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Molecular epidemiology of peste des petits ruminants virus emergence in critically endangered Mongolian saiga antelope and other wild ungulates

Peste des petits ruminants virus (PPRV) causes disease in domestic and wild ungulates, is the target of a Global Eradication Programme, and threatens biodiversity. Understanding the epidemiology and evolution of PPRV in wildlife is important but hampered by the paucity of wildlife-origin PPRV genome...

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Autores principales: Benfield, Camilla T O, Hill, Sarah, Shatar, Munkduuren, Shiilegdamba, Enkhtuvshin, Damdinjav, Batchuluun, Fine, Amanda, Willett, Brian, Kock, Richard, Bataille, Arnaud
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8570150/
https://www.ncbi.nlm.nih.gov/pubmed/34754511
http://dx.doi.org/10.1093/ve/veab062
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author Benfield, Camilla T O
Hill, Sarah
Shatar, Munkduuren
Shiilegdamba, Enkhtuvshin
Damdinjav, Batchuluun
Fine, Amanda
Willett, Brian
Kock, Richard
Bataille, Arnaud
author_facet Benfield, Camilla T O
Hill, Sarah
Shatar, Munkduuren
Shiilegdamba, Enkhtuvshin
Damdinjav, Batchuluun
Fine, Amanda
Willett, Brian
Kock, Richard
Bataille, Arnaud
author_sort Benfield, Camilla T O
collection PubMed
description Peste des petits ruminants virus (PPRV) causes disease in domestic and wild ungulates, is the target of a Global Eradication Programme, and threatens biodiversity. Understanding the epidemiology and evolution of PPRV in wildlife is important but hampered by the paucity of wildlife-origin PPRV genomes. In this study, full PPRV genomes were generated from three Mongolian saiga antelope, one Siberian ibex, and one goitered gazelle from the 2016–2017 PPRV outbreak. Phylogenetic analysis showed that for Mongolian and Chinese PPRV since 2013, the wildlife and livestock-origin genomes were closely related and interspersed. There was strong phylogenetic support for a monophyletic group of PPRV from Mongolian wildlife and livestock, belonging to a clade of lineage IV PPRV from livestock and wildlife from China since 2013. Discrete diffusion analysis found strong support for PPRV spread into Mongolia from China, and phylogeographic analysis indicated Xinjiang Province as the most likely origin, although genomic surveillance for PPRV is poor and lack of sampling from other regions could bias this result. Times of most recent common ancestor (TMRCA) were June 2015 (95 per cent highest posterior density (HPD): August 2014 to March 2016) for all Mongolian PPRV genomes and May 2016 (95 per cent HPD: October 2015 to October 2016) for Mongolian wildlife-origin PPRV. This suggests that PPRV was circulating undetected in Mongolia for at least 6 months before the first reported outbreak in August 2016 and that wildlife were likely infected before livestock vaccination began in October 2016. Finally, genetic variation and positively selected sites were identified that might be related to PPRV emergence in Mongolian wildlife. This study is the first to sequence multiple PPRV genomes from a wildlife outbreak, across several host species. Additional full PPRV genomes and associated metadata from the livestock–wildlife interface are needed to enhance the power of molecular epidemiology, support PPRV eradication, and safeguard the health of the whole ungulate community.
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spelling pubmed-85701502021-11-08 Molecular epidemiology of peste des petits ruminants virus emergence in critically endangered Mongolian saiga antelope and other wild ungulates Benfield, Camilla T O Hill, Sarah Shatar, Munkduuren Shiilegdamba, Enkhtuvshin Damdinjav, Batchuluun Fine, Amanda Willett, Brian Kock, Richard Bataille, Arnaud Virus Evol Research Article Peste des petits ruminants virus (PPRV) causes disease in domestic and wild ungulates, is the target of a Global Eradication Programme, and threatens biodiversity. Understanding the epidemiology and evolution of PPRV in wildlife is important but hampered by the paucity of wildlife-origin PPRV genomes. In this study, full PPRV genomes were generated from three Mongolian saiga antelope, one Siberian ibex, and one goitered gazelle from the 2016–2017 PPRV outbreak. Phylogenetic analysis showed that for Mongolian and Chinese PPRV since 2013, the wildlife and livestock-origin genomes were closely related and interspersed. There was strong phylogenetic support for a monophyletic group of PPRV from Mongolian wildlife and livestock, belonging to a clade of lineage IV PPRV from livestock and wildlife from China since 2013. Discrete diffusion analysis found strong support for PPRV spread into Mongolia from China, and phylogeographic analysis indicated Xinjiang Province as the most likely origin, although genomic surveillance for PPRV is poor and lack of sampling from other regions could bias this result. Times of most recent common ancestor (TMRCA) were June 2015 (95 per cent highest posterior density (HPD): August 2014 to March 2016) for all Mongolian PPRV genomes and May 2016 (95 per cent HPD: October 2015 to October 2016) for Mongolian wildlife-origin PPRV. This suggests that PPRV was circulating undetected in Mongolia for at least 6 months before the first reported outbreak in August 2016 and that wildlife were likely infected before livestock vaccination began in October 2016. Finally, genetic variation and positively selected sites were identified that might be related to PPRV emergence in Mongolian wildlife. This study is the first to sequence multiple PPRV genomes from a wildlife outbreak, across several host species. Additional full PPRV genomes and associated metadata from the livestock–wildlife interface are needed to enhance the power of molecular epidemiology, support PPRV eradication, and safeguard the health of the whole ungulate community. Oxford University Press 2021-06-25 /pmc/articles/PMC8570150/ /pubmed/34754511 http://dx.doi.org/10.1093/ve/veab062 Text en © The Author(s) 2021. Published by Oxford University Press. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Benfield, Camilla T O
Hill, Sarah
Shatar, Munkduuren
Shiilegdamba, Enkhtuvshin
Damdinjav, Batchuluun
Fine, Amanda
Willett, Brian
Kock, Richard
Bataille, Arnaud
Molecular epidemiology of peste des petits ruminants virus emergence in critically endangered Mongolian saiga antelope and other wild ungulates
title Molecular epidemiology of peste des petits ruminants virus emergence in critically endangered Mongolian saiga antelope and other wild ungulates
title_full Molecular epidemiology of peste des petits ruminants virus emergence in critically endangered Mongolian saiga antelope and other wild ungulates
title_fullStr Molecular epidemiology of peste des petits ruminants virus emergence in critically endangered Mongolian saiga antelope and other wild ungulates
title_full_unstemmed Molecular epidemiology of peste des petits ruminants virus emergence in critically endangered Mongolian saiga antelope and other wild ungulates
title_short Molecular epidemiology of peste des petits ruminants virus emergence in critically endangered Mongolian saiga antelope and other wild ungulates
title_sort molecular epidemiology of peste des petits ruminants virus emergence in critically endangered mongolian saiga antelope and other wild ungulates
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8570150/
https://www.ncbi.nlm.nih.gov/pubmed/34754511
http://dx.doi.org/10.1093/ve/veab062
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