The Effects of Fat Body Tyramine Level on Gustatory Responsiveness of Honeybees (Apis mellifera) Differ between Behavioral Castes

Abstract

Division of labor is a hallmark of social insects. In the honeybee (Apis mellifera) each sterile female worker performs a series of social tasks. The most drastic changes in behavior occur when a nurse bee, who takes care of the brood and the queen in the hive, transitions to foraging behavior. Foragers provision the colony with pollen, nectar or water. Nurse bees and foragers differ in numerous behaviors, including responsiveness to gustatory stimuli. Differences in gustatory responsiveness, in turn, might be involved in regulating division of labor through differential sensory response thresholds. Biogenic amines are important modulators of behavior. Tyramine and octopamine have been shown to increase gustatory responsiveness in honeybees when injected into the thorax, thereby possibly triggering social organization. So far, most of the experiments investigating the role of amines on gustatory responsiveness have focused on the brain. The potential role of the fat body in regulating sensory responsiveness and division of labor has large been neglected. We here investigated the role of the fat body in modulating gustatory responsiveness through tyramine signaling in different social roles of honeybees. We quantified levels of tyramine, tyramine receptor gene expression and the effect of elevating fat body tyramine titers on gustatory responsiveness in both nurse bees and foragers. Our data suggest that elevating the tyramine titer in the fat body pharmacologically increases gustatory responsiveness in foragers, but not in nurse bees. This differential effect of tyramine on gustatory responsiveness correlates with a higher natural gustatory responsiveness of foragers, with a higher tyramine receptor (Amtar1) mRNA expression in fat bodies of foragers and with lower baseline tyramine titers in fat bodies of foragers compared to those of nurse bees. We suggest that differential tyramine signaling in the fat body has an important role in the plasticity of division of labor through changing gustatory responsiveness.

Individual differences in learning and biogenic amine levels influence the behavioural division between foraging honeybee scouts and recruits

“…Scouts have elevated amounts of tyramine in their brains compared to recruits (Figure c). These biogenic amines have been implicated in learning and foraging behaviour (Scheiner, Reim, Eirik, Entler, & Barron, ; Scheiner et al., ). Previous research found a QTL for learning differences using the same LI assay was linked to a specific area of the genome, Pln2 (or lrn1; 17).…”

Gene expression is stronger associated with behaviour than with age and fertility in ant workers

“…Similar to Vg, malvolio underwent duplication and subfunctionalization in multiple social and subsocial insects, which raises the question as to whether the role of malvolio in honey bees can be extended to other insects [63]. The neuromodulators tyramine and its precursor octopamine promote the onset of foraging, are involved into the rewarding system in honey bee foragers and increase gustatory responsiveness [28,64–66], but their role in other species is unknown.…”

“…As age and fertility additionally influence gene expression [22,28,67,68], studies that did not experimentally control for age and physiology when comparing gene expression between brood carers and foragers [e.g. 28,31,46,56,57,69–73] might have produced results driven not only by behaviour, but also by age and fertility. Such confounded transcriptomic analyses are not a problem specific to research on insect behaviour but occur across study systems and contexts.…”

Levels and activity of cyclic guanosine monophosphate‐dependent protein kinase in nurse and forager honeybees

“…S1). Like in earlier studies (Behrends et al, ; Thamm and Scheiner, ; Değirmenci et al, ; Scheiner et al , ; ). Foragers were more responsive to sucrose than nurse bees were, supporting the hypothesis that nutrition‐related pathways are possibly involved in the regulation of task allocation.…”

“…In the GG, about 40 motoneurons are involved in controlling the proboscis extension response (Rehder, 1989). In the mushroom bodies, several sensory modalities, including gustatory and mechanosensory information, converge (Schröter and Menzel, 2003). Experiments with blowflies suggest that these structures are involved in the feeding threshold determination (Nisimura et al, 2005).…”