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

Abstract

While SARS-CoV-2 has sporadically infected a wide range of animal species worldwide1, the virus has been repeatedly and frequently detected in white-tailed deer in North America2–7. The zoonotic origins of this pandemic virus highlight the need to fill the vast gaps in our knowledge of SARS-CoV-2 ecology and evolution in non-human hosts. Here, we detected 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, which disseminated across hundreds of kilometers. We discovered that alpha and delta variants evolved in white-tailed deer at three-times the rate observed in humans. Newly developed Bayesian phylogenetic methods quantified how SARS-CoV-2 evolution is not only faster in white-tailed deer but driven by different mutational biases and selection pressures. White-tailed deer are not just short-term recipients of human viral diversity but serve as reservoirs for alpha and other variants to evolve in new directions after going extinct in humans. The long-term effect of this accelerated evolutionary rate remains to be seen as no critical phenotypic changes were observed in our animal model experiments using viruses isolated from white-tailed deer. Still, SARS-CoV-2 viruses have 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.

Surveillance of Vermont wildlife in 2021-2022 reveals no detected SARS-CoV-2 viral RNA

“…While it has not been established how SARS-CoV-2 is introduced into wild deer populations, it seems likely that this occurs via human-to-deer transmission, deer-to-deer transmission, or a combination of the two 26,28 . Vermont may have multiple features that reduced farmed animals (such as mink) and farm employees that care for them has been well documented for viruses including SARS-CoV-2 and is a plausible route for the initial introduction of SARS-CoV-2 into deer populations as well 30 .…”

Epidemiological Dynamics of SARS-CoV-2 in White-tailed Deer

“…Phylogenetic studies of surveillance data estimate the number and timing of spillover events within the dataset [2][3][4][5]18]. However, the number and rate of disease transmission events from humans to deer can be difficult to estimate at a national population level because of challenges with sampling designs (i.e., both human and deer sampling designs are biased and deer abundances are unknown).…”

“…From October 2021 through March 2022 there were 10,217 nasal or oral swab samples from WTD tested from 27 states and Washington, DC. SARS-CoV-2 viral RNA was detected in 13% (1,307) of the 10,217 samples [17,18]. The raw, apparent prevalence summaries are descriptive statistics that do not account for the opportunistic sample collection.…”

“…When available, hunters were asked to disclose the county of removal, but in lieu of removal county, the check station county where the sample was collected was used. Nasal or oral swabs were collected and tested for the presence of SARS-CoV-2 viral RNA via rRT-PCR as previously described [17,18].…”

“…Deer-to-deer transmission may occur within wild populations beyond the initial introduction period. Surveillance studies in WTD have shown persistence of SARS-CoV-2 alpha and gamma variants in populations 4-6 months after their peak circulation and extinction in the human population [4,5,17,18]. These data describing susceptibility and transmission capabilities of SARS-CoV-2 in WTD and the fact that WTD are abundant and share a variety of habitats with humans across the United States [19], highlight the need to understand potential infection dynamics of SARS-CoV-2 in WTD across the range of the species.…”