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Global estimates of mammalian viral diversity accounting for host sharing

Nature Ecology & Evolution volume 3, pages 1070–1075 (2019)Cite this article

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Abstract

Present estimates suggest there are over 1 million virus species found in mammals alone, with about half a million posing a possible threat to human health. Although previous estimates assume linear scaling between host and virus diversity, we show that ecological network theory predicts a non-linear relationship, produced by patterns of host sharing among virus species. To account for host sharing, we fit a power law scaling relationship for host–virus species interaction networks. We estimate that there are about 40,000 virus species in mammals (including ~10,000 viruses with zoonotic potential), a reduction of two orders of magnitude from present projections of viral diversity. We expect that the increasing availability of host–virus association data will improve the precision of these estimates and their use in the sampling and surveillance of pathogens with pandemic potential. We suggest host sharing should be more widely included in macroecological approaches to estimating biodiversity.

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Fig. 1: Fitting power law relationships between affiliates and host diversity, with shape A ∝ bHz.

Silhouettes are from http://phylopic.org/ (Gareth Monger (nematode)) (https://creativecommons.org/licenses/by/3.0/)

Fig. 2: Bipartite rarefaction curves on the known viral network.

Silhouettes are from http://phylopic.org/ (Rebecca Groom (fox), Sarah Werning (opossum, koala, sloth and elephant), Roberto Díaz Sibaja (hedgehog) and Jan A. Venter, Herbert H.T. Prins, David A. Balfour and Rob Slotow (rhinoceros)) (https://creativecommons.org/licenses/by/3.0/)

Data availability

All data in this study are from previous studies and available online for researchers to reproduce our results. Original sources can be found as follows: global diversity of viruses in mammal hosts can be found in Carroll et al.13; plant–pollinator interactions can be found in Robertson32 and reproduced in Marlin et al.33; myccorhizal networks are described in Toju et al.36; and the host–helminth network can be obtained from the Natural History Museum London’s Helminth Database, through the helminthR API (ref. 37). All data are also available on the Github repository for the project, at github.com/cjcarlson/brevity

Code availability

All code is available on a Github repository found at github.com/cjcarlson/brevity. The codependent R package39 is available at github.com/cjcarlson/codependent

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Acknowledgements

We thank T. A. Dallas, P. P. A. Staniczenko, T. Poisot, A. Barner and three anonymous reviewers for thoughtful comments and discussion about the manuscript and the methodology. We also acknowledge T. A. Dallas for assistance with the codependent package. This work was supported by the National Socio-Environmental Synthesis Center (SESYNC) under funding received from the National Science Foundation DBI-1639145 and by a Georgetown Environment Initiative fellowship to C.J.C.

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Authors and Affiliations

  1. Department of Biology, Georgetown University, Washington, DC, USA

    Colin J. Carlson, Casey M. Zipfel, Romain Garnier & Shweta Bansal

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  1. Colin J. Carlson
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Contributions

C.J.C., C.M.Z., R.G. and S.B. conceived of the study. C.J.C. and C.M.Z. performed all analyses. All authors contributed to the writing and approved the final draft.

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Correspondence to Colin J. Carlson.

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Supplementary Discussion, Supplementary References, Supplementary Figs. 1–4 and Supplementary Tables 1–7

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Carlson, C.J., Zipfel, C.M., Garnier, R. et al. Global estimates of mammalian viral diversity accounting for host sharing. Nat Ecol Evol 3, 1070–1075 (2019). https://doi.org/10.1038/s41559-019-0910-6

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