Abstract

The mite Varroa destructor is a serious threat to honeybee populations. Selective breeding for Varroa mite tolerance could be accelerated by biomarkers within individual bees that could be applied to evaluate a colony phenotype. Previously, we demonstrated differences in kinase-mediated signaling between bees from colonies of extreme phenotypes of mite susceptibility. We expand these findings by defining a panel of 19 phosphorylation events that differ significantly between individual pupae from multiple colonies with distinct Varroa mite tolerant phenotypes. The predictive capacity of these biomarkers was evaluated by analyzing uninfested pupae from eight colonies representing a spectrum of mite tolerance. The pool of biomarkers effectively discriminated individual pupae on the basis of colony susceptibility to mite infestation. Kinome analysis of uninfested pupae from mite tolerant colonies highlighted an increased innate immune response capacity. The implication that differences in innate immunity contribute to mite susceptibility is supported by the observation that induction of innate immune signaling responses to infestation is compromised in pupae of the susceptible colonies. Collectively, biomarkers within individual pupae that are predictive of the susceptibility of colonies to mite infestation could provide a molecular tool for selective breeding of tolerant colonies.

Highlights

  • The feasibility of genetic selection for Varroa mite resistance is supported by the historic example of Asian honeybees (Apis ceranae) who, in the face of evolutionary pressures imposed by the parasite, developed protective mechanisms, including behavioral characteristics and immune adaptations[17,18]

  • We expand on the findings of our previous investigation of the utility for kinome analysis to reveal biomarkers and mechanisms of Varroa mite tolerance in honeybees by identifying a panel of 19 phosphorylation events with significant (p < 0.01) differences in phosphorylation when comparing individual pupae (n = 5/phenotype) selected from two colonies of each high and low susceptibility to the parasite

  • In addition to offering insight into the cellular processes underlying Varroa mite tolerance, this investigation enabled identification of a group of biomarkers that could be applied at the level of individual pupae to predict phenotypes at a population level

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Summary

Introduction

The feasibility of genetic selection for Varroa mite resistance is supported by the historic example of Asian honeybees (Apis ceranae) who, in the face of evolutionary pressures imposed by the parasite, developed protective mechanisms, including behavioral characteristics (such as grooming and hygienic traits) and immune adaptations[17,18]. A number of molecular approaches, including at the levels of the transcriptome[26,27,28,29] and proteome[30,31], have been applied to honeybees in efforts to understand the cellular mechanisms of Varroa resistance as well as to identify biomarkers of these traits This is a daunting task due to the potential complexities of the molecular mechanisms underlying these phenotypes, coupled with the challenges of deciphering biology within a mixed genetic population. We expand on the findings of our previous investigation of the utility for kinome analysis to reveal biomarkers and mechanisms of Varroa mite tolerance in honeybees by identifying a panel of 19 phosphorylation events with significant (p < 0.01) differences in phosphorylation when comparing individual pupae (n = 5/phenotype) selected from two colonies of each high and low susceptibility to the parasite. In addition to offering insight into the cellular processes underlying Varroa mite tolerance, this investigation enabled identification of a group of biomarkers that could be applied at the level of individual pupae to predict phenotypes at a population (colony) level

Methods
Results
Conclusion

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