1887

Abstract

In recent years, the notion of co-speciation between species and their hosts was discarded in favour of a more likely explanation: preferential host switching. However, the relative importance of this last process in shaping the evolutionary history of hantaviruses remains uncertain, given the present limited knowledge not only of virus–host relationships but also of the pathogen and reservoir phylogenies. In South America, more than 25 hantavirus genotypes were detected; several of them act as aetiological agents of hantavirus pulmonary syndrome (HPS). An understanding of the diversity of hantaviruses and of the processes underlying host switching is critical since human cases of HPS are almost exclusively the result of human–host interactions. In this study, we tested if preferential host switching is the main process driving hantavirus diversification in South America, by performing a co-phylogenetic analysis of the viruses and their primary hosts. We also suggest a new level of amino acid divergence to define virus species in the group. Our results indicate that preferential host switching would not be the main process driving virus diversification. The historical geographical proximity among rodent hosts emerges as an alternative hypothesis to be tested.

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2015-09-01
2019-12-06
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References

  1. Agrellos R. , Bonvicino C.R. , Travassos da Rosa E.S. , Marques A.A.R. , D'Andrea O.S. , Weksler M. . ( 2012;). The taxonomic status of the Castelo dos Sonhos hantavirus reservoir, Oligoryzomys utiaritensis Allen 1916 (Rodentia: Cricetidae: Sigmodontinae). Zootaxa 3220: 1–28.
    [Google Scholar]
  2. Almeida F.C. , Bonvicino C.R. , Cordeiro-Estrela P. . ( 2007;). Phylogeny and temporal diversification of Calomys (Rodentia, Sigmodontinae): implications for the biogeography of an endemic genus of the open/dry biomes of South America. Mol Phylogenet Evol 42: 449–466 [CrossRef] [PubMed].
    [Google Scholar]
  3. Arai S. , Bennett S.N. , Sumibcay L. , Cook J.A. , Song J.W. , Hope A. , Parmenter C. , Nerurkar V.R. , Yates T.L. , Yanagihara R. . ( 2008;). Phylogenetically distinct hantaviruses in the masked shrew (Sorex cinereus) and dusky shrew (Sorex monticolus) in the United States. Am J Trop Med Hyg 78: 348–351 [PubMed].
    [Google Scholar]
  4. Bohlman M.C. , Morzunov S.P. , Meissner J. , Taylor M.B. , Ishibashi K. , Rowe J. , Levis S. , Enria D. , St Jeor S.C. . ( 2002;). Analysis of hantavirus genetic diversity in Argentina: S segment-derived phylogeny. J Virol 76: 3765–3773 [CrossRef] [PubMed].
    [Google Scholar]
  5. Cabrera A.L. , Willink A. . ( 1973;). Biogeografía de América Latina Biology Series, Monograph no. 13 Washington: OEA;.
    [Google Scholar]
  6. Carbajo A.E. , Teta P. . ( 2009;). Distribution of the hantavirus reservoir Oligoryzomys nigripes in Argentina: choosing spatial models for the actual and potential distribution of the black-footed colilargo. Mammalia 73: 313–321 [CrossRef].
    [Google Scholar]
  7. Charleston M.A. . ( 1998;). Jungles: a new solution to the host/parasite phylogeny reconciliation problem. Math Biosci 149: 191–223 [CrossRef] [PubMed].
    [Google Scholar]
  8. Charleston M.A. , Robertson D.L. . ( 2002;). Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Syst Biol 51: 528–535 [CrossRef] [PubMed].
    [Google Scholar]
  9. Chu Y.K. , Owen R.D. , Gonzalez L.M. , Jonsson C.B. . ( 2003;). The complex ecology of hantavirus in Paraguay. Am J Trop Med Hyg 69: 263–268 [PubMed].
    [Google Scholar]
  10. Chu Y.K. , Milligan B. , Owen R.D. , Goodin D.G. , Jonsson C.B. . ( 2006;). Phylogenetic and geographical relationships of hantavirus strains in eastern and western Paraguay. Am J Trop Med Hyg 75: 1127–1134 [PubMed].
    [Google Scholar]
  11. Coyne J.A. , Orr H.A. . ( 2004;). Speciation Sunderland, MA: Sinauer Associates;.
    [Google Scholar]
  12. Cruz C.D. , Forshey B.M. , Vallejo E. , Agudo R. , Vargas J. , Blazes D.L. , Guevara C. , Laguna-Torres V.A. , Halsey E.S. , Kochel T.J. . ( 2012;). Novel strain of Andes virus associated with fatal human infection, central Bolivia. Emerg Infect Dis 18: 750–757 [PubMed].[CrossRef]
    [Google Scholar]
  13. D'Elía G. , Pardiñas U.F. , Jayat J.P. , Salazar-Bravo J. . ( 2008;). Systematics of Necromys (Rodentia, Cricetidae, Sigmodontinae): species limits and groups, with comments on historical biogeography. J Mammal 89: 778–790 [CrossRef].
    [Google Scholar]
  14. de Oliveira R.C. , Padula P.J. , Gomes R. , Martinez V.P. , Bellomo C. , Bonvicino C.R. , Freire e Lima D.I. , Bragagnolo C. , Caldas A.C.S. , other authors . ( 2011;). Genetic characterization of hantaviruses associated with sigmodontine rodents in an endemic area for hantavirus pulmonary syndrome in southern Brazil. Vector Borne Zoonotic Dis 11: 301–314 [CrossRef] [PubMed].
    [Google Scholar]
  15. de Oliveira R.C. , Guterres A. , Schrago C.G. , Fernandes J. , Teixeira B.R. , Zeccer S. , Bonvicino C.R. , D'Andrea P.S. , de Lemos E.R.S. . ( 2012;). Detection of the first incidence of Akodon paranaensis naturally infected with the Jabora virus strain (Hantavirus) in Brazil. Mem Inst Oswaldo Cruz 107: 424–428 [CrossRef] [PubMed].
    [Google Scholar]
  16. Delfraro A. , Tomé L. , D'Elía G. , Clara M. , Achával F. , Russi J.C. , Arbiza Rodonz J.R. . ( 2008;). Juquitiba-like hantavirus from 2 nonrelated rodent species, Uruguay. Emerg Infect Dis 14: 1447–1451 [CrossRef] [PubMed].
    [Google Scholar]
  17. Figueiredo L.T.M. , Moreli M.L. , de-Sousa R.L.M. , Borges A.A. , de-Figueiredo G.G. , Machado A.M. , Bisordi I. , Nagasse-Sugahara T.K. , Suzuki A. , other authors . ( 2009;). Hantavirus pulmonary syndrome, central plateau, southeastern, and southern Brazil. Emerg Infect Dis 15: 561–567 [CrossRef] [PubMed].
    [Google Scholar]
  18. Firth C. , Tokarz R. , Simith D.B. , Nunes M.R.T. , Bhat M. , Rosa E.S. , Medeiros D.B.A. , Palacios G. , Vasconcelos P.F.C. , Lipkin W.I. . ( 2012;). Diversity and distribution of hantaviruses in South America. J Virol 86: 13756–13766 [CrossRef] [PubMed].
    [Google Scholar]
  19. Fulhorst C.F. , Monroe M.C. , Salas R.A. , Duno G. , Utrera A. , Ksiazek T.G. , Nichol S.T. , de Manzione N.M.C. , Tovar D. , Tesh R.B. . ( 1997;). Isolation, characterization and geographic distribution of Caño Delgadito virus, a newly discovered South American hantavirus (family Bunyaviridae). Virus Res 51: 159–171 [CrossRef] [PubMed].
    [Google Scholar]
  20. Goloboff P. , Farris S. , Nixon K. . ( 2008;). tnt, a free program for phylogenetic analysis. Cladistics 24: 774–786 [CrossRef].
    [Google Scholar]
  21. González-Ittig R.E. , Salazar-Bravo J. , Barquez R.M. , Gardenal C.N. . ( 2010;). Phylogenetic relationships among species of the genus Oligoryzomys (Rodentia, Cricetidae) from Central and South America. Zool Scr 39: 511–526 [CrossRef].
    [Google Scholar]
  22. González-Ittig R.E. , Rivera P.C. , Levis S.C. , Calderón G.E. , Gardenal C.N. . ( 2014;). The molecular phylogenetics of the genus Oligoryzomys (Rodentia: Cricetidae) clarifies rodent host–hantavirus associations. Zool J Linn Soc 171: 457–474 [CrossRef].
    [Google Scholar]
  23. Haag T. , Muschner V.C. , Freitas L.B. , Oliveira L.F.B. , Langguth A.R. , Mattevi M.S. . ( 2007;). Phylogenetic relationships among species of the genus Calomys with emphasis on South American lowland taxa. J Mammal 88: 769–776 [CrossRef].
    [Google Scholar]
  24. Hanson J.D. , Utrera A. , Fulhorst C.F. . ( 2011;). The delicate pygmy rice rat (Oligoryzomys delicatus) is the principal host of Maporal virus (family Bunyaviridae, genus Hantavirus). Vector Borne Zoonotic Dis 11: 691–696 [CrossRef] [PubMed].
    [Google Scholar]
  25. Hjelle B. , Torres-Pérez F. . ( 2010;). Hantaviruses in the Americas and their role as emerging pathogens. Viruses 2: 2559–2586 [CrossRef] [PubMed].
    [Google Scholar]
  26. Hughes A.L. , Friedman R. . ( 2000;). Evolutionary diversification of protein-coding genes of hantaviruses. Mol Biol Evol 17: 1558–1568 [CrossRef] [PubMed].
    [Google Scholar]
  27. Jackson A.P. , Charleston M.A. . ( 2004;). A cophylogenetic perspective of RNA-virus evolution. Mol Biol Evol 21: 45–57 [CrossRef] [PubMed].
    [Google Scholar]
  28. Johnson A.M. , Bowen M.D. , Ksiazek T.G. , Williams R.J. , Bryan R.T. , Mills J.N. , Peters C.J. , Nichol S.T. . ( 1997;). Laguna Negra virus associated with HPS in western Paraguay and Bolivia. Virology 238: 115–127 [CrossRef] [PubMed].
    [Google Scholar]
  29. Johnson A.M. , de Souza L.T.M. , Ferreira I.B. , Pereira L.E. , Ksiazek T.G. , Rollin P.E. , Peters C.J. , Nichol S.T. . ( 1999;). Genetic investigation of novel hantaviruses causing fatal HPS in Brazil. J Med Virol 59: 527–535 [CrossRef] [PubMed].
    [Google Scholar]
  30. Kumar S. , Tamura K. , Nei M. . ( 2004;). mega3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150–163 [CrossRef] [PubMed].
    [Google Scholar]
  31. Levis S. , Morzunov S.P. , Rowe J.E. , Enría D. , Pini N. , Calderón G. , Sabattini M. , St Jeor S.C. . ( 1998;). Genetic diversity and epidemiology of hantaviruses in Argentina. J Infect Dis 177: 529–538 [CrossRef] [PubMed].
    [Google Scholar]
  32. Levis S. , García J. , Pini N. , Calderón G. , Ramírez J. , Bravo D. , St Jeor S. , Ripoll C. , Bego M. , other authors . ( 2004;). Hantavirus pulmonary syndrome in northwestern Argentina: circulation of Laguna Negra virus associated with Calomys callosus . Am J Trop Med Hyg 71: 658–663 [PubMed].
    [Google Scholar]
  33. Londoño A.F. , Díaz F.J. , Agudelo-Flórez P. , Levis S. , Rodas J.D. . ( 2011;). Genetic evidence of hantavirus infections in wild rodents from northwestern Colombia. Vector Borne Zoonotic Dis 11: 701–708 [CrossRef] [PubMed].
    [Google Scholar]
  34. López N. , Padula P. , Rossi C. , Lázaro M.E. , Franze-Fernández M.T. . ( 1996;). Genetic identification of a new hantavirus causing severe pulmonary syndrome in Argentina. Virology 220: 223–226 [CrossRef] [PubMed].
    [Google Scholar]
  35. Maes P. , Klempa B. , Clement J. , Matthijnssens J. , Gajdusek D.C. , Krüger D.H. , Van Ranst M. . ( 2009;). A proposal for new criteria for the classification of hantaviruses, based on S and M segment protein sequences. Infect Genet Evol 9: 813–820 [CrossRef] [PubMed].
    [Google Scholar]
  36. Matheus S. , Lavergne A. , de Thoisy B. , Dussart P. , Lacoste V. . ( 2012;). Complete genome sequence of a novel hantavirus variant of Rio Mamoré virus. Maripa virus, from French Guiana. J Virol 86: 5399 [CrossRef] [PubMed].
    [Google Scholar]
  37. Medeiros D.B.A. , da Rosa E.S. , Marques A. , Simith D.B. , Carneiro A.R. , Chiang J.O. , Prazeres I.T.E. , Vasconcelos P.F.C. , Nunes M.R.T. . ( 2010;). Circulation of hantaviruses in the influence area of the Cuiabá-Santarém Highway. Mem Inst Oswaldo Cruz 105: 665–671 [CrossRef] [PubMed].
    [Google Scholar]
  38. Melo-Silva C.R. , Maranhão A.Q. , Nagasse-Sugahara T.K. , Bisordi I. , Suzuki A. , Brigido M.M. . ( 2009;). Characterization of hantaviruses circulating in Central Brazil. Infect Genet Evol 9: 241–247 [CrossRef] [PubMed].
    [Google Scholar]
  39. Mendes W.S. , Aragão N.J.L. , Santos H.J. , Raposo L. , Vasconcelos P.F.C. , Rosa E.S. , Elkhoury M.R. . ( 2001;). Hantavirus pulmonary syndrome in Anajatuba, Maranhão, Brazil. Rev Inst Med Trop Sao Paulo 43: 237–240 [CrossRef] [PubMed].
    [Google Scholar]
  40. Miller M.A. , Pfeiffer W. , Schwartz T. . ( 2010;). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. . In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November, 2010, pp. 1–8 New Orleans, LA: IEEE Publisher.
    [Google Scholar]
  41. Mills J.N. , Ksiazek T.G. , Peters C.J. , Childs J.E. . ( 1999;). Long-term studies of hantavirus reservoir populations in the southwestern United States: a synthesis. Emerg Infect Dis 5: 135–142 [CrossRef] [PubMed].
    [Google Scholar]
  42. Musser G.G. , Carleton M.D. . ( 2005;). Superfamily Muroidea. . In Mammal Species of the World: a Taxonomic and Geographic Reference vol. 2 , 3rd edn.., pp. 894–1531. Edited by Wilson D. E. , Reeder D. M. . Baltimore, MD: Johns Hopkins University Press;.
    [Google Scholar]
  43. Nelson R. , Cañate R. , Pascale J.M. , Dragoo J.W. , Armien B. , Armien A.G. , Koster F. . ( 2010;). Confirmation of Choclo virus as the cause of hantavirus cardiopulmonary syndrome and high serum antibody prevalence in Panama. J Med Virol 82: 1586–1593 [CrossRef] [PubMed].
    [Google Scholar]
  44. Padula P. , Figueroa R. , Navarrete M. , Pizarro E. , Cádiz R. , Bellomo C. , Jofre C. , Zaror L. , Rodriguez E. , Murúa R. . ( 2004;). Transmission study of Andes hantavirus infection in wild sigmodontine rodents. J Virol 78: 11972–11979 [CrossRef] [PubMed].
    [Google Scholar]
  45. Padula P. , Martinez V.P. , Bellomo C. , Maidana S. , San Juan J. , Tagliaferri P. , Bargardi S. , Vazquez C. , Colucci N. , other authors . ( 2007;). Pathogenic hantaviruses, northeastern Argentina and eastern Paraguay. Emerg Infect Dis 13: 1211–1214 [CrossRef] [PubMed].
    [Google Scholar]
  46. Plyusnin A. , Morzunov S.P. . ( 2001;). Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr Top Microbiol Immunol 256: 47–75 [PubMed].
    [Google Scholar]
  47. Plyusnin A. , Vapalahti O. , Vaheri A. . ( 1996;). Hantaviruses: genome structure, expression and evolution. J Gen Virol 77: 2677–2687 [CrossRef] [PubMed].
    [Google Scholar]
  48. Plyusnin A. , Beaty B.J. , Elliott R.M. , Goldbach R. , Kormelink R. , Lundkvist Å. , Schmaljohn C.S. , Tesh R.B. . ( 2012;). Bunyaviridae. In Virus Taxonomy: Classification and Nomenclature of Viruses – Ninth Report of the International Committee on Taxonomy of Viruses, pp. 725–741. Edited by King A. M. Q. , Adams M. J. , Carstens E. B. , Lefkowitz E. J. . San Diego, CA: Elsevier;.
    [Google Scholar]
  49. Posada D. . ( 2008;). jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253–1256 [CrossRef] [PubMed].
    [Google Scholar]
  50. Raboni S.M. , Probst C.M. , Bordignon J. , Zeferino A. , dos Santos C.N. . ( 2005;). Hantaviruses in central South America: phylogenetic analysis of the S segment from HPS cases in Paraná, Brazil. J Med Virol 76: 553–562 [CrossRef] [PubMed].
    [Google Scholar]
  51. Raboni S.M. , Hoffmann F.G. , Oliveira R.C. , Teixeira B.R. , Bonvicino C.R. , Stella V. , Carstensen S. , Bordignon J. , D'Andrea P.S. , other authors . ( 2009;). Phylogenetic characterization of hantaviruses from wild rodents and hantavirus pulmonary syndrome cases in the state of Parana (southern Brazil). J Gen Virol 90: 2166–2171 [CrossRef] [PubMed].
    [Google Scholar]
  52. Rambaut A. , Drummond A.J. . ( 2007;). Tracer, Version 1.5., Oxford: University of Oxford; http://tree.bio.ed.ac.uk/software/tracer/.
    [Google Scholar]
  53. Ramsden C. , Melo F.L. , Figueiredo L.M. , Holmes E.C. , Zanotto P.M.A. , Consortium VGDN . ( 2008;). High rates of molecular evolution in hantaviruses. Mol Biol Evol 25: 1488–1492 [CrossRef] [PubMed].
    [Google Scholar]
  54. Ramsden C. , Holmes E.C. , Charleston M.A. . ( 2009;). Hantavirus evolution in relation to its rodent and insectivore hosts: no evidence for codivergence. Mol Biol Evol 26: 143–153 [CrossRef] [PubMed].
    [Google Scholar]
  55. Ronquist F. , Teslenko M. , van der Mark P. , Ayres D.L. , Darling A. , Höhna S. , Larget B. , Liu L. , Suchard M.A. , Huelsenbeck J.P. . ( 2012;). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61: 539–542 [CrossRef] [PubMed].
    [Google Scholar]
  56. Rosa E.S. , Mills J.N. , Padula P.J. , Elkhoury M.R. , Ksiazek T.G. , Mendes W.S. , Santos E.D. , Araújo G.C.B. , Martinez V.P. , other authors . ( 2005;). Newly recognized hantaviruses associated with hantavirus pulmonary syndrome in northern Brazil: partial genetic characterization of viruses and serologic implication of likely reservoirs. Vector Borne Zoonotic Dis 5: 11–19 [CrossRef] [PubMed].
    [Google Scholar]
  57. Song J.W. , Baek L.J. , Schmaljohn C.S. , Yanagihara R. . ( 2007;). Thottapalayam virus, a prototype shrewborne hantavirus. Emerg Infect Dis 13: 980–985 [CrossRef] [PubMed].
    [Google Scholar]
  58. Steppan S. , Adkins R. , Anderson J. . ( 2004;). Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol 53: 533–553 [CrossRef] [PubMed].
    [Google Scholar]
  59. Toro J. , Vega J.D. , Khan A.S. , Mills J.N. , Padula P. , Terry W. , Yadón Z. , Valderrama R. , Ellis B.A. , other authors . ( 1998;). An outbreak of hantavirus pulmonary syndrome, Chile, 1997. Emerg Infect Dis 4: 687–694 [CrossRef] [PubMed].
    [Google Scholar]
  60. Travassos da Rosa E.S. , Sampaio de Lemos E.R. , de Almeida Medeiros D.B. , Simith D.B. , de Souza Pereira A. , Elkhoury M.R. , Mendes W.S. , Vidigal J.R.B. , de Oliveira R.C. , other authors . ( 2010;). Hantaviruses and hantavirus pulmonary syndrome, Maranhao, Brazil. Emerg Infect Dis 16: 1952–1955 [CrossRef] [PubMed].
    [Google Scholar]
  61. Travassos da Rosa E.S. , Medeiros D.B.A. , Nunes M.R.T. , Simith D.B. , de Souza Pereira A. , Elkhoury M.R. , Lavocat M. , Marques A.A.R. , Via A.V. , other authors . ( 2011;). Pygmy rice rat as potential host of Castelo dos Sonhos hantavirus. Emerg Infect Dis 17: 1527–1530 [CrossRef] [PubMed].
    [Google Scholar]
  62. Travassos da Rosa E.S. , Medeiros D.B.A. , Nunes M.R.T. , Simith D.B. , Pereira A.S. , Elkhoury M.R. , Santos E.D. , Lavocat M. , Marques A.A. , other authors . ( 2012;). Molecular epidemiology of Laguna Negra virus, Mato Grosso State, Brazil. Emerg Infect Dis 18: 982–985 [CrossRef] [PubMed].
    [Google Scholar]
  63. Upham N.S. , Patterson B.D. . ( 2012;). Diversification and biogeography of the neotropical caviomorph lineage Octodontoidea (Rodentia: Hystricognathi). Mol Phylogenet Evol 63: 417–429 [CrossRef] [PubMed].
    [Google Scholar]
  64. Vasconcelos M.I. , Lima V.P. , Iversson L.B. , Rosa M.D.B. , da Rosa A.P. , da Rosa E.S. , Pereira L.E. , Nassar E. , Katz G. , other authors . ( 1997;). Hantavirus pulmonary syndrome in the rural area of Juquitiba, São Paulo metropolitan area, Brazil. Rev Inst Med Trop Sao Paulo 39: 237–238 [PubMed].
    [Google Scholar]
  65. Vincent M.J. , Quiroz E. , Gracia F. , Sanchez A.J. , Ksiazek T.G. , Kitsutani P.T. , Ruedas L.A. , Tinnin D.S. , Caceres L. , other authors . ( 2000;). Hantavirus pulmonary syndrome in Panama: identification of novel hantaviruses and their likely reservoirs. Virology 277: 14–19 [CrossRef] [PubMed].
    [Google Scholar]
  66. Wiens J.J. . ( 2006;). Missing data and the design of phylogenetic analyses. J Biomed Inform 39: 34–42 [CrossRef] [PubMed].
    [Google Scholar]
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