Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra's model

Desiderato Annoscia, Sam P. Brown, Gennaro Di Prisco, Emanuele De Paoli, Simone Del Fabbro, Davide Frizzera, Virginia Zanni, David A. Galbraith, Emilio Caprio, Christina M. Grozinger, Francesco Pennacchio, Francesco Nazzi

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

The association between the deformed wing virus and the parasitic mite Varroa destructor has been identified as a major cause of worldwide honeybee colony losses. The mite acts as a vector of the viral pathogen and can trigger its replication in infected bees. However, the mechanistic details underlying this tripartite interaction are still poorly defined, and, particularly, the causes of viral proliferation in mite-infested bees. Here, we develop and test a novel hypothesis that mite feeding destabilizes viral immune control through the removal of both virus and immune effectors, triggering uncontrolled viral replication. Our hypothesis is grounded on the predator-prey theory developed by Volterra, which predicts prey proliferation when both predators and preys are constantly removed from the system. Consistent with this hypothesis, we show that the experimental removal of increasing volumes of haemolymph from individual bees results in increasing viral densities. By contrast, we do not find consistent support for alternative proposed mechanisms of viral expansion via mite immune suppression or within-host viral evolution. Our results suggest that haemolymph removal plays an important role in the enhanced pathogen virulence observed in the presence of feeding Varroa mites. Overall, these results provide a new model for the mechanisms driving pathogen-parasite interactions in bees, which ultimately underpin honeybee health decline and colony losses.

Original languageEnglish (US)
Article number20190331
JournalProceedings of the Royal Society B: Biological Sciences
Volume286
Issue number1901
DOIs
StatePublished - Apr 24 2019

Fingerprint

Varroidae
bee viruses
Varroa
Hemolymph
Mites
Bees
Pathogens
Viruses
mite
bee
hemolymph
mites
virus
Apoidea
pathogen
honeybee
pathogens
Deformed wing virus
parasitic mites
predators

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Environmental Science(all)
  • Agricultural and Biological Sciences(all)

Cite this

Annoscia, Desiderato ; Brown, Sam P. ; Di Prisco, Gennaro ; De Paoli, Emanuele ; Del Fabbro, Simone ; Frizzera, Davide ; Zanni, Virginia ; Galbraith, David A. ; Caprio, Emilio ; Grozinger, Christina M. ; Pennacchio, Francesco ; Nazzi, Francesco. / Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra's model. In: Proceedings of the Royal Society B: Biological Sciences. 2019 ; Vol. 286, No. 1901.
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abstract = "The association between the deformed wing virus and the parasitic mite Varroa destructor has been identified as a major cause of worldwide honeybee colony losses. The mite acts as a vector of the viral pathogen and can trigger its replication in infected bees. However, the mechanistic details underlying this tripartite interaction are still poorly defined, and, particularly, the causes of viral proliferation in mite-infested bees. Here, we develop and test a novel hypothesis that mite feeding destabilizes viral immune control through the removal of both virus and immune effectors, triggering uncontrolled viral replication. Our hypothesis is grounded on the predator-prey theory developed by Volterra, which predicts prey proliferation when both predators and preys are constantly removed from the system. Consistent with this hypothesis, we show that the experimental removal of increasing volumes of haemolymph from individual bees results in increasing viral densities. By contrast, we do not find consistent support for alternative proposed mechanisms of viral expansion via mite immune suppression or within-host viral evolution. Our results suggest that haemolymph removal plays an important role in the enhanced pathogen virulence observed in the presence of feeding Varroa mites. Overall, these results provide a new model for the mechanisms driving pathogen-parasite interactions in bees, which ultimately underpin honeybee health decline and colony losses.",
author = "Desiderato Annoscia and Brown, {Sam P.} and {Di Prisco}, Gennaro and {De Paoli}, Emanuele and {Del Fabbro}, Simone and Davide Frizzera and Virginia Zanni and Galbraith, {David A.} and Emilio Caprio and Grozinger, {Christina M.} and Francesco Pennacchio and Francesco Nazzi",
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Annoscia, D, Brown, SP, Di Prisco, G, De Paoli, E, Del Fabbro, S, Frizzera, D, Zanni, V, Galbraith, DA, Caprio, E, Grozinger, CM, Pennacchio, F & Nazzi, F 2019, 'Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra's model', Proceedings of the Royal Society B: Biological Sciences, vol. 286, no. 1901, 20190331. https://doi.org/10.1098/rspb.2019.0331

Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra's model. / Annoscia, Desiderato; Brown, Sam P.; Di Prisco, Gennaro; De Paoli, Emanuele; Del Fabbro, Simone; Frizzera, Davide; Zanni, Virginia; Galbraith, David A.; Caprio, Emilio; Grozinger, Christina M.; Pennacchio, Francesco; Nazzi, Francesco.

In: Proceedings of the Royal Society B: Biological Sciences, Vol. 286, No. 1901, 20190331, 24.04.2019.

Research output: Contribution to journalArticle

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T1 - Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra's model

AU - Annoscia, Desiderato

AU - Brown, Sam P.

AU - Di Prisco, Gennaro

AU - De Paoli, Emanuele

AU - Del Fabbro, Simone

AU - Frizzera, Davide

AU - Zanni, Virginia

AU - Galbraith, David A.

AU - Caprio, Emilio

AU - Grozinger, Christina M.

AU - Pennacchio, Francesco

AU - Nazzi, Francesco

PY - 2019/4/24

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N2 - The association between the deformed wing virus and the parasitic mite Varroa destructor has been identified as a major cause of worldwide honeybee colony losses. The mite acts as a vector of the viral pathogen and can trigger its replication in infected bees. However, the mechanistic details underlying this tripartite interaction are still poorly defined, and, particularly, the causes of viral proliferation in mite-infested bees. Here, we develop and test a novel hypothesis that mite feeding destabilizes viral immune control through the removal of both virus and immune effectors, triggering uncontrolled viral replication. Our hypothesis is grounded on the predator-prey theory developed by Volterra, which predicts prey proliferation when both predators and preys are constantly removed from the system. Consistent with this hypothesis, we show that the experimental removal of increasing volumes of haemolymph from individual bees results in increasing viral densities. By contrast, we do not find consistent support for alternative proposed mechanisms of viral expansion via mite immune suppression or within-host viral evolution. Our results suggest that haemolymph removal plays an important role in the enhanced pathogen virulence observed in the presence of feeding Varroa mites. Overall, these results provide a new model for the mechanisms driving pathogen-parasite interactions in bees, which ultimately underpin honeybee health decline and colony losses.

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