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An inhibitory sex pheromone tastes bitter for Drosophila males.

Lacaille F, Hiroi M, Twele R, Inoshita T, Umemoto D, Manière G, Marion-Poll F, Ozaki M, Francke W, Cobb M, Everaerts C, Tanimura T, Ferveur JF - PLoS ONE (2007)

Bottom Line: In Drosophila melanogaster, as in many insects, cuticular hydrocarbons are thought to be involved in sex recognition and in mating behavior, but there is no direct neuronal evidence of their pheromonal effect.Cross-adaptation between Z-7-tricosene and bitter stimuli further indicates that these two very different substances are processed by the same neural pathways.Furthermore, the two substances induced similar behavioral responses both in courtship and feeding tests.

View Article: PubMed Central - PubMed

Affiliation: Université de Bourgogne, CNRS-UMR5548, Dijon, France.

ABSTRACT
Sexual behavior requires animals to distinguish between the sexes and to respond appropriately to each of them. In Drosophila melanogaster, as in many insects, cuticular hydrocarbons are thought to be involved in sex recognition and in mating behavior, but there is no direct neuronal evidence of their pheromonal effect. Using behavioral and electrophysiological measures of responses to natural and synthetic compounds, we show that Z-7-tricosene, a Drosophila male cuticular hydrocarbon, acts as a sex pheromone and inhibits male-male courtship. These data provide the first direct demonstration that an insect cuticular hydrocarbon is detected as a sex pheromone. Intriguingly, we show that a particular type of gustatory neurons of the labial palps respond both to Z-7-tricosene and to bitter stimuli. Cross-adaptation between Z-7-tricosene and bitter stimuli further indicates that these two very different substances are processed by the same neural pathways. Furthermore, the two substances induced similar behavioral responses both in courtship and feeding tests. We conclude that the inhibitory pheromone tastes bitter to the fly.

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Caffeine and 7-T are detected by the same gustatory sensory neuron in i-type sensilla.(A) Above: 50 mM sucrose stimulated the L1 cell (on the left, spikes shown in gray = 0.2–0.3 mV). Below: in the same sensillum, caffeine excited the L2 cell, while 10−8M 7-T elicited a single class of spikes with an amplitude equivalent to those from the L2 cell (black spikes shown on the left = 0.1–0.2 mV). Bottom: a mixture of caffeine and 7-T (with similar concentrations as above) elicits high levels of activity in a single class of spikes. This indicates that 7-T activates the L2 cell but not the L1 cell. Recordings are shown for 4 sec and the stimulus application lasted for 2 sec. n = 10 (obtained with 5 male flies). (B) Caffeine and 7-T show cross-adaptation. Neuronal responses to caffeine were reduced following pre-stimulation with 7-T, supporting the hypothesis that 7-T and caffeine are detected by the same taste neuron. This effect was highly significant two minutes after pre-stimulation with 7-T (**: p = 0.0016; two tailed paired t-test). In contrast, the response to sucrose remained unaffected by pre-stimulation with 7-T. The response ratio was calculated from the number of spikes induced by a given substance, before and after prestimulation. The filled bar represents the response of the L2 cell to caffeine; the empty bar represents the response of the L1 cell to sucrose. The numbers represent the number of stimulated sensilla (each recording was made with a different fly).
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pone-0000661-g004: Caffeine and 7-T are detected by the same gustatory sensory neuron in i-type sensilla.(A) Above: 50 mM sucrose stimulated the L1 cell (on the left, spikes shown in gray = 0.2–0.3 mV). Below: in the same sensillum, caffeine excited the L2 cell, while 10−8M 7-T elicited a single class of spikes with an amplitude equivalent to those from the L2 cell (black spikes shown on the left = 0.1–0.2 mV). Bottom: a mixture of caffeine and 7-T (with similar concentrations as above) elicits high levels of activity in a single class of spikes. This indicates that 7-T activates the L2 cell but not the L1 cell. Recordings are shown for 4 sec and the stimulus application lasted for 2 sec. n = 10 (obtained with 5 male flies). (B) Caffeine and 7-T show cross-adaptation. Neuronal responses to caffeine were reduced following pre-stimulation with 7-T, supporting the hypothesis that 7-T and caffeine are detected by the same taste neuron. This effect was highly significant two minutes after pre-stimulation with 7-T (**: p = 0.0016; two tailed paired t-test). In contrast, the response to sucrose remained unaffected by pre-stimulation with 7-T. The response ratio was calculated from the number of spikes induced by a given substance, before and after prestimulation. The filled bar represents the response of the L2 cell to caffeine; the empty bar represents the response of the L1 cell to sucrose. The numbers represent the number of stimulated sensilla (each recording was made with a different fly).

Mentions: The L2 cell in i-type sensilla is known to respond to bitter molecules [22], [23]. To investigate whether the same neuron processes both 7-T and bitter substances, we carried out a series of experiments. When stimulated with a mixture of 7-T and caffeine, the L2 cell elicited an increased number of spikes with the same amplitude than when stimulated with either substance alone (Fig. 4A). 7-T and bitter substances also show cross-adaptation: pre-stimulation with 7-T significantly reduced the response of L2 cells to caffeine but not to sucrose (Fig. 4B). Taken together, these additive and cross-adaptative effects strongly indicate that 7-T and bitter stimuli are processed by the same taste neuron, the L2 cell, in the responsive i-type sensilla of the labial palps.


An inhibitory sex pheromone tastes bitter for Drosophila males.

Lacaille F, Hiroi M, Twele R, Inoshita T, Umemoto D, Manière G, Marion-Poll F, Ozaki M, Francke W, Cobb M, Everaerts C, Tanimura T, Ferveur JF - PLoS ONE (2007)

Caffeine and 7-T are detected by the same gustatory sensory neuron in i-type sensilla.(A) Above: 50 mM sucrose stimulated the L1 cell (on the left, spikes shown in gray = 0.2–0.3 mV). Below: in the same sensillum, caffeine excited the L2 cell, while 10−8M 7-T elicited a single class of spikes with an amplitude equivalent to those from the L2 cell (black spikes shown on the left = 0.1–0.2 mV). Bottom: a mixture of caffeine and 7-T (with similar concentrations as above) elicits high levels of activity in a single class of spikes. This indicates that 7-T activates the L2 cell but not the L1 cell. Recordings are shown for 4 sec and the stimulus application lasted for 2 sec. n = 10 (obtained with 5 male flies). (B) Caffeine and 7-T show cross-adaptation. Neuronal responses to caffeine were reduced following pre-stimulation with 7-T, supporting the hypothesis that 7-T and caffeine are detected by the same taste neuron. This effect was highly significant two minutes after pre-stimulation with 7-T (**: p = 0.0016; two tailed paired t-test). In contrast, the response to sucrose remained unaffected by pre-stimulation with 7-T. The response ratio was calculated from the number of spikes induced by a given substance, before and after prestimulation. The filled bar represents the response of the L2 cell to caffeine; the empty bar represents the response of the L1 cell to sucrose. The numbers represent the number of stimulated sensilla (each recording was made with a different fly).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1937024&req=5

pone-0000661-g004: Caffeine and 7-T are detected by the same gustatory sensory neuron in i-type sensilla.(A) Above: 50 mM sucrose stimulated the L1 cell (on the left, spikes shown in gray = 0.2–0.3 mV). Below: in the same sensillum, caffeine excited the L2 cell, while 10−8M 7-T elicited a single class of spikes with an amplitude equivalent to those from the L2 cell (black spikes shown on the left = 0.1–0.2 mV). Bottom: a mixture of caffeine and 7-T (with similar concentrations as above) elicits high levels of activity in a single class of spikes. This indicates that 7-T activates the L2 cell but not the L1 cell. Recordings are shown for 4 sec and the stimulus application lasted for 2 sec. n = 10 (obtained with 5 male flies). (B) Caffeine and 7-T show cross-adaptation. Neuronal responses to caffeine were reduced following pre-stimulation with 7-T, supporting the hypothesis that 7-T and caffeine are detected by the same taste neuron. This effect was highly significant two minutes after pre-stimulation with 7-T (**: p = 0.0016; two tailed paired t-test). In contrast, the response to sucrose remained unaffected by pre-stimulation with 7-T. The response ratio was calculated from the number of spikes induced by a given substance, before and after prestimulation. The filled bar represents the response of the L2 cell to caffeine; the empty bar represents the response of the L1 cell to sucrose. The numbers represent the number of stimulated sensilla (each recording was made with a different fly).
Mentions: The L2 cell in i-type sensilla is known to respond to bitter molecules [22], [23]. To investigate whether the same neuron processes both 7-T and bitter substances, we carried out a series of experiments. When stimulated with a mixture of 7-T and caffeine, the L2 cell elicited an increased number of spikes with the same amplitude than when stimulated with either substance alone (Fig. 4A). 7-T and bitter substances also show cross-adaptation: pre-stimulation with 7-T significantly reduced the response of L2 cells to caffeine but not to sucrose (Fig. 4B). Taken together, these additive and cross-adaptative effects strongly indicate that 7-T and bitter stimuli are processed by the same taste neuron, the L2 cell, in the responsive i-type sensilla of the labial palps.

Bottom Line: In Drosophila melanogaster, as in many insects, cuticular hydrocarbons are thought to be involved in sex recognition and in mating behavior, but there is no direct neuronal evidence of their pheromonal effect.Cross-adaptation between Z-7-tricosene and bitter stimuli further indicates that these two very different substances are processed by the same neural pathways.Furthermore, the two substances induced similar behavioral responses both in courtship and feeding tests.

View Article: PubMed Central - PubMed

Affiliation: Université de Bourgogne, CNRS-UMR5548, Dijon, France.

ABSTRACT
Sexual behavior requires animals to distinguish between the sexes and to respond appropriately to each of them. In Drosophila melanogaster, as in many insects, cuticular hydrocarbons are thought to be involved in sex recognition and in mating behavior, but there is no direct neuronal evidence of their pheromonal effect. Using behavioral and electrophysiological measures of responses to natural and synthetic compounds, we show that Z-7-tricosene, a Drosophila male cuticular hydrocarbon, acts as a sex pheromone and inhibits male-male courtship. These data provide the first direct demonstration that an insect cuticular hydrocarbon is detected as a sex pheromone. Intriguingly, we show that a particular type of gustatory neurons of the labial palps respond both to Z-7-tricosene and to bitter stimuli. Cross-adaptation between Z-7-tricosene and bitter stimuli further indicates that these two very different substances are processed by the same neural pathways. Furthermore, the two substances induced similar behavioral responses both in courtship and feeding tests. We conclude that the inhibitory pheromone tastes bitter to the fly.

Show MeSH
Related in: MedlinePlus