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

View ORCID ProfileCamilla T. O. Benfield, Sarah Hill, Munkduuren Shatar, Enkhtuvshin Shiilegdamba, Batchuluun Damdinjav, Amanda Fine, Brian Willett, Richard Kock, Arnaud Bataille
doi: https://doi.org/10.1101/2021.05.08.443216
Camilla T. O. Benfield
1Department of Pathobiology and Population Sciences, The Royal Veterinary College, UK
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  • For correspondence: cbenfield@rvc.ac.uk
Sarah Hill
1Department of Pathobiology and Population Sciences, The Royal Veterinary College, UK
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Munkduuren Shatar
2Department of Veterinary Services of Dundgobi province, General Authority for Veterinary Services of Mongolia (GAVS), Mongolia
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Enkhtuvshin Shiilegdamba
3Wildlife Conservation Society, Ulaanbaatar, Mongolia
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Batchuluun Damdinjav
4State Central Veterinary Laboratory, Mongolia
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Amanda Fine
5Wildlife Conservation Society, Health Program, Bronx, NY, USA
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Brian Willett
6MRC-University of Glasgow Centre for Virus Research, Glasgow, UK
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Richard Kock
1Department of Pathobiology and Population Sciences, The Royal Veterinary College, UK
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Arnaud Bataille
7CIRAD, UMR ASTRE, F-34398 Montpellier, France
8ASTRE, University of Montpellier, CIRAD, INRA, Montpellier, France
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Abstract

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 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% HPD: August 2014 – March 2016) for all Mongolian PPRV genomes and May 2016 (95% HPD: October 2015 – October 2016) for Mongolian wildlife-origin PPRV. This suggests that PPRV was circulating undetected in Mongolia for at least six 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.

Author Summary Recent mass mortality of critically endangered Mongolian saiga antelope due to peste des petits ruminants virus (PPRV) has dramatically highlighted the threat this viral disease represents for biodiversity. The genome of viruses such as PPRV evolve fast, so virus genetic data gathered from infected animals can be used to trace disease spread between livestock and wildlife, and to determine if the virus is adapting to infect wildlife more efficiently. Here we obtained PPRV virus genomes from Mongolian wildlife and compared them with other published PPRV genomes. Using a molecular clock, we estimated that the disease was circulating in Mongolia well before it was first reported. Genetic analyses support the hypothesis of virus spread from livestock to wildlife, with genetic changes potentially helping infection in Asian wild ungulates. However, more PPR virus genomes and epidemiology data are needed from disease outbreaks in areas shared between livestock and wildlife to confirm these results and take efficient actions to safeguard the health of the whole ungulate community.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://microreact.org/project/5WNeX14MRFvwe8YLhn5a1S/e2d5dafd

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Molecular epidemiology of peste des petits ruminants virus emergence in critically endangered Mongolian saiga antelope and other wild ungulates
Camilla T. O. Benfield, Sarah Hill, Munkduuren Shatar, Enkhtuvshin Shiilegdamba, Batchuluun Damdinjav, Amanda Fine, Brian Willett, Richard Kock, Arnaud Bataille
bioRxiv 2021.05.08.443216; doi: https://doi.org/10.1101/2021.05.08.443216
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Molecular epidemiology of peste des petits ruminants virus emergence in critically endangered Mongolian saiga antelope and other wild ungulates
Camilla T. O. Benfield, Sarah Hill, Munkduuren Shatar, Enkhtuvshin Shiilegdamba, Batchuluun Damdinjav, Amanda Fine, Brian Willett, Richard Kock, Arnaud Bataille
bioRxiv 2021.05.08.443216; doi: https://doi.org/10.1101/2021.05.08.443216

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