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From Society to Genes with the Honey Bee

A combination of environmental, genetic, hormonal and neurobiological factors determine a bee's progression through a series of life stages

Gene Robinson

Inhibitory Interactions

Figure 4. Older beesClick to Enlarge Image

How do bees perceive changes in colony needs and adjust their behavioral development to perform the tasks most in demand? Postdoctoral associate Zachary Huang and I found that the rate of endocrine-mediated behavioral development is influenced by inhibitory social interactions. That is, older bees inhibit the behavioral development of younger bees. Bees reared in isolation in a laboratory for seven days have forager-like levels of juvenile hormone and forage precociously when placed in colonies. By carefully manipulating a colony's age demography but keeping other characteristics unchanged, we found that the rate of behavioral development is negatively correlated with the proportion of older bees in a colony. So depleting a colony's foragers stimulates younger bees to forage earlier than normal. Conversely, younger bees forage later than normal if a colony's foragers stay in the hive for several days because a sprinkler aimed at the hive entrance makes them think it's raining.

Someone might imagine that bees could learn about their colony's condition by monitoring the combs in their hive. For instance, a young bee might notice a food shortage in the combs, which might result in a neuorendocrine response that triggers precocious behavioral development. To explore the possibility that bees pay attention to the combs in this way, Huang, graduate student David Schulz and I recently tested the effects of starvation on the rate of behavioral development. Young bees from starved colonies do start foraging a few days earlier than bees from well-fed colonies. This starvation effect, however, is not mediated by perceiving a shortage of food in the honeycomb. We showed this by keeping a colony well fed from a sugar feeder while we constantly—but discretely—vacuumed any stored food out of their honeycomb. This was accomplished by drilling small holes at the base of each honeycomb cell. Well-fed bees in an empty hive started to forage at ages similar to bees in colonies with ample food stores and not nearly as early in life as did bees in truly starved colonies.

Inhibitory social interactions that influence the rate of behavioral development involve chemical communication between colony members. This is strikingly similar to pheromone regulation of sexual maturation in rodent societies. For example, a queen's mandibular glands produce a pheromone that inhibits behavioral development. (See "The Essence of Royalty: Honey Bee Queen Pheromone" by Mark Winston and Keith Slessor in the July–August 1992 issue of American Scientist.) Queen mandibular pheromone has been known for some time to exert long-lasting effects on worker physiology and behavior by inhibiting the rearing of new queens. More recently, Mark Winston and Tanya Pankiw of Simon Fraser University, Huang and I demonstrated that queen mandibular pheromone depresses blood levels of juvenile hormone and, more important, delays the onset of foraging.

The primary modulator of behavioral development, however, appears to come from the workers themselves. The mandibular glands of workers contain compounds similar to those found in queen mandibular glands. Huang, Erika Plettner, a graduate student at Simon Fraser University, and I recently found that there must be direct social contact between bees for older ones to inhibit the development of younger ones. Moreover, older bees with their mandibular glands removed do not inhibit behavioral development. The mandibular glands of workers contain compounds similar to those found in queen mandibular glands. The inhibition that results from worker-worker interactions might come from exchanging a pheromone, which might be in the mandibular glands or somewhere else. When we removed the glands, that could have eliminated the inhibition because it removed the source of the pheromone or it simply blocked the pheromone's flow from another location. Clearly, more work must be done here.

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