Vector-borne transmission imposes a severe bottleneck on an RNA virus population.

RNA viruses typically occur in genetically diverse populations due to their error-prone genome replication. Genetic diversity is thought to be important in allowing RNA viruses to explore sequence space, facilitating adaptation to changing environments and hosts. Some arboviruses that infect both a...

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Main Authors: Naomi L Forrester, Mathilde Guerbois, Robert L Seymour, Heidi Spratt, Scott C Weaver
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-09-01
Series:PLoS Pathogens
Online Access:http://europepmc.org/articles/PMC3441635?pdf=render
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spelling doaj-fb58ed523dbc4766b5f6fcb884cccda52020-11-25T01:47:01ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742012-09-0189e100289710.1371/journal.ppat.1002897Vector-borne transmission imposes a severe bottleneck on an RNA virus population.Naomi L ForresterMathilde GuerboisRobert L SeymourHeidi SprattScott C WeaverRNA viruses typically occur in genetically diverse populations due to their error-prone genome replication. Genetic diversity is thought to be important in allowing RNA viruses to explore sequence space, facilitating adaptation to changing environments and hosts. Some arboviruses that infect both a mosquito vector and a mammalian host are known to experience population bottlenecks in their vectors, which may constrain their genetic diversity and could potentially lead to extinction events via Muller's ratchet. To examine this potential challenge of bottlenecks for arbovirus perpetuation, we studied Venezuelan equine encephalitis virus (VEEV) enzootic subtype IE and its natural vector Culex (Melanoconion) taeniopus, as an example of a virus-vector interaction with a long evolutionary history. Using a mixture of marked VEEV clones to infect C. taeniopus and real-time RT-PCR to track these clones during mosquito infection and dissemination, we observed severe bottleneck events that resulted in a significant drop in the number of clones present. At higher initial doses, the midgut was readily infected and there was a severe bottleneck at the midgut escape. Following a lower initial dose, the major bottleneck occurred at initial midgut infection. A second, less severe bottleneck was identified at the salivary gland infection stage following intrathoracic inoculation. Our results suggest that VEEV consistently encounters bottlenecks during infection, dissemination and transmission by its natural enzootic vector. The potential impacts of these bottlenecks on viral fitness and transmission, and the viral mechanisms that prevent genetic drift leading to extinction, deserve further study.http://europepmc.org/articles/PMC3441635?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Naomi L Forrester
Mathilde Guerbois
Robert L Seymour
Heidi Spratt
Scott C Weaver
spellingShingle Naomi L Forrester
Mathilde Guerbois
Robert L Seymour
Heidi Spratt
Scott C Weaver
Vector-borne transmission imposes a severe bottleneck on an RNA virus population.
PLoS Pathogens
author_facet Naomi L Forrester
Mathilde Guerbois
Robert L Seymour
Heidi Spratt
Scott C Weaver
author_sort Naomi L Forrester
title Vector-borne transmission imposes a severe bottleneck on an RNA virus population.
title_short Vector-borne transmission imposes a severe bottleneck on an RNA virus population.
title_full Vector-borne transmission imposes a severe bottleneck on an RNA virus population.
title_fullStr Vector-borne transmission imposes a severe bottleneck on an RNA virus population.
title_full_unstemmed Vector-borne transmission imposes a severe bottleneck on an RNA virus population.
title_sort vector-borne transmission imposes a severe bottleneck on an rna virus population.
publisher Public Library of Science (PLoS)
series PLoS Pathogens
issn 1553-7366
1553-7374
publishDate 2012-09-01
description RNA viruses typically occur in genetically diverse populations due to their error-prone genome replication. Genetic diversity is thought to be important in allowing RNA viruses to explore sequence space, facilitating adaptation to changing environments and hosts. Some arboviruses that infect both a mosquito vector and a mammalian host are known to experience population bottlenecks in their vectors, which may constrain their genetic diversity and could potentially lead to extinction events via Muller's ratchet. To examine this potential challenge of bottlenecks for arbovirus perpetuation, we studied Venezuelan equine encephalitis virus (VEEV) enzootic subtype IE and its natural vector Culex (Melanoconion) taeniopus, as an example of a virus-vector interaction with a long evolutionary history. Using a mixture of marked VEEV clones to infect C. taeniopus and real-time RT-PCR to track these clones during mosquito infection and dissemination, we observed severe bottleneck events that resulted in a significant drop in the number of clones present. At higher initial doses, the midgut was readily infected and there was a severe bottleneck at the midgut escape. Following a lower initial dose, the major bottleneck occurred at initial midgut infection. A second, less severe bottleneck was identified at the salivary gland infection stage following intrathoracic inoculation. Our results suggest that VEEV consistently encounters bottlenecks during infection, dissemination and transmission by its natural enzootic vector. The potential impacts of these bottlenecks on viral fitness and transmission, and the viral mechanisms that prevent genetic drift leading to extinction, deserve further study.
url http://europepmc.org/articles/PMC3441635?pdf=render
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