Accelerated evolution of SARS-CoV-2 in free-ranging white-tailed deer

Dillon S. McBride, Sofya K. Garushyants, John Franks, Andrew F. Magee, Steven H. Overend, Devra Huey, Amanda M. Williams, Seth A. Faith, Ahmed Kandeil, Sanja Trifkovic, Lance Miller, Trushar Jeevan, Anami Patel, Jacqueline M. Nolting, Michael J. Tonkovich, J. Tyler Genders, Andrew J. Montoney, Kevin Kasnyik, Timothy J. Linder, Sarah N. Bevins, Julianna B. Lenoch, Jeffrey C. Chandler, Thomas J. DeLiberto, Eugene V. Koonin, Marc A. Suchard, Philippe Lemey, Richard J. Webby, Martha I. Nelson () and Andrew S. Bowman ()
Additional contact information
Dillon S. McBride: The Ohio State University College of Veterinary Medicine
Sofya K. Garushyants: National Institutes of Health
John Franks: St Jude Children’s Research Hospital
Andrew F. Magee: University of California, Los Angeles
Steven H. Overend: The Ohio State University College of Veterinary Medicine
Devra Huey: The Ohio State University College of Veterinary Medicine
Amanda M. Williams: The Ohio State University
Seth A. Faith: The Ohio State University
Ahmed Kandeil: St Jude Children’s Research Hospital
Sanja Trifkovic: St Jude Children’s Research Hospital
Lance Miller: St Jude Children’s Research Hospital
Trushar Jeevan: St Jude Children’s Research Hospital
Anami Patel: PathAI Diagnostics
Jacqueline M. Nolting: The Ohio State University College of Veterinary Medicine
Michael J. Tonkovich: Division of Wildlife
J. Tyler Genders: Animal and Plant Health Inspection Service, Wildlife Services
Andrew J. Montoney: Animal and Plant Health Inspection Service, Wildlife Services
Kevin Kasnyik: Columbus and Franklin County Metro Parks
Timothy J. Linder: National Wildlife Disease Program
Sarah N. Bevins: National Wildlife Disease Program
Julianna B. Lenoch: National Wildlife Disease Program
Jeffrey C. Chandler: Wildlife Disease Diagnostic Laboratory
Thomas J. DeLiberto: Animal and Plant Health Inspection Service, Wildlife Services
Eugene V. Koonin: National Institutes of Health
Marc A. Suchard: University of California, Los Angeles
Philippe Lemey: Rega Institute, KU Leuven
Richard J. Webby: St Jude Children’s Research Hospital
Martha I. Nelson: National Institutes of Health
Andrew S. Bowman: The Ohio State University College of Veterinary Medicine

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract The zoonotic origin of the COVID-19 pandemic virus highlights the need to fill the vast gaps in our knowledge of SARS-CoV-2 ecology and evolution in non-human hosts. Here, we detected that SARS-CoV-2 was introduced from humans into white-tailed deer more than 30 times in Ohio, USA during November 2021-March 2022. Subsequently, deer-to-deer transmission persisted for 2–8 months, disseminating across hundreds of kilometers. Newly developed Bayesian phylogenetic methods quantified how SARS-CoV-2 evolution is not only three-times faster in white-tailed deer compared to the rate observed in humans but also driven by different mutational biases and selection pressures. The long-term effect of this accelerated evolutionary rate remains to be seen as no critical phenotypic changes were observed in our animal models using white-tailed deer origin viruses. Still, SARS-CoV-2 has transmitted in white-tailed deer populations for a relatively short duration, and the risk of future changes may have serious consequences for humans and livestock.

Date: 2023
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DOI: 10.1038/s41467-023-40706-y

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