Evolution and spread of Venezuelan equine encephalitis complex alphavirus in the Americas

Naomi L. Forrester; Joel O. Wertheim; Vivian G. Dugan; Albert J. Auguste; David Lin; A. Paige Adams; Rubing Chen; Rodion Gorchakov; Grace Leal; Jose G. Estrada-Franco; Jyotsna Pandya; Rebecca A. Halpin; Kumar Hari; Ravi Jain; Timothy B. Stockwell; Suman R. Das; David E. Wentworth; Martin D. Smith; Sergei L. Kosakovsky Pond; Scott C. Weaver

doi:10.1371/journal.pntd.0005693

Evolution and spread of Venezuelan equine encephalitis complex alphavirus in the Americas

Naomi L. Forrester, Joel O. Wertheim, Vivian G. Dugan, Albert J. Auguste, David Lin, A. Paige Adams, Rubing Chen, Rodion Gorchakov, Grace Leal, Jose G. Estrada-Franco, Jyotsna Pandya, Rebecca A. Halpin, Kumar Hari, Ravi Jain, Timothy B. Stockwell, Suman R. Das, David E. Wentworth, Martin D. Smith, Sergei L. Kosakovsky Pond, Scott C. Weaver

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47 Scopus citations

Abstract

Venezuelan equine encephalitis (VEE) complex alphaviruses are important re-emerging arboviruses that cause life-threatening disease in equids during epizootics as well as spillover human infections. We conducted a comprehensive analysis of VEE complex alphaviruses by sequencing the genomes of 94 strains and performing phylogenetic analyses of 130 isolates using complete open reading frames for the nonstructural and structural polyproteins. Our analyses confirmed purifying selection as a major mechanism influencing the evolution of these viruses as well as a confounding factor in molecular clock dating of ancestors. Times to most recent common ancestors (tMRCAs) could be robustly estimated only for the more recently diverged subtypes; the tMRCA of the ID/IAB/IC/II and IE clades of VEE virus (VEEV) were estimated at ca. 149–973 years ago. Evolution of the IE subtype has been characterized by a significant evolutionary shift from the rest of the VEEV complex, with an increase in structural protein substitutions that are unique to this group, possibly reflecting adaptation to its unique enzootic mosquito vector Culex (Melanoconion) taeniopus. Our inferred tree topologies suggest that VEEV is maintained primarily in situ, with only occasional spread to neighboring countries, probably reflecting the limited mobility of rodent hosts and mosquito vectors.

Original language	English
Article number	e0005693
Journal	PLoS Neglected Tropical Diseases
Volume	11
Issue number	8
DOIs	https://doi.org/10.1371/journal.pntd.0005693
State	Published - Aug 2017
Externally published	Yes

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Forrester, N. L., Wertheim, J. O., Dugan, V. G., Auguste, A. J., Lin, D., Adams, A. P., Chen, R., Gorchakov, R., Leal, G., Estrada-Franco, J. G., Pandya, J., Halpin, R. A., Hari, K., Jain, R., Stockwell, T. B., Das, S. R., Wentworth, D. E., Smith, M. D., Kosakovsky Pond, S. L., & Weaver, S. C. (2017). Evolution and spread of Venezuelan equine encephalitis complex alphavirus in the Americas. PLoS Neglected Tropical Diseases, 11(8), Article e0005693. https://doi.org/10.1371/journal.pntd.0005693

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title = "Evolution and spread of Venezuelan equine encephalitis complex alphavirus in the Americas",

abstract = "Venezuelan equine encephalitis (VEE) complex alphaviruses are important re-emerging arboviruses that cause life-threatening disease in equids during epizootics as well as spillover human infections. We conducted a comprehensive analysis of VEE complex alphaviruses by sequencing the genomes of 94 strains and performing phylogenetic analyses of 130 isolates using complete open reading frames for the nonstructural and structural polyproteins. Our analyses confirmed purifying selection as a major mechanism influencing the evolution of these viruses as well as a confounding factor in molecular clock dating of ancestors. Times to most recent common ancestors (tMRCAs) could be robustly estimated only for the more recently diverged subtypes; the tMRCA of the ID/IAB/IC/II and IE clades of VEE virus (VEEV) were estimated at ca. 149–973 years ago. Evolution of the IE subtype has been characterized by a significant evolutionary shift from the rest of the VEEV complex, with an increase in structural protein substitutions that are unique to this group, possibly reflecting adaptation to its unique enzootic mosquito vector Culex (Melanoconion) taeniopus. Our inferred tree topologies suggest that VEEV is maintained primarily in situ, with only occasional spread to neighboring countries, probably reflecting the limited mobility of rodent hosts and mosquito vectors.",

author = "Forrester, {Naomi L.} and Wertheim, {Joel O.} and Dugan, {Vivian G.} and Auguste, {Albert J.} and David Lin and Adams, {A. Paige} and Rubing Chen and Rodion Gorchakov and Grace Leal and Estrada-Franco, {Jose G.} and Jyotsna Pandya and Halpin, {Rebecca A.} and Kumar Hari and Ravi Jain and Stockwell, {Timothy B.} and Das, {Suman R.} and Wentworth, {David E.} and Smith, {Martin D.} and {Kosakovsky Pond}, {Sergei L.} and Weaver, {Scott C.}",

year = "2017",

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Forrester, NL, Wertheim, JO, Dugan, VG, Auguste, AJ, Lin, D, Adams, AP, Chen, R, Gorchakov, R, Leal, G, Estrada-Franco, JG, Pandya, J, Halpin, RA, Hari, K, Jain, R, Stockwell, TB, Das, SR, Wentworth, DE, Smith, MD, Kosakovsky Pond, SL & Weaver, SC 2017, 'Evolution and spread of Venezuelan equine encephalitis complex alphavirus in the Americas', PLoS Neglected Tropical Diseases, vol. 11, no. 8, e0005693. https://doi.org/10.1371/journal.pntd.0005693

TY - JOUR

T1 - Evolution and spread of Venezuelan equine encephalitis complex alphavirus in the Americas

AU - Forrester, Naomi L.

AU - Wertheim, Joel O.

AU - Dugan, Vivian G.

AU - Auguste, Albert J.

AU - Lin, David

AU - Adams, A. Paige

AU - Chen, Rubing

AU - Gorchakov, Rodion

AU - Leal, Grace

AU - Estrada-Franco, Jose G.

AU - Pandya, Jyotsna

AU - Halpin, Rebecca A.

AU - Hari, Kumar

AU - Jain, Ravi

AU - Stockwell, Timothy B.

AU - Das, Suman R.

AU - Wentworth, David E.

AU - Smith, Martin D.

AU - Kosakovsky Pond, Sergei L.

AU - Weaver, Scott C.

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N2 - Venezuelan equine encephalitis (VEE) complex alphaviruses are important re-emerging arboviruses that cause life-threatening disease in equids during epizootics as well as spillover human infections. We conducted a comprehensive analysis of VEE complex alphaviruses by sequencing the genomes of 94 strains and performing phylogenetic analyses of 130 isolates using complete open reading frames for the nonstructural and structural polyproteins. Our analyses confirmed purifying selection as a major mechanism influencing the evolution of these viruses as well as a confounding factor in molecular clock dating of ancestors. Times to most recent common ancestors (tMRCAs) could be robustly estimated only for the more recently diverged subtypes; the tMRCA of the ID/IAB/IC/II and IE clades of VEE virus (VEEV) were estimated at ca. 149–973 years ago. Evolution of the IE subtype has been characterized by a significant evolutionary shift from the rest of the VEEV complex, with an increase in structural protein substitutions that are unique to this group, possibly reflecting adaptation to its unique enzootic mosquito vector Culex (Melanoconion) taeniopus. Our inferred tree topologies suggest that VEEV is maintained primarily in situ, with only occasional spread to neighboring countries, probably reflecting the limited mobility of rodent hosts and mosquito vectors.

AB - Venezuelan equine encephalitis (VEE) complex alphaviruses are important re-emerging arboviruses that cause life-threatening disease in equids during epizootics as well as spillover human infections. We conducted a comprehensive analysis of VEE complex alphaviruses by sequencing the genomes of 94 strains and performing phylogenetic analyses of 130 isolates using complete open reading frames for the nonstructural and structural polyproteins. Our analyses confirmed purifying selection as a major mechanism influencing the evolution of these viruses as well as a confounding factor in molecular clock dating of ancestors. Times to most recent common ancestors (tMRCAs) could be robustly estimated only for the more recently diverged subtypes; the tMRCA of the ID/IAB/IC/II and IE clades of VEE virus (VEEV) were estimated at ca. 149–973 years ago. Evolution of the IE subtype has been characterized by a significant evolutionary shift from the rest of the VEEV complex, with an increase in structural protein substitutions that are unique to this group, possibly reflecting adaptation to its unique enzootic mosquito vector Culex (Melanoconion) taeniopus. Our inferred tree topologies suggest that VEEV is maintained primarily in situ, with only occasional spread to neighboring countries, probably reflecting the limited mobility of rodent hosts and mosquito vectors.

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U2 - 10.1371/journal.pntd.0005693

DO - 10.1371/journal.pntd.0005693

M3 - Artículo

SN - 1935-2727

VL - 11

JO - PLoS Neglected Tropical Diseases

JF - PLoS Neglected Tropical Diseases

IS - 8

M1 - e0005693

ER -

Evolution and spread of Venezuelan equine encephalitis complex alphavirus in the Americas

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