Use of waggle dance information in honey bees is linked to gene expression in the antennae, but not in the brain

Abstract

Communication is essential for social animals, but deciding how to utilize information provided by conspecifics is a complex process that depends on environmental and intrinsic factors. Honey bees use a unique form of communication, the waggle dance, to inform nestmates about the location of food sources. However, as in many other animals, experienced individuals often ignore this social information and prefer to rely on prior experiences, i.e. private information. The neurosensory factors that drive the decision to use social information are not yet understood. Here we test whether the decision to use social dance information or private information is linked to gene expression differences in different parts of the nervous system. We trained bees to collect food from sugar water feeders and observed whether they utilize social or private information when exposed to dances for a new food source. We performed transcriptome analysis of four brain parts critical for cognition: the subesophageal ganglion, the central brain, the mushroom bodies, and the antennal lobes but, unexpectedly, detected no differences between social or private information users. In contrast, we found 413 differentially expressed genes in the antennae, suggesting that variation in sensory perception mediate the decision to use social information. Social information users were characterized by the upregulation of dopamine and serotonin genes while private information users upregualted several genes coding for odor perception. These results highlight that decision making in honey bees might also depend on peripheral processes of perception rather than higher-order brain centers of information integration.

Machine learning models identify gene predictors of waggle dance behaviour in honeybees

“…More functional approaches are needed to move beyond correlation and investigate whether a causal link exists between the expression levels of the genes that we identified and the performance of dance behaviour. For example, a recent study has revealed that gene expression associated with sensory perception rather than high cognitive functions is more important for bees following a dance when deciding whether to use personal information vs. social cues (the waggle dance) when engaging in the next foraging trip (Kennedy et al, 2021): it could be tested whether sensory perception has a role in the regulation of dance behaviour as well, by analysing gene expression in other brain parts such as the antennal or optic lobes that are clearly linked to the processing of sensory inputs. We are aware that other internal or external factors could contribute to define the patterns of gene expression in the honeybees that we analysed, as the brain is a complex organ that responds to a wide range of factors and stimuli that we could not control totally, such as bee age or number of dances performed, just to mention a few.…”

“…Despite this, we still do not have a complete picture of how the waggle dance is regulated at the brain level. Pioneering studies have started to reveal some of the key players at the levels of molecules (Barron et al, 2007; Kennedy et al, 2021; Linn et al, 2020), cell types (Kiya et al, 2007) and genetic pathways (Sen Sarma et al, 2009, 2010) associated with dance communication, but it is unclear what genes in the honeybee brain trigger the performance of dance behaviour once activated.…”

Early Life Exposure to Queen Mandibular Pheromone Mediates Persistent Transcriptional Changes in the Brain of Honey bee Foragers

“…The antennae were cut off and stored in 100 µL of Trizol™ (Invitrogen, USA). The mushroom bodies and antennal lobes were removed by making incisions through the antennal base, eyes, compound eye, and ocellus (52). The cuticles, glands, retina and tissue around the brain were removed and the exposed tissues of the head were submerged with cooled bee saline (154 mM NaCl, 2 mM NaH 2 PO 4 , 5.5 mM Na 2 HPO 4 , pH 7.2).…”

“…To further investigate QMP treatment effects on specific genes, we focused on candidate genes involved in key individual and social behaviors and traits. We compiled lists of genes and molecular pathways associated with foraging behavior and division of labor in honey bees (52,(60)(61)(62)(63)(64)(65)(66)(67)(68)(69)(70)(71)(72)(73)(74). Furthermore, we searched for genes that play roles in aging (52,(75)(76)(77)(78), immunity (79,80), and reproduction (33,34), i.e.…”

“…We compiled lists of genes and molecular pathways associated with foraging behavior and division of labor in honey bees (52,(60)(61)(62)(63)(64)(65)(66)(67)(68)(69)(70)(71)(72)(73)(74). Furthermore, we searched for genes that play roles in aging (52,(75)(76)(77)(78), immunity (79,80), and reproduction (33,34), i.e. processes known to be affected by queen signals (see Tables S1 for a complete list of the candidate genes).…”