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DURHAM, N.C. -- For the first time in any animal, Duke
University Medical Center researchers have linked a single
pheromone receptor in the fruit fly to a specific sexual
behavior.

Pheromones are chemical signals exuded by many animals --
including humans -- that serve as stimuli to evoke behavioral
responses in other individuals of the same species. Pheromones
often attract members of the opposite sex and provide important
cues during courtship and mating.

Yet little is known about pheromone receptors, which are the
protein switches nestled in cell membranes that trigger
responses to pheromones, said Duke Medical Center geneticist
Hubert Amrein, Ph.D., senior author of the study.

Now, he and co-author Steven Bray, also of Duke, report that
male Drosophila fruit flies lacking one type of taste receptor
have difficulty recognizing females. Although the males
initiate the courtship ritual, the flies' mating dance stalls
when they apparently fail to detect the proper chemical cue
from females. The sexually aberrant flies otherwise behaved
normally, the researchers report in the Sept. 11, 2003, issue
of Neuron.

"Scientists have been chasing pheromone receptors in animals
for a long time with little success," Amrein said, noting that
although putative receptors have been found, tying those to
specific behaviors had remained a major challenge. "Now, we
have identified a receptor and a very specific aspect of
courtship for which it is required."

The work was funded by a grant from the National Institutes
of Health.

Like mammals, insects display complex mating behaviors, many
of which are triggered automatically in response to pheromones
or other stimuli, Amrein said. Although the same principles
likely underlie the behavior in all animals, he added, flies'
simpler nervous system makes them an ideal model for study.

Courtship in Drosophila includes a regular sequence of
behaviors, which are critical for mating, Amrein explained.
First, a male identifies a female visually. The male then
approaches the female and touches her with his forelegs --
which contain one of the flies' taste organs -- in a behavior
known as tapping. After detecting pheromones from the female,
the male produces a courtship song through rapid wing
vibrations. The receptive female slows, allowing the male to
investigate further with his labellum, the fly equivalent of a
tongue. Finally, the male fly begins bending its abdomen as
required for copulation, and the two mate.

In their search for pheromone receptor genes, the
researchers explored the location of some 25 of 70 known taste
receptors on the fly's body. They found that one such candidate
pheromone receptor, encoded by a gene called Gr68a, showed up
only on the forelegs that males use in the tapping stage of
courtship. Also, found the researchers, the activity of the
Gr68a gene was governed by a gene that controls many aspects of
sexual differentiation in flies.

The researchers found that male flies lacking the neurons
that express the Gr68a receptor spent less time courting
females and, as a result, mated significantly less often than
normal flies did. Those deficient flies that did mate
successfully took twice as long to do so in comparison to
intact males.

Also, found the researchers, males lacking the
Gr68a-expressing neurons initiated courtship more often than
normal but the ritual stalled after the tapping stage, when
males apparently failed to receive the pheromone cue from
females. Flies lacking only Gr68a showed the same dysfunction
as those lacking the neurons completely, a result which links
the behavior directly to the taste receptor, Amrein said.

"It's quite remarkable that a single gene receptor,
expressed in just a few cells of the entire male fly, plays
such a crucial role in the courtship process," Amrein said.
"When you knock out the function of the gene, the flies show a
serious mating deficit."

Although an earlier study found that mice lacking 16 genes
thought to include pheromone receptors exhibited abnormal
sexual and aggressive behavior, this is the first study to
clearly link a single pheromone receptor to a specific mating
behavior, Amrein said.

Besides chemical sensing, courtship in flies involves visual
and auditory cues. Therefore, Amrein said, the finding in fruit
flies is a step toward understanding how the brain integrates
different kinds of sensory input and translates those signals
into complex behaviors critical to reproduction and
survival.