Experimental Evolution of West Nile Virus at Higher Temperatures Facilitates Broad Adaptation and Increased Genetic Diversity

West Nile virus (WNV, <i>Flaviviridae</i>, Flavivirus) is a mosquito-borne flavivirus introduced to North America in 1999. Since 1999, the Earth’s average temperature has increased by 0.6 °C. Mosquitoes are ectothermic organisms, reliant on environmental heat sources. Temperature impacts...

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Main Authors: Rachel L. Fay, Kiet A. Ngo, Lili Kuo, Graham G. Willsey, Laura D. Kramer, Alexander T. Ciota
Format: Article
Language:English
Published: MDPI AG 2021-09-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/13/10/1889
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author Rachel L. Fay
Kiet A. Ngo
Lili Kuo
Graham G. Willsey
Laura D. Kramer
Alexander T. Ciota
author_facet Rachel L. Fay
Kiet A. Ngo
Lili Kuo
Graham G. Willsey
Laura D. Kramer
Alexander T. Ciota
author_sort Rachel L. Fay
collection DOAJ
description West Nile virus (WNV, <i>Flaviviridae</i>, Flavivirus) is a mosquito-borne flavivirus introduced to North America in 1999. Since 1999, the Earth’s average temperature has increased by 0.6 °C. Mosquitoes are ectothermic organisms, reliant on environmental heat sources. Temperature impacts vector–virus interactions which directly influence arbovirus transmission. RNA viral replication is highly error-prone and increasing temperature could further increase replication rates, mutation frequencies, and evolutionary rates. The impact of temperature on arbovirus evolutionary trajectories and fitness landscapes has yet to be sufficiently studied. To investigate how temperature impacts the rate and extent of WNV evolution in mosquito cells, WNV was experimentally passaged 12 times in <i>Culex tarsalis</i> cells, at 25 °C and 30 °C. Full-genome deep sequencing was used to compare genetic signatures during passage, and replicative fitness was evaluated before and after passage at each temperature. Our results suggest adaptive potential at both temperatures, with unique temperature-dependent and lineage-specific genetic signatures. Further, higher temperature passage was associated with significantly increased replicative fitness at both temperatures and increases in nonsynonymous mutations. Together, these data indicate that if similar selective pressures exist in natural systems, increases in temperature could accelerate emergence of high-fitness strains with greater phenotypic plasticity.
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spelling doaj.art-7ae7791eaf03481a8691e1e4926bf75a2023-11-22T20:17:40ZengMDPI AGViruses1999-49152021-09-011310188910.3390/v13101889Experimental Evolution of West Nile Virus at Higher Temperatures Facilitates Broad Adaptation and Increased Genetic DiversityRachel L. Fay0Kiet A. Ngo1Lili Kuo2Graham G. Willsey3Laura D. Kramer4Alexander T. Ciota5Department of Biomedical Sciences, State University of New York at Albany School of Public Health, Rensselaer, NY 12144, USAThe Arbovirus Laboratory, Wadsworth Center, New York State Department of Health, Slingerlands, NY 12159, USAThe Arbovirus Laboratory, Wadsworth Center, New York State Department of Health, Slingerlands, NY 12159, USADivision of Infectious Diseases, Wadsworth Center, New York State Department of Health, Albany, NY 12208, USADepartment of Biomedical Sciences, State University of New York at Albany School of Public Health, Rensselaer, NY 12144, USADepartment of Biomedical Sciences, State University of New York at Albany School of Public Health, Rensselaer, NY 12144, USAWest Nile virus (WNV, <i>Flaviviridae</i>, Flavivirus) is a mosquito-borne flavivirus introduced to North America in 1999. Since 1999, the Earth’s average temperature has increased by 0.6 °C. Mosquitoes are ectothermic organisms, reliant on environmental heat sources. Temperature impacts vector–virus interactions which directly influence arbovirus transmission. RNA viral replication is highly error-prone and increasing temperature could further increase replication rates, mutation frequencies, and evolutionary rates. The impact of temperature on arbovirus evolutionary trajectories and fitness landscapes has yet to be sufficiently studied. To investigate how temperature impacts the rate and extent of WNV evolution in mosquito cells, WNV was experimentally passaged 12 times in <i>Culex tarsalis</i> cells, at 25 °C and 30 °C. Full-genome deep sequencing was used to compare genetic signatures during passage, and replicative fitness was evaluated before and after passage at each temperature. Our results suggest adaptive potential at both temperatures, with unique temperature-dependent and lineage-specific genetic signatures. Further, higher temperature passage was associated with significantly increased replicative fitness at both temperatures and increases in nonsynonymous mutations. Together, these data indicate that if similar selective pressures exist in natural systems, increases in temperature could accelerate emergence of high-fitness strains with greater phenotypic plasticity.https://www.mdpi.com/1999-4915/13/10/1889West Nile virusviral evolutionclimate change
spellingShingle Rachel L. Fay
Kiet A. Ngo
Lili Kuo
Graham G. Willsey
Laura D. Kramer
Alexander T. Ciota
Experimental Evolution of West Nile Virus at Higher Temperatures Facilitates Broad Adaptation and Increased Genetic Diversity
Viruses
West Nile virus
viral evolution
climate change
title Experimental Evolution of West Nile Virus at Higher Temperatures Facilitates Broad Adaptation and Increased Genetic Diversity
title_full Experimental Evolution of West Nile Virus at Higher Temperatures Facilitates Broad Adaptation and Increased Genetic Diversity
title_fullStr Experimental Evolution of West Nile Virus at Higher Temperatures Facilitates Broad Adaptation and Increased Genetic Diversity
title_full_unstemmed Experimental Evolution of West Nile Virus at Higher Temperatures Facilitates Broad Adaptation and Increased Genetic Diversity
title_short Experimental Evolution of West Nile Virus at Higher Temperatures Facilitates Broad Adaptation and Increased Genetic Diversity
title_sort experimental evolution of west nile virus at higher temperatures facilitates broad adaptation and increased genetic diversity
topic West Nile virus
viral evolution
climate change
url https://www.mdpi.com/1999-4915/13/10/1889
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