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

Cédric Alaux,Cynthia M McDonnell,Emma Durbesson,Hugues Parrinello,Yves Le Conte,Didier Crauser,Jean-Pierre Desvignes,Dominique Beslay

doi:10.1186/1472-6785-13-25

Cédric Alaux, Cynthia M McDonnell + Show 6 more

Open Access

https://doi.org/10.1186/1472-6785-13-25

Copy DOI

Abstract

BackgroundExclusion 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.ResultsAnalysis 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.ConclusionsParasitism 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.

Highlights

Exclusion from a social group is an effective way to avoid parasite transmission
In social insects, parasitized individuals can remove themselves from the group, which corresponds to an altruistic self-removal [10], or nestmates can modify their interaction with those individuals to prevent parasite transmission [6,9]
The hydrocarbons were extracted from control and parasitized bees and analyzed and identified using gas chromatography (GC) followed by mass spectrometry (MS)

Summary

Introduction

Exclusion from a social group is an effective way to avoid parasite transmission This type of social removal has 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. Despite parasite modification of host behavior being widespread in animals, the underlying physiological and neuronal mechanisms are poorly understood, especially in social insects

Methods

Results

Discussion

Conclusion