volume: 114 start-page: E4324 issue: 22 year: 2017 ident: 2021101111442524700_evab196-B44 article-title: Energetic cost of building a virus publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.1701670114 contributor: fullname: Mahmoudabadi – volume: 9 start-page: 689 issue: 9 year: 2008 ident: 2021101111442524700_evab196-B52 article-title: The functional repertoires of metazoan genomes publication-title: Nat Rev Genet doi: 10.1038/nrg2413 contributor: fullname: Ponting – volume: 5 start-page: e12735 year: 2016 ident: 2021101111442524700_evab196-B21 article-title: Elevation of CpG frequencies in influenza A genome attenuates pathogenicity but enhances host response to infection publication-title: Elife doi: 10.7554/eLife.12735 contributor: fullname: Gaunt – volume: 16 start-page: e28 issue: 4 year: 2018 ident: 2021101111442524700_evab196-B74 article-title: STADIUM: species-specific tRNA adaptive index compendium publication-title: Genomics Inform doi: 10.5808/GI.2018.16.4.e28 contributor: fullname: Yoon – volume: 183 start-page: 1325 issue: 5 year: 2020 ident: 2021101111442524700_evab196-B6 article-title: SARS-CoV-2 disrupts splicing, translation, and protein trafficking to suppress host defenses publication-title: Cell doi: 10.1016/j.cell.2020.10.004 contributor: fullname: Banerjee – volume: 42 start-page: 4527 issue: 7 year: 2014 ident: 2021101111442524700_evab196-B4 article-title: The influence of CpG and UpA dinucleotide frequencies on RNA virus replication and characterization of the innate cellular pathways underlying virus attenuation and enhanced replication publication-title: Nucleic Acids Res doi: 10.1093/nar/gku075 contributor: fullname: Atkinson – volume: 89 start-page: 10762 issue: 21 year: 2015 ident: 2021101111442524700_evab196-B17 article-title: Generation of live attenuated influenza virus by using codon usage bias publication-title: J Virol doi: 10.1128/JVI.01443-15 contributor: fullname: Fan – volume: 30 start-page: 772 issue: 4 year: 2013 ident: 2021101111442524700_evab196-B32 article-title: MAFFT multiple sequence alignment software version 7: improvements in performance and usability publication-title: Mol Biol Evol doi: 10.1093/molbev/mst010 contributor: fullname: Katoh – ident: 2021101111442524700_evab196-B19 – volume: 18 start-page: 146 issue: 1 year: 2020 ident: 2021101111442524700_evab196-B57 article-title: Large-scale in silico mutagenesis experiments reveal optimization of genetic code and codon usage for protein mutational robustness publication-title: BMC Biol doi: 10.1186/s12915-020-00870-9 contributor: fullname: Schwersensky – volume: 23 start-page: 1670 issue: 9 year: 2006 ident: 2021101111442524700_evab196-B29 article-title: Amino acid cost and codon-usage biases in 6 prokaryotic genomes: a whole-genome analysis publication-title: Mol Biol Evol doi: 10.1093/molbev/msl029 contributor: fullname: Heizer – year: 2021 ident: 2021101111442524700_evab196-B67 contributor: fullname: Tonkin-Hill – volume: 5 start-page: vez038 issue: 2 year: 2019 ident: 2021101111442524700_evab196-B27 article-title: Dinucleotide evolutionary dynamics in influenza A virus publication-title: Virus Evol doi: 10.1093/ve/vez038 contributor: fullname: Gu – volume: 2 start-page: 150 issue: 2 year: 1985 ident: 2021101111442524700_evab196-B39 article-title: A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes publication-title: Mol Biol Evol contributor: fullname: Li – year: 2020 ident: 2021101111442524700_evab196-B22 contributor: fullname: Genomic Epidemiology of Novel Coronavirus – Global Subsampling – volume: 239 start-page: 226 issue: 2 year: 2006 ident: 2021101111442524700_evab196-B56 article-title: Comparisons of dN/dS are time dependent for closely related bacterial genomes publication-title: J Theor Biol doi: 10.1016/j.jtbi.2005.08.037 contributor: fullname: Rocha – volume: 100 start-page: 164 year: 2020 ident: 2021101111442524700_evab196-B5 article-title: Comprehensive evolution and molecular characteristics of a large number of SARS-CoV-2 genomes reveal its epidemic trends publication-title: Int J Infect Dis doi: 10.1016/j.ijid.2020.08.066 contributor: fullname: Bai – volume: 5 start-page: e00408 year: 2020 ident: 2021101111442524700_evab196-B62 article-title: Rampant C -> U hypermutation in the genomes of SARS-CoV-2 and other coronaviruses: causes and consequences for their short- and long-term evolutionary trajectories publication-title: Msphere doi: 10.1128/mSphere.00408-20 contributor: fullname: Simmonds – volume: 225 start-page: 1025 issue: 5237 year: 1970 ident: 2021101111442524700_evab196-B55 article-title: Non-Darwinian evolution: a critique publication-title: Nature doi: 10.1038/2251025a0 contributor: fullname: Richmond – volume: 11 start-page: 725 year: 1994 ident: 2021101111442524700_evab196-B24 article-title: Codon-based model of nucleotide substitution for protein-coding DNA sequences publication-title: Mol Biol Evol contributor: fullname: Goldman – year: 2020 ident: 2021101111442524700_evab196-B51 article-title: Phylodynamic analysis of SARS-CoV-2 | Update 2020-03-06 publication-title: Virological. Edinburgh contributor: fullname: Hill – volume: 182 start-page: 1295 issue: 5 year: 2020 ident: 2021101111442524700_evab196-B63 article-title: Deep mutational scanning of SARS-CoV-2 receptor binding domain reveals constraints on folding and ACE2 binding publication-title: Cell doi: 10.1016/j.cell.2020.08.012 contributor: fullname: Starr – year: 2021 ident: 2021101111442524700_evab196-B16 doi: 10.1101/2021.02.24.432721 contributor: fullname: Dunham – volume: 138 start-page: 110018 year: 2020 ident: 2021101111442524700_evab196-B50 article-title: Time series prediction of COVID-19 by mutation rate analysis using recurrent neural network-based LSTM model publication-title: Chaos Solitons Fractals doi: 10.1016/j.chaos.2020.110018 contributor: fullname: Pathan – volume: 38 start-page: 575 issue: 2 year: 2021 ident: 2021101111442524700_evab196-B36 article-title: Biased mutation and selection in RNA viruses publication-title: Mol Biol Evol doi: 10.1093/molbev/msaa247 contributor: fullname: Kustin – volume: 181 start-page: 914 issue: 4 year: 2020 ident: 2021101111442524700_evab196-B34 article-title: The architecture of SARS-CoV-2 transcriptome publication-title: Cell doi: 10.1016/j.cell.2020.04.011 contributor: fullname: Kim – volume: 2 start-page: 237 issue: 2 year: 2018 ident: 2021101111442524700_evab196-B41 article-title: Evolutionary determinants of genome-wide nucleotide composition publication-title: Nat Ecol Evol doi: 10.1038/s41559-017-0425-y contributor: fullname: Long – year: 2021 ident: 2021101111442524700_evab196-B47 article-title: Transcription, mRNA export and immune evasion shape the codon usage of viruses publication-title: Genome Biol Evol doi: 10.1093/gbe/evab106 contributor: fullname: Mordstein – volume: 556 start-page: 62 year: 2021 ident: 2021101111442524700_evab196-B53 article-title: Potential APOBEC-mediated RNA editing of the genomes of SARS-CoV-2 and other coronaviruses and its impact on their longer term evolution publication-title: Virology doi: 10.1016/j.virol.2020.12.018 contributor: fullname: Ratcliff – volume: 11 start-page: e01206 year: 2020 ident: 2021101111442524700_evab196-B35 article-title: Selection for reducing energy cost of protein production drives the GC content and amino acid composition bias in gene transfer agents publication-title: Mbio contributor: fullname: Kogay – volume: 442 start-page: E11 issue: 7105 year: 2006 ident: 2021101111442524700_evab196-B31 article-title: Protein evolution: causes of trends in amino-acid gain and loss publication-title: Nature doi: 10.1038/nature05137 contributor: fullname: Hurst – volume: 11 start-page: 1168 issue: 5 year: 2011 ident: 2021101111442524700_evab196-B40 article-title: The characteristics of the synonymous codon usage in enterovirus 71 virus and the effects of host on the virus in codon usage pattern publication-title: Infect Genet Evol doi: 10.1016/j.meegid.2011.02.018 contributor: fullname: Liu – year: 2020 ident: 2021101111442524700_evab196-B20 doi: 10.5281/zenodo.3685264 contributor: fullname: Nekrutenko – volume: 34 start-page: 108872 issue: 11 year: 2021 ident: 2021101111442524700_evab196-B30 article-title: Translational adaptation of human viruses to the tissues they infect publication-title: Cell Rep doi: 10.1016/j.celrep.2021.108872 contributor: fullname: Hernandez-Alias – volume: 22 issue: 13 year: 2017 ident: 2021101111442524700_evab196-B60 article-title: GISAID: global initiative on sharing all influenza data – from vision to reality publication-title: Euro Surveill doi: 10.2807/1560-7917.ES.2017.22.13.30494 contributor: fullname: Shu – volume: 7 start-page: 1012 issue: 6 year: 2020 ident: 2021101111442524700_evab196-B66 article-title: On the origin and continuing evolution of SARS-CoV-2 publication-title: Natl Sci Rev doi: 10.1093/nsr/nwaa036 contributor: fullname: Tang – volume: 27 start-page: 2406 issue: 10 year: 2010 ident: 2021101111442524700_evab196-B49 article-title: A method to correct for the effects of purifying selection on genealogical inference publication-title: Mol Biol Evol doi: 10.1093/molbev/msq132 contributor: fullname: O’Fallon – volume: 13 start-page: 22 issue: 2 year: 2011 ident: 2021101111442524700_evab196-B69 article-title: The NumPy array: a structure for efficient numerical computation publication-title: Comput Sci Eng doi: 10.1109/MCSE.2011.37 contributor: fullname: Walt – volume: 38 start-page: 67 issue: 1 year: 2021 ident: 2021101111442524700_evab196-B54 article-title: Evidence for strong mutation bias towards, and selection against, U content in SARS-CoV-2: implications for vaccine design publication-title: Mol Biol Evol doi: 10.1093/molbev/msaa188 contributor: fullname: Rice – volume: 71 start-page: 713 issue: 15 year: 2020 ident: 2021101111442524700_evab196-B58 article-title: Genomic diversity of severe acute respiratory syndrome–coronavirus 2 in patients with coronavirus disease 2019 publication-title: Clin Infect Dis doi: 10.1093/cid/ciaa203 contributor: fullname: Shen – volume: 2 start-page: research0049 issue: 11 year: 2001 ident: 2021101111442524700_evab196-B23 article-title: Optimality of the genetic code with respect to protein stability and amino-acid frequencies publication-title: Genome Biol doi: 10.1186/gb-2001-2-11-research0049 contributor: fullname: Gilis – volume: 7 start-page: e1002283 issue: 9 year: 2011 ident: 2021101111442524700_evab196-B8 article-title: Atypical at skew in firmicute genomes results from selection and not from mutation publication-title: PLoS Genet doi: 10.1371/journal.pgen.1002283 contributor: fullname: Charneski – volume: 37 start-page: 1530 issue: 5 year: 2020 ident: 2021101111442524700_evab196-B45 article-title: IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era publication-title: Mol Biol Evol doi: 10.1093/molbev/msaa015 contributor: fullname: Minh – volume: 26 start-page: 1569 issue: 12 year: 2010 ident: 2021101111442524700_evab196-B64 article-title: DendroPy: a Python library for phylogenetic computing publication-title: Bioinformatics doi: 10.1093/bioinformatics/btq228 contributor: fullname: Sukumaran – volume: 83 start-page: 104351 year: 2020 ident: 2021101111442524700_evab196-B68 article-title: Emergence of genomic diversity and recurrent mutations in SARS-CoV-2 publication-title: Infect Genet Evol doi: 10.1016/j.meegid.2020.104351 contributor: fullname: van Dorp – volume: 13 issue: 5 year: 2021 ident: 2021101111442524700_evab196-B11 article-title: Mutation rates and selection on synonymous mutations in SARS-CoV-2 publication-title: Genome Biol Evol doi: 10.1093/gbe/evab087 contributor: fullname: De Maio – volume: 36 start-page: 679 issue: 4 year: 2019 ident: 2021101111442524700_evab196-B70 article-title: Physicochemical amino acid properties better describe substitution rates in large populations publication-title: Mol Biol Evol doi: 10.1093/molbev/msz003 contributor: fullname: Weber – volume: 24 start-page: 102116 issue: 2 year: 2021 ident: 2021101111442524700_evab196-B25 article-title: Mutational signatures and heterogeneous host response revealed via large-scale characterization of SARS-CoV-2 genomic diversity publication-title: Iscience doi: 10.1016/j.isci.2021.102116 contributor: fullname: Graudenzi – volume: 38 start-page: W7 issue: Web Server issue year: 2010 ident: 2021101111442524700_evab196-B1 article-title: TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations publication-title: Nucleic Acids Res doi: 10.1093/nar/gkq291 contributor: fullname: Abascal – volume: 4 start-page: 589 issue: 4 year: 2020 ident: 2021101111442524700_evab196-B9 article-title: Dissimilation of synonymous codon usage bias in virus-host coevolution due to translational selection publication-title: Nat Ecol Evol doi: 10.1038/s41559-020-1124-7 contributor: fullname: Chen – volume: 6 start-page: veaa032 issue: 1 year: 2020 ident: 2021101111442524700_evab196-B26 article-title: Multivariate analyses of codon usage of SARS-CoV-2 and other betacoronaviruses publication-title: Virus Evol doi: 10.1093/ve/veaa032 contributor: fullname: Gu – volume: 320 start-page: 1784 issue: 5884 year: 2008 ident: 2021101111442524700_evab196-B10 article-title: Virus attenuation by genome-scale changes in codon pair bias publication-title: Science doi: 10.1126/science.1155761 contributor: fullname: Coleman – volume: 523 start-page: 463 issue: 7561 year: 2015 ident: 2021101111442524700_evab196-B73 article-title: Parent-progeny sequencing indicates higher mutation rates in heterozygotes publication-title: Nature doi: 10.1038/nature14649 contributor: fullname: Yang – volume: 117 start-page: 23652 issue: 38 year: 2020 ident: 2021101111442524700_evab196-B12 article-title: A SARS-CoV-2 vaccine candidate would likely match all currently circulating variants publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.2008281117 contributor: fullname: Dearlove – volume: 33 start-page: 412 issue: 5 year: 1991 ident: 2021101111442524700_evab196-B28 article-title: A quantitative measure of error minimization in the genetic code publication-title: J Mol Evol doi: 10.1007/BF02103132 contributor: fullname: Haig – volume: 6 start-page: veaa061 issue: 2 year: 2020 ident: 2021101111442524700_evab196-B15 article-title: Temporal signal and the phylodynamic threshold of SARS-CoV-2 publication-title: Virus Evol doi: 10.1093/ve/veaa061 contributor: fullname: Duchene – volume: 290 start-page: 331 issue: 5490 year: 2000 ident: 2021101111442524700_evab196-B33 article-title: Deleterious mutations and the evolution of sex publication-title: Science doi: 10.1126/science.290.5490.331 contributor: fullname: Keightley – volume-title: A global phylogeny of SARS-CoV-2 sequences from GISAID year: 2020 ident: 2021101111442524700_evab196-B37 contributor: fullname: Lanfear – volume: 32 start-page: 5036 issue: 17 year: 2004 ident: 2021101111442524700_evab196-B14 article-title: Solving the riddle of codon usage preferences: a test for translational selection publication-title: Nucleic Acids Res doi: 10.1093/nar/gkh834 contributor: fullname: dos Reis – volume: 372 issue: 6539 year: 2021 ident: 2021101111442524700_evab196-B43 article-title: SARS-CoV-2 within-host diversity and transmission publication-title: Science doi: 10.1126/science.abg0821 contributor: fullname: Lythgoe – volume: 18 start-page: 5793 issue: 19 year: 1990 ident: 2021101111442524700_evab196-B59 article-title: Selection against Cpg dinucleotides in lentiviral genes – a possible role of methylation in regulation of viral expression publication-title: Nucleic Acids Res doi: 10.1093/nar/18.19.5793 contributor: fullname: Shpaer – volume: 11 start-page: e01661 issue: 6 year: 2020 ident: 2021101111442524700_evab196-B61 article-title: Pervasive RNA secondary structure in the genomes of SARS-CoV-2 and other coronaviruses publication-title: Mbio doi: 10.1128/mBio.01661-20 contributor: fullname: Simmonds |
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Owing to a lag between a deleterious mutation’s appearance and its selective removal, gold-standard methods for mutation rate estimation assume no... Owing to a lag between a deleterious mutation's appearance and its selective removal, gold-standard methods for mutation rate estimation assume no meaningful... Owing to a lag between a deleterious mutation’s appearance and its selective removal, gold-standard methods for mutation rate estimation assume no meaningful... |
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SubjectTerms | Codon Usage Codon, Nonsense COVID-19 - virology Evolution, Molecular Humans Models, Genetic Mutation Mutation Rate Mutation, Missense Polymorphism, Single Nucleotide SARS-CoV-2 - genetics Selection, Genetic Silent Mutation |
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Title | Causes and Consequences of Purifying Selection on SARS-CoV-2 |
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