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 A. Miller, Trushar Jeevan, Anami Patel, Jacqueline M. Nolting, Michael J. Tonkovich, J. Tyler Genders, Andrew J. Montoney, Kevin Kasnyik, Timothy 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, Andrew S. Bowman
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.