Phylogenetic analysis of North American West Nile virus isolates, 2001–2004: Evidence for the emergence of a dominant genotype

Davis, C. Todd; Ebel, Gregory D.; Lanciotti, Robert S.; Brault, Aaron C.; Guzmán, Hilda; Siirin, Marina; Lambert, Amy J.; Parsons, Ray E.; Beasley, David W.C.; Novak, Robert J.; Elizondo-Quiroga, Darwin; Green, Emily N.; Young, David; Stark, Lillian M.; Drebot, Michael A.; Artsob, Harvey; Tesh, Robert B.; Kramer, Laura D.; Barrett, Alan D.T.

doi:10.1016/j.virol.2005.07.022

Cited by 231 publications

(174 citation statements)

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“…Alternatively, stochastic events leading to a genetic bottleneck event within or among hosts may also lead to the emergence of new genetic variants that could compete with existing viral populations and may ultimately form new genetic clades. Such replacement events are not unique to DENV and have also been reported for other flaviviruses, such as Japanese encephalitis and West Nile viruses (25)(26)(27).…”

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confidence: 61%

Increased Replicative Fitness of a Dengue Virus 2 Clade in Native Mosquitoes: Potential Contribution to a Clade Replacement Event in Nicaragua

Quiner

Parameswaran

Ciota

et al. 2014

J Virol

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The four dengue virus (DENV) serotypes (DENV serotype 1 [DENV-1] to DENV-4) are transmitted by Aedes aegypti and A. albopictus mosquitoes, causing up to 390 million DENV infections worldwide each year. We previously reported a clade replacement of the DENV-2 Asian-American genotype NI-1 clade by the NI-2B clade in Managua, Nicaragua. Here, we describe our studies of the replicative ability of NI-1 and NI-2B viruses in an A. aegypti cell line (Aag2) and A. aegypti mosquitoes reared from eggs collected in Managua. In coinfection experiments, several different pairs of NI-1 and NI-2B clinical isolates were used to infect Aag2 cells or blood-fed A. aegypti mosquitoes. Results consistently showed a significant replicative advantage of NI-2B over NI-1 viruses early after infection in vitro, and in mosquitoes, NI-2B viruses attained a higher replicative index than NI-1 isolates 3 to 7 days postinfection (dpi). At 7 dpi, NI-2B viruses displayed a significantly higher replicative index in legs and salivary glands; however, this advantage was lost by 14 and 21 dpi. We also found that the percentage of mosquitoes in which NI-2B viruses were dominant was significantly higher than that in which NI-1 viruses were dominant on day 7 but not at later time points. Taken together, these data demonstrate that clade NI-2B holds a replicative advantage over clade NI-1 early in infection that wanes at later time points. This early fitness advantage of NI-2B viruses over NI-1 viruses in the native vector, A. aegypti, suggests a shorter extrinsic incubation period for NI-2B viruses, which could have contributed to the clade replacement event in Managua. IMPORTANCEDengue virus (DENV), one of the most medically important arthropod-borne viruses, is transmitted to humans by Aedes aegypti and A. albopictus mosquitoes in tropical and subtropical regions worldwide. Dengue epidemics continue to increase in frequency, geographic range, and severity and are a major public health concern. This is due to globalization, unplanned urbanization, and climate change, as well as host genetics and immune responses and viral genetic changes. DENV consists of four serotypes, in turn composed of genotypes and genetically distinct clades. What drives the frequent replacement of a previously circulating DENV clade by another is unclear. Here, we investigate the replicative fitness of two clades of DENV serotype 2 in Aedes aegypti cells and mosquitoes collected from the region where the viruses circulated and conclude that increased replicative fitness could have contributed to a DENV clade replacement event in Nicaragua. These findings provide insight into vectordriven evolution of DENV epidemics. Dengue virus (DENV) is an arbovirus of global importance comprised of four phylogenetically related serotypes, DENV serotype 1 (DENV-1) to DENV-4. DENV is transmitted by Aedes aegypti and A. albopictus mosquitoes, which are typically found in tropical and subtropical regions of the world. However, due to a complex combination of factors that include migratio...

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confidence: 61%

Increased Replicative Fitness of a Dengue Virus 2 Clade in Native Mosquitoes: Potential Contribution to a Clade Replacement Event in Nicaragua

Quiner

Parameswaran

Ciota

et al. 2014

J Virol

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“…Notably, this New World WNV exhibits higher avian virulence than other lineage I viruses (16), which has been associated with a single Thr-to-Pro amino acid change at residue 249 in the viral helicase (encoded by NS3) (17). Also of importance is a Val159Ala amino acid substitution in the viral envelope (E) gene, which was first documented in 2002; viruses carrying this mutation quickly replaced those WNV strains previously circulating in the United States (18). The E-Val159Ala mutation is now fixed in the North American WNV population and has been linked to adaptation to the main Culex spp.…”

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confidence: 99%

Fluid Spatial Dynamics of West Nile Virus in the United States: Rapid Spread in a Permissive Host Environment

Giallonardo

Geoghegan

Docherty

et al. 2016

J Virol

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The introduction of West Nile virus (WNV) into North America in 1999 is a classic example of viral emergence in a new environment, with its subsequent dispersion across the continent having a major impact on local bird populations. Despite the importance of this epizootic, the pattern, dynamics, and determinants of WNV spread in its natural hosts remain uncertain. In particular, it is unclear whether the virus encountered major barriers to transmission, or spread in an unconstrained manner, and if specific viral lineages were favored over others indicative of intrinsic differences in fitness. To address these key questions in WNV evolution and ecology, we sequenced the complete genomes of approximately 300 avian isolates sampled across the United States between 2001 and 2012. Phylogenetic analysis revealed a relatively star-like tree structure, indicative of explosive viral spread in the United States, although with some replacement of viral genotypes through time. These data are striking in that viral sequences exhibit relatively limited clustering according to geographic region, particularly for those viruses sampled from birds, and no strong phylogenetic association with well-sampled avian species. The genome sequence data analyzed here also contain relatively little evidence for adaptive evolution, particularly of structural proteins, suggesting that most viral lineages are of similar fitness and that WNV is well adapted to the ecology of mosquito vectors and diverse avian hosts in the United States. In sum, the molecular evolution of WNV in North America depicts a largely unfettered expansion within a permissive host and geographic population with little evidence of major adaptive barriers. IMPORTANCE How viruses spread in new host

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“…Both hypotheses warrant further investigation. Interestingly, a viral-strain shift was observed in the northeast United States in 2002 (12). Although the effects of this strain shift on crow pathogenesis, immune response, and survival are unknown, this 2002 strain was observed to be slightly attenuated in mice (11).…”

Section: Resultsmentioning

confidence: 99%

Declining Mortality in American Crow (Corvus brachyrhynchos) Following Natural West Nile Virus Infection

Reed¹,

Johansson²,

Panella³

et al. 2009

Avian Diseases

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Phylogenetic analysis of North American West Nile virus isolates, 2001–2004: Evidence for the emergence of a dominant genotype

Cited by 231 publications

References 20 publications

Increased Replicative Fitness of a Dengue Virus 2 Clade in Native Mosquitoes: Potential Contribution to a Clade Replacement Event in Nicaragua

Increased Replicative Fitness of a Dengue Virus 2 Clade in Native Mosquitoes: Potential Contribution to a Clade Replacement Event in Nicaragua

Fluid Spatial Dynamics of West Nile Virus in the United States: Rapid Spread in a Permissive Host Environment

Declining Mortality in American Crow (Corvus brachyrhynchos) Following Natural West Nile Virus Infection

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