Fat body lipolysis connects poor nutrition to hypopharyngeal gland degradation in Apis mellifera

Abstract

The hypopharyngeal glands (HGs) of honey bee nurse workers secrete the major protein fraction of jelly, a protein and lipid rich substance fed to developing larvae, other worker bees, and queens. A hallmark of poorly nourished nurses is their small HGs, which actively degrade due to hormone-induced autophagy. To better connect nutritional stress with HG degradation, we looked to honey bees and other insect systems, where nutrient stress is often accompanied by fat body degradation. The fat body contains stored lipids that are likely a substrate for ecdysteroid synthesis, so we tested whether starvation caused increased fat body lipolysis. Ecdysteroid signaling and response pathways and IIS/TOR are tied to nutrient-dependent autophagy in honey bees and other insects, and so we also tested whether and where genes in these pathways were differentially regulated in the head and fat body. Last, we injected nurse-aged bees with the honey bee ecdysteroid makisterone A to determine whether this hormone influenced HG size and autophagy. We find that starved nurse aged bees exhibited increased fat body lipolysis and increased expression of ecdysteroid production and response genes in the head. Genes in the IIS/TOR pathway were not impacted by starvation in either the head or fat body. Additionally, bees injected with makisterone A had smaller HGs and increased expression of autophagy genes. These data support the hypothesis that nutritional stress induces fat body lipolysis, which may liberate the sterols important for ecdysteroid production, and that increased ecdysteroid levels induce autophagic HG degradation.