1887

Abstract

Mosquito-borne arboviruses, including a diverse array of alphaviruses and flaviviruses, lead to hundreds of millions of human infections each year. Current methods for species-level classification of arboviruses adhere to guidelines prescribed by the International Committee on Taxonomy of Viruses (ICTV), and generally apply a polyphasic approach that might include information about viral vectors, hosts, geographical distribution, antigenicity, levels of DNA similarity, disease association and/or ecological characteristics. However, there is substantial variation in the criteria used to define viral species, which can lead to the establishment of artificial boundaries between species and inconsistencies when inferring their relatedness, variation and evolutionary history. In this study, we apply a single, uniform principle – that underlying the Biological Species Concept (BSC) – to define biological species of arboviruses based on recombination between genomes. Given that few recombination events have been documented in arboviruses, we investigate the incidence of recombination within and among major arboviral groups using an approach based on the ratio of homoplastic sites (recombinant alleles) to non-homoplastic sites (vertically transmitted alleles). This approach supports many ICTV-designations but also recognizes several cases in which a named species comprises multiple biological species. These findings demonstrate that this metric may be applied to all lifeforms, including viruses, and lead to more consistent and accurate delineation of viral species.

Funding
This study was supported by the:
  • Directorate for Biological Sciences (Award DEB-1831730)
    • Principle Award Recipient: HowardOchman
  • National Institute of General Medical Sciences (Award R35GM118038)
    • Principle Award Recipient: HowardOchman
  • Directorate for Biological Sciences (Award DEB-1551092)
    • Principle Award Recipient: NotApplicable
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/content/journal/jgv/10.1099/jgv.0.001572
2021-04-08
2021-10-28
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References

  1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW et al. The global distribution and burden of dengue. Nature 2013; 496:504–507 [View Article][PubMed]
    [Google Scholar]
  2. Vasilakis N, Gubler DJ. Arboviruses: Molecular Biology, Evolution and Control UK: Caister Academic Press. Poole; 2016
    [Google Scholar]
  3. Braack L, Gouveia de Almeida AP, Cornel AJ, Swanepoel R, de Jager C. Mosquito-Borne arboviruses of African origin: review of key viruses and vectors. Parasit Vectors 2018; 11:29 [View Article][PubMed]
    [Google Scholar]
  4. Chen C, Jiang D, Ni M, Li J, Chen Z et al. Phylogenomic analysis unravels evolution of yellow fever virus within hosts. PLoS Negl Trop Dis 2018; 12:e0006738 [View Article][PubMed]
    [Google Scholar]
  5. Halbach R, Junglen S, van Rij RP. Mosquito-specific and mosquito-borne viruses: evolution, infection, and host defense. Curr Opin Insect Sci 2017; 22:16–27 [View Article][PubMed]
    [Google Scholar]
  6. Simmonds P, Becher P, Bukh J, Gould EA, Meyers G et al. ICTV virus taxonomy profile: Flaviviridae. J Gen Virol 2017; 98:2–3 [View Article][PubMed]
    [Google Scholar]
  7. Kutchko KM, Madden EA, Morrison C, Plante KS, Sanders W et al. Structural divergence creates new functional features in alphavirus genomes. Nucleic Acids Res 2018; 46:3657–3670 [View Article][PubMed]
    [Google Scholar]
  8. Simmonds P, Adams MJ, Benkő M, Breitbart M, Brister JR et al. Consensus statement: virus taxonomy in the age of metagenomics. Nat Rev Microbiol 2017; 15:161–168 [View Article][PubMed]
    [Google Scholar]
  9. Lefkowitz EJ, Dempsey DM, Hendrickson RC, Orton RJ, Siddell SG et al. Virus taxonomy: the database of the International Committee on taxonomy of viruses (ICTV). Nucleic Acids Res 2018; 46:D708–D717 [View Article][PubMed]
    [Google Scholar]
  10. Adams MJ, Lefkowitz EJ, King AMQ, Carstens EB. Recently agreed changes to the International Code of virus classification and nomenclature. Arch Virol 2013; 158:2633–2639 [View Article][PubMed]
    [Google Scholar]
  11. Costa RL, Voloch CM, Schrago CG. Comparative evolutionary epidemiology of dengue virus serotypes. Infect Genet Evol 2012; 12:309–314 [View Article][PubMed]
    [Google Scholar]
  12. Henchal EA, Putnak JR. The dengue viruses. Clin Microbiol Rev 1990; 3:376–396 [View Article][PubMed]
    [Google Scholar]
  13. Shrivastava S, Tiraki D, Diwan A, Lalwani SK, Modak M et al. Co-circulation of all the four dengue virus serotypes and detection of a novel clade of DENV-4 (genotype I) virus in Pune, India during 2016 season. PLoS One 2018; 13:e0192672 [View Article][PubMed]
    [Google Scholar]
  14. Mayr E. The biological species concept. In Wheeler QD, Meier R. (editors) Species Concepts and Phylogenetic Theory: A Debate NY: Columbia University Press; 2000 pp 17–29
    [Google Scholar]
  15. Bobay L-M, Ochman H. Biological species are universal across Life’s domains. Genome Biol Evol 2017; 9:491–501
    [Google Scholar]
  16. Bobay L-M, O'Donnell AC, Ochman H. Recombination events are concentrated in the spike protein region of Betacoronaviruses. PLoS Genet 2020; 16:e1009272 [View Article][PubMed]
    [Google Scholar]
  17. Bobay L-M, Ochman H. Biological species in the viral world. Proc Natl Acad Sci U S A 2018; 115:6040–6045 [View Article][PubMed]
    [Google Scholar]
  18. Pérez-Losada M, Arenas M, Galán JC, Palero F, González-Candelas F. Recombination in viruses: mechanisms, methods of study, and evolutionary consequences. Infect Genet Evol 2015; 30:296–307 [View Article][PubMed]
    [Google Scholar]
  19. Aaskov J, Buzacott K, Field E, Lowry K, Berlioz-Arthaud A et al. Multiple recombinant dengue type 1 viruses in an isolate from a dengue patient. J Gen Virol 2007; 88:3334 [View Article][PubMed]
    [Google Scholar]
  20. Taucher C, Berger A, Mandl CW. A trans-complementing recombination trap demonstrates a low propensity of flaviviruses for intermolecular recombination. J Virol 2010; 84:599–611 [View Article][PubMed]
    [Google Scholar]
  21. Weaver SC, Costa F, Garcia-Blanco MA, Ko AI, Ribeiro GS et al. Zika virus: history, emergence, biology, and prospects for control. Antiviral Res 2016; 130:69–80 [View Article][PubMed]
    [Google Scholar]
  22. Holmes EC, Worobey M, Rambaut A. Phylogenetic evidence for recombination in dengue virus. Mol Biol Evol 1999; 16:405–409 [View Article][PubMed]
    [Google Scholar]
  23. Worobey M, Rambaut A, Holmes EC. Widespread intra-serotype recombination in natural populations of dengue virus. Proc Natl Acad Sci U S A 1999; 96:7352–7357 [View Article][PubMed]
    [Google Scholar]
  24. Pickett BE, Sadat EL, Zhang Y, Noronha JM, Squires RB et al. ViPR: an open bioinformatics database and analysis resource for virology research. Nucleic Acids Res 2012; 40:D593–D598 [View Article][PubMed]
    [Google Scholar]
  25. Bobay L-M, Ellis BS-H, Ochman H. ConSpeciFix: classifying prokaryotic species based on gene flow. Bioinformatics 2018; 34:3738–3740 [View Article][PubMed]
    [Google Scholar]
  26. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  27. Komsta L. Tests for outliers. https://CRAN.R-project.org/package=outliers ; 2011
  28. Slater GSC, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 2005; 6:31 [View Article][PubMed]
    [Google Scholar]
  29. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article][PubMed]
    [Google Scholar]
  30. Fall G, Di Paola N, Faye M, Dia M, Freire CCdeM et al. Biological and phylogenetic characteristics of West African lineages of West Nile virus. PLoS Negl Trop Dis 2017; 11:e0006078 [View Article][PubMed]
    [Google Scholar]
  31. Cadar D, Lühken R, van der Jeugd H, Garigliany M, Ziegler U et al. Widespread activity of multiple lineages of Usutu virus, Western Europe, 2016. Euro Surveill 2017; 22:30452 [View Article][PubMed]
    [Google Scholar]
  32. Engel D, Jöst H, Wink M, Börstler J, Bosch S et al. Reconstruction of the evolutionary history and dispersal of Usutu virus, a neglected emerging arbovirus in Europe and Africa. mBio 2016; 7:e01938–15 [View Article][PubMed]
    [Google Scholar]
  33. Roesch F, Fajardo A, Moratorio G, Vignuzzi M. Usutu virus: an arbovirus on the rise. Viruses 2019; 11:640 [View Article][PubMed]
    [Google Scholar]
  34. Gong Z, Xu X, Han G-Z. The diversification of Zika virus: are there two distinct lineages?. Genome Biol Evol 2017; 9:2940–2945 [View Article][PubMed]
    [Google Scholar]
  35. Pollett S, Melendrez MC, Maljkovic Berry I, Duchêne S, Salje H et al. Understanding dengue virus evolution to support epidemic surveillance and counter-measure development. Infect Genet Evol 2018; 62:279–295 [View Article][PubMed]
    [Google Scholar]
  36. Waman VP, Kolekar P, Ramtirthkar MR, Kale MM, Kulkarni-Kale U. Analysis of genotype diversity and evolution of dengue virus serotype 2 using complete genomes. PeerJ 2016b; 4:e2326 [View Article][PubMed]
    [Google Scholar]
  37. Waman VP, Kale MM, Kulkarni-Kale U. Genetic diversity and evolution of dengue virus serotype 3: a comparative genomics study. Infect Genet Evol 2017; 49:234–240 [View Article][PubMed]
    [Google Scholar]
  38. Waman VP, Kasibhatla SM, Kale MM, Kulkarni-Kale U. Population genomics of dengue virus serotype 4: insights into genetic structure and evolution. Arch Virol 2016a; 161:2133–2148 [View Article][PubMed]
    [Google Scholar]
  39. Beasley DWC, McAuley AJ, Bente DA. Yellow fever virus: genetic and phenotypic diversity and implications for detection, prevention and therapy. Antiviral Res 2015; 115:48–70 [View Article][PubMed]
    [Google Scholar]
  40. Chen R, Mukhopadhyay S, Merits A, Bolling B, Nasar F et al. ICTV virus taxonomy profile: Togaviridae. J Gen Virol 2018; 99:761–762 [View Article][PubMed]
    [Google Scholar]
  41. Arrigo NC, Adams AP, Weaver SC. Evolutionary patterns of eastern equine encephalitis virus in North versus South America suggest ecological differences and taxonomic revision. J Virol 2010b; 84:1014–1025 [View Article][PubMed]
    [Google Scholar]
  42. Lednicky JA, White SK, Mavian CN, El Badry MA, Telisma T et al. Emergence of Madariaga virus as a cause of acute febrile illness in children, Haiti, 2015-2016. PLoS Negl Trop Dis 2019; 13:e0006972 [View Article][PubMed]
    [Google Scholar]
  43. Bergren NA, Auguste AJ, Forrester NL, Negi SS, Braun WA et al. Western equine encephalitis virus: evolutionary analysis of a declining alphavirus based on complete genome sequences. J Virol 2014; 88:9260–9267 [View Article][PubMed]
    [Google Scholar]
  44. Ling J, Smura T, Lundström JO, Pettersson JH-O, Sironen T et al. Introduction and dispersal of Sindbis virus from central Africa to Europe. J Virol 2019; 93:e00620–19 [View Article][PubMed]
    [Google Scholar]
  45. Lundström JO, Pfeffer M. Phylogeographic structure and evolutionary history of Sindbis virus. Vector Borne Zoonotic Dis 2010; 10:889–907 [View Article][PubMed]
    [Google Scholar]
  46. Pickering P, Aaskov JG, Liu W. Complete genomic sequence of an Australian Sindbis virus isolated 44 years ago reveals unique indels in the E2 and NSP3 proteins. Microbiol Resour Announc 2019; 8:e00246–19 [View Article][PubMed]
    [Google Scholar]
  47. Schneider AdeB, Ochsenreiter R, Hostager R, Hofacker IL, Janies D et al. Updated phylogeny of Chikungunya virus suggests lineage-specific RNA architecture. Viruses 2019; 11:798 [View Article][PubMed]
    [Google Scholar]
  48. Gascuel O. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 1997; 14:685–695 [View Article][PubMed]
    [Google Scholar]
  49. Rambaut A, Grassly NC. Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comput Appl Biosci 1997; 13:235–238 [View Article][PubMed]
    [Google Scholar]
  50. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 2015; 1:vev003 [View Article][PubMed]
    [Google Scholar]
  51. Martin D, Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000; 16:562–563 [View Article][PubMed]
    [Google Scholar]
  52. Padidam M, Sawyer S, Fauquet CM. Possible emergence of new geminiviruses by frequent recombination. Virology 1999; 265:218–225 [View Article][PubMed]
    [Google Scholar]
  53. Martin DP, Posada D, Crandall KA, Williamson C. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 2005; 21:98–102 [View Article][PubMed]
    [Google Scholar]
  54. Smith JM. Analyzing the mosaic structure of genes. J Mol Evol 1992; 34:126–129 [View Article][PubMed]
    [Google Scholar]
  55. Posada D, Crandall KA. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 2001; 98:13757–13762 [View Article][PubMed]
    [Google Scholar]
  56. Gibbs MJ, Armstrong JS, Gibbs AJ. Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 2000; 16:573–582 [View Article][PubMed]
    [Google Scholar]
  57. Lam HM, Ratmann O, Boni MF. Improved algorithmic complexity for the 3SEQ recombination detection algorithm. Mol Biol Evol 2018; 35:247–251 [View Article][PubMed]
    [Google Scholar]
  58. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article][PubMed]
    [Google Scholar]
  59. Yu G, Smith DK, Zhu H, Guan Y, TTY L. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecol and Evol 2017; 8:28–36
    [Google Scholar]
  60. Pickett BE, Lefkowitz EJ. Recombination in West Nile virus: minimal contribution to genomic diversity. Virol J 2009; 6:165 [View Article][PubMed]
    [Google Scholar]
  61. Liu W, Pickering P, Duchêne S, Holmes EC, Aaskov JG. Highly divergent dengue virus type 2 in traveler returning from Borneo to Australia. Emerg Infect Dis 2016; 22:2146–2148 [View Article][PubMed]
    [Google Scholar]
  62. Beaver JT, Lelutiu N, Habib R, Skountzou I. Evolution of two major Zika virus lineages: implications for pathology, immune response, and vaccine development. Front Immunol 2018; 9:1640 [View Article][PubMed]
    [Google Scholar]
  63. Bryant JE, Holmes EC, Barrett ADT. Out of Africa: a molecular perspective on the introduction of yellow fever virus into the Americas. PLoS Pathog 2007; 3:e75 [View Article][PubMed]
    [Google Scholar]
  64. Nunes MRT, Palacios G, Cardoso JF, Martins LC, Sousa EC et al. Genomic and phylogenetic characterization of Brazilian yellow fever virus strains. J Virol 2012; 86:13263–13271 [View Article][PubMed]
    [Google Scholar]
  65. Twiddy SS, Holmes EC. The extent of homologous recombination in members of the genus flavivirus. J Gen Virol 2003; 84:429–440 [View Article][PubMed]
    [Google Scholar]
  66. McGee CE, Tsetsarkin KA, Guy B, Lang J, Plante K et al. Stability of yellow fever virus under recombinatory pressure as compared with Chikungunya virus. PLoS One 2011; 6:e23247 [View Article][PubMed]
    [Google Scholar]
  67. Arrigo NC, Adams AP, Watts DM, Newman PC, Weaver SC. Cotton rats and house sparrows as hosts for North and South American strains of eastern equine encephalitis virus. Emerg Infect Dis 2010a; 16:1373–1380 [View Article][PubMed]
    [Google Scholar]
  68. Carrera J-P, Forrester N, Wang E, Vittor AY, Haddow AD et al. Eastern equine encephalitis in Latin America. N Engl J Med 2013; 369:732–744 [View Article][PubMed]
    [Google Scholar]
  69. Vittor AY, Armien B, Gonzalez P, Carrera J-P, Dominguez C et al. Epidemiology of emergent madariaga encephalitis in a region with endemic Venezuelan equine encephalitis: initial host studies and human cross-sectional study in Darien, Panama. PLoS Negl Trop Dis 2016; 10:e0004554 [View Article][PubMed]
    [Google Scholar]
  70. Hahn CS, Lustig S, Strauss EG, Strauss JH. Western equine encephalitis virus is a recombinant virus. Proc Natl Acad Sci U S A 1988; 85:5997–6001 [View Article][PubMed]
    [Google Scholar]
  71. Weaver SC, Kang W, Shirako Y, Rumenapf T, Strauss EG et al. Recombinational history and molecular evolution of Western equine encephalomyelitis complex alphaviruses. J Virol 1997; 71:613–623 [View Article][PubMed]
    [Google Scholar]
  72. Chen R, Puri V, Fedorova N, Lin D, Hari KL et al. Comprehensive genome scale phylogenetic study provides new insights on the global expansion of Chikungunya virus. J Virol 2016; 90:10600–10611 [View Article][PubMed]
    [Google Scholar]
  73. Volk SM, Chen R, Tsetsarkin KA, Adams AP, Garcia TI et al. Genome-Scale phylogenetic analyses of Chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates. J Virol 2010; 84:6497–6504 [View Article][PubMed]
    [Google Scholar]
  74. Chuang CK, Chen WJ. Experimental evidence that RNA recombination occurs in the Japanese encephalitis virus. Virology 2009; 394:286–297 [View Article][PubMed]
    [Google Scholar]
  75. Twiddy SS, Holmes EC, Rambaut A. Inferring the rate and time-scale of dengue virus evolution. Mol Biol Evol 2003; 20:122–129 [View Article][PubMed]
    [Google Scholar]
  76. Wang E, Ni H, Xu R, Barrett AD, Watowich SJ et al. Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses. J Virol 2000; 74:3227–3234 [View Article][PubMed]
    [Google Scholar]
  77. Vasilakis N, Durbin AP, da Rosa APAT, Munoz-Jordan JL, Tesh RB et al. Antigenic relationships between sylvatic and endemic dengue viruses. Am J Trop Med Hyg 2008; 79:128–132[PubMed]
    [Google Scholar]
  78. Hadinegoro SR, Arredondo-García JL, Capeding MR, Deseda C, Chotpitayasunondh T et al. Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N Engl J Med 2015; 373:1195–1206 [View Article][PubMed]
    [Google Scholar]
  79. Villar L, Dayan GH, Arredondo-García JL, Rivera DM, Cunha R et al. Efficacy of a tetravalent dengue vaccine in children in Latin America. N Engl J Med 2015; 372:113–123 [View Article][PubMed]
    [Google Scholar]
  80. Filomatori CV, Bardossy ES, Merwaiss F, Suzuki Y, Henrion A et al. RNA recombination at Chikungunya virus 3'UTR as an evolutionary mechanism that provides adaptability. PLoS Pathog 2019; 15:e1007706 [View Article][PubMed]
    [Google Scholar]
  81. Langsjoen RM, Haller SL, Roy CJ, Vinet-Oliphant H, Bergren NA et al. Chikungunya virus strains show lineage-specific variations in virulence and cross-protective ability in murine and nonhuman primate models. mBio 2018; 9:e02449–17 [View Article][PubMed]
    [Google Scholar]
  82. Sieg M, Schmidt V, Ziegler U, Keller M, Höper D et al. Outbreak and cocirculation of three different Usutu virus strains in eastern Germany. Vector Borne Zoonotic Dis 2017; 17:662–664 [View Article][PubMed]
    [Google Scholar]
  83. Strauss EG, Rice CM, Strauss JH. Complete nucleotide sequence of the genomic RNA of Sindbis virus. Virol 1984; 133:92–110 [View Article][PubMed]
    [Google Scholar]
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