Reproductive behavior in Drosophila has both stereotyped and plastic components that are driven by age- and sex-specific chemical cues. Males who unsuccessfully court virgin females subsequently avoid females that are of the same age as the trainer. In contrast, males trained with mature mated females associate volatile appetitive and aversive pheromonal cues and learn to suppress courtship of all females. Here we show that the volatile aversive pheromone that leads to generalized learning with mated females is (Z)-11-octadecenyl acetate (cis-vaccenyl acetate, cVA). cVA is a major component of the male cuticular hydrocarbon profile, but it is not found on virgin females. During copulation, cVA is transferred to the female in ejaculate along with sperm and peptides that decrease her sexual receptivity. When males sense cVA (either synthetic or from mated female or male extracts) in the context of female pheromone, they develop a generalized suppression of courtship. The effects of cVA on initial courtship of virgin females can be blocked by expression of tetanus toxin in Or65a, but not Or67d neurons, demonstrating that the aversive effects of this pheromone are mediated by a specific class of olfactory neuron. These findings suggest that transfer of cVA to females during mating may be part of the male's strategy to suppress reproduction by competing males.
These results demonstrate that social context exerts a regulatory influence on the expression of chemical signals, while modulating sexual behavior in the fruit fly.
A hallmark of behavior is that animals respond to environmental change by switching from one behavioral state to another. However, information on the molecular underpinnings of these behavioral shifts and how they are mediated by the environment is lacking. The ant Pheidole pallidula with its morphologically and behaviorally distinct major and minor workers is an ideal system to investigate behavioral shifts. The physically larger majors are predisposed to defend the ant nest, whereas the smaller minors are the foragers. Despite this predisposition, majors are able to shift to foraging according to the needs of the colony. We show that the ant foraging (ppfor) gene, which encodes a cGMP-dependent protein kinase (PKG), mediates this shift. Majors have higher brain PKG activities than minors, and the spatial distribution of the PPFOR protein differs in these workers. Specifically, majors express the PPFOR protein in 5 cells in the anterior face of the ant brain, whereas minors do not. Environmental manipulations show that PKG is lower in the presence of a foraging stimulus and higher when defense is required. Finally, pharmacological activation of PKG increases defense and reduces foraging behavior. Thus, PKG signaling plays a critical role in P. pallidula behavioral shifts.cGMP-dependent protein kinase ͉ defense ͉ foraging M ajor genes for normal individual differences in behavior are now familiar in a variety of species (1). However, an important feature of behavioral traits is that they are responsive to environmental change. Animals are able to switch from one behavioral state to another, yet little is known about the molecular basis of these behavioral shifts and how they are mediated by the environment. Eusocial insects are excellent models for studying these gene-environment interdependencies because their social organization relies on individuals who belong to behaviorally specialized castes. Wilson (2) showed that, despite this behavioral specialization, individuals of one caste can rapidly modify their behavior, depending on colony requirements; he called this the flexibility of behavioral castes. These quick changes in caste behavioral repertoires provide enough flexibility in colony response to maintain the colony when the environment goes through rapid changes. For example, ants whose role is to defend the nest are able to switch to foraging, depending on the needs of the colony. How might this switch from one behavioral state to another be accomplished?The ant Pheidole pallidula provides us with an excellent system to investigate the molecular underpinnings of flexibilities in behavioral predispositions. This species has 2 morphologically distinct worker castes, called majors and minors (3), that we will refer to here as subcastes. Both reach the same stage of maturity and work outside the nest. Majors have large heads and mandibles and specialize in colony defense; they guard the nest, patrol outside the nest entrance, and kill intruders. Minors are smaller and perform foraging behaviors, including ...
Suppression of memory by new learning demonstrates that the dynamics of memory consolidation are subject to plasticity in Drosophila. This type of metaplasticity is essential for navigation of experience-rich natural environments.
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