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Transmission of SARS-CoV-2 in domestic cats imposes a narrow bottleneck

View ORCID ProfileKatarina M. Braun, View ORCID ProfileGage K. Moreno, View ORCID ProfilePeter J. Halfmann, View ORCID ProfileEmma B. Hodcroft, David A. Baker, Emma C. Boehm, Andrea M. Weiler, View ORCID ProfileAmelia K. Haj, Masato Hatta, Shiho Chiba, Tadashi Maemura, View ORCID ProfileYoshihiro Kawaoka, View ORCID ProfileKatia Koelle, View ORCID ProfileDavid H. O’Connor, View ORCID ProfileThomas C. Friedrich
doi: https://doi.org/10.1101/2020.11.16.384917
Katarina M. Braun
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, United States of America
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  • ORCID record for Katarina M. Braun
Gage K. Moreno
2Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, United States of America
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Peter J. Halfmann
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, United States of America
3Influenza Research Institute, School of Veterinary Sciences, University of Wisconsin-Madison, Madison, WI, United States
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Emma B. Hodcroft
4Institute of Social and Preventative Medicine, University of Bern, Bern, Switzerland
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David A. Baker
2Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, United States of America
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Emma C. Boehm
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, United States of America
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Andrea M. Weiler
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, United States of America
5Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, United States of America
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Amelia K. Haj
2Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, United States of America
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  • ORCID record for Amelia K. Haj
Masato Hatta
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, United States of America
3Influenza Research Institute, School of Veterinary Sciences, University of Wisconsin-Madison, Madison, WI, United States
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Shiho Chiba
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, United States of America
3Influenza Research Institute, School of Veterinary Sciences, University of Wisconsin-Madison, Madison, WI, United States
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Tadashi Maemura
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, United States of America
3Influenza Research Institute, School of Veterinary Sciences, University of Wisconsin-Madison, Madison, WI, United States
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Yoshihiro Kawaoka
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, United States of America
3Influenza Research Institute, School of Veterinary Sciences, University of Wisconsin-Madison, Madison, WI, United States
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Katia Koelle
5Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, United States of America
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  • ORCID record for Katia Koelle
David H. O’Connor
2Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI, United States of America
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Thomas C. Friedrich
1Department of Pathobiological Sciences, University of Wisconsin-Madison, Madison, WI, United States of America
5Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, United States of America
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  • For correspondence: tfriedri@wisc.edu
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Abstract

The evolutionary mechanisms by which SARS-CoV-2 viruses adapt to mammalian hosts and, potentially, undergo antigenic evolution depend on the ways genetic variation is generated and selected within and between individual hosts. Using domestic cats as a model, we show that SARS-CoV-2 consensus sequences remain largely unchanged over time within hosts, while dynamic sub-consensus diversity reveals processes of genetic drift and weak purifying selection. We further identify a notable variant at amino acid position 655 in Spike (H655Y), which was previously shown to confer escape from human monoclonal antibodies. This variant arises rapidly and persists at intermediate frequencies in index cats. It also becomes fixed following transmission in two of three pairs. These dynamics suggest this site may be under positive selection in this system and illustrate how a variant can quickly arise and become fixed in parallel across multiple transmission pairs. Transmission of SARS-CoV-2 in cats involved a narrow bottleneck, with new infections founded by fewer than ten viruses. In RNA virus evolution, stochastic processes like narrow transmission bottlenecks and genetic drift typically act to constrain the overall pace of adaptive evolution. Our data suggest that here, positive selection in index cats followed by a narrow transmission bottleneck may have instead accelerated the fixation of S H655Y, a potentially beneficial SARS-CoV-2 variant. Overall, our study suggests species- and context-specific adaptations are likely to continue to emerge. This underscores the importance of continued genomic surveillance for new SARS-CoV-2 variants as well as heightened scrutiny for signatures of SARS-CoV-2 positive selection in humans and mammalian model systems.

Author summary Through ongoing human adaptation, spill-back events from other animal intermediates, or with the distribution of vaccines and therapeutics, the landscape of SARS-CoV-2 genetic variation is certain to change. The evolutionary mechanisms by which SARS-CoV-2 will continue to adapt to mammalian hosts depend on genetic variation generated within and between hosts. Here, using domestic cats as a model, we show that within-host SARS-CoV-2 genetic variation is predominantly influenced by genetic drift and purifying selection. Transmission of SARS-CoV-2 between hosts is defined by a narrow transmission bottleneck, involving 2-5 viruses. We further identify a notable variant at amino acid position 655 in Spike (H655Y), which arises rapidly and is transmitted in cats. Spike H655Y has been previously shown to confer escape from human monoclonal antibodies and is currently found in over 1000 human sequences. Overall, our study suggests species- and context-specific adaptations are likely to continue to emerge, underscoring the importance of continued genomic surveillance in humans and non-human mammalian hosts.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://www.ncbi.nlm.nih.gov/bioproject/666926

  • https://github.com/katarinabraun/SARSCoV2_transmission_in_domestic_cats

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted January 04, 2021.
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Transmission of SARS-CoV-2 in domestic cats imposes a narrow bottleneck
Katarina M. Braun, Gage K. Moreno, Peter J. Halfmann, Emma B. Hodcroft, David A. Baker, Emma C. Boehm, Andrea M. Weiler, Amelia K. Haj, Masato Hatta, Shiho Chiba, Tadashi Maemura, Yoshihiro Kawaoka, Katia Koelle, David H. O’Connor, Thomas C. Friedrich
bioRxiv 2020.11.16.384917; doi: https://doi.org/10.1101/2020.11.16.384917
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Transmission of SARS-CoV-2 in domestic cats imposes a narrow bottleneck
Katarina M. Braun, Gage K. Moreno, Peter J. Halfmann, Emma B. Hodcroft, David A. Baker, Emma C. Boehm, Andrea M. Weiler, Amelia K. Haj, Masato Hatta, Shiho Chiba, Tadashi Maemura, Yoshihiro Kawaoka, Katia Koelle, David H. O’Connor, Thomas C. Friedrich
bioRxiv 2020.11.16.384917; doi: https://doi.org/10.1101/2020.11.16.384917

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