Gene plays key evolutionary role in food-gathering behaviors

April 25, 2002

CHAMPAIGN, Ill. -- A new discovery in the brain of honeybees has researchers at three institutions suggesting that the gene they studied has played a key evolutionary role in the changes of food-gathering behaviors in many creatures.

When honeybees (Apis mellifera) grow up and leave the hive to begin foraging, their transition is helped along by an increase in the activity of the foraging gene (for). It stimulates an activity-boosting enzyme in some of the brain's visual processing centers, the researchers report in the April 26 issue of Science. Precocious foragers - bees stimulated to forage early - also have significantly higher brain levels of the gene's messenger RNA and four-fold higher levels of the enzyme, a cyclic GMP-dependent protein kinase called PKG.

Two forms of for previously had been found to influence naturally occurring variation in foraging behavior in Drosophila. "Rover" flies that cover large areas have high levels of PKG, while "sitter" flies that gather food nearby have low levels. PKG also has been linked to feeding arousal in some other invertebrates and vertebrates.

Honeybees live in a social world known for its distinct age-related division of labor. They begin their adult life working inside the hive as sanitation workers and nursemaids, among other roles. Foraging begins at two to three weeks of age, or whenever the needs of a colony require it. Nurse bees "loosely resemble sitter flies because they obtain food only in the more restricted confines of the beehive, while forager bees display rover-like behavior by ranging widely throughout the environment," the researchers wrote.

"The fact that at the molecular level there is a loose analogy between sitter flies and nurse bees on one hand and rover flies and foragers on the other hand is interesting for two reasons," said Gene Robinson, a professor of entomology and neuroscience at the University of Illinois.

First, it supports the idea that for may have had an evolutionary role in the changes of food-gathering behaviors in many creatures. Second, it demonstrates how the same gene in different species can be responsive to change over vastly different time scales - an evolutionary time scale in flies and a maturational or developmental one in bees," he said.

Before becoming foragers, honeybees make the transition from their role as nurses by going through a series of gradually widening orientation flights. During this time there are changes in brain chemistry and structure, endocrine activity and gene expression. Robinson and colleagues theorized that increased gene activity was necessary to drive behavioral change. Other genes had been implicated, but for is the first one shown to actually affect division of labor in honeybee colonies.

The researchers measured levels of the gene and its enzyme activity in precocious foragers to assure that the brain changes were not simply a natural result of age. Higher levels of gene expression and enzyme activity occurred in both in foragers making the transition in typical fashion (two to three weeks) and in those manipulated to forage at seven to nine days.

Additionally, the researchers used a pharmacological approach, feeding an experimental group of young bees with an analog that stimulated PKG activity. The treated bees started to forage precociously, while untreated bees did not.

The researchers believe that for and other genes that affect similar behaviors in different species might represent a class of genes that are particularly important to understanding the ways that genes influence behavior.
The authors of the paper are Robinson, Yehuda Ben-Shahar, a doctoral student in the UI entomology department; M.B. Sokolowski of the zoology department at the University of Toronto's Mississauga campus; and A. Robichon of the National Center for Scientific Research at the University of Bourgogne in France. The National Institutes of Health, Burroughs-Wellcome Trust and Canada Research Chair Program funded the research.

University of Illinois at Urbana-Champaign

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