Abstract
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.
Highlights
Honeybees (Apis mellifera), like any living organism, are constantly exposed to a wide variety of biotic and abiotic stressors
While the N. ceranae-fipronil combination induced the highest honeybee mortality, it did not lead to a synergistic effect as previously reported [39]
No synergy between N. ceranae and fipronil treatments has been observed in the present work while they led to a synergistic effect on honeybee mortality in previous studies [38,39]
Summary
Honeybees (Apis mellifera), like any living organism, are constantly exposed to a wide variety of biotic and abiotic stressors. The microsporidian parasite Nosema ceranae, one of the most common pathogens of the honeybee, is a unicellular eukaryote and invasive intracellular parasite infecting A. mellifera midgut and inducing a disease named nosemosis [5]. This worldwide emerging parasite presents a high prevalence in honeybee colonies [6,7]. Honeybees are frequently exposed to neonicotinoid and phenylpyrazole insecticides which are neurotoxic compounds intensively used on crops worldwide against arthropod pests [17,18]. Low doses of the phenylpyrazole fipronil or the neonicotinoid imidacloprid can lead to a significant decrease in honeybee survival following chronic exposure [32,33,34]
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