Abstract
The expression of morphological differences between the castes of social bees is triggered by dietary regimes that differentially activate nutrient-sensing pathways and the endocrine system, resulting in differential gene expression during larval development. In the honey bee, Apis mellifera, mitochondrial activity in the larval fat body has been postulated as a link that integrates nutrient-sensing via hypoxia signaling. To understand regulatory mechanisms in this link, we measured reactive oxygen species (ROS) levels, oxidative damage to proteins, the cellular redox environment, and the expression of genes encoding antioxidant factors in the fat body of queen and worker larvae. Despite higher mean H2O2 levels in queens, there were no differences in ROS-mediated protein carboxylation levels between the two castes. This can be explained by their higher expression of antioxidant genes (MnSOD, CuZnSOD, catalase, and Gst1) and the lower ratio between reduced and oxidized glutathione (GSH/GSSG). In worker larvae, the GSG/GSSH ratio is elevated and antioxidant gene expression is delayed. Hence, the higher ROS production resulting from the higher respiratory metabolism in queen larvae is effectively counterbalanced by the up-regulation of antioxidant genes, avoiding oxidative damage. In contrast, the delay in antioxidant gene expression in worker larvae may explain their endogenous hypoxia response.
Highlights
The evolution of morphologically and functionally different adult castes represents a major transition in the highly eusocial organization of insects and vertebrates, as it literally sets a point of no return back to a communal or solitary lifestyle (Wilson and Hölldobler, 2005)
For the GSH/GSSG ratio (Figure 2C) there were no overall significant differences for the factors caste, developmental stage, or interaction, but the Bonferroni post-hoc test showed a significant difference in the redox state of fat body cells for the early fifth instar larvae (F1-stage, t=2.936, p
The coordinated, transient overexpression of antioxidant genes in early fifth instar larvae may be relevant for controlling oxidative stress, as expressed in the well balanced GSH/GSSG ratio throughout queen development (Figure 2)
Summary
The evolution of morphologically and functionally different adult castes represents a major transition in the highly eusocial organization of insects and vertebrates, as it literally sets a point of no return back to a communal or solitary lifestyle (Wilson and Hölldobler, 2005). Apis mellifera, a young female larva has the potential to develop into either a queen or a worker, contingent on the nutritional regime to which it is exposed during larval development (Haydak, 1970; Hartfelder et al, 2015), and as a consequence of these distinct feeding regimes, adult queens and workers differ in their external and internal morphologies and their reproductive capacities, and in their lifespans Understanding this remarkable developmental plasticity requires insights into how the differential larval feeding regimes are converted into meaningful systemic responses. The resulting elevated JH levels in the hemolymph of queen larvae (Rembold, 1987) prevent the onset of programmed cell death in the larval ovaries and, guarantee the high reproductive capacity of the adult queens (Hartfelder et al, 2018)
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