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

Abstract

Nutritional stress, especially a dearth of pollen, has been linked to honey bee colony losses. Colony-level experiments are critical for understanding the mechanisms by which nutritional stress affects individual honey bee physiology and pushes honey bee colonies to collapse. In this study, we investigated the impact of pollen restriction on key markers of honey bee physiology, main elements of the immune system, and predominant honey bee viruses. To achieve this objective, we uncoupled the effects of behavior, age, and nutritional conditions using a new colony establishment technique designed to control size, demography, and genetic background. Our results showed that the expression of storage proteins, including vitellogenin (vg) and royal jelly major protein 1 (mrjp1), were significantly associated with nursing, pollen ingestion, and older age. On the other hand, genes involved in hormonal regulation including insulin-like peptides (ilp1 and ilp2) and methyl farnesoate epoxidase (mfe), exhibited higher expression levels in young foragers from colonies not experiencing pollen restriction. In contrast, pollen restriction induced higher levels of insulin-like peptides in old nurses. On the other hand, we found a strong effect of behavior on the expression of all immune genes, with higher expression levels in foragers. In contrast, the effects of nutrition and age were significant only the expression of the regulatory gene dorsal. We also found multiple interactions of the experimental variables on viral titers, including higher Deformed wing virus (DWV) titers associated with foraging and age-related decline. In addition, nutrition significantly affected DWV titers in young nurses, with higher titers induced by pollen ingestion. In contrast, higher levels of Black queen cell virus (BQCV) were associated with pollen restriction. Finally, correlation, PCA, and NMDS analyses proved that behavior had had the strongest effect on gene expression and viral titers, followed by age and nutrition. These analyses also support multiple interactions among genes and virus analyzed, including negative correlations between the expression of genes encoding storage proteins associated with pollen ingestion and nursing (vg and mrjp1) with the expression of immune genes and DWV titers. Our results provide new insights into the proximal mechanisms by which nutritional stress is associated with changes in honey bee physiology, immunity, and viral titers.

Co-infection with two iflaviruses (deformed wing virus and sacbrood virus) affects viral and immune dynamics and synergistically increases honey bee mortality

“…Similarly to our results, one study [67] found that inhibition of defensin-1 can occur in parallel to the activation of the RNAi pathway in DWV-B inoculated bees. Our study shows that there may be concurrent inhibition of the melanisation pathway, which was not the case in other studies [40,68]. Conversely, when observed, AMP production was activated on 6 dpi but not on 3 dpi, confirming that AMPs are used as a late defence system that may remain active for longer times [61].…”

Behavioral and genetic correlates of heterogeneity in learning performance in individual honeybees, Apis mellifera

“…However, less is known about differences between young and old foragers. Only a few studies addressed this question [ 114 , 115 ]. The correlation with the gene set specific for the cAMP second messenger pathway can explain the higher sensitivity of the high performer bees compared to their low performing counterparts.…”

Detection and characterization of Deformed wing virus (DWV) in apiaries with stationary and migratory management in the province of Entre Ríos, Argentina

“…While we assumed that the lack of nutritional diversity could be a factor affecting colony health; however, this assumption must be considered cautiously, and further analysis of the protein contribution provided by this type of pollen is required. Nevertheless, several studies have demonstrated the impact of nutritional stress, revealing a positive relationship between multi oral areas and the annual survival of hives 49,50 .…”