A Strategy To Estimate Unknown Viral Diversity in Mammals
ABSTRACT The majority of emerging zoonoses originate in wildlife, and many are caused by viruses. However, there are no rigorous estimates of total viral diversity (here termed “virodiversity”) for any wildlife species, despite the utility of this to future surveillance and control of emerging zoono...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2013-11-01
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| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00598-13 |
| _version_ | 1818750808901025792 |
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| author | Simon J. Anthony Jonathan H. Epstein Kris A. Murray Isamara Navarrete-Macias Carlos M. Zambrana-Torrelio Alexander Solovyov Rafael Ojeda-Flores Nicole C. Arrigo Ariful Islam Shahneaz Ali Khan Parviez Hosseini Tiffany L. Bogich Kevin J. Olival Maria D. Sanchez-Leon William B. Karesh Tracey Goldstein Stephen P. Luby Stephen S. Morse Jonna A. K. Mazet Peter Daszak W. Ian Lipkin |
| author_facet | Simon J. Anthony Jonathan H. Epstein Kris A. Murray Isamara Navarrete-Macias Carlos M. Zambrana-Torrelio Alexander Solovyov Rafael Ojeda-Flores Nicole C. Arrigo Ariful Islam Shahneaz Ali Khan Parviez Hosseini Tiffany L. Bogich Kevin J. Olival Maria D. Sanchez-Leon William B. Karesh Tracey Goldstein Stephen P. Luby Stephen S. Morse Jonna A. K. Mazet Peter Daszak W. Ian Lipkin |
| author_sort | Simon J. Anthony |
| collection | DOAJ |
| description | ABSTRACT The majority of emerging zoonoses originate in wildlife, and many are caused by viruses. However, there are no rigorous estimates of total viral diversity (here termed “virodiversity”) for any wildlife species, despite the utility of this to future surveillance and control of emerging zoonoses. In this case study, we repeatedly sampled a mammalian wildlife host known to harbor emerging zoonotic pathogens (the Indian Flying Fox, Pteropus giganteus) and used PCR with degenerate viral family-level primers to discover and analyze the occurrence patterns of 55 viruses from nine viral families. We then adapted statistical techniques used to estimate biodiversity in vertebrates and plants and estimated the total viral richness of these nine families in P. giganteus to be 58 viruses. Our analyses demonstrate proof-of-concept of a strategy for estimating viral richness and provide the first statistically supported estimate of the number of undiscovered viruses in a mammalian host. We used a simple extrapolation to estimate that there are a minimum of 320,000 mammalian viruses awaiting discovery within these nine families, assuming all species harbor a similar number of viruses, with minimal turnover between host species. We estimate the cost of discovering these viruses to be ~$6.3 billion (or ~$1.4 billion for 85% of the total diversity), which if annualized over a 10-year study time frame would represent a small fraction of the cost of many pandemic zoonoses. IMPORTANCE Recent years have seen a dramatic increase in viral discovery efforts. However, most lack rigorous systematic design, which limits our ability to understand viral diversity and its ecological drivers and reduces their value to public health intervention. Here, we present a new framework for the discovery of novel viruses in wildlife and use it to make the first-ever estimate of the number of viruses that exist in a mammalian host. As pathogens continue to emerge from wildlife, this estimate allows us to put preliminary bounds around the potential size of the total zoonotic pool and facilitates a better understanding of where best to allocate resources for the subsequent discovery of global viral diversity. |
| first_indexed | 2024-12-18T04:25:34Z |
| format | Article |
| id | doaj.art-f32ecba3a5ea46be98ef144342eab4be |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-18T04:25:34Z |
| publishDate | 2013-11-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-f32ecba3a5ea46be98ef144342eab4be2022-12-21T21:21:07ZengAmerican Society for MicrobiologymBio2150-75112013-11-014510.1128/mBio.00598-13A Strategy To Estimate Unknown Viral Diversity in MammalsSimon J. Anthony0Jonathan H. Epstein1Kris A. Murray2Isamara Navarrete-Macias3Carlos M. Zambrana-Torrelio4Alexander Solovyov5Rafael Ojeda-Flores6Nicole C. Arrigo7Ariful Islam8Shahneaz Ali Khan9Parviez Hosseini10Tiffany L. Bogich11Kevin J. Olival12Maria D. Sanchez-Leon13William B. Karesh14Tracey Goldstein15Stephen P. Luby16Stephen S. Morse17Jonna A. K. Mazet18Peter Daszak19W. Ian Lipkin20Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York, USAEcoHealth Alliance, New York, New York, USAEcoHealth Alliance, New York, New York, USACenter for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York, USAEcoHealth Alliance, New York, New York, USACenter for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York, USAFacultad de Medicina Veterinaria and Zootecnia, Universidad Nacional Autónoma de México, Ciudad Universitaria, Mexico City, Distrito Federal, MexicoCenter for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York, USAEcoHealth Alliance, New York, New York, USAChittagong Veterinary and Animal Sciences University, Chittagong, BangladeshEcoHealth Alliance, New York, New York, USAPrinceton University, Department of Ecology and Evolutionary Biology, Princeton, New Jersey, USAEcoHealth Alliance, New York, New York, USACenter for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York, USAEcoHealth Alliance, New York, New York, USAOne Health Institute & Wildlife Health Center, School of Veterinary Medicine, University of California Davis, Davis, California, USAInternational Center for Diarrhoeal Disease Research, Dhaka, BangladeshOne Health Institute & Wildlife Health Center, School of Veterinary Medicine, University of California Davis, Davis, California, USAOne Health Institute & Wildlife Health Center, School of Veterinary Medicine, University of California Davis, Davis, California, USAEcoHealth Alliance, New York, New York, USACenter for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York, USAABSTRACT The majority of emerging zoonoses originate in wildlife, and many are caused by viruses. However, there are no rigorous estimates of total viral diversity (here termed “virodiversity”) for any wildlife species, despite the utility of this to future surveillance and control of emerging zoonoses. In this case study, we repeatedly sampled a mammalian wildlife host known to harbor emerging zoonotic pathogens (the Indian Flying Fox, Pteropus giganteus) and used PCR with degenerate viral family-level primers to discover and analyze the occurrence patterns of 55 viruses from nine viral families. We then adapted statistical techniques used to estimate biodiversity in vertebrates and plants and estimated the total viral richness of these nine families in P. giganteus to be 58 viruses. Our analyses demonstrate proof-of-concept of a strategy for estimating viral richness and provide the first statistically supported estimate of the number of undiscovered viruses in a mammalian host. We used a simple extrapolation to estimate that there are a minimum of 320,000 mammalian viruses awaiting discovery within these nine families, assuming all species harbor a similar number of viruses, with minimal turnover between host species. We estimate the cost of discovering these viruses to be ~$6.3 billion (or ~$1.4 billion for 85% of the total diversity), which if annualized over a 10-year study time frame would represent a small fraction of the cost of many pandemic zoonoses. IMPORTANCE Recent years have seen a dramatic increase in viral discovery efforts. However, most lack rigorous systematic design, which limits our ability to understand viral diversity and its ecological drivers and reduces their value to public health intervention. Here, we present a new framework for the discovery of novel viruses in wildlife and use it to make the first-ever estimate of the number of viruses that exist in a mammalian host. As pathogens continue to emerge from wildlife, this estimate allows us to put preliminary bounds around the potential size of the total zoonotic pool and facilitates a better understanding of where best to allocate resources for the subsequent discovery of global viral diversity.https://journals.asm.org/doi/10.1128/mBio.00598-13 |
| spellingShingle | Simon J. Anthony Jonathan H. Epstein Kris A. Murray Isamara Navarrete-Macias Carlos M. Zambrana-Torrelio Alexander Solovyov Rafael Ojeda-Flores Nicole C. Arrigo Ariful Islam Shahneaz Ali Khan Parviez Hosseini Tiffany L. Bogich Kevin J. Olival Maria D. Sanchez-Leon William B. Karesh Tracey Goldstein Stephen P. Luby Stephen S. Morse Jonna A. K. Mazet Peter Daszak W. Ian Lipkin A Strategy To Estimate Unknown Viral Diversity in Mammals mBio |
| title | A Strategy To Estimate Unknown Viral Diversity in Mammals |
| title_full | A Strategy To Estimate Unknown Viral Diversity in Mammals |
| title_fullStr | A Strategy To Estimate Unknown Viral Diversity in Mammals |
| title_full_unstemmed | A Strategy To Estimate Unknown Viral Diversity in Mammals |
| title_short | A Strategy To Estimate Unknown Viral Diversity in Mammals |
| title_sort | strategy to estimate unknown viral diversity in mammals |
| url | https://journals.asm.org/doi/10.1128/mBio.00598-13 |
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