ABSTRACT
Understanding pathogen emergence in new host species is fundamental for developing prevention and response plans for human and animal health. We leveraged a large-scale surveillance dataset coordinated by United States Department of Agriculture, Animal and Plant Health Inspection Service and state natural resources agencies to quantify outbreak dynamics of SARS-CoV-2 in North American white-tailed deer (Odocoileus virginianus; WTD) throughout its range in the United States. Local epidemics in WTD were well approximated by a single outbreak peak followed by fade out. Outbreaks peaked earliest in the northeast and mid-Atlantic. Local effective reproduction numbers of SARS-CoV-2 were between 1 and 2.5. Ten percent of variability in peak prevalence was explained by human infection pressure. This, together with the similar peak infection prevalence times across many counties and single-peak outbreak dynamics followed by fade out, suggest that widespread transmission via human-to-deer spillover may have been an important driver of the patterns and persistence. We provide a framework for inferring population-level epidemiological processes through joint analysis of many sparsely-observed local outbreaks (landscape scale surveillance data) and linking epidemiological parameters to ecological risk factors. The framework combines mechanistic and statistical models that can identify and track local outbreaks in long-term infection surveillance monitoring data.
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.
ABSTRACT
Human-to-animal spillover of SARS-CoV-2 virus has occurred in a wide range of animals, but thus far, the establishment of a new natural animal reservoir has not been detected. Here, we detected SARS-CoV-2 virus using rRT-PCR in 129 out of 360 (35.8%) free-ranging white-tailed deer (Odocoileus virginianus) from northeast Ohio (USA) sampled between January-March 2021. Deer in 6 locations were infected with at least 3 lineages of SARS-CoV-2 (B.1.2, B.1.596, B.1.582). The B.1.2 viruses, dominant in Ohio at the time, spilled over multiple times into deer populations in different locations. Deer-to-deer transmission may have occurred in three locations. The establishment of a natural reservoir of SARS-CoV-2 in white-tailed deer could facilitate divergent evolutionary trajectories and future spillback to humans, further complicating long-term COVID-19 control strategies.