Multiple spillovers and onward transmission of SARS-CoV-2 in free-living and captive white-tailed deer

Abstract

Many animal species are susceptible to SARS-CoV-2 and could potentially act as reservoirs, yet transmission of the virus in non-human free-living animals has not been documented. White-tailed deer (Odocoileus virginianus), the predominant cervid in North America, are susceptible to SARS-CoV-2 infection, and experimentally infected fawns can transmit the virus. To test the hypothesis that SARS-CoV-2 may be circulating in deer, we tested 283 retropharyngeal lymph node (RPLN) samples collected from 151 free-living and 132 captive deer in Iowa from April 2020 through December of 2020 for the presence of SARS-CoV-2 RNA. Ninety-four of the 283 deer (33.2%; 95% CI: 28, 38.9) samples were positive for SARS-CoV-2 RNA as assessed by RT-PCR. Notably, between November 23, 2020 and January 10, 2021, 80 of 97 (82.5%; 95% CI 73.7, 88.8) RPLN samples had detectable SARS-CoV-2 RNA by RT-PCR. Whole genome sequencing of the 94 positive RPLN samples identified 12 SARS-CoV-2 lineages, with B.1.2 (n = 51; 54.5%), and B.1.311 (n = 19; 20%) accounting for ~75% of all samples. The geographic distribution and nesting of clusters of deer and human lineages strongly suggest multiple zooanthroponotic spillover events and deer-to-deer transmission. The discovery of sylvatic and enzootic SARS-CoV-2 transmission in deer has important implications for the ecology and long-term persistence, as well as the potential for spillover to other animals and spillback into humans. These findings highlight an urgent need for a robust and proactive “One Health” approach to obtaining a better understanding of the ecology and evolution of SARS-CoV-2.One-Sentence SummarySARS-CoV-2 was detected in one-third of sampled white-tailed deer in Iowa between September 2020 and January of 2021 that likely resulted from multiple human-to-deer spillover and deer-to-deer transmission events.

Selection analysis identifies unusual clustered mutational changes in Omicron lineage BA.1 that likely impact Spike function

“…Relative to evolution during normal SARS-CoV-2 person-to-person transmission, evolution within the context of either long-term infections or an alternative animal host could potentially have occurred at an accelerated pace 22,42 . In the context of either chronic infections of immunosuppressed individuals 4,22,29 , or animals that naturally sustain long-term SARS-CoV-2 infections (such as may be the case for white tailed deer given the extraordinarily high frequencies of ongoing SARS-CoV-2 infections discovered in these 43,44 ), purifying selection may have been relaxed somewhat relative to that occurring during normal human-to-human transmission: enough so for genomes carrying suboptimal combinations of epistatically interacting mutations to remain viable while fitter combinations were discovered via additional mutations and genetic recombination. In addition, chronic infections are not impacted by the tight transmission bottlenecks that can stochastically purge nascent adaptive mutations during normal transmission 45,46 .…”

Possible Cross Reactivity of Feline and White-tailed Deer Antibodies Against the SARS-CoV-2 Receptor Binding Domain

“…It is quite possible that this is the same etiological agent generating anti-RBD responses in North American cats. However, SARS-CoV-2 sequences were recently isolated from the retropharyngeal lymph nodes of wild and captive deer [69]. Regardless, further work is needed to determine the prevalence, spread, and identity of a coronavirus-like infection in North American deer.…”

Phylogenetic Tests of Models of Viral Transmission

“…This tree has implications for several aspects of the relationship between ACE2 and the occurrence of SARS-CoV-2. Palmer et al (31) stated that the ACE2 of deer and humans "share a high degree of similarity" and suggest this could account for the recent transmission of SARS-CoV-2 from humans to deer (32) 17) confuse similarity with phylogenetic relationships, and the ACE2 genes from humans, mink, and deer are far apart phylogenetically (Supplementary Figure 1). In addition, bats, pangolins and humans are also phylogenetically distant, meaning that bat-human viral transmission occurs over relatively great evolutionary distances [as do transmissible spongiform encephalopathies; (33)].…”