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Host and viral traits predict zoonotic spillover from mammals
Open accessAbstract
The majority of human emerging infectious diseases are zoonotic, with viruses that originate in wild mammals of particular concern (for example, HIV, Ebola and SARS). Understanding patterns of viral diversity in wildlife and determinants of successful cross-species transmission, or spillover, are therefore key goals for pandemic surveillance programs. However, few analytical tools exist to identify which host species are likely to harbour the next human virus, or which viruses can cross species boundaries. Here we conduct a comprehensive analysis of mammalian host-virus relationships and show that both the total number of viruses that infect a given species and the proportion likely to be zoonotic are predictable. After controlling for research effort, the proportion of zoonotic viruses per species is predicted by phylogenetic relatedness to humans, host taxonomy and human population within a species range-which may reflect human-wildlife contact. We demonstrate that bats harbour a significantly higher proportion of zoonotic viruses than all other mammalian orders. We also identify the taxa and geographic regions with the largest estimated number of 'missing viruses' and 'missing zoonoses' and therefore of highest value for future surveillance. We then show that phylogenetic host breadth and other viral traits are significant predictors of zoonotic potential, providing a novel framework to assess if a newly discovered mammalian virus could infect people.
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“Cross-species transmission results from a complex interplay between the characteristics of the pathogen (2, 10–12): the original host’s infection, behavior, and ecology; how the pathogen is shed into and survives in the environment; how humans are exposed to the pathogen; and how susceptible those humans are to infection (4, 12–16).”
From Impacts of biodiversity and biodiversity loss on zoonotic diseases (2021) · cites this paper as [11]
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“In recent analyses, rodents have also emerged as the most likely source (21, 23) or one of the most likely (11, 27).”
From Impacts of biodiversity and biodiversity loss on zoonotic diseases (2021) · cites this paper as [11]
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“Even fruit bats are kept as pets [176] and it is known that bats harbor a higher proportion of zoonoses than all other mammalian orders, including rabies-like viruses that are highly pathogenic for people. [177].”
From A One Health Perspective on the Human-Companion Animal Relationship with Emphasis on Zoonotic Aspects. (2020) · cites this paper as [177]
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Citations
Cites
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662
APE: analyses of phylogenetics and evolution in R language
Paradis, E., Claude, J., & Strimmer, K. (2004) · Bioinformatics · doi:10.1093/bioinformatics/btg412 · Cited by 11,335
Phylogenies and the Comparative Method
Felsenstein, J. (1985) · The American Naturalist · doi:10.1086/284325 · Cited by 9,793
Global trends in emerging infectious diseases
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L., & Daszak, P. (2008) · Nature · doi:10.1038/nature06536 · Cited by 8,338
Self-citationA Rapid Bootstrap Algorithm for the RAxML Web Servers
Stamatakis, A., Hoover, P., & Rougemont, J. (2008) · Systematic Biology · doi:10.1080/10635150802429642 · Cited by 7,028
TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE
Blomberg, S. P., Garland, T., & Ives, A. R. (2003) · Evolution · doi:10.1111/j.0014-3820.2003.tb00285.x · Cited by 4,678
Risk factors for human disease emergence
Taylor, L. H., Latham, S. M., & woolhouse, M. E. J. (2001) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2001.0888 · Cited by 2,835
Cellular Scaling Rules for the Brains of Marsupials: Not as “Primitive” as Expected
Santos, S. E. D., Porfírio, J., Cunha, F., Manger, P. R., Tavares, W. C., Pessôa, L. M., Raghanti, M. A., Sherwood, C. C., & Herculano‐Houzel, S. (2017) · Brain Behavior and Evolution · doi:10.1159/000452856 · Cited by 2,652
Grafen, A. (1989) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1989.0106 · Cited by 2,142
The delayed rise of present-day mammals
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L., & Purvis, A. (2007) · Nature · doi:10.1038/nature05634 · Cited by 2,082
Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor
Ge, X.-Y., Li, J.-L., Yang, X.-L., Chmura, A. A., Zhu, G., Epstein, J. H., Mazet, J. K., Hu, B., Zhang, W., Peng, C., et al. (2013) · Nature · doi:10.1038/nature12711 · Cited by 1,778
Self-citationJones, K. E., Bielby, J., Cardillo, M., Fritz, S. A., O'Dell, J., Orme, C. D. L., Safi, K., Sechrest, W., Boakes, E. H., Carbone, C., et al. (2009) · Ecology · doi:10.1890/08-1494.1 · Cited by 1,662
Host Range and Emerging and Reemerging Pathogens
Woolhouse, M. E. J., & Gowtage-Sequeria, S. (2005) · Emerging Infectious Diseases · doi:10.3201/eid1112.050997 · Cited by 1,586
Bats: Important Reservoir Hosts of Emerging Viruses
Calisher, C. H., Childs, J. E., Field, H. E., Holmes, K. V., & Schountz, T. (2006) · Clinical Microbiology Reviews · doi:10.1128/cmr.00017-06 · Cited by 1,520
An Update of Wallace’s Zoogeographic Regions of the World
Holt, B. G., Lessard, J., Borregaard, M. K., Fritz, S. A., Araújo, M. B., Dimitrov, D., Fabre, P., Graham, C. H., Graves, G. R., Jønsson, K. A., et al. (2012) · Science · doi:10.1126/science.1228282 · Cited by 1,456
Klein Goldewijk, K., Beusen, A., van Drecht, G., & de Vos, M. (2011) · Global Ecology and Biogeography · doi:10.1111/j.1466-8238.2010.00587.x · Cited by 1,270
Prediction and prevention of the next pandemic zoonosis.
Morse, S. S., Mazet, J. A., Woolhouse, M., Parrish, C. R., Carroll, D., Karesh, W. B., Zambrana-Torrelio, C., Lipkin, W. I., & Daszak, P. (2012) · The Lancet · doi:10.1016/s0140-6736(12)61684-5 · Cited by 1,070
Self-citationIn all likelihood : statistical modelling and inference using likelihood
Pawitan, Y. (2001) · Cited by 1,068
Practical variable selection for generalized additive models
Marra, G., & Wood, S. N. (2011) · Computational Statistics & Data Analysis · doi:10.1016/j.csda.2011.02.004 · Cited by 874
In All Likelihood: Statistical Modelling and Inference Using Likelihood
Pawitan, Y. (2001) · doi:10.1093/oso/9780198507659.001.0001 · Cited by 874
Cross-Species Virus Transmission and the Emergence of New Epidemic Diseases
Parrish, C. R., Holmes, E. C., Morens, D. M., Park, E.-C., Burke, D. S., Calisher, C. H., Laughlin, C. A., Saif, L. J., & Daszak, P. (2008) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00004-08 · Cited by 834
Self-citationA comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special?
Luis, A. D., Hayman, D. T. S., O’Shea, T. J., Cryan, P. M., Gilbert, A. T., Pulliam, J. R. C., Mills, J. N., Timonin, M. E., Willis, C. K. R., Cunningham, A. A., et al. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.2753 · Cited by 748
Emerging pathogens: the epidemiology and evolution of species jumps
Woolhouse, M. E. J., Haydon, D. T., & Antia, R. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.02.009 · Cited by 720
Bats host major mammalian paramyxoviruses
Drexler, J. F., Corman, V. M., Müller, M. A., Maganga, G. D., Vallo, P., Binger, T., Gloza‐Rausch, F., Cottontail, V. M., Rasche, A., Yordanov, S., et al. (2012) · Nature Communications · doi:10.1038/ncomms1796 · Cited by 701
Rodent reservoirs of future zoonotic diseases
Han, B. A., Schmidt, J. P., Bowden, S. E., & Drake, J. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501598112 · Cited by 629
Fritz, S. A., Bininda‐Emonds, O. R. P., & Purvis, A. (2009) · Ecology Letters · doi:10.1111/j.1461-0248.2009.01307.x · Cited by 585
A database of vertebrate longevity records and their relation to other life‐history traits
DE MAGALHÃES, J. P., & COSTA, J. (2009) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2009.01783.x · Cited by 543
Host Phylogeny Constrains Cross-Species Emergence and Establishment of Rabies Virus in Bats
Streicker, D. G., Turmelle, A. S., Vonhof, M. J., Kuzmin, I. V., McCracken, G. F., & Rupprecht, C. E. (2010) · Science · doi:10.1126/science.1188836 · Cited by 476
Carroll, D., Daszak, P., WOLFE, N. D., Gao, G. F., Morel, C. M., Morzaria, S., Pablos-Méndez, A., Tomori, O., & Mazet, J. A. K. (2018) · Science · doi:10.1126/science.aap7463 · Cited by 461
Self-citationAN EIGENVECTOR METHOD FOR ESTIMATING PHYLOGENETIC INERTIA
Diniz‐Filho, J. A. F., de Sant’Ana, C. E. R., & Bini, L. M. (1998) · Evolution · doi:10.1111/j.1558-5646.1998.tb02006.x · Cited by 451
A Strategy To Estimate Unknown Viral Diversity in Mammals
Anthony, S. J., Epstein, J. H., Murray, K. A., Navarrete‐Macias, I., Zambrana‐Torrelio, C., Solovyov, A., Flores, R. O., Arrigo, N. C., Islam, A., Khan, S. A., et al. (2013) · mBio · doi:10.1128/mbio.00598-13 · Cited by 432
Self-citationThe Evolution and Genetics of Virus Host Shifts
Longdon, B., Brockhurst, M. A., Russell, C. A., Welch, J. J., & Jiggins, F. M. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004395 · Cited by 371
Phylogenetic structure and host abundance drive disease pressure in communities
Parker, I. M., Saunders, M. A., Bontrager, M., Weitz, A. P., Hendricks, R., Magarey, R. D., Suiter, K. A., & Gilbert, G. S. (2015) · Nature · doi:10.1038/nature14372 · Cited by 366
Host specificity in phylogenetic and geographic space
Poulin, R., Krasnov, B. R., & Mouillot, D. (2011) · Trends in Parasitology · doi:10.1016/j.pt.2011.05.003 · Cited by 356
Contraction of the type I IFN locus and unusual constitutive expression of IFN-α in bats
Zhou, P., Tachedjian, M., Wynne, J. W., Boyd, V., Cui, J., Smith, I., Cowled, C. J., Ng, J. H. J., Mok, L., Michalski, W. P., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518240113 · Cited by 329
Phylogeny and geography predict pathogen community similarity in wild primates and humans
Davies, T. J., & Pedersen, A. B. (2008) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2008.0284 · Cited by 314
Messenger, A. M., Barnes, A. N., & Gray, G. C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089055 · Cited by 278
Global drivers of human pathogen richness and prevalence
Dunn, R. R., Davies, T. J., Harris, N. C., & Gavin, M. C. (2010) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.0340 · Cited by 267
Parasite specialization from a phylogenetic perspective: a new index of host specificity
Poulin, R., & Mouillot, D. (2003) · Parasitology · doi:10.1017/s0031182003002993 · Cited by 257
New directions in conservation medicine: applied cases of ecological health
(2013) · Choice Reviews Online · doi:10.5860/choice.50-3886 · Cited by 239
An Eigenvector Method for Estimating Phylogenetic Inertia
Diniz‐Filho, J. A. F., de Sant’Ana, C. E. R., & Bini, L. M. (1998) · Evolution · doi:10.2307/2411294 · Cited by 191
Phylogenetic host specificity and understanding parasite sharing in primates
Cooper, N., Griffin, R., Franz, M., Omotayo, M. O., & Nunn, C. L. (2012) · Ecology Letters · doi:10.1111/j.1461-0248.2012.01858.x · Cited by 180
Virological factors that increase the transmissibility of emerging human viruses
Geoghegan, J. L., Senior, A. M., Di Giallonardo, F., & Holmes, E. C. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1521582113 · Cited by 155
Nunn, C. L., & Altizer, S. (2005) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.20041 · Cited by 141
Gómez, J. M., Nunn, C. L., & Verdú, M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220716110 · Cited by 138
On the selection of phylogenetic eigenvectors for ecological analyses
Diniz‐Filho, J. A. F., Bini, L. M., Rangel, T. F., Morales‐Castilla, I., Olalla‐Tárraga, M. Á., Rodríguez, M. Á., & Hawkins, B. A. (2011) · Ecography · doi:10.1111/j.1600-0587.2011.06949.x · Cited by 131
Host Longevity and Parasite Species Richness in Mammals
Cooper, N., Kamilar, J. M., & Nunn, C. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042190 · Cited by 115
Viral factors in influenza pandemic risk assessment
Lipsitch, M., Barclay, W., Raman, R., Russell, C. J., Belser, J. A., Cobey, S. E., Kasson, P. M., Lloyd‐Smith, J. O., Maurer‐Stroh, S., Riley, S., et al. (2016) · eLife · doi:10.7554/elife.18491 · Cited by 106
Quantifying Global Drivers of Zoonotic Bat Viruses: A Process-Based Perspective
Brierley, L., Vonhof, M. J., Olival, K. J., Daszak, P., & Jones, K. E. (2016) · The American Naturalist · doi:10.1086/684391 · Cited by 102
Self-citationAbility to Replicate in the Cytoplasm Predicts Zoonotic Transmission of Livestock Viruses
Pulliam, J. R. C., & Dushoff, J. G. (2009) · The Journal of Infectious Diseases · doi:10.1086/596510 · Cited by 68
Examining the Origins of Emerging Viruses
Morse, S. S. (1993) · doi:10.1093/oso/9780195074444.003.0002 · Cited by 62
The Significant but Understudied Impact of Pathogen Transmission from Humans to Animals
Epstein, J. H., & Price, J. T. (2009) · Mount Sinai Journal of Medicine A Journal of Translational and Personalized Medicine · doi:10.1002/msj.20140 · Cited by 55
Organtini, L. J., Allison, A. B., Lukk, T., Parrish, C. R., & Hafenstein, S. L. (2014) · Journal of Virology · doi:10.1128/jvi.02611-14 · Cited by 46
Targeting Surveillance for Zoonotic Virus Discovery
Levinson, J. A., Bogich, T. L., Olival, K. J., Epstein, J. H., Johnson, C. K., Karesh, W. B., & Daszak, P. (2013) · Emerging infectious diseases · doi:10.3201/eid1905.121042 · Cited by 43
Self-citationA SIMPLE MODEL EXPLAINS THE DYNAMICS OF PREFERENTIAL HOST SWITCHING AMONG MAMMAL RNA VIRUSES
Cuthill, J. F. H., & Charleston, M. (2013) · Evolution · doi:10.1111/evo.12064 · Cited by 23
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Research works printed but not linked: 1
- Fauquet, C ., Mayo, M. A ., Maniloff, J ., Desselberger, U. & Ball, L. A. Virus taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses. (Elsevier Academic Press, 2005)
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Zhou, P., Fan, H., Lan, T., Yang, X., Shi, W., Zhang, W., Zhu, Y., Zhang, Y., Xie, Q., Mani, S., et al. (2018) · Nature · doi:10.1038/s41586-018-0010-9 · Cited by 767
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Metadata
- Authors
- Olival, K. J., Hosseini, P. R., Zambrana-Torrelio, C., Ross, N., Bogich, T. L., & Daszak, P.
- Affiliations
- EcoHealth Alliance (US)
- Corresponding author
- Olival, Kevin J.
- Venue
- Nature
- Published
- 2017-06-21
- Volume
- 546
- Issue
- 7660
- Pages
- 646-650
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5570460
- OpenAlex
- W2700382303
- Semantic Scholar
- 5833bef1f77157d1e3e6e1553ee9fdd2ff049ee0
- Cited by
- 1,130
- References
- 54
- Citations by year
- 2026: 83 · 2025: 109 · 2024: 109 · 2023: 137 · 2022: 130 · 2021: 192 · 2020: 152 · 2019: 99 · 2018: 81 · 2017: 33
- FWCI
- 93.99
- Type
- journal article
- Language
- en
- Update notices
- erratum (2017-08-23)
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Nature (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
- Funders
- United States Agency for International Development
- National Institute of Allergy and Infectious Diseases (R01AI110964, R01AI079231)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Zoonotic diseases and public health
- Health Sciences › Medicine › Infectious Diseases › Viral Infections and Outbreaks Research
- Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
- Keywords
- zoonotic spillover, host-virus interaction, mammalian viruses, interspecies transmission, emerging infectious diseases, bats, phylogenetic relatedness, host breadth, human-wildlife contact, pandemic surveillance
- MeSH terms
- Animals, Humans, Mammals, Viruses, Zoonoses, Biodiversity, Host-Pathogen Interactions, Host Specificity
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