Article

Hierarchical chemosensory regulation of male-male social interactions in Drosophila

Division of Biology, California Institute of Technology, Pasadena, California, USA.
Nature Neuroscience (Impact Factor: 14.98). 06/2011; 14(6):757-62. DOI: 10.1038/nn.2800
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ABSTRACT 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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    • "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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    • "These data suggest that feminization of pheromone-sensing neurons can affect other classes of gustatory receptor neurons, possibly via indirect mechanisms. These data also further support the possible sensory crosstalk between canonical taste sensory pathways and the pheromonal input pathways as has been shown for the bitter receptors Gr66a, Gr33a, and Gr32a (Koganezawa et al., 2010; Lacaille et al., 2009; Miyamoto and Amrein, 2008; Moon et al., 2009; Wang et al., 2011). Previously, we have shown that sexually-dimorphic ppk23- expressing neurons represent the primary fru-expressing GRNs in the male appendages (Lu et al., 2012). "
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    Biology Open 01/2014; 3(2). DOI:10.1242/bio.20147369 · 2.42 Impact Factor
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    • "To test whether activation of Tk-GAL4 1 neurons could compensate for the absence of these cues, we paired thermogenetically activated tester flies with target ''oeÀ flies,'' which are depleted of most CHs via genetic ablation of oenocytes (Billeter et al., 2009). The oeÀ target flies evoked significantly less aggression from +; UAS-dTRPA1 flies than did control oe+ flies (Figure 7C, gray boxes; Ferná ndez et al., 2010; Wang et al., 2011). Remarkably , thermogenetic activation of Tk-GAL4 1 neurons in tester flies restored aggression toward oeÀ target flies to a level indistinguishable from that exhibited toward oe+ targets (Figure 7C, magenta boxes). "
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