Lipidomic specializations of honeybee (Apis mellifera) castes and ethotypes

[Display omitted] •Castes and ethotypes of Apis mellifera form qualitatively distinct classes of membrane lipid composition.•Cardiolipins are the lipid class most strongly differentiating castes and ethotypes.•Sexuals and cell-heater bees are characterized by highly-saturated, short-chained cardiolipins.•Forager bees show an inverse pattern.•Lipid composition can be experimentally influenced through fatty acids and brood rearing temperature. Honeybees of the same colony combine a near-homogeneous genetic background with a high level of phenotypic plasticity, making them ideal models for functional lipidomics. The only external lipid source of the colony is pollen, a diet rich in polyunsaturated fatty acids (PUFA). It has been suggested that differences in exposure to pollen-derived PUFA could partly explain differences in longevity between honeybee castes. We here investigated whether the membrane composition of honeybees plays roles in the physiological adaptation to tasks of individuals within the colony. Membranes of cell heaters, a group of workers producing heat from their flight muscles to uphold brood nest temperature, were compared to those of different types of non-heaters. We found that the lipidomic profiles of these groups fall into clearly different “lipotypes”, characterized by chain length and saturation of phospholipid-bound fatty acyl residues. The nutritional exposure to PUFA during early adult life and pupal development at the lower edge of the natural range of brood nest temperature both suppressed the expression of the cell heater-“lipotype”. Because cardiolipins (CL) are the lipid class most clearly differentiating honeybee phenotypes, and CL plays central roles in mitochondrial function, dysfunction and aging, our findings could help to understand these processes in other animals and humans. Taken together, the lipidome analysis of different life stages of workers, fertile queens, and drones lead to the hypothesis that honeybee “lipotypes” might represent adaptations to different energetic profiles and the likelihood of exposure to low temperatures.