Regulation of forager honey bee appetite independent of the glucose-insulin signaling pathway

Authors: GHANEM, SALEH - Sabanci University; AKULKU, IREM - Sabanci University; GUZLE, KUBRA - Sabanci University; KHAN, ZAEEMA - Sabanci University; Mayack, Christopher

Submitted to: Frontiers in Insect Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/30/2024
Publication Date: 2/15/2024
Citation: Ghanem, S., Akulku, I., Guzle, K., Khan, Z., Mayack, C.L. 2024. Regulation of forager honey bee appetite independent of the glucose-insulin signaling pathway. Frontiers in Insect Science. 4-2024. https://doi.org/10.3389/finsc.2024.1335350.
DOI: https://doi.org/10.3389/finsc.2024.1335350

Interpretive Summary: To ensure that there is enough energy, but not an excess, to carry out life activities, hunger and appetite regulate food intake. How the two communicate and regulate one another remains largely unknown and this is especially true for insects where the main sugar found in their blood is trehalose and not glucose. This is in contrast to vertebrates where glucose acts as the primary sugar indicating what level of hunger an individual should have to maintain energetic balance. Honey bee foragers undergo energetically demanding activities such as sustaining flight for foraging. Therefore, they serve as a useful model organism to determine if there are alternative pathways responsible for more direct and rapid regulation of appetite. We investigated which sugar levels in the blood influence certain brain neurotransmitters and in turn change appetite levels as the bee ages. We found in forager honey bees only that there is a connection between blood trehalose levels, two neurotransmitters in the brain, and appetite levels. These changes were independent of insulin production. Our results suggest that forager bees may have an alternative pathway for appetite regulation that is based on the amount of the trehalose sugar found in the blood. This pathway may be present in other insects where they typically have little room for fat storage, but yet perform energy demanding activities such as sustaining flight. We suspect that this regulatory pathway is not found in vertebrates where glucose levels are the predominate signal involved in appetite regulation and there is no presence of trehalose in the blood.

Technical Abstract: To maintain energetic homeostasis the energetic state of the individual needs to communicate with appetite regulatory mechanisms on a regular basis. Although hunger levels indicated by the energetic state and appetite levels, the desire for food intake, tend to be correlated, and on their own are well studied, how the two cross-talk and regulate one another is less known. Insects, in contrast to vertebrates, tend to have trehalose as the primary sugar found in the hemolymph, which could possibly serve as an alternative monitor of the energetic state in comparison to the glucose insulin signaling pathway, found in vertebrates. We investigate how manipulating hemolymph sugar levels alter the biogenic amines in the honey bee brain, appetite levels, and insulin like peptide gene expression, across three age classes, to determine how the energetic state of the honey bee might be connected to appetite regulation. We found that only in the forager bees, with a lowering of hemolymph trehalose levels, there was an increase in octopamine and a decrease in tyramine levels in the honey bee brain that corresponded with increased appetite levels, while there was no significant changes in ILP gene expression. Our findings suggest that hemolymph trehalose levels aid in regulating appetite levels, in forager bees, via octopamine and tyramine, and this regulation appears to be functioning independent of the glucose insulin signaling pathway. Whether this potentially more direct and rapid appetite regulatory pathway can be generalized to other insects, which also undergo energy demanding activities, remains to be investigated.