Antennal Protein Profile in Honeybees: Caste and Task Matter More Than Age

Abstract

Reproductive and task partitioning in large colonies of social insects suggest that colony members belonging to different castes or performing different tasks during their life (polyethism) may produce specific semiochemicals and be differently sensitive to the variety of pheromones involved in intraspecific chemical communication. The main peripheral olfactory organs are the antennal chemosensilla, where the early olfactory processes take place. At this stage, members of two different families of soluble chemosensory proteins [odorant-binding proteins (OBPs) and chemosensory proteins (CSPs)] show a remarkable affinity for different odorants and act as carriers while a further family, the Niemann-Pick type C2 proteins (NPC2) may have a similar function, although this has not been fully demonstrated. Sensillar lymph also contains Odorant degrading enzymes (ODEs) which are involved in inactivation through degradation of the chemical signals, once the message is conveyed. Despite their importance in chemical communication, little is known about how proteins involved in peripheral olfaction and, more generally antennal proteins, differ in honeybees of different caste, task and age. Here, we investigate for the first time, using a shotgun proteomic approach, the antennal profile of honeybees of different castes (queens and workers) and workers performing different tasks (nurses, guards, and foragers) by controlling for the potential confounding effect of age. Regarding olfactory proteins, major differences were observed between queens and workers, some of which were found to be more abundant in queens (OBP3, OBP18, and NPC2-1) and others to be more abundant in workers (OBP15, OBP21, CSP1, and CSP3); while between workers performing different tasks, OBP14 was more abundant in nurses with respect to guards and foragers. Apart from proteins involved in olfaction, we have found that the antennal proteomes are mainly characterized by castes and tasks, while age has no effect on antennal protein profile. Among the main differences, the strong decrease in vitellogenins found in guards and foragers is not associated with age.

Gene expression is more strongly associated with behavioural specialization than with age or fertility in ant workers

“…Worker gene expression was most strongly associated with behavioural specialization, as, for example, illustrated by the finding of ten times more differentially expressed genes (DEGs) between brood carers and foragers than between young and old, or fertile and infertile workers. Gene expression being more strongly associated with behavioural specialization than with age is consistent with previous age‐controlled transcriptomic (Alaux et al, ; Whitfield et al, ) and proteomic (Iovinella et al, ) studies on honeybee workers but has so far not been shown in other social insects. In contrast, an age‐controlled comparison of queens and workers revealed more DEGs associated with age than with caste in the ant Lasius niger (Lucas et al, ).…”

Expression Profile and Ligand Screening of a Putative Odorant-Binding Protein, AcerOBP6, from the Asian Honeybee

“…The potential biological significance of genes could be derived from their transcript expression profiles [24]. It is widely believed that the OBPs specifically expressed in antennae play a role in the olfaction of insects [25,26], while the ones expressed elsewhere may get involved in the non-chemosensory processes [27][28][29]. According to the qRT-PCR results, the AcerOBP6 transcript was primarily expressed in the antennae of forager bees and significantly more expressed than in the antennae of drones, suggesting that AcerOBP6 may play an essential role in recognizing general odorants compared to sex pheromones.…”

Social complexity, life-history and lineage influence the molecular basis of caste in a major transition in evolution

“…ATP-synthase has caste specific expression in the weaver ant 46 (OG0006255 and OG0006612) and esterase E4-like (OG0000783) is upregulated in young honeybee queens compared to nurses at the proteomic level 47 . There are also other genes of interest, which to our knowledge have not previously associated with caste, including Toll-like receptor 8 (OG0001441) (see Supplementary Table S4).…”