Decoupling the effects of nutrition, age and behavioral caste on honey bee physiology,immunity, and colony health

Authors: Corona, Miguel; BRANCHICCELA, BELEN - Instituto Nacional De Investigacion Argropecuaria, Urugary; Alburaki, Mohamed; Palmer-Young, Evan; Madella, Shayne; Chen, Yanping - Judy; Evans, Jay

Submitted to: Frontiers in Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/22/2023
Publication Date: 3/13/2023
Citation: Corona, M.V., Branchiccela, B., Alburaki, M., Palmer-Young, E.C., Madella, S., Chen, Y., Evans, J.D. 2023. Decoupling the effects of nutrition, age and behavioral caste on honey bee physiology,immunity, and colony health. Frontiers in Physiology. 14: Article e1149840. https://doi.org/10.3389/fphys.2023.1149840.
DOI: https://doi.org/10.3389/fphys.2023.1149840

Interpretive Summary: Although impaired colony health and, ultimately, colony collapse, are anticipated outcomes of nutritional stress, the mechanisms by which this phenomenon occurs are still not well understood. In particular, little is known about how nutrition induces changes in honeybee physiology associated with behavioral development and its influence in immunity and susceptibility to diseases. The lack of understanding of this process reflects several factors, including the experimental complexity of uncoupling confounding factors at colony colony-level. In this study, we used a technique that allow us to uncouple the effects of age, behavior, and nutrition. Our results provide important information on the physiological mechanisms by which nutritional stress induces abnormal worker’s behavioral development (precocious foraging), reduced brood production and unbalanced colony demography. In addition, this study also reveals valuable insights into the evolutionary mechanisms that connect reproduction, immunity, and lifespan in honeybee castes. In contrast with foraging, nursing behavioral/physiological state is associated with reduced extrinsic risk of mortality. We found that nursing-associated genes are positively correlated with nutrition but negatively correlated with the expression of immune genes and levels of honeybee virus. To explain these results, we propose that low expression of immune genes in nurses is an indicator of a reduced level of infections. This study opens new perspectives into the understanding of the physiological and evolutionary mechanisms underlying the effects of nutrition on honeybee division of labor and immunity.

Technical Abstract: Nutritional stress, and especially a dearth of pollen, is considered an important factor associated with honey bee colony losses. Although impaired colony health and colony collapse are anticipated outcomes of nutritional stress, the mechanisms by which this phenomenon occurs are still not well understood. In particular, little is known about how nutrition induces changes in honey bee physiology, behavioral development and its influence in immunity and susceptibility to diseases. Among the factors that have prevented a better understanding of this process it is the experimental complexity of colony-level experiments that complicate the uncoupling of confounding variables. In this study, we used pollen-restricted colonies as a model to study the nutritional stress conditions experienced in colonies within intensively cultivated agricultural areas. This model was complemented by the establishment of an experimental design, which allowed us to uncouple the effect of nutrition, behavior and age. We used this system to determine the effect of pollen restriction on workers’ behavioral development. Then, we analyzed the effect of nutritional stress, behavior and age on the expression of nutritionally-regulated genes associated with nursing and foraging. Finally, we analyzed the effects of these variables on the expression of immune genes and virus titers. Our results show that behavioral transition was associated with important changes in the expression of genes involved in physiological activity, immunity and viral titers. The expression of immune genes was primarily affected by behavior, with higher levels in foragers. DWV titers were significantly affected by behavior and nutritional status. Correlation analyses support the predominant effect of behavior on immunity and susceptibility to viral infection, revealing that both immune genes and DWV exhibited strong negative correlations with genes associated with nursing, but positive correlations with genes associated with foraging. Our results provide valuable insights into the physiological mechanisms by which nutritional stress is associated with colony losses.