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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

Brain Remodeling

Figure 5. Changes in a bee's brainClick to Enlarge Image

How does a bee's brain support the striking changes in behavior that take place during maturation? A small part of the answer lies in the mushroom bodies, a brain region thought to be the center of learning and memory in insects. Graduate student Ginger Withers, Fahrbach and I discovered about a 20 percent increase in the volume of a specific area of the mushroom bodies as worker honey bees mature. This volume increase occurs in a mushroom-body subregion where synapses, or connections, are made between neurons from other brain regions that are devoted to sensory input. This was the first report of such brain plasticity in an invertebrate, and it was particularly exciting because volume increases in brain regions in vertebrates reflect increases in certain cognitive abilities.

It seemed that the increase in the mushroom bodies might be learning-related. Young workers take orientation flights prior to the onset of foraging to learn their way around outside the hive, and the increase in volume in the mushroom bodies begins at that time. To test flying's effect on mushroom-body volume, Withers, Fahrbach and I made what we called "big-back bees." By attaching a large tag to each bee's back and placing a screen at the hive's entrance, we prevented some workers from flying out of the hive but allowed them to interact with other bees. Big-back bees showed normal increases in mushroom-body volume despite their deprivation from orientation flights. So far, the volume increase is unstoppable. Fahrbach, Darrell Moore of East Tennessee State University, graduate student Sarah Farris, postdoctoral associate Elizabeth Capaldi and I showed that it takes place even in bees reared in social isolation and complete darkness in a laboratory.

Still, it might be premature to exclude the idea of a connection between the plasticity of the mushroom bodies and orientation flights in honey bees. Our results indicate that a bee's mushroom bodies need not increase because of taking orientation flights, but we have not ruled out a volume increase that prepares a bee for those flights. In other words, the mushroom bodies might need to increase in volume to provide the necessary brain space for a bee to learn how to get around outside its hive, and how to get back.

After learning to orient outside the hive, a bee learns to forage, and that might also involve an increase in the mushroom bodies. Withers, Fahrbach and I showed that the mushroom bodies increase in volume more rapidly in precocious foragers than in nurse bees of the same age. This result has been confirmed in the laboratory of Randolf Menzel in Berlin, using a somewhat different neuroanatomical analysis. These results suggest that the structure of the mushroom bodies might be sensitive to changes in social context that are associated with the onset of foraging.

While we continue our efforts to unravel the significance of a volume increase in the mushroom bodies, we also wonder how the region gets bigger. The number of cells in the mushroom bodies is highly stable in adult life. The production of new neurons is not detectable, and there is no evidence for cell death, according to research with Fahrbach that was performed by undergraduates Jennifer Strande and Jennifer Mehren. Accordingly, the volume increase in the mushroom bodies probably represents an increased arborization of some subpopulation of brain cells that already exists. This increased proliferation of neuronal branches would likely result in an increase in the number of synapses per neuron, which would impact the processing of information in the mushroom bodies.

Beyond structural changes in a worker bee's brain, neurochemical analyses have revealed striking changes in levels of biogenic amines, which are well known as modulators of nervous-system function and organismal behavior in animals, including humans. Alison Mercer, her colleagues from the University of Otago in New Zealand and I found changes in brain levels of two biogenic amines—dopamine and serotonin—during behavioral development. Jeffrey Harris and Joseph Woodring at Louisiana State University reported similar findings. Recently, graduate students Christine Wagener-Hulme and David Schulz, research technician Jack Kuehn and I showed that another biogenic amine, octopamine, appears to be most important in honey bee behavioral development. When a bee receives treatments of juvenile hormone, levels of octopamine increase, but dopamine and serotonin do not. Looking specifically at the antennal lobes, a brain region that receives sensory information from a bee's antennae, we found high levels of octopamine in the antennal lobes of foragers as compared with nurse bees, regardless of worker age. In contrast, levels of all three amines in the mushroom bodies are intimately associated with worker age, but not behavioral status.

These results suggest that octopamine might influence behavioral development by modulating a bee's sensitivity to the stimuli that elicit the performance of age-specific tasks. We presume that these stimuli are mostly chemical, because bees live in a dark hive and possess modest auditory acuity, at least relative to their renowned chemosensory prowess. That is why we are so encouraged to find behaviorally related changes specifically in the antennal lobes. The hypothesis that octopamine is playing a causal role in behavioral development is currently being tested by chronic administration of octopamine to the brain, followed by behavioral assays. Studies of biogenic amines might also provide some of the missing links between endocrine regulation and behavioral development in honey bees.

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