Starving honey bee (Apis mellifera) larvae signal pheromonally to worker bees

Abstract

Cooperative brood care is diagnostic of animal societies. This is particularly true for the advanced social insects, and the honey bee is the best understood of the insect societies. A brood pheromone signaling the presence of larvae in a bee colony has been characterised and well studied, but here we explored whether honey bee larvae actively signal their food needs pheromonally to workers. We show that starving honey bee larvae signal to workers via increased production of the volatile pheromone E-β-ocimene. Analysis of volatile pheromones produced by food-deprived and fed larvae with gas chromatography-mass spectrometry showed that starving larvae produced more E-β-ocimene. Behavioural analyses showed that adding E-β-ocimene to empty cells increased the number of worker visits to those cells, and similarly adding E-β-ocimene to larvae increased worker visitation rate to the larvae. RNA-seq and qRT-PCR analysis identified 3 genes in the E-β-ocimene biosynthetic pathway that were upregulated in larvae following 30 minutes of starvation, and these genes also upregulated in 2-day old larvae compared to 4-day old larvae (2-day old larvae produce the most E-β-ocimene). This identifies a pheromonal mechanism by which brood can beg for food from workers to influence the allocation of resources within the colony.

Odorant cues linked to social immunity induce lateralized antenna stimulation in honey bees (Apis mellifera L.)

“…4a; Pearson coefficient = 0.84; P = 0.0059; α = 0.0063; Bonferroni correction). Given that this compound is a familiar brood pheromone that is already known to increase worker visits to cells24, this is a remarkable result. Interestingly, β-ocimene was also consistently one of the most intense peaks observed in the chromatograms of dead brood (Fig.…”

“…5, Table 2). This finding is intriguing for two reasons: 1) β-ocimene has previously been shown to increase the frequency of worker visits to brood24 and 2) an independent study found that a different brood pheromone (brood ester pheromone; BEP) was also significantly more abundant in parasitized brood23. By increasing worker visits to brood cells that should otherwise not require attendance, β-ocimene may attract the attention of bees that can perform HB.…”

“…β-ocimene is a well-known brood pheromone which plays multiple roles in regulating worker behaviour and anatomy243435363738. Young larvae normally release β-ocimene to stimulate workers to feed them24, with levels tapering off with age.…”

“…Young larvae normally release β-ocimene to stimulate workers to feed them24, with levels tapering off with age. β-ocimene also plays a role in regulating forager activity38 and inhibits worker ovary development36, but, to our knowledge, its release has not been previously associated with the FKB assay or HB.…”

Behavioural, physiological and molecular changes in alloparental caregivers may be responsible for selection response for female reproductive investment in honey bees

“…Individual esters or ester subsets also have some biological activity (Slessor et al, 2005). Additionally, β-ocimene, a highly volatile component, is emitted by larvae to modulate honey bee behavioural maturation and nursing behaviour (He et al, 2016;Maisonnasse, Lenoir, Beslay, Crauser, & Le Conte, 2010;Traynor, Le Conte, & Page, 2015). These brood signals are mainly perceived by the antennae (Robertson & Wanner, 2006), the central olfactory organ of all insects, in which odourant transduction occurs within a few milliseconds from the boundary layer of the antenna to olfactory receptor neurons (Leal, 2013;Szyszka, Gerkin, Galizia, & Smith, 2014).…”