BioEd Online

Honeybee queens produce a chemical cocktail that politicians would swarm to get their hands on: the scent of a queen keeps her drones and workers loyal to the throne, dutifully feeding and grooming their ruler.

Now it seems that this chemical perfume also prevents worker bees from developing aversions. This means that undergoing a negative experience around a queen won't lead a worker bee to learn to hate her.

"They can still respond to something nasty," says entomologist Alison Mercer of the University of Otago in Dunedin, New Zealand. "But what they can't do is learn to associate particular stimuli with nasty outcomes."

Negative association

Mercer and her colleagues tested this by training bees to associate a particular smell (not from the queen) with a mild electrical shock. They strapped the bees down, released the odour, and administered the shock. The bees extended their stingers in response to the jolt.

After a few repetitions of scent and shock, the smell alone was enough to trigger the stinger reflex even without a jolt of electricity — so long as the bees didn't scent their queen.

Bees exposed to the queen's pheromones, and specifically to a compound called homovanillyl alcohol (HVA), did not learn to associate the smell with the shock. They could, however, still learn to associate a particular smell with food, showing that HVA was acting specifically on aversion rather than general learning or physical responsiveness. The results are published this week in Science¹.

Previous work had shown that HVA acts on the bee brain via a signalling molecule called dopamine. In humans, dopamine plays a role in motor control and reward-seeking behaviour. In insects, however, dopamine is responsible for motor control and aversion. A different chemical, called octopamine, mediates positive associations, which could explain why HVA did not affect responses to food.

Smells like queen spirit

HVA is just one of many compounds within the queen mandibular pheromone coating the queen's body. The queen's attendant workers groom her with their proboscises and by rubbing her with their antennae. Then, when they mix with the rest of the hive, they distribute her pheromones to other bees. This calms the crowd and prevents reproduction among worker bees. "As soon as you put a queen into a colony, the young workers are less active and less aggressive," says Mercer.

So why would a queen need to chemically prevent the workers from learning to hate her? One possibility, suggests Mercer, is that the queens may have a problem with body odour: in high concentrations, their heady mix of pheromones become repellent.

"You can overdo any odorant," says Mercer. "We experience that in humans, too." If worker bees, particularly those closest to the queen, were to get a whiff of that stench too many times, they may begin to avoid her. And that could spell the end of the queen.

Entomologist Mark Winston of Simon Fraser University in Vancouver, Canada, says the study provides an exciting glimpse into the relationship between genes and behaviour, but he finds the 'stinky queen' explanation unlikely. "I doubt that pheromone concentrations ever get high enough in a colony to be repellent," he says. But he says suppressing aversion may still be important for other bee activities.