Multiple Introductions of SARS-CoV-2 Alpha and Delta Variants into White-Tailed Deer in Pennsylvania

Marques, Andrew; Sherrill-Mix, Scott; Everett, J.K.; Adhikari, Hriju; Reddy, Shantan; Ellis, Julie C.; Zeliff, Haley; Greening, Sabrina S.; Cannuscio, Carolyn C.; Strelau, Katherine M.; Collman, Ronald G.; Kelly, Brendan J; Rodino, Kyle G.; Bushman, Frederic D.; Gagne, Roderick B.; Anis, Eman

doi:10.1128/mbio.02101-22

Cited by 42 publications

(33 citation statements)

References 50 publications

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“…While intralineage recombination serves as an opportunity for the virus to gain additive adaptations and phenotypic advantages from distantly related circulating variants, before the emergence of XBB, recombinants have exerted only a minor impact on the course of the pandemic at present (Box 2 ). Furthermore, although there is currently very limited evidence for the establishment of long-term circulation and evolution in animal reservoir species, intensive and active surveillance of susceptible species is needed as reverse zoonosis is being documented 4 , 5 , 186 . There are many countries with low sequencing capacity, or places with previously good surveillance that are decreasing or phasing out sequencing altogether.…”

Section: Discussionmentioning

confidence: 99%

“…SARS-CoV-2 has proven to be a highly capable human pathogen, but also a generalist in terms of host tropism, establishing infections in a variety of mammalian species, including infections in farmed mink 4 , a stable reservoir in white-tailed deer 5 , 6 and incidental infections of many other animal species 7 . Once SARS-CoV-2 was in humans, the first months of SARS-CoV-2 evolution were characterized by limited adaptation and phenotypic change relative to its later evolution 8 .…”

Section: Introductionmentioning

confidence: 99%

“…The lack of intermediate sequences has led to several hypotheses of VOC origins 198 : (1) circulation in geographically undersampled regions; (2) cryptic circulation within an animal reservoir following reverse zoonosis of an early variant; (3) evolution within a chronic infection in an immunosuppressed host or multiple human hosts. Although there is evidence for establishment of stable animal reservoirs for SARS-CoV-2, particularly in farmed mink and white-tailed deer 4 , 5 , 186 , at present the ‘chronic infection hypothesis’ of variant emergence is the best supported of these scenarios 67 , 183 . Chronic infections are known to drive mutational profiles that are highly similar to those of VOCs 113 , 184 , 199 – 201 .…”

Section: Introductionmentioning

confidence: 99%

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SARS-CoV-2 variant biology: immune escape, transmission and fitness

et al. 2023

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In late 2020, after circulating for almost a year in the human population, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) exhibited a major step change in its adaptation to humans. These highly mutated forms of SARS-CoV-2 had enhanced rates of transmission relative to previous variants and were termed ‘variants of concern’ (VOCs). Designated Alpha, Beta, Gamma, Delta and Omicron, the VOCs emerged independently from one another, and in turn each rapidly became dominant, regionally or globally, outcompeting previous variants. The success of each VOC relative to the previously dominant variant was enabled by altered intrinsic functional properties of the virus and, to various degrees, changes to virus antigenicity conferring the ability to evade a primed immune response. The increased virus fitness associated with VOCs is the result of a complex interplay of virus biology in the context of changing human immunity due to both vaccination and prior infection. In this Review, we summarize the literature on the relative transmissibility and antigenicity of SARS-CoV-2 variants, the role of mutations at the furin spike cleavage site and of non-spike proteins, the potential importance of recombination to virus success, and SARS-CoV-2 evolution in the context of T cells, innate immunity and population immunity. SARS-CoV-2 shows a complicated relationship among virus antigenicity, transmission and virulence, which has unpredictable implications for the future trajectory and disease burden of COVID-19.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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SARS-CoV-2 variant biology: immune escape, transmission and fitness

et al. 2023

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“…These findings placed WTD—a species broadly distributed in North America with an estimated population size of 30 million animals ( 11 )—at the center of investigations, which demonstrated exposure of free-ranging WTD to SARS-CoV-2 and highlighted their potential to serve as a reservoir for SARS-CoV-2 in North America. Notably, results from the first studies revealed prevalence rates varying from ~30 to 40%, with animals testing positive for SARS-CoV-2 antibodies and/or viral RNA ( 12 – 16 ). Importantly, detection of SARS-CoV-2 RNA in respiratory secretions and tissues from several of the sampled animals suggested recent infection with the virus ( 12 – 14 ).…”

mentioning

confidence: 99%

White-tailed deer ( Odocoileus virginianus ) may serve as a wildlife reservoir for nearly extinct SARS-CoV-2 variants of concern

Caserta

Martins

Butt

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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The spillover of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from humans to white-tailed deer (WTD) and its ability to transmit from deer to deer raised concerns about the role of WTD in the epidemiology and ecology of the virus. Here, we present a comprehensive cross-sectional study assessing the prevalence, genetic diversity, and evolution of SARS-CoV-2 in WTD in the State of New York (NY). A total of 5,462 retropharyngeal lymph node samples collected from free-ranging hunter-harvested WTD during the hunting seasons of 2020 (Season 1, September to December 2020, n = 2,700) and 2021 (Season 2, September to December 2021, n = 2,762) were tested by SARS-CoV-2 real-time RT–PCR (rRT-PCR). SARS-CoV-2 RNA was detected in 17 samples (0.6%) from Season 1 and in 583 samples (21.1%) from Season 2. Hotspots of infection were identified in multiple confined geographic areas of NY. Sequence analysis of SARS-CoV-2 genomes from 164 samples demonstrated the presence of multiple SARS-CoV-2 lineages and the cocirculation of three major variants of concern (VOCs) (Alpha, Gamma, and Delta) in WTD. Our analysis suggests the occurrence of multiple spillover events (human to deer) of the Alpha and Delta lineages with subsequent deer-to-deer transmission and adaptation of the viruses. Detection of Alpha and Gamma variants in WTD long after their broad circulation in humans in NY suggests that WTD may serve as a wildlife reservoir for VOCs no longer circulating in humans. Thus, implementation of continuous surveillance programs to monitor SARS-CoV-2 dynamics in WTD is warranted, and measures to minimize virus transmission between humans and animals are urgently needed.

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“…So far, most of the SARS-CoV-2 isolated and reported in deer has been similar to lineages circulating among humans in the same region, which has led to proposal of multiple, recent, spillover events 27,28 . Also, a divergent Alpha-like virus has been reported in deer, providing some evidence of sustained transmission in deer 29 . Persistence of SARS-CoV-2 in wild animals might conceivably result in viral evolution through adaptation to the animal host.…”

Section: Potential Deer-to-human Transmissionmentioning

confidence: 96%

Divergent SARS-CoV-2 variant emerges in white-tailed deer with deer-to-human transmission

et al. 2022

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Wildlife reservoirs of broad-host-range viruses have the potential to enable evolution of viral variants that can emerge to infect humans. In North America, there is phylogenomic evidence of continual transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) from humans to white-tailed deer (Odocoileus virginianus) through unknown means, but no evidence of transmission from deer to humans. We carried out an observational surveillance study in Ontario, Canada during November and December 2021 (n = 300 deer) and identified a highly divergent lineage of SARS-CoV-2 in white-tailed deer (B.1.641). This lineage is one of the most divergent SARS-CoV-2 lineages identified so far, with 76 mutations (including 37 previously associated with non-human mammalian hosts). From a set of five complete and two partial deer-derived viral genomes we applied phylogenomic, recombination, selection and mutation spectrum analyses, which provided evidence for evolution and transmission in deer and a shared ancestry with mink-derived virus. Our analysis also revealed an epidemiologically linked human infection. Taken together, our findings provide evidence for sustained evolution of SARS-CoV-2 in white-tailed deer and of deer-to-human transmission.

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Multiple Introductions of SARS-CoV-2 Alpha and Delta Variants into White-Tailed Deer in Pennsylvania

Cited by 42 publications

References 50 publications

SARS-CoV-2 variant biology: immune escape, transmission and fitness

SARS-CoV-2 variant biology: immune escape, transmission and fitness

White-tailed deer ( Odocoileus virginianus ) may serve as a wildlife reservoir for nearly extinct SARS-CoV-2 variants of concern

Divergent SARS-CoV-2 variant emerges in white-tailed deer with deer-to-human transmission

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