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1. Variation in predicted COVID‐19 risk among lemurs and lorises

Author

Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Natural Environment Research Council (UK), Ministerio de Ciencia, Innovación y Universidades (España), Instituto de Salud Carlos III, Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), European Commission, Generalitat de Catalunya, Fundación la Caixa, Howard Hughes Medical Institute, National Institutes of Health (US), Rockefeller University, Melin, Amanda D. [0000-0002-0612-2514], Orkin, Joseph D. [0000-0001-6922-2072], Janiak, Mareike C. [0000-0002-7759-2556], Valenzuela, Alejandro [0000-0002-2252-3887], Kuderna, Lukas F. K. [0000-0002-9992-9295], Marrone, Frank [0000-0002-1735-0723], Ramangason, Hasinala [0000-0003-4222-7476], Horvath, Julie E. [0000-0002-6426-035X], Roos, Christian [0000-0003-0190-4266], Kitchener, Andrew C. [0000-0003-2594-0827], Khor, Chiea Chuen [0000-0002-1128-4729], Lim, Weng Khong [0000-0003-4391-1130], Umapathy, Govindhaswamy [0000-0003-4086-7445], Raveendran, Muthuswamy [0000-0001-6185-4059], Harris, R. Alan [0000-0002-7333-4752], Gut, Ivo [0000-0001-7219-632X], Gut, Marta [0000-0002-4063-7159], Lizano, Esther 0000-0003-3304-9807], Zinner, Dietmar [0000-0003-3967-8014], Manu, Sivakumara [0000-0002-9114-8793], Johnson, Steig E. [0000-0003-2257-8949], Fedrigo, Olivier [0000-0002-6450-7551], Farh, Kyle Kai-How [0000-0001-6947-8537], Rogers, Jeffrey [0000-0002-7374-6490], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Navarro, Arcadi [0000-0003-2162-8246], Juan, David [0000-0003-1912-9667], Arora, Paramjit S. [0000-0001-5315-401X], Higham, James P. [0000-0002-1133-2030], Melin, Amanda D., Orkin, Joseph D., Janiak, Mareike C., Valenzuela, Alejandro, Kuderna, Lukas F. K., Marrone, Frank, Ramangason, Hasinala, Horvath, Julie E., Roos, Christian, Kitchener, Andrew C., Khor, Chiea Chuen, Lim, Weng Khong, Lee, Jessica G. H., Tan, Patrick, Umapathy, Govindhaswamy, Raveendran, Muthuswamy, Harris, R. Alan, Gut, Ivo, Gut, Marta, Lizano, Esther, Nadler, Tilo, Zinner, Dietmar, Le, Minh D., Manu, Sivakumara, Rabarivola, Clément J., Zaramody, Alphonse, Andriaholinirina, Nicole, Johnson, Steig E., Jarvis, Erich D., Fedrigo, Olivier, Wu, Dongdong, Zhang, Guojie, Farh, Kyle Kai-How, Rogers, Jeffrey, Marqués-Bonet, Tomàs, Navarro, Arcadi, Juan, David, Arora, Paramjit S., Higham, James P., Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Natural Environment Research Council (UK), Ministerio de Ciencia, Innovación y Universidades (España), Instituto de Salud Carlos III, Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), European Commission, Generalitat de Catalunya, Fundación la Caixa, Howard Hughes Medical Institute, National Institutes of Health (US), Rockefeller University, Melin, Amanda D. [0000-0002-0612-2514], Orkin, Joseph D. [0000-0001-6922-2072], Janiak, Mareike C. [0000-0002-7759-2556], Valenzuela, Alejandro [0000-0002-2252-3887], Kuderna, Lukas F. K. [0000-0002-9992-9295], Marrone, Frank [0000-0002-1735-0723], Ramangason, Hasinala [0000-0003-4222-7476], Horvath, Julie E. [0000-0002-6426-035X], Roos, Christian [0000-0003-0190-4266], Kitchener, Andrew C. [0000-0003-2594-0827], Khor, Chiea Chuen [0000-0002-1128-4729], Lim, Weng Khong [0000-0003-4391-1130], Umapathy, Govindhaswamy [0000-0003-4086-7445], Raveendran, Muthuswamy [0000-0001-6185-4059], Harris, R. Alan [0000-0002-7333-4752], Gut, Ivo [0000-0001-7219-632X], Gut, Marta [0000-0002-4063-7159], Lizano, Esther 0000-0003-3304-9807], Zinner, Dietmar [0000-0003-3967-8014], Manu, Sivakumara [0000-0002-9114-8793], Johnson, Steig E. [0000-0003-2257-8949], Fedrigo, Olivier [0000-0002-6450-7551], Farh, Kyle Kai-How [0000-0001-6947-8537], Rogers, Jeffrey [0000-0002-7374-6490], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Navarro, Arcadi [0000-0003-2162-8246], Juan, David [0000-0003-1912-9667], Arora, Paramjit S. [0000-0001-5315-401X], Higham, James P. [0000-0002-1133-2030], Melin, Amanda D., Orkin, Joseph D., Janiak, Mareike C., Valenzuela, Alejandro, Kuderna, Lukas F. K., Marrone, Frank, Ramangason, Hasinala, Horvath, Julie E., Roos, Christian, Kitchener, Andrew C., Khor, Chiea Chuen, Lim, Weng Khong, Lee, Jessica G. H., Tan, Patrick, Umapathy, Govindhaswamy, Raveendran, Muthuswamy, Harris, R. Alan, Gut, Ivo, Gut, Marta, Lizano, Esther, Nadler, Tilo, Zinner, Dietmar, Le, Minh D., Manu, Sivakumara, Rabarivola, Clément J., Zaramody, Alphonse, Andriaholinirina, Nicole, Johnson, Steig E., Jarvis, Erich D., Fedrigo, Olivier, Wu, Dongdong, Zhang, Guojie, Farh, Kyle Kai-How, Rogers, Jeffrey, Marqués-Bonet, Tomàs, Navarro, Arcadi, Juan, David, Arora, Paramjit S., and Higham, James P.

Abstract

The novel coronavirus SARS‐CoV‐2, which in humans leads to the disease COVID‐19, has caused global disruption and more than 2 million fatalities since it first emerged in late 2019. As we write, infection rates are at their highest point globally and are rising extremely rapidly in some areas due to more infectious variants. The primary target of SARS‐CoV‐2 is the cellular receptor angiotensin‐converting enzyme‐2 (ACE2). Recent sequence analyses of the ACE2 gene predict that many nonhuman primates are also likely to be highly susceptible to infection. However, the anticipated risk is not equal across the Order. Furthermore, some taxonomic groups show high ACE2 amino acid conservation, while others exhibit high variability at this locus. As an example of the latter, analyses of strepsirrhine primate ACE2 sequences to date indicate large variation among lemurs and lorises compared to other primate clades despite low sampling effort. Here, we report ACE2 gene and protein sequences for 71 individual strepsirrhines, spanning 51 species and 19 genera. Our study reinforces previous results while finding additional variability in other strepsirrhine species, and suggests several clades of lemurs have high potential susceptibility to SARS‐CoV‐2 infection. Troublingly, some species, including the rare and endangered aye‐aye (Daubentonia madagascariensis), as well as those in the genera Avahi and Propithecus, may be at high risk. Given that lemurs are endemic to Madagascar and among the primates at highest risk of extinction globally, further understanding of the potential threat of COVID‐19 to their health should be a conservation priority. All feasible actions should be taken to limit their exposure to SARS‐CoV‐2.

Published
2021

2. Variation in predicted COVID-19 risk among lemurs and lorises

Author

Jeffrey Rogers, Dietmar Zinner, Tilo Nadler, Chiea Chuen Khor, Muthuswamy Raveendran, Weng Khong Lim, Tomas Marques-Bonet, Kyle Kai-How Farh, Frank Marrone, Alejandro E. J. Valenzuela, C. Rabarivola, Minh Duc Le, Erich D. Jarvis, Govindhaswamy Umapathy, Joseph D. Orkin, Hasinala Ramangason, Andrew C. Kitchener, Nicole Volasoa Andriaholinirina, Dong-Dong Wu, Paramjit S. Arora, Ivo Gut, Amanda D. Melin, Lukas F. K. Kuderna, Sivakumara Manu, Esther Lizano, Alphonse Zaramody, Olivier Fedrigo, Guojie Zhang, Mareike C Janiak, R. Alan Harris, Patrick Tan, Arcadi Navarro, Steig E. Johnson, David Juan, Christian Roos, James P. Higham, Marta Gut, Jessica G. H. Lee, Julie E. Horvath, Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Natural Environment Research Council (UK), Ministerio de Ciencia, Innovación y Universidades (España), Instituto de Salud Carlos III, Agencia Estatal de Investigación (España), Ministerio de Economía y Competitividad (España), European Commission, Generalitat de Catalunya, Fundación 'la Caixa', Howard Hughes Medical Institute, National Institutes of Health (US), Rockefeller University, Melin, Amanda D. [0000-0002-0612-2514], Orkin, Joseph D. [0000-0001-6922-2072], Janiak, Mareike C. [0000-0002-7759-2556], Valenzuela, Alejandro [0000-0002-2252-3887], Kuderna, Lukas F. K. [0000-0002-9992-9295], Marrone, Frank [0000-0002-1735-0723], Ramangason, Hasinala [0000-0003-4222-7476], Horvath, Julie E. [0000-0002-6426-035X], Roos, Christian [0000-0003-0190-4266], Kitchener, Andrew C. [0000-0003-2594-0827], Khor, Chiea Chuen [0000-0002-1128-4729], Lim, Weng Khong [0000-0003-4391-1130], Umapathy, Govindhaswamy [0000-0003-4086-7445], Raveendran, Muthuswamy [0000-0001-6185-4059], Harris, R. Alan [0000-0002-7333-4752], Gut, Ivo [0000-0001-7219-632X], Gut, Marta [0000-0002-4063-7159], Lizano, Esther 0000-0003-3304-9807], Zinner, Dietmar [0000-0003-3967-8014], Manu, Sivakumara [0000-0002-9114-8793], Johnson, Steig E. [0000-0003-2257-8949], Fedrigo, Olivier [0000-0002-6450-7551], Farh, Kyle Kai-How [0000-0001-6947-8537], Rogers, Jeffrey [0000-0002-7374-6490], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Navarro, Arcadi [0000-0003-2162-8246], Juan, David [0000-0003-1912-9667], Arora, Paramjit S. [0000-0001-5315-401X], Higham, James P. [0000-0002-1133-2030], Melin, Amanda D., Orkin, Joseph D., Janiak, Mareike C., Valenzuela, Alejandro, Kuderna, Lukas F. K., Marrone, Frank, Ramangason, Hasinala, Horvath, Julie E., Roos, Christian, Kitchener, Andrew C., Khor, Chiea Chuen, Lim, Weng Khong, Umapathy, Govindhaswamy, Raveendran, Muthuswamy, Harris, R. Alan, Gut, Ivo, Gut, Marta, Zinner, Dietmar, Manu, Sivakumara, Johnson, Steig E., Fedrigo, Olivier, Farh, Kyle Kai-How, Rogers, Jeffrey, Marqués-Bonet, Tomàs, Navarro, Arcadi, Juan, David, Arora, Paramjit S., and Higham, James P.

Subjects
0106 biological sciences, Propithecus, Endangered species, Lemur, Locus (genetics), COVID-19 (Malaltia), 010603 evolutionary biology, 01 natural sciences, Lèmurs, Article, Lorisidae, 03 medical and health sciences, 0302 clinical medicine, Risk Factors, biology.animal, Animals, 0501 psychology and cognitive sciences, Primate, 030212 general & internal medicine, Taxonomic rank, 050102 behavioral science & comparative psychology, Clade, Ecology, Evolution, Behavior and Systematics, Research Articles, 030304 developmental biology, 0303 health sciences, Extinction, biology, Lorísids, 05 social sciences, Primate Diseases, COVID-19, biology.organism_classification, Evolutionary biology, Animal Science and Zoology, Angiotensin-Converting Enzyme 2, Genètica, Research Article
Abstract

Versión preprint disponible en: http://hdl.handle.net/10261/229066, The novel coronavirus SARS‐CoV‐2, which in humans leads to the disease COVID‐19, has caused global disruption and more than 2 million fatalities since it first emerged in late 2019. As we write, infection rates are at their highest point globally and are rising extremely rapidly in some areas due to more infectious variants. The primary target of SARS‐CoV‐2 is the cellular receptor angiotensin‐converting enzyme‐2 (ACE2). Recent sequence analyses of the ACE2 gene predict that many nonhuman primates are also likely to be highly susceptible to infection. However, the anticipated risk is not equal across the Order. Furthermore, some taxonomic groups show high ACE2 amino acid conservation, while others exhibit high variability at this locus. As an example of the latter, analyses of strepsirrhine primate ACE2 sequences to date indicate large variation among lemurs and lorises compared to other primate clades despite low sampling effort. Here, we report ACE2 gene and protein sequences for 71 individual strepsirrhines, spanning 51 species and 19 genera. Our study reinforces previous results while finding additional variability in other strepsirrhine species, and suggests several clades of lemurs have high potential susceptibility to SARS‐CoV‐2 infection. Troublingly, some species, including the rare and endangered aye‐aye (Daubentonia madagascariensis), as well as those in the genera Avahi and Propithecus, may be at high risk. Given that lemurs are endemic to Madagascar and among the primates at highest risk of extinction globally, further understanding of the potential threat of COVID‐19 to their health should be a conservation priority. All feasible actions should be taken to limit their exposure to SARS‐CoV‐2., ADM is supported bythe Natural Sciences and Engineering Research Council of Canada(NSERC Discovery Grant) and Canada Research Chairs Program.MCJ's postdoctoral appointment is supported by funding from theNatural Environment Research Council (NERC NE/T000341/1). IGand MG acknowledge the support of the Spanish Ministry of Scienceand Innovation through the Instituto de Salud Carlos III and the2014–2020 Smart Growth Operating Program, to the EMBL part-nership and cofinancing with the European Regional DevelopmentFund (MINECO/FEDER, BIO201571792P). We also acknowledgethe support of the Centro de Excelencia Severo Ochoa, and theGeneralitat de Catalunya through the Departament de Salut, De-partament d'Empresa i Coneixement and the CERCA Programme.TMB is supported by funding from the European Research Council(ERC) under the European Union's Horizon 2020 research and in-novation program (grant agreement No. 864203), BFU201786471P (MINECO/FEDER, UE), “Unidad de Excelencia María de Maeztu”,funded by the AEI (CEX2018000792M), Howard Hughes Interna-tional Early Career, Obra Social "La Caixa" and Secretaria d'Uni-versitats i Recerca and CERCA Programme del Departamentd'Economia i Coneixement de la Generalitat de Catalunya (GRC2017 SGR 880). PSA thanks the National Institutes of Health(R35GM130333) for financial support. EL is supported by CGL201782654P (MINECO/FEDER, UE). EDJ and OF's contributions weresupported by funds from Howard Hughes Medical Institute and theRockefeller University. Chris Smith drew the images for Figure 1. Theauthors would like to thank the Veterinary and Zoology staff atWildlife Reserves Singapore for their help in obtaining the tissuesamples, as well as the Lee Kong Chian Natural History Museum forstorage and provision of the tissue samples. Finally, we thank tworeviewers for quick and constructive comments, and Karen Bales forher supportive editorial oversight

Published
2021

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