Adaptive evolution and environmental durability jointly structure phylodynamic patterns in avian influenza viruses.

Avian influenza viruses (AIVs) have been pivotal to the origination of human pandemic strains. Despite their scientific and public health significance, however, there remains much to be understood about the ecology and evolution of AIVs in wild birds, where major pools of genetic diversity are gener...

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Main Authors: Benjamin Roche, John M Drake, Justin Brown, David E Stallknecht, Trevor Bedford, Pejman Rohani
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-08-01
Series:PLoS Biology
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/25116957/?tool=EBI
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spelling doaj-a0224597c68441a0b280fadbf36183722021-07-02T16:25:37ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852014-08-01128e100193110.1371/journal.pbio.1001931Adaptive evolution and environmental durability jointly structure phylodynamic patterns in avian influenza viruses.Benjamin RocheJohn M DrakeJustin BrownDavid E StallknechtTrevor BedfordPejman RohaniAvian influenza viruses (AIVs) have been pivotal to the origination of human pandemic strains. Despite their scientific and public health significance, however, there remains much to be understood about the ecology and evolution of AIVs in wild birds, where major pools of genetic diversity are generated and maintained. Here, we present comparative phylodynamic analyses of human and AIVs in North America, demonstrating (i) significantly higher standing genetic diversity and (ii) phylogenetic trees with a weaker signature of immune escape in AIVs than in human viruses. To explain these differences, we performed statistical analyses to quantify the relative contribution of several potential explanations. We found that HA genetic diversity in avian viruses is determined by a combination of factors, predominantly subtype-specific differences in host immune selective pressure and the ecology of transmission (in particular, the durability of subtypes in aquatic environments). Extending this analysis using a computational model demonstrated that virus durability may lead to long-term, indirect chains of transmission that, when coupled with a short host lifespan, can generate and maintain the observed high levels of genetic diversity. Further evidence in support of this novel finding was found by demonstrating an association between subtype-specific environmental durability and predicted phylogenetic signatures: genetic diversity, variation in phylogenetic tree branch lengths, and tree height. The conclusion that environmental transmission plays an important role in the evolutionary biology of avian influenza viruses-a manifestation of the "storage effect"-highlights the potentially unpredictable impact of wildlife reservoirs for future human pandemics and the need for improved understanding of the natural ecology of these viruses.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/25116957/?tool=EBI
collection DOAJ
language English
format Article
sources DOAJ
author Benjamin Roche
John M Drake
Justin Brown
David E Stallknecht
Trevor Bedford
Pejman Rohani
spellingShingle Benjamin Roche
John M Drake
Justin Brown
David E Stallknecht
Trevor Bedford
Pejman Rohani
Adaptive evolution and environmental durability jointly structure phylodynamic patterns in avian influenza viruses.
PLoS Biology
author_facet Benjamin Roche
John M Drake
Justin Brown
David E Stallknecht
Trevor Bedford
Pejman Rohani
author_sort Benjamin Roche
title Adaptive evolution and environmental durability jointly structure phylodynamic patterns in avian influenza viruses.
title_short Adaptive evolution and environmental durability jointly structure phylodynamic patterns in avian influenza viruses.
title_full Adaptive evolution and environmental durability jointly structure phylodynamic patterns in avian influenza viruses.
title_fullStr Adaptive evolution and environmental durability jointly structure phylodynamic patterns in avian influenza viruses.
title_full_unstemmed Adaptive evolution and environmental durability jointly structure phylodynamic patterns in avian influenza viruses.
title_sort adaptive evolution and environmental durability jointly structure phylodynamic patterns in avian influenza viruses.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2014-08-01
description Avian influenza viruses (AIVs) have been pivotal to the origination of human pandemic strains. Despite their scientific and public health significance, however, there remains much to be understood about the ecology and evolution of AIVs in wild birds, where major pools of genetic diversity are generated and maintained. Here, we present comparative phylodynamic analyses of human and AIVs in North America, demonstrating (i) significantly higher standing genetic diversity and (ii) phylogenetic trees with a weaker signature of immune escape in AIVs than in human viruses. To explain these differences, we performed statistical analyses to quantify the relative contribution of several potential explanations. We found that HA genetic diversity in avian viruses is determined by a combination of factors, predominantly subtype-specific differences in host immune selective pressure and the ecology of transmission (in particular, the durability of subtypes in aquatic environments). Extending this analysis using a computational model demonstrated that virus durability may lead to long-term, indirect chains of transmission that, when coupled with a short host lifespan, can generate and maintain the observed high levels of genetic diversity. Further evidence in support of this novel finding was found by demonstrating an association between subtype-specific environmental durability and predicted phylogenetic signatures: genetic diversity, variation in phylogenetic tree branch lengths, and tree height. The conclusion that environmental transmission plays an important role in the evolutionary biology of avian influenza viruses-a manifestation of the "storage effect"-highlights the potentially unpredictable impact of wildlife reservoirs for future human pandemics and the need for improved understanding of the natural ecology of these viruses.
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/25116957/?tool=EBI
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