Purifying Selection Can Obscure the Ancient Age of Viral Lineages

Abstract Statistical methods for molecular dating of viral origins have been used extensively to infer the time of most common recent ancestor for many rapidly evolving pathogens. However, there are a number of cases, in which epidemiological, historical, or genomic evidence suggests much older viral origins than those obtained via molecular dating. We demonstrate how pervasive purifying selection can mask the ancient origins of recently sampled pathogens, in part due to the inability of nucleotide-based substitution models to properly account for complex patterns of spatial and temporal variability in selective pressures. We use codon-based substitution models to infer the length of branches in viral phylogenies; these models produce estimates that are often considerably longer than those obtained with traditional nucleotide-based substitution models. Correcting the apparent underestimation of branch lengths suggests substantially older origins for measles, Ebola, and avian influenza viruses. This work helps to reconcile some of the inconsistencies between molecular dating and other types of evidence concerning the age of viral lineages.

[1]  W. Mcneill Plagues and Peoples , 1977, The Review of Politics.

[2]  Sergei L. Kosakovsky Pond,et al.  HyPhy: hypothesis testing using phylogenies , 2005, Bioinform..

[3]  Sergei L. Kosakovsky Pond,et al.  Adaptation to Different Human Populations by HIV-1 Revealed by Codon-Based Analyses , 2006, PLoS Comput. Biol..

[4]  Jeffery K. Taubenberger,et al.  Characterization of the 1918 influenza virus polymerase genes , 2005, Nature.

[5]  M. Woodhams Can deleterious mutations explain the time dependency of molecular rate estimates? , 2006, Molecular biology and evolution.

[6]  S. Muse,et al.  A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. , 1994, Molecular biology and evolution.

[7]  Edward C Holmes,et al.  Avian influenza virus exhibits rapid evolutionary dynamics. , 2006, Molecular biology and evolution.

[8]  S. Tavaré Some probabilistic and statistical problems in the analysis of DNA sequences , 1986 .

[9]  E. Holmes,et al.  Bayesian Estimates of the Evolutionary Rate and Age of Hepatitis B Virus , 2007, Journal of Molecular Evolution.

[10]  T. Gojobori,et al.  The origin and evolution of Ebola and Marburg viruses. , 1997, Molecular biology and evolution.

[11]  Z. Yang,et al.  Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. , 1998, Molecular biology and evolution.

[12]  R. Shafer,et al.  A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution , 2008, Proceedings of the National Academy of Sciences.

[13]  P. Sharp,et al.  Evidence for two independent domestications of cattle. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Edward C. Holmes,et al.  Patterns of Intra- and Interhost Nonsynonymous Variation Reveal Strong Purifying Selection in Dengue Virus , 2003, Journal of Virology.

[15]  N. Goldman,et al.  A codon-based model of nucleotide substitution for protein-coding DNA sequences. , 1994, Molecular biology and evolution.

[16]  L. Real,et al.  Wave-Like Spread of Ebola Zaire , 2005, PLoS biology.

[17]  O. Pybus,et al.  Bayesian coalescent inference of past population dynamics from molecular sequences. , 2005, Molecular biology and evolution.

[18]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[19]  M. Worobey,et al.  Point, counterpoint: The evolution of pathogenic viruses and their human hosts , 2007 .

[20]  L. Goatley,et al.  The genome sequence of the virulent Kabete 'O' strain of rinderpest virus: comparison with the derived vaccine. , 1996, The Journal of general virology.

[21]  Andrew Rambaut,et al.  Pacing a small cage: mutation and RNA viruses , 2008, Trends in Ecology & Evolution.

[22]  K. Tang,et al.  A quick fuse and the emergence of Taura syndrome virus. , 2009, Virology.

[23]  C. Hon,et al.  Evidence of the Recombinant Origin of a Bat Severe Acute Respiratory Syndrome (SARS)-Like Coronavirus and Its Implications on the Direct Ancestor of SARS Coronavirus , 2007, Journal of Virology.

[24]  V. Volchkov,et al.  GP mRNA of Ebola virus is edited by the Ebola virus polymerase and by T7 and vaccinia virus polymerases. , 1995, Virology.

[25]  E. Holmes,et al.  Hitchhiking and the Population Genetic Structure of Avian Influenza Virus , 2009, Journal of Molecular Evolution.

[26]  T. Percival On the Small-Pox and Measles , 2013 .

[27]  H. Philippe,et al.  A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. , 2004, Molecular biology and evolution.

[28]  P. Roques,et al.  Island Biogeography Reveals the Deep History of SIV , 2010, Science.

[29]  S. Muse,et al.  Site-to-site variation of synonymous substitution rates. , 2005, Molecular biology and evolution.

[30]  Allan C. Wilson,et al.  Mitochondrial DNA sequences of primates: Tempo and mode of evolution , 2005, Journal of Molecular Evolution.

[31]  Joel O. Wertheim,et al.  Dating the Age of the SIV Lineages That Gave Rise to HIV-1 and HIV-2 , 2009, PLoS Comput. Biol..

[32]  Ø. Skare,et al.  Improved Sampling‐Importance Resampling and Reduced Bias Importance Sampling , 2003 .

[33]  Marc A. Suchard,et al.  Many-core algorithms for statistical phylogenetics , 2009, Bioinform..

[34]  A. Katzourakis,et al.  Endogenous Viral Elements in Animal Genomes , 2010, PLoS genetics.

[35]  C. Seoighe,et al.  Frequent Toggling between Alternative Amino Acids Is Driven by Selection in HIV-1 , 2008, PLoS pathogens.

[36]  Anne-Mieke Vandamme,et al.  Genetic Variability and Molecular Evolution of the Human Respiratory Syncytial Virus Subgroup B Attachment G Protein , 2005, Journal of Virology.

[37]  E. Holmes,et al.  Rates of evolutionary change in viruses: patterns and determinants , 2008, Nature Reviews Genetics.

[38]  Arnold J. Levine,et al.  Unexpected Inheritance: Multiple Integrations of Ancient Bornavirus and Ebolavirus/Marburgvirus Sequences in Vertebrate Genomes , 2010, PLoS pathogens.

[39]  C. Feschotte,et al.  Genomic Fossils Calibrate the Long-Term Evolution of Hepadnaviruses , 2010, PLoS biology.

[40]  D. Perkins,et al.  Fauna of �atal H�y�k: Evidence for Early Cattle Domestication in Anatolia , 1969, Science.

[41]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[42]  S. Jeffery Evolution of Protein Molecules , 1979 .

[43]  A. Sanchez,et al.  The virion glycoproteins of Ebola viruses are encoded in two reading frames and are expressed through transcriptional editing. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[44]  T. Pupko,et al.  A combined empirical and mechanistic codon model. , 2006, Molecular biology and evolution.

[45]  Konrad Scheffler,et al.  Evolutionary fingerprinting of genes. , 2010, Molecular biology and evolution.

[46]  Alexei J Drummond,et al.  Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. , 2006, Molecular biology and evolution.

[47]  J. Wertheim The Re-Emergence of H1N1 Influenza Virus in 1977: A Cautionary Tale for Estimating Divergence Times Using Biologically Unrealistic Sampling Dates , 2010, PloS one.

[48]  E. Holmes,et al.  The Evolutionary and Epidemiological Dynamics of the Paramyxoviridae , 2008, Journal of Molecular Evolution.

[49]  Alexei J Drummond,et al.  Phylogenetic evidence for deleterious mutation load in RNA viruses and its contribution to viral evolution. , 2007, Molecular biology and evolution.

[50]  M. Emerman,et al.  Paleovirology—Modern Consequences of Ancient Viruses , 2010, PLoS biology.

[51]  Steven Wolinsky,et al.  Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960 , 2008, Nature.

[52]  S. Sawyer,et al.  Two-stepping through time: mammals and viruses. , 2011, Trends in microbiology.

[53]  H. Munro,et al.  Mammalian protein metabolism , 1964 .

[54]  M. Worobey,et al.  Relaxed Selection and the Evolution of RNA Virus Mucin-Like Pathogenicity Factors , 2009, Journal of Virology.

[55]  C H Woelk,et al.  Immune and artificial selection in the haemagglutinin (H) glycoprotein of measles virus. , 2001, The Journal of general virology.

[56]  W. Fitch,et al.  Effects of passage history and sampling bias on phylogenetic reconstruction of human influenza A evolution. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  James E. Byers,et al.  MODEL SELECTION IN PHYLOGENETICS , 2005 .

[58]  J. Rolleston The History of the Acute Exanthemata , 1937, The Indian Medical Gazette.

[59]  W. Bellini,et al.  Comparison of sequences of the H, F, and N coding genes of measles virus vaccine strains. , 1994, Virus research.

[60]  H. Oshitani,et al.  Origin of measles virus: divergence from rinderpest virus between the 11th and 12th centuries , 2010, Virology Journal.

[61]  T. Jukes CHAPTER 24 – Evolution of Protein Molecules , 1969 .

[62]  T. Gojobori,et al.  Endogenous non-retroviral RNA virus elements in mammalian genomes , 2010, Nature.

[63]  M. Zvelebil,et al.  A model of directional selection applied to the evolution of drug resistance in HIV-1. , 2007, Molecular biology and evolution.

[64]  Jeremy Bruenn,et al.  Filoviruses are ancient and integrated into mammalian genomes , 2010, BMC Evolutionary Biology.

[65]  Z. Yang,et al.  Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. , 1993, Molecular biology and evolution.

[66]  Edward C. Holmes,et al.  Molecular Clocks and the Puzzle of RNA Virus Origins , 2003, Journal of Virology.

[67]  W. Moss Measles Control and the Prospect of Eradication , 2009, Current topics in microbiology and immunology.

[68]  Alexei J Drummond,et al.  Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. , 2005, Molecular biology and evolution.

[69]  M. Nei,et al.  A new method of inference of ancestral nucleotide and amino acid sequences. , 1995, Genetics.

[70]  O. Pybus,et al.  Macroevolution of Complex Retroviruses , 2009, Science.

[71]  O. Pybus,et al.  Increased positive selection pressure in persistent (SSPE) versus acute measles virus infections. , 2002, The Journal of general virology.

[72]  Daniel J. Wilson,et al.  Evolution of the Human Immunodeficiency Virus Envelope Gene Is Dominated by Purifying Selection , 2006, Genetics.

[73]  F. Black,et al.  Measles endemicity in insular populations: critical community size and its evolutionary implication. , 1966, Journal of theoretical biology.

[74]  R. May,et al.  Plagues and peoples , 2006, IUBMB life.

[75]  P. Taberlet,et al.  The origin of European cattle: evidence from modern and ancient DNA. , 2006, Proceedings of the National Academy of Sciences of the United States of America.