The Dynamics of Deformed Wing Virus Concentration and Host Defensive Gene Expression after Varroa Mite Parasitism in Honey Bees, Apis mellifera.

Matthew Heerman,Robyn Rose,Michael Simone-Finstrom,Steven C Cook,Jay D Evans,Zhiguo Li,Songkun Su,Gloria Degrandi-Hoffman,Cristina Rodríguez-García,Yanping Chen,Jianghong Li,Wenjun Peng,Yazhou Zhao,Olubukola Banmeke,Michele Hamilton

doi:10.3390/insects10010016

Abstract

The synergistic interactions between the ectoparasitic mite Varroa destructor and Deformed wing virus (DWV) lead to the reduction in lifespan of the European honey bee Apis mellifera and often have been implicated in colony losses worldwide. However, to date, the underlying processes and mechanisms that form the multipartite interaction between the bee, mite, and virus have not been fully explained. To gain a better understanding of honey bees’ defense response to Varroa mite infestation and DWV infection, the DWV titers and transcription profiles of genes originating from RNAi, immunity, wound response, and homeostatic signaling pathways were monitored over a period of eight days. With respect to DWV, we observed low viral titers at early timepoints that coincided with high levels of Toll pathway transcription factor Dorsal, and its downstream immune effector molecules Hymenoptaecin, Apidaecin, Abaecin, and Defensin 1. However, we observed a striking increase in viral titers beginning after two days that coincided with a decrease in Dorsal levels and its corresponding immune effector molecules, and the small ubiquitin-like modifier (SUMO) ligase repressor of Dorsal, PIAS3. We observed a similar expression pattern for genes expressing transcripts for the RNA interference (Dicer/Argonaute), wound/homeostatic (Janus Kinase), and tissue growth (Map kinase/Wnt) pathways. Our results demonstrate that on a whole, honey bees are able to mount an immediate, albeit, temporally limited, immune and homeostatic response to Varroa and DWV infections, after which downregulation of these pathways leaves the bee vulnerable to expansive viral replication. The critical insights into the defense response upon Varroa and DWV challenges generated in this study may serve as a solid base for future research on the development of effective and efficient disease management strategies in honey bees.

Highlights

The European honeybee (Apis mellifera) is the predominantly managed pollinator and provides economically important pollination services worldwide that are estimated to exceed $153 billion annually [1,2]
Honeybees were collected from apiaries of Apis mellifera ligustica, which were managed by the USDA-ARS Bee Research Laboratory, Beltsville, MD, USA
Deformed wing virus (DWV) levels were significantly higher (p < 0.01) in bees exposed to Varroa (Figure 1A)

Summary

Introduction

The European honeybee (Apis mellifera) is the predominantly managed pollinator and provides economically important pollination services worldwide that are estimated to exceed $153 billion annually [1,2]. Pathogens, pesticides, climate change, landscape alteration, agricultural intensification and their cumulative interactions have contributed extensively to honey bee colony losses [6,7,8,9,10,11]. Of critical importance is the question of how all of these deleterious facets that affect survival and performance of honey bee colonies are correlated to the ectoparasitic mite Varroa destructor; a primary agent of colony decline [7,12]. Varroa mite infestations occurred originally only in the Asian honey bee Apis cerana, and was first introduced to the European honey bee over 70 years ago [13]. Varroa feed on the hemolymph of pupal and adult stages of honey bees, weakening the bees and shortening their lifespan and vectoring viruses and other pathogens [13]

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Results

Discussion

Conclusion