Queen pheromone modulates brain dopamine function in worker honey bees

Abstract

Honey bee queens produce a sophisticated array of chemical signals (pheromones) that influence both the behavior and physiology of their nest mates. Most striking are the effects of queen mandibular pheromone (QMP), a chemical blend that induces young workers to feed and groom the queen and primes bees to perform colony-related tasks. But how does this pheromone operate at the cellular level? This study reveals that QMP has profound effects on dopamine pathways in the brain, pathways that play a central role in behavioral regulation and motor control. In young worker bees, dopamine levels, levels of dopamine receptor gene expression, and cellular responses to this amine are all affected by QMP. We identify homovanillyl alcohol as a key contributor to these effects and provide evidence linking QMPinduced changes in the brain to changes at a behavioral level. This study offers exciting insights into the mechanisms through which QMP operates and a deeper understanding of the queen's ability to regulate the behavior of her offspring.Apis mellifera ͉ biogenic amines ͉ neuroethology ͉ neuromodulation ͉ pheromonal communication C omplex social interactions require systems of communication that are reliable and unambiguous. The honey bee, Apis mellifera, employs Ͼ50 substances to communicate with and to organize its colony, and the information that is conveyed between colony members is both subtle and sophisticated (1-3).Maintaining colony organization is a primary role of the queen, whose pheromones enable her to regulate not only the behavior but also the physiology of her nest mates. The most striking effects are those of queen mandibular pheromone (QMP), a chemical blend that induces young workers to feed and groom the queen (Fig. 1) and primes bees to perform colonyrelated tasks (4, 5). The retinue of workers that attend the queen facilitates the distribution of QMP throughout the colony, where it inhibits the rearing of new queens (6), helps prevent the development of worker ovaries (7), influences comb-building activities, (8) and affects the biosynthesis of juvenile hormone (9) [and hence the age-related behavioral ontogeny of recipient workers (10)]. Despite QMP's central role in the normal functioning and organization of honey bee colonies, very little is known about the cellular mechanisms through which it operates.We were intrigued by one of the key components of QMP, homovanillyl alcohol (HVA) (4). HVA (4-hydroxy-3-methoxyphenylethanol) bears a striking structural resemblance to dopamine (see Fig. 1 Right), a biogenic amine that plays a central role in insect behavioral regulation and motor control (11-18). The presence of this compound within the pheromone blend suggested to us that dopamine function in the brain of recipient bees might be affected by exposure to QMP. To test this hypothesis, we exposed young workers to QMP and examined its effects on brain dopamine levels, levels of dopamine receptor gene expression, and cellular responses to this amine. The results provide compelling evidence that QMP al...

The role of the queen mandibular gland pheromone in honeybees (Apis mellifera): honest signal or suppressive agent?

“…The rise in HVA seems to be associated with ovary activation that typically occurs after mating Engels et al 1997). Beggs et al (2007) showed that HVA reduces dopamine levels in the honeybee's brain. Because feeding of dopamine to worker bees elevates rates of ovarian activation (Dombroski et al 2003), HVA might be a potential agent within QMP involved in regulating worker sterility.…”

Queen mandibular pheromone: questions that remain to be resolved

“…Interestingly, bees exposed to QMP early in adult life tend to have lower levels of Amdop1 expression in the antennae and brain than bees that have never been exposed to this pheromone (Beggs et al 2007;Vergoz et al 2009). Moreover, young workers showing strong attraction to QMP have been found to have higher Amdop3 transcript levels, and levels of transcript for the octopamine receptor, Amoa1, than bees not strongly attracted to this pheromone.…”

“…Harris and Woodring found that one consequence of removing the queen from a honey bee colony was that brain DA levels in young worker bees increase (Harris and Woodring 1995). QMP, and HVA alone, have subsequently been shown to reduce DA levels in young worker bees and QMP transiently alters levels of DA receptor gene expression in the brain (Beggs et al 2007). In an experiment in which DA receptors were expressed in vitro, HVA was found to selectively activate AmDOP3 receptors while having no effect on the two other honey bee DA receptors, AmDOP1 and AmDOP2 (Beggs and Mercer 2009).…”

“…For example, QMP not only reduces the rate of JH biosynthesis causing delays in the ontogeny of foraging behaviour (Kaatz et al 1992;Pankiw et al 1998;Slessor et al 2005), but in young bees it can also reduce levels of DA in the brain (Beggs et al 2007). Nurses and foragers have different gene expression profiles , and QMP treatments have been found to activate nurse genes and to repress forager genes in the brain of worker bees (Grozinger et al 2003).…”

Neurogenic and Neuroendocrine Effects of Goldfish Pheromones

“…Pheromones are a class of environmental cues that are known to exert profound effects in insect brains (Grozinger et al, 2003Alaux and Robinson, 2007;Beggs et al, 2007;Grozinger and Robinson, 2007;Vergoz et al, 2007). In mice, odors from soiled bedding of dominant males have been shown to stimulate neurogenesis in the olfactory bulb and the hippocampus of adult females (Mak et al, 2007).…”