First insights into the honey bee (Apis mellifera) brain lipidome and its neonicotinoid-induced alterations associated with reduced self-grooming behavior

Abstract

Introduction: Honey bees (Apis mellifera) play key roles in food production performing complex behaviors, like self-grooming to remove parasites. However, the lipids of their central nervous system have not been examined, even though they likely play a crucial role in the performance of cognitive process to perform intricate behaviors. Lipidomics has greatly advanced our understanding of neuropathologies in mammals and could provide the same for honey bees.

Objectives: The objectives of this study were to characterize the brain lipidome of adult honey bees and to assess the effect of clothianidin (a neurotoxic insecticide) on the brain lipid composition, gene expression, and performance of self-grooming behavior under controlled conditions (cage experiments).

Methods: After seven days of exposure to oral sublethal doses of clothianidin, the bees were assessed for self-grooming behavior; their brains were dissected to analyze the lipidome using an untargeted lipidomics approach and to perform a high throughput RNAseq analysis.

Results: Compared to all other organisms, healthy bee brain lipidomes contain unusually high levels of alkyl-ether linked (plasmanyl) phospholipids (51.42%) and low levels of plasmalogens (plasmenyl phospholipids; 3.46%). This could make it more susceptible to the effects of toxins in the environment. A positive correlation between CL 18:3/18:1/14:0/22:6, TG 6:0/11:2/18:1, LPE 18:0e and intense self-grooming was found. Sublethal doses of a neonicotinoid altered PC 20:3e/15:0, PC 16:0/18:3, PA 18:0/24:1, and TG 18:1/18:1/18/1 levels, and affected gene expression linked to GPI-anchor biosynthesis pathway and energy metabolism that may be partially responsible for the altered lipid composition.

Conclusion: This study showed that lipidomics can reveal honey bee neuropathologies associated with reduced grooming behavior due to sublethal neonicotinoid exposure. The ease of use, unusual brain lipidome as well as characterized behaviors that are affected by the environment make honey bees a promising model organism for studying the neurolipidome and associations with neurobehavioral disorders.

Keywords: Brain; Grooming; Honey bees; Lipidome; Neonicotinoids; Social immunity.