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

Authors: Corby-Harris, Vanessa; Snyder, Lucy; Meador, Charlotte

Submitted to: Journal of Insect Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/2/2019
Publication Date: 4/3/2019
Citation: Corby-Harris, V.L., Snyder, L.A., Meador, C.A. 2019. Fat body lipolysis connects poor nutrition to hypopharyngeal gland degradation in Apis mellifera. Journal of Insect Physiology. 116:1-9.

Interpretive Summary: Honey bees perform a variety of tasks in the hive according to their age. For example, foragers are generally older worker bees (~ >2 weeks old), while nurse workers are generally younger (~1-2 weeks old). Nurse workers “nurse”, or feed, larvae and the queen with jelly secreted from their hypopharyngeal glands (HGs). The size of these HGs is dependent on many factors, most importantly diet. If nurses are fed low amounts of pollen during their first week of life, their HGs are small. We showed previously that this was because the HGs of starved nurses undergo cell death, which is under the control of ecdysteroid hormones. Cholesterol is the substrate of the ecdysteroid steroid production pathway and is stored in the insect fat body. Fat body breakdown is also very common in stressed insects. We wondered whether these factors were connected. Specifically, we tested whether starved nurses exhibited reduced HG size, evidence of HG cell death, increased fat body breakdown, increased levels of circulating cholesterol, and increased expression of ecdysteroid production and response genes. We found that this was the case. Our results support the idea that nutritional stress causes small nurse worker HGs because these nurses’ fat bodies break down, which releases cholesterol that is liberated into the body for use in ecdysteroid hormone synthesis. We discuss the relevance of the nurse response to nutritional stress in a broader context to include other stressors.

Technical 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 programmed cell death. In an effort 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 cholesterol and cholesterol is a substrate for ecdysteroid synthesis, and so we tested whether starvation caused increased fat body lipolysis and the liberation of cholesterol into the hemolymph. Because both ecdysteroid signaling and response pathways and IIS/TOR have been implicated in fat body mobilization, we also tested whether and where genes in these pathways were differentially regulated. We find that starved nurse bee have smaller HGs with decreased function and increased signatures of autophagy. Starved nurses also exhibited increased fat body lipolysis, increased hemolymph cholesterol levels, 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. These data support the hypothesis that nutritional stress induces fat body lipolysis, which liberates cholesterol that is used in the ecdysteroid production that leads to HG degradation.