Transcriptional, translational, and physiological signatures of undernourished honey bees (Apis mellifera) suggest a role for hormonal factors in hypopharyngeal gland degradation

Authors: Corby-Harris, Vanessa; Meador, Charlotte; Snyder, Lucy; SCHWAN, MELISSA - Former ARS Employee; MAES, PATRICK - University Of Arizona; JONES, BERYL - University Of Illinois; WALTON, ALEXANDER - Iowa State University; Anderson, Kirk

Submitted to: Journal of Insect Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/30/2015
Publication Date: 12/2/2015
Citation: Corby-Harris, V.L., Meador, C.A., Snyder, L.A., Schwan, M.R., Maes, P., Jones, B., Walton, A., Anderson, K.E. 2015. Transcriptional, translational, and physiological signatures of undernourished honey bees (Apis mellifera) suggest a role for hormonal factors in hypopharyngeal gland degradation. Journal of Insect Physiology. 85:65-75. https://doi.org/10.1016/j.jinsphys.2015.11.016.
DOI: https://doi.org/10.1016/j.jinsphys.2015.11.016

Interpretive Summary: Nurse worker bees take care of young bees and the queen in the hive by secreting royal and worker jelly from glands in their head. The size that these glands grow to is dependent on many factors, including diet; bees fed low amounts of protein and/or pollen have smaller glands that well-nourished bees. Glands start growing by 3d of adult age and up to this age are of similar size irrespective of their diet. However, in a very small window of early adulthood, differences in gland size start to emerge. This led us to the question of whether glands simply don’t grow or if they do grow and are actively degraded in this window. Through a combination of gene and protein studies and physiological assays we find support for the latter hypothesis. In addition, we find evidence that many of the same pathways that control gland growth in other insects also operate in bees. This work is relevant because it demonstrates why gland size responds to diet but also allows us to target specific pathways to increase gland size or at least prevent their degradation in colonies so nurse bees can properly nourish hive larvae under stressful conditions.

Technical Abstract: Honey bee colonies function as a superorganism, where facultatively sterile female workers perform various tasks that support the hive. Nurse workers undergo numerous anatomical and physiological changes in preparation for brood rearing, including the growth of hypopharyngeal glands (HGs). These glands produce the major protein fraction of a protein- and lipid-rich jelly used to sustain developing larvae. Pollen intake is positively correlated with HG growth, but growth in the first three days is similar regardless of diet, suggesting that initial growth is a pre-determined process while later HG development depends on nutrient availability during a critical window in early adulthood (>3 d). It is unclear whether the resultant size differences in nurse HG are simply due to growth arrest or active degradation of the tissue. To determine what processes cause such differences in HG size, we catalogued the differential expression of both gene transcripts and proteins in the HGs of 8 d old bees that were fed diets containing pollen or no pollen. 3438 genes and 367 proteins were differentially regulated due to nutrition. Of the genes and proteins differentially expressed, undernourished bees exhibited more gene and protein up-regulation compared to well-nourished bees, with the affected processes including salivary gland apoptosis, oogenesis, and hormone signaling. Protein secretion was virtually the only process up-regulated in well-nourished bees. Further assays demonstrated that inhibition of ultraspiracle, one component of the ecdysteroid receptor, in the fat body caused larger HGs. Undernourished bees also had higher acid phosphatase activity, a physiological marker of cell death, compared to well-nourished bees. These results support a connection between poor nutrition, hormonal signaling, and HG degradation.