Global estimates of mammalian viral diversity accounting for host sharing

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 AbHz.

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

References

  1. 1.

    Colwell, R. K. et al. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J. Plant Ecol. 5, 3–21 (2012).

    Article  Google Scholar 

  2. 2.

    Larsen, B. B., Miller, E. C., Rhodes, M. K. & Wiens, J. J. Inordinate fondness multiplied and redistributed: the number of species on earth and the new pie of life. Q. Rev. Biol. 92, 229–265 (2017).

    Article  Google Scholar 

  3. 3.

    Windsor, D. A. Controversies in parasitology: most of the species on earth are parasites. Int. J. Parasitol. 28, 1939–1941 (1998).

    CAS  Article  Google Scholar 

  4. 4.

    Bacher, S. Still not enough taxonomists: reply to Joppa et al. Trends Ecol. Evol. 27, 65–66 (2012).

    Article  Google Scholar 

  5. 5.

    Colwell, R. K. & Coddington, J. A. Estimating terrestrial biodiversity through extrapolation. Philos. Trans. R. Soc. Lond. B 345, 101–118 (1994).

    CAS  Article  Google Scholar 

  6. 6.

    Poulin, R. & Morand, S. Parasite Biodiversity (Smithsonian, 2004).

  7. 7.

    Quicke, D. L. We know too little about parasitoid wasp distributions to draw any conclusions about latitudinal trends in species richness, body size and biology. PLoS One 7, e32101 (2012).

    CAS  Article  Google Scholar 

  8. 8.

    May, R. M. How many species? Philos. Trans. R. Soc. Lond. B 330, 293–304 (1990).

    Article  Google Scholar 

  9. 9.

    Dobson, A., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. & Jetz, W. Homage to Linnaeus: how many parasites? how many hosts? Proc. Natl Acad. Sci. USA 105, 11482–11489 (2008).

    CAS  Article  Google Scholar 

  10. 10.

    Strona, G. & Fattorini, S. Parasitic worms: how many really? Int. J. Parasitol. 44, 269–272 (2014).

    Article  Google Scholar 

  11. 11.

    Delmas, E. et al. Analysing ecological networks of species interactions. Biol. Rev. 94, 16–36 (2019).

    Article  Google Scholar 

  12. 12.

    Pellissier, L. et al. Comparing species interaction networks along environmental gradients. Biol. Rev. 93, 785–800 (2018).

    Article  Google Scholar 

  13. 13.

    Carroll, D. et al. The global virome project. Science 359, 872–874 (2018).

    CAS  Article  Google Scholar 

  14. 14.

    Olival, K. J. et al. Host and viral traits predict zoonotic spillover from mammals. Nature 546, 646–650 (2017).

    CAS  Article  Google Scholar 

  15. 15.

    Johnson, C. K. et al. Spillover and pandemic properties of zoonotic viruses with high host plasticity. Sci. Rep. 5, 14830 (2015).

    Article  Google Scholar 

  16. 16.

    Gómez, J. M., Nunn, C. L. & Verdú, M. Centrality in primate–parasite networks reveals the potential for the transmission of emerging infectious diseases to humans. Proc. Natl Acad. Sci. USA 110, 7738–7741 (2013).

    Article  Google Scholar 

  17. 17.

    Harte, J., Smith, A. B. & Storch, D. Biodiversity scales from plots to biomes with a universal species–area curve. Ecol. Lett. 12, 789–797 (2009).

    Article  Google Scholar 

  18. 18.

    Wilber, M. Q., Kitzes, J. & Harte, J. Scale collapse and the emergence of the power law species–area relationship. Glob. Ecol. Biogeogr. 24, 883–895 (2015).

    Article  Google Scholar 

  19. 19.

    Ignacio-Espinoza, J. C., Solonenko, S. A. & Sullivan, M. B. The global virome: not as big as we thought? Curr. Opin. Virol. 3, 566–571 (2013).

    Article  Google Scholar 

  20. 20.

    Grubaugh, N. D. et al. An amplicon-based sequencing framework for accurately measuring intrahost virus diversity using primalseq and ivar. Genome Biol. 20 https://doi.org/10.1186/s13059-018-1618-7 (2019).

  21. 21.

    Luis, A. D. et al. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc. Biol. Sci. 280, 20122753 (2013).

    Article  Google Scholar 

  22. 22.

    Brook, C. E. & Dobson, A. P. Bats as ‘special’ reservoirs for emerging zoonotic pathogens. Trends Microbiol. 23, 172–180 (2015).

    CAS  Article  Google Scholar 

  23. 23.

    Han, B. A., Kramer, A. M. & Drake, J. M. Global patterns of zoonotic disease in mammals. Trends Parasitol. 32, 565–577 (2016).

    Article  Google Scholar 

  24. 24.

    Woolhouse, M. E. & Gowtage-Sequeria, S. Host range and emerging and reemerging pathogens. Emerging Infect. Dis. 11, 1842 (2005).

    Article  Google Scholar 

  25. 25.

    Levinson, J. et al. Targeting surveillance for zoonotic virus discovery. Emerging Infect. Dis. 19, 743 (2013).

    Article  Google Scholar 

  26. 26.

    Young, C. C. & Olival, K. J. Optimizing viral discovery in bats. PLoS One 11, e0149237 (2016).

    Article  Google Scholar 

  27. 27.

    Restif, O. et al. Model-guided fieldwork: practical guidelines for multidisciplinary research on wildlife ecological and epidemiological dynamics. Ecol. Lett. 15, 1083–1094 (2012).

    Article  Google Scholar 

  28. 28.

    Dallas, T., Park, A. W. & Drake, J. M. Predicting cryptic links in host–parasite networks. PLoS Comput. Biol. 13, e1005557 (2017).

    Article  Google Scholar 

  29. 29.

    Elmasri, M., Farrell, M., & Stephens, D. A. A hierarchical Bayesian model for predicting host–parasite interactions using phylogenetic information. Preprint at https://arxiv.org/abs/1707.08354 (2017).

  30. 30.

    Shi, M. et al. The evolutionary history of vertebrate RNA viruses. Nature 556, 197 (2018).

    CAS  Article  Google Scholar 

  31. 31.

    Geoghegan, J. L. et al. Hidden diversity and evolution of viruses in market fish. Virus Evol. 4, vey031 (2018).

    Article  Google Scholar 

  32. 32.

    Robertson, C. Flowers and Insects (Science Press, 1929).

  33. 33.

    Marlin, J. C. & LaBerge, W. E. The native bee fauna of Carlinville, Illinois, revisited after 75 years: a case for persistence. Conserv. Ecol. 5, 9 (2001).

    Article  Google Scholar 

  34. 34.

    Schleuning, M. et al. Specialization and interaction strength in a tropical plant–frugivore network differ among forest strata. Ecology 92, 26–36 (2011).

    Article  Google Scholar 

  35. 35.

    Interaction Web Database (NCEAS, accessed 1 September 2018); http://www.nceas.ucsb.edu/interactionweb.

  36. 36.

    Toju, H., Tanabe, A. S. & Sato, H. Network hubs in root-associated fungal metacommunities. Microbiome 6, 116 (2018).

    Article  Google Scholar 

  37. 37.

    Dallas, T. helminthr: an r interface to the London Natural History Museum’s host–parasite database. Ecography 39, 391–393 (2016).

    Article  Google Scholar 

  38. 38.

    Dallas, T. et al. Gauging support for macroecological patterns in helminth parasites. Glob. Ecol. Biogeogr. 27, 1437–1447 (2018).

    Article  Google Scholar 

  39. 39.

    Carlson, C. J. codependent: an R package for network-based estimation of affiliate species richness. Version 1.0 https://github.com/cjcarlson/codependent (2019).

  40. 40.

    Jordano, P. Sampling networks of ecological interactions. Funct. Ecol. 30, 1883–1893 (2016).

    Article  Google Scholar 

  41. 41.

    Lloyd-Smith, J. O. Infectious diseases: predictions of virus spillover across species. Nature 546, 603 (2017).

    CAS  Article  Google Scholar 

  42. 42.

    Pilosof, S., Morand, S., Krasnov, B. R. & Nunn, C. L. Potential parasite transmission in multi-host networks based on parasite sharing. PLoS One 10, e0117909 (2015).

    Article  Google Scholar 

  43. 43.

    Schult, D. A. Exploring network structure, dynamics, and function using NetworkX. In Proc. 7th Python in Science Conference (SciPy2008) (Eds Varoquaux, G. et al.) 11–15 (SciPy, 2008); https://conference.scipy.org/proceedings/scipy2008/paper_2/full_text.pdf.

  44. 44.

    Bastian, M., Heymann, S., & Jacomy, M. Gephi: an open source software for exploring and manipulating networks. Version 0.9.2 (International AAAI Conference on Weblogs and Social Media, 2009).

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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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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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