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
Source: PubMed

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.

Download full-text


Available from: Tetsuya Miyamoto, Mar 28, 2014
  • Source
    • "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]. "
    [Show abstract] [Hide abstract]
    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
  • Source
    • "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). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The response of individual animals to mating signals depends on the sexual identity of the individual and the genetics of the mating targets, which represent the mating social context (social environment). However, how social signals are sensed and integrated during mating decisions remains a mystery. One of the models for understanding mating behaviors in molecular and cellular terms is the male courtship ritual in the fruit fly (Drosophila melanogaster). We have recently shown that a subset of gustatory receptor neurons (GRNs) that are enriched in the male appendages and express the ion channel ppk23 play a major role in the initiation and maintenance of male courtship via the perception of cuticular contact pheromones, and are likely to represent the main chemosensory pathway that influences mating decisions by males. Here we show that genetic feminization of ppk23-expressing GRNs in male flies resulted in a significant increase in male-male sexual attraction without an apparent impact on sexual attraction to females. Furthermore, we show that this increase in male-male sexual attraction is sensory specific, which can be modulated by variable social contexts. Finally, we show that feminization of ppk23-expressing sensory neurons lead to major transcriptional shifts, which may explain the altered interpretation of the social environment by feminized males. Together, these data indicate that the sexual cellular identity of pheromone sensing GRNs plays a major role in how individual flies interpret their social environment in the context of mating decisions.
    Biology Open 01/2014; 3(2). DOI:10.1242/bio.20147369 · 2.42 Impact Factor
  • Source
    • "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). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Males of most species are more aggressive than females, but the neural mechanisms underlying this dimorphism are not clear. Here, we identify a neuron and a gene that control the higher level of aggression characteristic of Drosophila melanogaster males. Males, but not females, contain a small cluster of FruM(+) neurons that express the neuropeptide tachykinin (Tk). Activation and silencing of these neurons increased and decreased, respectively, intermale aggression without affecting male-female courtship behavior. Mutations in both Tk and a candidate receptor, Takr86C, suppressed the effect of neuronal activation, whereas overexpression of Tk potentiated it. Tk neuron activation overcame reduced aggressiveness caused by eliminating a variety of sensory or contextual cues, suggesting that it promotes aggressive arousal or motivation. Tachykinin/Substance P has been implicated in aggression in mammals, including humans. Thus, the higher aggressiveness of Drosophila males reflects the sexually dimorphic expression of a neuropeptide that controls agonistic behaviors across phylogeny.
    Cell 01/2014; 156(1-2):221-35. DOI:10.1016/j.cell.2013.11.045 · 33.12 Impact Factor
Show more