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International audience; Honeybees (Apis mellifera) are constantly exposed to a wide variety of environmental stressors such as parasites and pesticides. Among them, Nosema ceranae and neurotoxic insecticides might act in combination and lead to a higher honeybee mortality. We investigated the molecular response of honeybees exposed to N. ceranae, to insecticides (fipronil or imidacloprid), and to a combination of both stressors. Midgut transcriptional changes induced by these stressors were measured in two independent experiments combining a global RNA-Seq transcriptomic approach with the screening of the expression of selected genes by quantitative RT-PCR. Although N. ceranae-insecticide combinations induced a significant increase in honeybee mortality, we observed that they did not lead to a synergistic effect. According to gene expression profiles, chronic exposure to insecticides had no significant impact on detoxifying genes but repressed the expression of immunity-related genes. Honeybees treated with N. ceranae, alone or in combination with an insecticide, showed a strong alteration of midgut immunity together with modifications affecting cuticle coatings and trehalose metabolism. An increasing impact of treatments on gene expression profiles with time was identified suggesting an absence of stress recovery which could be linked to the higher mortality rates observed.

SUMMARYThe microsporidian parasiteNosema ceranaeis a common pathogen of the Western honeybee (Apis mellifera) whose variable virulence could be related to its genetic polymorphism and/or its polyphenism responding to environmental cues. Since the genotyping ofN. ceranaebased on unique marker sequences had been unsuccessful, we tested whether amultilocusapproach, assessing the diversity of ten genetic markers – encoding nine proteins and the small ribosomal RNA subunit – allowed the discrimination betweenN. ceranaevariants isolated from singleA. melliferaindividuals in four distant locations. High nucleotide diversity and allele content were observed for all genes. Most importantly, the diversity was mainly present within parasite populations isolated from single honeybee individuals. In contrast the absence of isolate differentiation precluded anytaxadiscrimination, even through amultilocusapproach, but suggested that similar populations of parasites seem to infect honeybees in distant locations. As statistical evolutionary analyses showed that the allele frequency is under selective pressure, we discuss the origin and consequences ofN. ceranaeheterozygosity in a single host and lack of population divergence in the context of the parasite natural and evolutionary history.

Données supplémentaires disponibles sur le site de la revue: http://www.journals.elsevier.com/infection-genetics-and-evolution/; International audience; Genetic diversity of a host species is a key factor to counter infection by parasites. Since two separation events and the beginning of beekeeping, the Western honeybee, Apis mellifera, has diverged in many phylogenetically-related taxa that share common traits but also show specific physiological, behavioural and morphological traits. In this study, we tested the hypothesis that A. mellifera taxa living in a same habitat should respond differently to parasites like Nosema ceranae, a microsporidia living in host's midgut. We used the Poulin and Combes' concept of virulence to compare the susceptibility of three A. mellifera taxa to N. ceranae infection. Three criteria were measured 10 days post-infection (dpi): the host mortality, the host sugar consumption and the development success of the parasite (i.e. number of spores produced). Interestingly, we showed that the observed variation in susceptibility to infection by N. ceranae is not linked to honeybee taxa but results from the variability between colonies, and that those differences are probably linked to genetic variations. The use of these three criteria allows us to conclude that the differences in susceptibility are mediated by a genetic variability in honeybee workers from resistance to tolerance. Finally, we discuss the consequences of our findings for beekeeping management.

International audience; In ecosystems, a variety of biological, chemical and physical stressors may act in combination to induce illness in populations of living organisms. While recent surveys reported that parasite-insecticide interactions can synergistically and negatively affect honeybee survival, the importance of sequence in exposure to stressors has hardly received any attention. In this work, Western honeybees (Apis mellifera) were sequentially or simultaneously infected by the microsporidian parasite Nosema ceranae and chronically exposed to a sublethal dose of the insecticide fipronil, respectively chosen as biological and chemical stressors. Interestingly, every combination tested led to a synergistic effect on honeybee survival, with the most significant impacts when stressors were applied at the emergence of honeybees. Our study presents significant outcomes on beekeeping management but also points out the potential risks incurred by any living organism frequently exposed to both pathogens and insecticides in their habitat.

International audience; BACKGROUND: The honeybee, Apis mellifera, is undergoing a worldwide decline whose origin is still in debate. Studies performed for twenty years suggest that this decline may involve both infectious diseases and exposure to pesticides. Joint action of pathogens and chemicals are known to threaten several organisms but the combined effects of these stressors were poorly investigated in honeybees. Our study was designed to explore the effect of Nosema ceranae infection on honeybee sensitivity to sublethal doses of the insecticides fipronil and thiacloprid. METHODOLOGY/FINDING: Five days after their emergence, honeybees were divided in 6 experimental groups: (i) uninfected controls, (ii) infected with N. ceranae, (iii) uninfected and exposed to fipronil, (iv) uninfected and exposed to thiacloprid, (v) infected with N. ceranae and exposed 10 days post-infection (p.i.) to fipronil, and (vi) infected with N. ceranae and exposed 10 days p.i. to thiacloprid. Honeybee mortality and insecticide consumption were analyzed daily and the intestinal spore content was evaluated 20 days after infection. A significant increase in honeybee mortality was observed when N. ceranae-infected honeybees were exposed to sublethal doses of insecticides. Surprisingly, exposures to fipronil and thiacloprid had opposite effects on microsporidian spore production. Analysis of the honeybee detoxification system 10 days p.i. showed that N. ceranae infection induced an increase in glutathione-S-transferase activity in midgut and fat body but not in 7-ethoxycoumarin-O-deethylase activity. CONCLUSIONS/SIGNIFICANCE: After exposure to sublethal doses of fipronil or thiacloprid a higher mortality was observed in N. ceranae-infected honeybees than in uninfected ones. The synergistic effect of N. ceranae and insecticide on honeybee mortality, however, did not appear strongly linked to a decrease of the insect detoxification system. These data support the hypothesis that the combination of the increasing prevalence of N. ceranae with high pesticide content in beehives may contribute to colony depopulation.

International audience; Chaque année du début du prin - temps jusqu'aux premiers jours de l'automne, des milliards d'abeilles sortent de leurs ruches et partent visiter les fleurs des paysages environnants. Elles y trouvent nectars et pollens, éléments essentiels à la base de leur alimentation. C'est par cette intense activité de butinage que l'abeille domestique participe activement à la pollinisation des plantes sauvages et cultivées. Son influence directe sur la qualité et la quantité des récoltes ainsi que sur le maintien de la biodiversité florale est aujourd'hui largement validée et souligne le rôle prépondérant des abeilles (sauvages et domestiques) dans le fonctionnement des écosystèmes. En France, les abeilles domestiques, Apis mellifera (Hymenoptera: Apidae), sont l'outil de travail d'environ 70 000 apiculteurs professionnels et amateurs qui tirent bénéfice des labeurs de cet hyménoptère (environ 20 000 tonnes de miel récoltées en France en 2009).