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

• Published in: Nature communications Vol. 14; no. 1; pp. 5105 - 15
• Main Authors: McBride, Dillon S., Garushyants, Sofya K., Franks, John, Magee, Andrew F., Overend, Steven H., Huey, Devra, Williams, Amanda M., Faith, Seth A., Kandeil, Ahmed, Trifkovic, Sanja, Miller, Lance, Jeevan, Trushar, Patel, Anami, Nolting, Jacqueline M., Tonkovich, Michael J., Genders, J. Tyler, Montoney, Andrew J., Kasnyik, Kevin, Linder, Timothy J., Bevins, Sarah N., Lenoch, Julianna B., Chandler, Jeffrey C., DeLiberto, Thomas J., Koonin, Eugene V., Suchard, Marc A., Lemey, Philippe, Webby, Richard J., Nelson, Martha I., Bowman, Andrew S.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 28.08.2023; Nature Publishing Group; Nature Portfolio
• Subjects: 13/1; 13/106; 45/23; 45/88; 45/90; 631/181/735; 631/181/757; 631/326/596/4130; 692/699/255/2514; 692/700/478/174; Animal models; Animals; Bayes Theorem; Bayesian analysis; COVID-19; COVID-19 - veterinary; COVID-19 infection; Deer; Disease transmission; ecology; Epidemiology; Evolution; Humanities and Social Sciences; Humans; Livestock; long term effects; Mathematical models; multidisciplinary; Odocoileus virginianus; Ohio; Pandemics; phenotype; Phylogeny; Populations; risk; SARS-CoV-2 - genetics; Science; Science (multidisciplinary); Severe acute respiratory syndrome coronavirus 2; Viral diseases; Viruses; United States > US; Ohio
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-40706-y

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. White-tailed deer are an important reservoir of SARS-CoV-2 in the USA and continued monitoring of the virus in deer populations is needed. In this genomic epidemiology study from Ohio, the authors show that the virus has been introduced multiple times to deer from humans, and that it has evolved faster in deer.