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Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography

Pathogen Molecular Biology and Biochemistry Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK¹
Institut Pasteur de Dakar, Dakar, Senegal²
Unité de Virus Emergents, Faculté de Médecine, Boulevard Jean Moulin, 13005 Marseille, France³
Wellcome Trust Centre for the Epidemiology of Infectious Disease, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3FY, UK⁴
Centre for Ecology and Hydrology (formerly Institute of Virology and Environmental Microbiology), Mansfield Road, Oxford OX1 3SR, UK⁵
Institute of Poliomyelitis and Viral Encephalitis, Moscow, Russia⁶

Author for correspondence: Michael Gaunt (at the London School of Hygiene and Tropical Medicine). Fax +44 20 7636 5739. e-mail michael.gaunt{at}lshtm.ac.uk

Phylogenetic analysis of the Flavivirus genus, using either partial sequences of the non-structural 5 gene or the structural envelope gene, revealed an extensive series of clades defined by their epidemiology and disease associations. These phylogenies identified mosquito-borne, tick-borne and no-known-vector (NKV) virus clades, which could be further subdivided into clades defined by their principal vertebrate host. The mosquito-borne flaviviruses revealed two distinct epidemiological groups: (i) the neurotropic viruses, often associated with encephalitic disease in humans or livestock, correlated with the Culex species vector and bird reservoirs and (ii) the non-neurotropic viruses, associated with haemorrhagic disease in humans, correlated with the Aedes species vector and primate hosts. Thus, the tree topology describing the virus–host association may reflect differences in the feeding behaviour between Aedes and Culex mosquitoes. The tick-borne viruses also formed two distinct groups: one group associated with seabirds and the other, the tick-borne encephalitis complex viruses, associated primarily with rodents. The NKV flaviviruses formed three distinct groups: one group, which was closely related to the mosquito-borne viruses, associated with bats; a second group, which was more genetically distant, also associated with bats; and a third group associated with rodents. Each epidemiological group within the phylogenies revealed distinct geographical clusters in either the Old World or the New World, which for mosquito-borne viruses may reflect an Old World origin. The correlation between epidemiology, disease correlation and biogeography begins to define the complex evolutionary relationships between the virus, vector, vertebrate host and ecological niche.

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