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Open Access Highly Accessed Research article

Ecto- and endoparasite induce similar chemical and brain neurogenomic responses in the honey bee (Apis mellifera)

Cynthia M McDonnell1*, Cédric Alaux1, Hugues Parrinello2, Jean-Pierre Desvignes2, Didier Crauser1, Emma Durbesson1, Dominique Beslay1 and Yves Le Conte1

Author Affiliations

1 INRA, UR 406 Abeilles et Environnement, Site Agroparc, Domaine Saint-Paul, Avignon, Cedex 9, 84914, France

2 Institut de Génomique Fonctionnelle, UMR 5203 CNRS, U661 INSERM, Universités Montpellier 1 & 2, Montpellier Cedex 05, 34094, France

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BMC Ecology 2013, 13:25  doi:10.1186/1472-6785-13-25

Published: 17 July 2013

Abstract

Background

Exclusion from a social group is an effective way to avoid parasite transmission. This type of social removal has also been proposed as a form of collective defense, or social immunity, in eusocial insect groups. If parasitic modification of host behavior is widespread in social insects, the underlying physiological and neuronal mechanisms remain to be investigated. We studied this phenomenon in honey bees parasitized by the mite Varroa destructor or microsporidia Nosema ceranae, which make bees leave the hive precociously. We characterized the chemical, behavioral and neurogenomic changes in parasitized bees, and compared the effects of both parasites.

Results

Analysis of cuticular hydrocarbon (CHC) profiles by gas chromatography coupled with mass spectrophotometry (GC-MS) showed changes in honey bees parasitized by either Nosema ceranae or Varroa destructor after 5 days of infestation. Levels of 10-HDA, an antiseptic important for social immunity, did not change in response to parasitism. Behavioral analysis of N. ceranae- or V. destructor- parasitized bees revealed no significant differences in their behavioral acts or social interactions with nestmates. Digital gene expression (DGE) analysis of parasitized honey bee brains demonstrated that, despite the difference in developmental stage at which the bee is parasitized, Nosema and Varroa-infested bees shared more gene changes with each other than with honey bee brain expression gene sets for forager or nurse castes.

Conclusions

Parasitism by Nosema or Varroa induces changes to both the CHC profiles on the surface of the bee and transcriptomic profiles in the brain, but within the social context of the hive, does not result in observable effects on her behavior or behavior towards her. While parasitized bees are reported to leave the hive as foragers, their brain transcription profiles suggest that their behavior is not driven by the same molecular pathways that induce foraging behavior.

Keywords:
Varroa destructor; Nosema ceranae; Social immunity; Transcriptome; Cuticular hydrocarbons