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1. Promise and limitations of 18S genetic screening of extracted fecal DNA from wild capuchins

Author

Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Alberta Innovates Health Solutions, Queen Elizabeth II Graduate Scholarships in Science and Technology (Canada), Alberta Children's Hospital Research Institute, O'Brien Centre Summer Studentships, National Science Foundation (US), Fundación la Caixa, European Commission, Orkin, Joseph D. [0000-0001-6922-2072], Pinto, Swellan Luciann, Carvalho Henriquez, Megan, Cheves Hernández, Saúl, Duytschaever, Gwen, Wit, Janneke, Avramenko, Russell William, Gilleard, John Stuart, Orkin, Joseph D., Melin, Amanda D., Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, Alberta Innovates Health Solutions, Queen Elizabeth II Graduate Scholarships in Science and Technology (Canada), Alberta Children's Hospital Research Institute, O'Brien Centre Summer Studentships, National Science Foundation (US), Fundación la Caixa, European Commission, Orkin, Joseph D. [0000-0001-6922-2072], Pinto, Swellan Luciann, Carvalho Henriquez, Megan, Cheves Hernández, Saúl, Duytschaever, Gwen, Wit, Janneke, Avramenko, Russell William, Gilleard, John Stuart, Orkin, Joseph D., and Melin, Amanda D.

Abstract

Genomic screening of fecal DNA provides insight into diet, parasite infection dynamics, and other aspects of the ecology and pathogens of wild populations. Here, we amplify and sequence the V4/V5 regions of the eukaryotic 18S ribosomal RNA gene from fecal DNA of wild capuchin monkeys (Cebus imitator). We collected 94 fecal samples from 26 individuals, each sampled 1-4 times across a 19-month period and examined the eukaryotic diversity in 63 of these samples which had sufficient numbers and quality of reads during downstream analyses. We found a total of 234 distinct amplicon sequence variants (ASVs) classified as Eukaryotes in our samples. Of these, 66 were assigned to the phylum Nematoda. 64 ASVs are from taxa that possibly parasitize monkeys or their food items: 33 were assigned to lungworms (Superfamily Metastrongyloidae; genus Angiostrongylus), two to the genus Strongyloides, and one to the genus Austrostrongylus. The remaining 28 ASVs were assigned to nematodes that likely parasitize plants and/or invertebrates that the monkeys consume. Taken together with past dietary and coprological study of the same primate population, our results suggest that invertebrate consumption and parasitic infection, especially by lungworms, is common and widespread among this population of wild monkeys. We also discuss limitations of our approach, including the amplification of off-target ASVs, and make suggestions for future research. Overall, 18S screening shows promise for identifying various components of the capuchin gastrointestinal eukaryotic ecosystem, including parasitic helminths, and its utility will increase with the improvement of genetic databases.

Published
2023

2. A global catalog of whole-genome diversity from 233 primate species

Author

Fundación la Caixa, Vienna Science and Technology Fund, European Commission, Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brasil), International Primatological Society, Rufford Foundation, Margot Marsh Biodiversity Foundation, Primate Conservation, Fundação de Amparo à Pesquisa do Estado do Amazonas, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Brasil), German Research Foundation, National Science Foundation (US), Ministry of Science and Technology of Vietnam, Ministerio de Ciencia e Innovación (España), Agencia Estatal de Investigación (España), Generalitat de Catalunya, Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, European Research Council, Natural Environment Research Council (UK), UK Research and Innovation, Department of Biotechnology (India), San Diego Zoo Wildlife Alliance, Wenner-Gren Foundation, Leakey Foundation, National Geographic Society, National Institute on Aging (US), National Institutes of Health (US), Swedish Research Council, National Research Foundation Singapore, Government of Singapore, Kuderna, Lukas F. K. [0000-0002-9992-9295], Kuhlwilm, Martin [0000-0002-0115-1797], Orkin, Joseph D. [0000-0001-6922-2072], Valenzuela, Alejandro [0000-0001-6120-6246], Juan, David [0000-0003-1912-9667], Lizano, Esther [0000-0003-3304-9807], Navarro, Arcadi [0000-0003-2162-8246], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Kuderna, Lukas F. K., Gao, Hong, Janiak, Mareike C., Kuhlwilm, Martin, Orkin, Joseph D., Bataillon, Thomas, Manu, Shivakumara, Valenzuela, Alejandro, Bergman, Juraj, Rousselle, Marjolaine, Silva, Felipe Ennes, Agueda, Lidia, Blanc, Julie, Gut, Marta, Vries, Dorien de, Goodhead, Ian, Harris, R. Alan, Raveendran, Muthuswamy, Jensen, Axel, Chuma, Idrissa S., Horvath, Julie E., Hvilsom, Christina, Juan, David, Frandsen, Peter, Schraiber, Joshua G., Melo, Fabiano R. de, Bertuol, Fabrício, Byrne, Hazel, Sampaio, Iracilda, Farias, Izeni, Valsecchi, João, Messias, Malu, Silva, Maria N. F. da, Trivedi, Mihir, Rossi, Rogerio, Hrbek, Tomas, Andriaholinirina, Nicole, Rabarivola, Clément J., Zaramody, Alphonse, Jolly, Clifford J., Phillips-Conroy, Jane, Wilkerson, Gregory, Abee, Christian, Simmons, Joe H., Fernandez-Duque, Eduardo, Kanthaswamy, Sree, Shiferaw, Fekadu, Wu, Dongdong, Zhou, Long, Shao, Yong, Zhang, Guojie, Keyyu, Julius D., Knauf, Sascha, Le, Minh D., Lizano, Esther, Merker, Stefan, Navarro, Arcadi, Nadler, Tilo, Khor, Chiea Chuen, Lee, Jessica, Tan, Patrick, Lim, Weng Khong, Kitchener, Andrew C., Zinner, Dietmar, Gut, Ivo, Melin, Amanda D., Guschanski, Katerina, Schierup, Mikkel Heide, Beck, Robin M. D., Umapathy, Govindhaswamy, Roos, Christian, Boubli, Jean P., Rogers, Jeffrey, Farh, Kyle Kai-How, Marqués-Bonet, Tomàs, Fundación la Caixa, Vienna Science and Technology Fund, European Commission, Conselho Nacional de Desenvolvimento Científico e Tecnológico (Brasil), International Primatological Society, Rufford Foundation, Margot Marsh Biodiversity Foundation, Primate Conservation, Fundação de Amparo à Pesquisa do Estado do Amazonas, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Brasil), German Research Foundation, National Science Foundation (US), Ministry of Science and Technology of Vietnam, Ministerio de Ciencia e Innovación (España), Agencia Estatal de Investigación (España), Generalitat de Catalunya, Natural Sciences and Engineering Research Council of Canada, Canada Research Chairs, European Research Council, Natural Environment Research Council (UK), UK Research and Innovation, Department of Biotechnology (India), San Diego Zoo Wildlife Alliance, Wenner-Gren Foundation, Leakey Foundation, National Geographic Society, National Institute on Aging (US), National Institutes of Health (US), Swedish Research Council, National Research Foundation Singapore, Government of Singapore, Kuderna, Lukas F. K. [0000-0002-9992-9295], Kuhlwilm, Martin [0000-0002-0115-1797], Orkin, Joseph D. [0000-0001-6922-2072], Valenzuela, Alejandro [0000-0001-6120-6246], Juan, David [0000-0003-1912-9667], Lizano, Esther [0000-0003-3304-9807], Navarro, Arcadi [0000-0003-2162-8246], Marqués-Bonet, Tomàs [0000-0002-5597-3075], Kuderna, Lukas F. K., Gao, Hong, Janiak, Mareike C., Kuhlwilm, Martin, Orkin, Joseph D., Bataillon, Thomas, Manu, Shivakumara, Valenzuela, Alejandro, Bergman, Juraj, Rousselle, Marjolaine, Silva, Felipe Ennes, Agueda, Lidia, Blanc, Julie, Gut, Marta, Vries, Dorien de, Goodhead, Ian, Harris, R. Alan, Raveendran, Muthuswamy, Jensen, Axel, Chuma, Idrissa S., Horvath, Julie E., Hvilsom, Christina, Juan, David, Frandsen, Peter, Schraiber, Joshua G., Melo, Fabiano R. de, Bertuol, Fabrício, Byrne, Hazel, Sampaio, Iracilda, Farias, Izeni, Valsecchi, João, Messias, Malu, Silva, Maria N. F. da, Trivedi, Mihir, Rossi, Rogerio, Hrbek, Tomas, Andriaholinirina, Nicole, Rabarivola, Clément J., Zaramody, Alphonse, Jolly, Clifford J., Phillips-Conroy, Jane, Wilkerson, Gregory, Abee, Christian, Simmons, Joe H., Fernandez-Duque, Eduardo, Kanthaswamy, Sree, Shiferaw, Fekadu, Wu, Dongdong, Zhou, Long, Shao, Yong, Zhang, Guojie, Keyyu, Julius D., Knauf, Sascha, Le, Minh D., Lizano, Esther, Merker, Stefan, Navarro, Arcadi, Nadler, Tilo, Khor, Chiea Chuen, Lee, Jessica, Tan, Patrick, Lim, Weng Khong, Kitchener, Andrew C., Zinner, Dietmar, Gut, Ivo, Melin, Amanda D., Guschanski, Katerina, Schierup, Mikkel Heide, Beck, Robin M. D., Umapathy, Govindhaswamy, Roos, Christian, Boubli, Jean P., Rogers, Jeffrey, Farh, Kyle Kai-How, and Marqués-Bonet, Tomàs

Abstract

The rich diversity of morphology and behavior displayed across primate species provides an informative context in which to study the impact of genomic diversity on fundamental biological processes. Analysis of that diversity provides insight into long-standing questions in evolutionary and conservation biology and is urgent given severe threats these species are facing. Here, we present high-coverage whole-genome data from 233 primate species representing 86% of genera and all 16 families. This dataset was used, together with fossil calibration, to create a nuclear DNA phylogeny and to reassess evolutionary divergence times among primate clades. We found within-species genetic diversity across families and geographic regions to be associated with climate and sociality, but not with extinction risk. Furthermore, mutation rates differ across species, potentially influenced by effective population sizes. Lastly, we identified extensive recurrence of missense mutations previously thought to be human specific. This study will open a wide range of research avenues for future primate genomic research.

Published
2023

3. 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 Economía y Competitividad (España), Instituto de Salud Carlos III, European Commission, Generalitat de Catalunya, European Research Council, Ministerio de Ciencia, Innovación y Universidades (España), Agencia Estatal de Investigación (España), Howard Hughes Medical Institute, Obra Social la Caixa, Melin, Amanda D. [0000-0002-0612-2514], Orkin, Joseph D. [0000-0001-6922-2072], Janiak, Mareike C. [0000-0002-7759-2556], Kuderna, Lukas F. K. [0000-0002-9992-9295], Marrone, Frank [0000-0002-1735-0723], 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, 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 Economía y Competitividad (España), Instituto de Salud Carlos III, European Commission, Generalitat de Catalunya, European Research Council, Ministerio de Ciencia, Innovación y Universidades (España), Agencia Estatal de Investigación (España), Howard Hughes Medical Institute, Obra Social la Caixa, Melin, Amanda D. [0000-0002-0612-2514], Orkin, Joseph D. [0000-0001-6922-2072], Janiak, Mareike C. [0000-0002-7759-2556], Kuderna, Lukas F. K. [0000-0002-9992-9295], Marrone, Frank [0000-0002-1735-0723], 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, 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 1.5 million fatalities since it first emerged in late 2019. As we write, infection rates are currently at their highest point globally and are rising extremely rapidly in some areas due to more infectious variants. The primary viral target is the cellular receptor angiotensin-converting enzyme2 (ACE2). Recent sequence analyses of the ACE2 gene predicts 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 and finds 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

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

Author

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, 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 Economía y Competitividad (España), Instituto de Salud Carlos III, European Commission, Generalitat de Catalunya, European Research Council, Ministerio de Ciencia, Innovación y Universidades (España), Agencia Estatal de Investigación (España), Howard Hughes Medical Institute, Fundación 'la Caixa', Melin, Amanda D. [0000-0002-0612-2514], Orkin, Joseph D. [0000-0001-6922-2072], Janiak, Mareike C. [0000-0002-7759-2556], Kuderna, Lukas F. K. [0000-0002-9992-9295], Marrone, Frank [0000-0002-1735-0723], Arora, Paramjit S. [0000-0001-5315-401X], Higham, James P. [0000-0002-1133-2030], Melin, Amanda D., Orkin, Joseph D., Janiak, Mareike C., Kuderna, Lukas F. K., Marrone, Frank, Arora, Paramjit S., and Higham, James P.

Abstract

Versión editorial disponible en: http://hdl.handle.net/10261/239013, The novel coronavirus SARS-CoV-2, which in humans leads to the disease COVID-19, has caused global disruption and more than 1.5 million fatalities since it first emerged in late 2019. As we write, infection rates are currently at their highest point globally and are rising extremely rapidly in some areas due to more infectious variants. The primary viral target is the cellular receptor angiotensin-converting enzyme2 (ACE2). Recent sequence analyses of the ACE2 gene predicts 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 and finds 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 by the 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 the Natural Environment Research Council (NERC NE/T000341/1). IG and MG acknowledge the support of the Spanish Ministry of Science and Innovation through the Instituto de Salud Carlos III and the 2014–2020 Smart Growth Operating Program, to the EMBL partnership and cofinancing with the European Regional Development Fund (MINECO/FEDER, BIO2015-71792-P). We also acknowledge the support of the Centro de Excelencia Severo Ochoa, and the Generalitat de Catalunya through the Departament de Salut, Departament 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 innovation programme (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 International Early Career, Obra Social "La Caixa" and Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880). PSA thanks the National Institutes of Health (R35GM130333) for financial support. E.L is supported by CGL2017- 82654-P (MINECO/FEDER,UE). EDJ and OF's contributions were supported by funds from Howard Hughes Medical Institute and the Rockefeller University. Chris Smith drew the images for Figure 1. The authors would like to thank the Veterinary and Zoology staff at Wildlife Reserves Singapore for their help in obtaining the tissue samples, as well as the Lee Kong Chian Natural History Museum for storage and provision of the tissue samples.

Published
2021

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