Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection

Navajas, María; Migeon, Alain; Alaux, Cédric; Martin‐Magniette, Marie‐Laure; Robinson, Gene E.; Evans, Jay D.; Cros‐Arteil, Sandrine; Crauser, Didier; Conte, Yves Le

doi:10.1186/1471-2164-9-301

Cited by 176 publications

(180 citation statements)

References 67 publications

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“…3c, d). This difference may partially explain the results reported in the literature (Gregory et al, 2005;Navajas et al, 2008;, which could have been due to overlooked health conditions of the experimental populations. Host condition is an important factor that influences the bee response to any environmental challenge and the complex cross-talk between stress and immunity.…”

Section: Varroa Destructor Is a Vector Of Honeybee Viruscontrasting

confidence: 55%

Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera

Prisco

Pennacchio

Caprio

et al. 2010

Journal of General Virology

201

142

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The Israeli acute paralysis virus (IAPV) is a significant marker of honeybee colony collapse disorder (CCD). In the present work, we provide the first evidence that Varroa destructor is IAPV replication-competent and capable of vectoring IAPV in honeybees. The honeybees became infected with IAPV after exposure to Varroa mites that carried the virus. The copy number of IAPV in bees was positively correlated with the density of Varroa mites and time period of exposure to Varroa mites. Further, we showed that the mite-virus association could possibly reduce host immunity and therefore promote elevated levels of virus replication. This study defines an active role of Varroa mites in IAPV transmission and sheds light on the epidemiology of IAPV infection in honeybees.Varroatosis is one of the most serious honeybee diseases caused by a parasitic mite, Varroa destructor. Varroa mites use their piercing mouthparts to suck out haemolymph from honeybees. The repeated feeding results in a decline of colony vigour, shortened life span of the honeybees and eventual perishing of colonies (Rosenkranz et al., 2010). Further, the feeding of Varroa mites gives mites the potential to act as vectors of bee diseases, presenting additional threats to bee health. The role of Varroa mite as a vector in the transmission of bee viruses has been well documented (Bowen-Walker et al., 1999;Chen et al., 2004;Shen et al., 2005). However, it has not yet been demonstrated if this mite could act as a vector of Israeli acute paralysis virus (IAPV), a virus that was tightly correlated with honeybee colony collapse disorder (CCD), a malady that has decimated honeybee colonies across the USA (Cox-Foster et al., 2007;vanEngelsdorp et al., 2007) and around the world (Neumann & Carreck, 2010). The present study was undertaken to determine the possible role of Varroa mites in the transmission of IAPV and in the promotion of its replication in honeybees. Moreover, the expression of immune-related gene transcripts, apidaecin and eater that are involved in honeybee humoral and cellular immunity (Ertürk-Hasdemir & Silverman, 2005;Evans et al., 2006;Kocks et al., 2005;Simone et al., 2009) was measured in Varroa-challenged bees. Apidaecin is a proline-rich peptide and one of the most prominent components of the honeybee humoral defence against microbial invasion (Evans et al. 2006). Eater is a member of epidermal growth factor-family protein involved cellular immunity, as it plays an important role in phagocytosis (Ertürk-Hasdemir & Silverman, 2005;Kocks et al., 2005). Two strong bee colonies (i.e. with at least seven frames filled with capped brood and food, and covered with adult bees) and two weak colonies (i.e. with a low-adult bee population and fewer than four frames with a small patch of capped brood) that were determined to be free of IAPV infection by RT-PCR assay were selected for transmission studies. Further, the expression levels of vitellogenin, an indicator of the general health of the colonies (Amdam et al., 2005;Simone et al., 2009), were det...

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Section: Varroa Destructor Is a Vector Of Honeybee Viruscontrasting

confidence: 55%

Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera

Prisco

Pennacchio

Caprio

et al. 2010

Journal of General Virology

201

142

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“…The very close relationship between the mite and the virus, along with the complexity of the results from transcriptomic studies, have generated a somewhat contrasting picture, however. The initially proposed primary role for the parasitic mite in the induction of this immune syndrome (33) has been challenged by several studies that apparently do not support this hypothesis (12,22,(34)(35)(36), even though the possibility that Varroa feeding and its saliva may modulate immune effector molecules cannot be ruled out, as suggested by the effect of this secretion on insect hemocytes in vitro (37). Moreover, a direct immunosuppressive activity of DWV targeting the antiviral barriers under NF-κB control has been proposed in the framework of a bistable dynamic model that assumes a transition from immunostimulation to immunosuppression as the DWV titer increases and then exceeds a critical threshold (Ct) (10).…”

Section: Discussionmentioning

confidence: 99%

A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health

Prisco

Annoscia

Margiotta

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

203

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Honey bee colony losses are triggered by interacting stress factors consistently associated with high loads of parasites and/or pathogens. A wealth of biotic and abiotic stressors are involved in the induction of this complex multifactorial syndrome, with the parasitic mite Varroa destructor and the associated deformed wing virus (DWV) apparently playing key roles. The mechanistic basis underpinning this association and the evolutionary implications remain largely obscure. Here we narrow this research gap by demonstrating that DWV, vectored by the Varroa mite, adversely affects humoral and cellular immune responses by interfering with NF-κB signaling. This immunosuppressive effect of the viral pathogen enhances reproduction of the parasitic mite. Our experimental data uncover an unrecognized mutualistic symbiosis between Varroa and DWV, which perpetuates a loop of reciprocal stimulation with escalating negative effects on honey bee immunity and health. These results largely account for the remarkable importance of this mite-virus interaction in the induction of honey bee colony losses. The discovery of this mutualistic association and the elucidation of the underlying regulatory mechanisms sets the stage for a more insightful analysis of how synergistic stress factors contribute to colony collapse, and for the development of new strategies to alleviate this problem.Apis mellifera | Varroa destructor | deformed wing virus | mutualistic symbiosis | honeybee colony losses

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“…The mite-susceptible colonies produced almost twice the amount of honey compared to the mite-resistant colonies, and no major differences in swarming tendency were observed (Le Conte et al 2007). Navajas et al (2008) compared gene expression in honeybees of the Avignon mite-resistant population and local mite-susceptible honeybees. Their study interestingly found that several genes involved in olfactory cognition and neuronal excitability were upregulated in the mite-resistant honeybees (Navajas et al 2008).…”

Section: Avignon Francementioning

confidence: 99%

“…Navajas et al (2008) compared gene expression in honeybees of the Avignon mite-resistant population and local mite-susceptible honeybees. Their study interestingly found that several genes involved in olfactory cognition and neuronal excitability were upregulated in the mite-resistant honeybees (Navajas et al 2008). The Avignon miteresistant honeybees could have a higher sensitivity to environmental stimuli and be better adapted for detecting and removing mite-infested brood cells (Navajas et al 2008).…”

Section: Avignon Francementioning

confidence: 99%

Natural Varroa mite-surviving Apis mellifera honeybee populations

2015

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-The Varroa destructor mite is the largest threat to apiculture worldwide and has been responsible for devastating losses of wild honeybee populations in Europe and North America. However, Varroa mite-resistant populations of A. mellifera honeybees have been reported and documented around the world with a variety of explanations for their long-term survival with uncontrolled mite infestation. This review synthesizes the work on naturally occurring survival to Varroa mites and discusses what these honeybee populations can signify for apiculture.Varroa destructor / mite resistance / host-parasite adaptations / natural selection / apiculture

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Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection

Cited by 176 publications

References 67 publications

Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera

Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera

A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health

Natural Varroa mite-surviving Apis mellifera honeybee populations

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