Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees

Abstract

Previous research showed that the presence of older workers causes a delayed onset of foraging in younger individuals in honey bee colonies, but a specific worker inhibitory factor had not yet been identified. Here, we report on the identification of a substance produced by adult forager honey bees, ethyl oleate, that acts as a chemical inhibitory factor to delay age at onset of foraging. Ethyl oleate is synthesized de novo and is present in highest concentrations in the bee's crop. These results suggest that worker behavioral maturation is modulated via trophallaxis, a form of food exchange that also serves as a prominent communication channel in insect societies. Our findings provide critical validation for a model of self-organization explaining how bees are able to respond to fragmentary information with actions that are appropriate to the state of the whole colony.

Order, Disorder, Death: Lessons from a Superorganism

“…Chemosensory cues, in particular, play an important role in honeybee social organization (Sections IV-VI), having powerful effects on individual gene expression patterns (Grozinger et al, 2003), behavior (Leoncini et al, 2004b;Pankiw, 2004a;Pankiw and Page, 2003), and physiology (Hoover et al, 2003;Robinson, 1992, 1996). A unique phenomenon that emerges from integration of social chemosensory cues is the behavioral and physiological differentiation of temporal worker forms (Section IV).…”

“…Rather, a dynamic differentiation emerges through social signals produced by the workers themselves. The foragers synthesize a blend of cuticular hydrocarbons and pheromones that are specific to their stage (Leoncini et al, 2004b;Pankiw, 2004a). This signature is transferred by physical contact with the nurse bees (Huang and Robinson, 1992).…”

Effects of age and Reproductive Status on Tergal Gland Secretions in Queenless Honey bee Workers, Apis mellifera scutellata and A. m. capensis

“…Since workers were kept in cages without brood, we can exclude contamination as the source of these compounds. Traces of ethyl oleate have been found on honey bee worker cuticle (Leoncini et al 2004), while ethyl palmitate and ethyl oleate have been found on the cuticle of stingless bees Frieseomelitta vari (Nunes et al 2008). Ethyl palmitate has been implicated in inhibition of ovary activation in honey bee workers (Mohammedi et al 1998), while ethyl oleate delays transition of nurse honey bees into foragers (Castillo et al 2012).…”

“…Ethyl palmitate has been implicated in inhibition of ovary activation in honey bee workers (Mohammedi et al 1998), while ethyl oleate delays transition of nurse honey bees into foragers (Castillo et al 2012). The latter causes nurse bees to spend more time in the hive to tend to the brood and the queen (Leoncini et al 2004). Since reproductively dominant bees need more subordinate individuals to tend to their needs (Hillesheim et al 1989), one would expect that the signal for dominance should be more abundant in bees with activated ovaries.…”

Profile of Gene E. Robinson

“…Years later, Robinson collaborated with colleague Yves LeConte and found that the substance involved was the primer pheromone ethyl oleate (6). In between these findings, Robinson had uncovered other pheromones that contributed to maintaining the high plasticity of the honey bee labor system, including one produced by the brood, and another, mandibular pheromone, produced by the queen (7,8).…”