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Saturday, October 11, 2003

Honeybees: What Governs Here?

I was trying hard not to blog today, but this one is irresistable - the life and times of the honeybee (apis mellifera). Apparently the honeybee turns on and off 40 percent of her genes as she matures from "nurse" to forager in her short, busy life. Now some new research from a team lead by University of Illinois professor Gene Robinson suggests that studying how the factors governing this on-off process (or expression) work is telling us that genes and behavior are more closely related than we often believe, and more specifically that nature and nurture are not counterposed, but closely entwined. According to Robinson "about 40 percent of the genes change as the bee grows up and changes from taking care of baby bees in the hive to graduating and becoming a forager.......These changes are so consistent from individual to individual that a computer program can look at the expression profiles and characterize the individual as a nurse bee or a forager."

Robinson and his team created their own gene chip for the study - a plate on which chemicals react with active genetic products, glowing luminescently when exposed to certain lights, and they were able to track the development of 60 different bees as some genes switched off and others switched on. Honeybees live in colonies dominated by females, and males are used only for mating with the queen. The bees mature into new roles over a period of two to three weeks. Nurse bees care for the young for their first two to three weeks of life, then shift to foraging for nectar and pollen. But if the colony is short of foragers, for example, some of the nurse bees will mature more quickly. All of this happens fast. A honeybee typically lives just six weeks. "They pretty much fly themselves to death."

Robinson is quoted as saying that it is hard to know how much of this information translates to humans, who of course mature more slowly and in more complex ways than bees. But on the genetic level, we humans apparently have plenty in common with bees. In fact many of the genes looked at by Robinson's team have counterparts in humans and other animals. One example given is the MAP kinase gene, which is involved in learning and memory. In bees, this gene becomes more active as they become foragers. Obviously we should be careful in drawing too many conclusions, but the evident association between expression and behaviour is fascinating.

A honeybee's genes can tell you its job. Bees tending the nest have a different set of active genes in their brains to their nestmates out gathering food, researchers have found. There are many biological steps between DNA and deeds, says Gene Robinson of the University of Illinois in Urbana-Champaign. To find the two so closely linked is a surprise. "The genome is more heavily involved in orchestrating behaviour than one might have thought," he says. Bees could help us map similar links in humans. "We share many components in our nervous systems with the honeybee," says bee researcher Greg Hunt of Purdue University in West Lafayette, Indiana. In fruitflies, equivalents to the honeybee job genes are involved in learning, through their control of cell communication.

Robinson's team built a computer chip bearing DNA sequences representing about 5,500 honeybee genes - about half of the bee genome. Genes that are active in a tissue sample stick to their equivalent on the chip, creating a glowing spot. The busier the gene, the brighter the spot. About 40% of genes change their activity between nursemaids and foragers, the researchers found. This pattern is consistent enough to match bees to jobs on genes alone. The team tested samples from the brains of 60 insects from three hives. Such large-scale patterns are the best guide to the complex chemistry behind animal actions, reasons entomologist Robert Page of the University of California, Davis. "We're not going to find a gene for this and a gene for that," he says.

Young worker bees spend their first weeks helping out around the hive. They then swap to foraging in the outside world for the final month of their lives. So ageing influences bee employment. But the switch is not fixed - it can be accelerated, retarded or reversed. For example, old workers prevent an excess of foragers by releasing pheromones that slow younger bees' switching. Working out how honeybees mature might help us understand similar developments in other animals, Robinson points out. Young mammals, from example, switch from play to fighting, or mate-seeking. The honeybee genome, which should be completely sequenced in the next few months, will accelerate the understanding of behaviour and genetics tremendously, says Hunt. The experiments should be repeated with a spread of genetically different bees, to show which genes are most strongly linked to behaviour, he adds.
Source: Nature

Some of the really interesting conclusions of this study are perhaps drawn out in this piece from Science Daily:

Genes and behavior go together in honey bees so strongly that an individual bee's occupation can be predicted by knowing a profile of its gene expression in the brain, say researchers at the University of Illinois at Urbana-Champaign.

This strong relationship surfaced in a complex molecular study of 6,878 different genes replicated with 72 cDNA microarrays that captured the essence of brain gene activity within the natural world of the honey bee (Apis mellifera). Even though most of the differences in gene expression were small, the changes were observable in 40 percent of the genes studied, the scientists report in the Oct. 10 issue of the journal Science.

"We have discovered a clear molecular signature in the bee brain that is robustly associated with behavior," said principal researcher Gene E. Robinson, a professor of entomology and director of the Neuroscience Program at Illinois. "This provides a striking picture of the genome as a dynamic entity, more actively involved in modulating behavior in the adult brain than we previously thought."

Microarrays let researchers get a broad view of gene activity by generating simultaneous measurements of messenger RNA, which reflect levels of protein activity. The mRNA binds to specific sites on the array, allowing for the measurement of expression from thousands of genes.

Robinson, who also holds the G. William Arends Professorship in Integrative Biology at Illinois, and colleagues generated mRNA profiles from 60 different bees who were working either as nurses (taking care of the brood within the hive) or foragers (gathering food outside). A computer program was able to use the profiles to determine correctly, for 57 of 60 the bees, which individual belonged to what group.

Behavioral differences between nurses and foragers are part of an age-related, socially regulated division of bee labor. Nurses perform care-giving duties for their first two to three weeks of life, then shift to foraging for nectar and pollen. As the behavioral transition occurs the bees experience changes in brain structure, brain chemistry, and, as this new study shows, many changes in gene expression.

Robinson, whose research is part of a federally funded project to sequence the honey bee genome, has long been interested in the mechanisms involved in honey bee division of labor as a model to understand the relationships between genes, brain and behavior.

After an initial analysis showed differences between nurses and foragers, the researchers faced the problem of relating these differences to either age or behavior, because foragers are both behaviorally different and older than nurses. So Robinson and colleagues created colonies consisting entirely of same-aged bees. In the absence of older bees, some individuals in a hive will begin foraging up to two weeks earlier than usual while others will grow up normally and act as nurses, making for age-matched young nurses and foragers. Age-matched old foragers and old nurses also were obtained from these colonies.

A dominant pattern of gene expression emerged, and it "was clearly associated with behavior," the researchers wrote. Since precocious foraging is a response to the shortage of foragers, this finding indicates that the genome is responding dynamically to changes in the bee's social environment, Robinson said.

The study was unique, he said, because it focused on individual profiles. Previous studies of gene expression and behavior in mice and flies, for instance, have focused on group tendencies, looking at pools of individuals.
Source: Science Daily

And here is an introductory summary from Gene Robinson's Home Page :

"What is it that governs here, that issues orders, foresees the future...?" - Maeterlinck, 1927

Division of labor is fundamental to the organization of insect societies, and is thought to be one of the principal factors in their ecological success. Division of labor in insect colonies is characterized by two features: different activities are performed simultaneously, by groups of specialized individuals, which is assumed more efficient than if tasks are performed sequentially, by unspecialized individuals.

A key feature of the division of labor in insect colonies is its plasticity. Colonies respond to changing internal and external conditions by adjusting the ratios of individual workers engaged in the various tasks. This is accomplished in large part via the behavioral flexibility of the individual workers themselves. Worker behavioral flexibility contributes to the reproductive success of a colony by enabling it to continue to grow, develop, and ultimately produce a new generation of reproductive males and females during changing colony conditions.

Sensitivity to change within a structured labor system is important to social organization, but only now is beginning to be understood. The regulation of division of labor relates to one of the central problems in insect sociobiology, colony behavioral integration. Some of the most remarkable traits of social insects, such as their elaborate nests, potent defense strategies, sophisticated techniques of foraging, and intricate but flexible systems of division of labor involve the collective endeavors of perhaps thousands, or even hundreds of thousands, of workers. But it is unlikely that each individual can monitor the state of its whole colony and then perform the tasks that are needed most. In addition, it long has been recognized that highly eusocial insect societies function without a key form of control that exists in human societies. Although workers may play special roles in organizing specific tasks, there is no evidence for the occurrence of colony "leaders", i.e., individuals that perceive all or most of the colony's requirements and direct the activities of other colony members from one task to another. The challenge is to understand the mechanisms of integration that enable workers to respond to fragmentary information with actions that are appropriate to the state of the whole colony.

In most species of highly eusocial insects studied to date, there is age-related division of labor. Adult workers exhibit age polyethism, a form of behavioral development in which they perform different tasks at different ages. Young bees labor in the nest, while older individuals forage outside. During each stage of behavioral development a bee performs more-or-less the same kinds of jobs for a sustained period of time.

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