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Chemical detection triggers honey bee defense against a destructive parasitic threat

Nature Chemical Biology volume 17, pages 524–530 (2021)Cite this article

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Abstract

Invasive species events related to globalization are increasing, resulting in parasitic outbreaks. Understanding of host defense mechanisms is needed to predict and mitigate against the consequences of parasite invasion. Using the honey bee Apis mellifera and the mite Varroa destructor, as a host–parasite model, we provide a comprehensive study of a mechanism of parasite detection that triggers a behavioral defense associated with social immunity. Six Varroa-parasitization-specific (VPS) compounds are identified that (1) trigger Varroa-sensitive hygiene (VSH, bees’ key defense against Varroa sp.), (2) enable the selective recognition of a parasitized brood and (3) induce responses that mimic intrinsic VSH activity in bee colonies. We also show that individuals engaged in VSH exhibit a unique ability to discriminate VPS compounds from healthy brood signals. These findings enhance our understanding of a critical mechanism of host defense against parasites, and have the potential to apply the integration of pest management in the beekeeping sector.

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Fig. 1: Field bioassay to assess the hygienic behavior of honey bees toward brood cells treated with different Varroa extracts.
Fig. 2: Identification of six cuticular compounds that are specific to the Varroa-parasitized status of brood cells (VPS compounds).
Fig. 3: Quantification of the six VPS compounds in bee pupae and mites.
Fig. 4: Biological activity of VPS compounds in the VSH field bioassay.
Fig. 5: Adult bee perception and integration of the VPS compounds.

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Data availability

All data generated for the present study are available upon request to the corresponding author.

Code availability

All computer codes generated for the present study are available upon request to the corresponding author.

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Acknowledgements

We thank Y. Poquet for help in the collection of VSH bees and mites, F. Laas for providing mite-infested colonies, D. Crauser and J. Senechal for giving access to honey bee colonies, and GDR Mediatec for fruitful scientific discussions. This project was funded by grants provided by INRAE (SPE Department), the University of Otago and a Casdar fund from the French Ministry of Agriculture (Mosar). F.M. was supported by grants from the France–New Zealand Friendship Fund, by the French Ministry of Agriculture and a New Zealand international doctoral research scholarship. MS analyses were in part performed at the Plateforme d’Analyses Chimiques en Ecologie, technical facilities of the CeMEB.

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Authors and Affiliations

  1. INRAE, National Research Institute for Agriculture Food and Environment, UR 406 Abeilles et Environnement, Avignon, France

    Fanny Mondet, Solene Blanchard, Dominique Beslay, Celia Bordier, Benjamin Basso & Yves Le Conte

  2. Department of Zoology, University of Otago, Dunedin, New Zealand

    Fanny Mondet, Seo Hyun Kim & Alison R. Mercer

  3. UMT PrADE, Avignon, France

    Solene Blanchard, Dominique Beslay, Celia Bordier, Benjamin Basso & Yves Le Conte

  4. CEFE, Univ. Montpellier, CNRS, EPHE, IRD, Univ. Paul Valéry Montpellier 3, Montpellier, France

    Nicolas Barthes & Benoit Lapeyre

  5. INRAE, UR1115 Plantes et Systèmes de Culture Horticoles, Avignon, France

    Guy Costagliola

  6. National Research Institute for Agriculture, Food, and Environment, IGEPP, University of Rennes, Rennes, France

    Maxime R. Hervé

  7. ITSAP, Avignon, France

    Benjamin Basso

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Contributions

F.M., A.R.M. and Y.L.C. designed the project. F.M., S.B., D.B., N.B., B.L., C.B., S.H.K., B.B. and G.C. performed the experiments with contributions as follows. F.M., S.B., C.B., B.B. did the field assays. F.M., S.B. and D.B. did the GC analyses. F.M., N.B. and G.C. did the MS analyses. F.M. and S.H.K. performed the sucrose responsiveness assay. F.M. performed the learning assay. F.M., C.B. and B.L. did the EAGs. F.M. and M.H. analyzed the data. F.M., A.R.M. and Y.L.C. wrote the manuscript.

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Correspondence to Fanny Mondet.

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Extended data

Extended Data Fig. 1 One-hour memory recall in VSH bees and NVS bees.

Percentages of VSH bees and NVS bees displaying conditioned proboscis extension responses (PER) 1 hour after the final (6th) conditioning trial. All bees were trained to discriminate between an odorant paired with a sugar reward (CS+, healthy brood extract + VPS compounds) and a non-reinforced odorant (CS-, healthy brood extract). The figure shows the percentages of bees responding to the CS+, the CS- and to a novel odour not presented during the learning phase (Diff, Nonanol), (GLMM, nVSH = 32, nNVS = 28). Different letters indicate significant results in the analyses.

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Mondet, F., Blanchard, S., Barthes, N. et al. Chemical detection triggers honey bee defense against a destructive parasitic threat. Nat Chem Biol 17, 524–530 (2021). https://doi.org/10.1038/s41589-020-00720-3

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