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Fluorescent biomarkers demonstrate prospects for spreadable vaccines to control disease transmission in wild bats

Nature Ecology & Evolution volume 3, pages 1697–1704 (2019)Cite this article

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Matters Arising to this article was published on 16 March 2020

Abstract

Vaccines that autonomously transfer among individuals have been proposed as a strategy to control infectious diseases within inaccessible wildlife populations. However, rates of vaccine spread and epidemiological efficacy in real-world systems remain elusive. Here, we investigate whether topical vaccines that transfer among individuals through social contacts can control vampire bat rabies—a medically and economically important zoonosis in Latin America. Field experiments in three Peruvian bat colonies, which used fluorescent biomarkers as a proxy for the bat-to-bat transfer and ingestion of an oral vaccine, revealed that vaccine transfer would increase population-level immunity up to 2.6 times beyond the same effort using conventional, non-spreadable vaccines. Mathematical models showed that observed levels of vaccine transfer would reduce the probability, size and duration of rabies outbreaks, even at low but realistically achievable levels of vaccine application. Models further predicted that existing vaccines provide substantial advantages over culling bats—the policy currently implemented in North, Central and South America. Linking field studies with biomarkers to mathematical models can inform how spreadable vaccines may combat pathogens of health and conservation concern before costly investments in vaccine design and testing.

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Fig. 1: Transfer and ingestion of an orotopically spread gel biomarker in three vampire bat colonies.
Fig. 2: Bat contact heterogeneity revealed by ultraviolet powder transfers.
Fig. 3: Dynamic models of rabies transmission and spreadable vaccination.
Fig. 4: Simulating rabies outbreaks with vaccination.
Fig. 5: Comparison of the effects of culling and vaccination on rabies transmission.

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Data availability

Source data for Figs. 1 and 2 are provided with this Article at https://doi.org/10.1038/s41559-019-1032-x. The complete dataset describing ultraviolet and RB transfer is available from Dryad (https://doi.org/10.5061/dryad.64t161m).

Code availability

The R scripts used to estimate the RB transfer rates shown in Supplementary Fig. 2 and Supplementary Table 2 and to carry out the epidemiological modelling shown in Figs. 4 and 5 and Supplementary Figs. 3 and 5–9 are provided as Supplementary Software 1 and Supplementary Software 2.

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Acknowledgements

K.M.B. was supported by NIH award F32AI134016, and computational resources were provided by NIH award U01GM110712. D.G.S. was supported by a Sir Henry Dale Fellowship that was jointly funded by the Wellcome Trust and Royal Society (102507/Z/13/Z). Additional funding was provided via a Challenge Grant from the Royal Society to D.G.S., T.E.R., J.E.O., C.S. and N.F. (CH160097). The authors are grateful to D. Walsh, M. Viana and the Streicker Group for comments on earlier versions of this manuscript. Any use of trade, product or firm names does not imply endorsement by the US Government.

Author information

Authors and Affiliations

  1. Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK

    Kevin M. Bakker & Daniel G. Streicker

  2. Department of Statistics, University of Michigan, Ann Arbor, MI, USA

    Kevin M. Bakker

  3. US Geological Survey, National Wildlife Health Center, Madison, WI, USA

    Tonie E. Rocke & Rachel C. Abbott

  4. Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin–Madison, Madison, WI, USA

    Jorge E. Osorio

  5. ILLARIY (Asociación para el Desarrollo y Conservación de los Recursos Naturales), Lima, Peru

    Carlos Tello & William Valderrama

  6. Facultad de Ciencias, Universidad Nacional de Piura, Piura, Peru

    Jorge E. Carrera

  7. Universidad Autonoma de Barcelona, Barcelona, Spain

    William Valderrama

  8. Facultad de Medicina Veterinaria y Zootecnia, Universidad Peruana Cayetano, Lima, Peru

    Carlos Shiva & Nestor Falcon

  9. MRC–University of Glasgow Centre for Virus Research, Glasgow, UK

    Daniel G. Streicker

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Contributions

D.G.S., T.E.R. and J.E.O. conceived and designed the experiments. R.C.A., C.T. and J.E.C. performed the experiments. K.M.B. and D.G.S. analysed the data. T.E.R., J.E.O., W.V., C.S. and N.F. contributed materials and/or analysis tools. K.M.B. and D.G.S. wrote the first draft of the paper. All authors contributed revisions.

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Correspondence to Kevin M. Bakker or Daniel G. Streicker.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–9, Tables 1–3, methods and results.

Reporting Summary

Supplementary Software 1

R script to carry out least-squares estimation of RB transfer rates.

Supplementary Software 2

R script to carry out mathematical modelling.

Source data

Source Data Fig. 1

RB marking and detection histories for wild bats in the field study.

Source Data Fig. 2

Ultraviolet powder marking and detection histories for wild bats in the field study.

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Bakker, K.M., Rocke, T.E., Osorio, J.E. et al. Fluorescent biomarkers demonstrate prospects for spreadable vaccines to control disease transmission in wild bats. Nat Ecol Evol 3, 1697–1704 (2019). https://doi.org/10.1038/s41559-019-1032-x

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