Hierarchical chemosensory regulation of male-male social interactions in Drosophila

Division of Biology, California Institute of Technology, Pasadena, California, USA.
Nature Neuroscience (Impact Factor: 16.1). 06/2011; 14(6):757-62. DOI: 10.1038/nn.2800
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Pheromones regulate male social behaviors in Drosophila, but the identities and behavioral role(s) of these chemosensory signals, and how they interact, are incompletely understood. We found that (z)-7-tricosene, a male-enriched cuticular hydrocarbon that was previously shown to inhibit male-male courtship, was essential for normal levels of aggression. The mechanisms by which (z)-7-tricosene induced aggression and suppressed courtship were independent, but both required the gustatory receptor Gr32a. Sensitivity to (z)-7-tricosene was required for the aggression-promoting effect of 11-cis-vaccenyl acetate (cVA), an olfactory pheromone, but (z)-7-tricosene sensitivity was independent of cVA. (z)-7-tricosene and cVA therefore regulate aggression in a hierarchical manner. Furthermore, the increased courtship caused by depletion of male cuticular hydrocarbons was suppressed by a mutation in the olfactory receptor Or47b. Thus, male social behaviors are controlled by gustatory pheromones that promote aggression and suppress courtship, and whose influences are dominant to olfactory pheromones that enhance these behaviors.

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Available from: Tetsuya Miyamoto, Mar 28, 2014
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    • "D. melanogaster males lacking the gene encoding the Gr32a receptor court females from other species (Fan et al., 2013), court males from their own species (Miyamoto and Amrein, 2008) and have reduced aggression toward conspecific males (Wang et al., 2011; Andrews et al., 2014). Gr32a − mutant males are insensitive to 7-T indicating that Gr32a is a receptor for that pheromone (Wang et al., 2011). Although it probably has a mechanosensory component, one function of tapping during courtship appears to be connected to the chemosensory sensing of CH of conspecific and is in part connected to sex and species recognition (Kohatsu et al., 2011; Fan et al., 2013). "
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    ABSTRACT: Social living is beneficial because it allows conspecifics to interact in ways that increase their chances of survival and reproduction. A key mechanism underlying these benefits is the ability to recognize conspecifics; thus, allowing the production of coordinated social interactions. Identification of such individuals is often through chemical communication: the individuals' pheromonal profile indicates their sex, species, and even past experiences. However, we know little about how the chemosensory system of conspecifics detects and how the nervous system processes this information. One of the best documented pheromonal detection mechanisms is that of cis-Vaccenyl Acetate (cVA) made by male Drosophila melanogaster and transferred to females during mating. Sensing of cVA by males inhibits courtship behavior toward already mated females. Sensing of cVA on other males also inhibits courtship and increases aggression. In this hybrid review/research article, we discuss the pheromonal system of Drosophila putting an emphasis on the molecular and cellular mechanisms involved in cVA sensing by the olfactory system, perception by the nervous system and ultimately the regulation of social interactions. The behavioral effect of cVA is context- as well as experience-dependent leading us to conclude that cVA plays a modulatory role in regulating social interactions rather than being a recognition pheromone. We also provide new behavioral data on the function of the Odorant Binding Protein Lush, which binds cVA in olfactory sensilla and help sensing this chemical. Our data indicate that lush may be involved in the sensing of additional pheromones to cVA and suggest the existence of a lush-independent cVA detection system. Interpretation of our data in the light of our current knowledge about pheromonal recognition in Drosophila indicates that this system is incompletely understood.
    07/2015; 3. DOI:10.3389/fevo.2015.00075
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    • "As is mentioned briefly above, the power of cVA on its behavioral control differs depending on its olfactory context . For example, in addition to cVA, the presence of 7-tricosene, a cuticular component enriched in males, is essential to promote the full level of male–male aggression (Wang et al. 2011). Independently, Grillet et al. (2006) proposed the involvement of 7-tricosene in female mate choice. "
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    ABSTRACT: The male-specific lipid, cis-vaccenyl acetate (cVA) has multiple functions in intra-species communication in Drosophila melanogaster. The presence of cVA in a male suppresses courtship motivation of other males and averts male-male courtship. Meanwhile, aggression behaviors between males are promoted by a high amount of cVA caused by increased densities of male flies. cVA also works as a modifier of courtship memory, which is suppressed courtship motivation driven by previous unsuccessful courtship experience. Conversely, cVA in the courting male stimulates female reproductive motivation and increases the probability of copulation success. It also works as an aggregation pheromone, attracting both males and females at the gathering spot. Thus, cVA is a unique example of a single molecule leading to different behaviors in response to the social context. However, despite recent advances in understanding the molecular and neural machinery for cVA sensing, it is still largely unknown how cVA triggers a specific behavior as the situation demands. In this review article, I discuss two potential machineries that might determine cVA actions for behavior selection at the sensory level.
    Journal of Comparative Physiology 06/2015; 201(9). DOI:10.1007/s00359-015-1020-9 · 2.04 Impact Factor
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    • "We transferred CHCs from the white females to the oe− females by subjecting them to three medium vortex pulses lasting 20 seconds, with a 20 second break between pulses (method adapted from [33]). CHC transfer between individuals by physical contact or “rubbing” has been widely used to study CHC preferences in Drosophila [5], [8], [13], [33], [34], and a nearly identical version of this perfuming protocol has been used previously to successfully transfer CHCs to oe− females [35]. "
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    ABSTRACT: Many animal species communicate using chemical signals. In Drosophila, cuticular hydrocarbons (CHCs) are involved in species and sexual identification, and have long been thought to act as stimulatory pheromones as well. However, a previous study reported that D. melanogaster males were more attracted to females that were lacking CHCs. This surprising result is consistent with several evolutionary hypotheses but is at odds with other work demonstrating that female CHCs are attractive to males. Here, we investigated natural variation in male preferences for female pheromones using transgenic flies that cannot produce CHCs. By perfuming females with CHCs and performing mate choice tests, we found that some male genotypes prefer females with pheromones, some have no apparent preference, and at least one male genotype prefers females without pheromones. This variation provides an excellent opportunity to further investigate the mechanistic causes and evolutionary implications of divergent pheromone preferences in D. melanogaster males.
    PLoS ONE 01/2014; 9(1):e87509. DOI:10.1371/journal.pone.0087509 · 3.23 Impact Factor
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