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.

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Available from: Tetsuya Miyamoto, Mar 28, 2014
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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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    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.
    01/2014; 3(2). DOI:10.1242/bio.20147369
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    • "Drosophila males have developed complementary olfactory strategies to find their mates, based on inhibiting and/or stimulating olfactory signals. Enhancing olfactory cues for male courtship appears to be highly context-dependant (Grosjean et al., 2011; Wang et al., 2011). It would be very useful to know more about the integration process happening within male brains to compare sensory stimuli of different nature (olfactory, gustatory, auditory, visual). "
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    ABSTRACT: Odors are key sensory signals for social communication and food search in animals including insects. Drosophila melanogaster, is a powerful neurogenetic model commonly used to reveal molecular and cellular mechanisms involved in odorant detection. Males use olfaction together with other sensory modalities to find their mates. Here, we review known olfactory signals, their related olfactory receptors, and the corresponding neuronal architecture impacting courtship. OR67d receptor detects 11-cis-Vaccenyl Acetate (cVA), a male specific pheromone transferred to the female during copulation. Transferred cVA is able to reduce female attractiveness for other males after mating, and is also suspected to decrease male-male courtship. cVA can also serve as an aggregation signal, maybe through another OR. OR47b was shown to be activated by fly odors, and to enhance courtship depending on taste pheromones. IR84a detects phenylacetic acid (PAA) and phenylacetaldehyde (PA). These two odors are not pheromones produced by flies, but are present in various fly food sources. PAA enhances male courtship, acting as a food aphrodisiac. Drosophila males have thus developed complementary olfactory strategies to help them to select their mates.
    Frontiers in Physiology 04/2013; 4:72. DOI:10.3389/fphys.2013.00072 · 3.50 Impact Factor
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    • "7T and cVA are inhibitory compounds on males and 7,11-HD, and 7,11-ND are excitatory compounds on females (Ferveur, 2005; Jallon, 1984). 7P is abundant on males, with more complex roles in courtship (Ferveur, 2005; Jallon, 1984; Wang et al., 2011). Δppk23, Δppk29 and control males were paired with oe-males painted with 7T, 7P or cVA. "
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    ABSTRACT: The elaborate courtship ritual of Drosophila males is dictated by neural circuitry established by the transcription factor Fruitless and triggered by sex-specific sensory cues. Deciphering the role of different stimuli in driving courtship behavior has been limited by the inability to selectively target appropriate sensory classes. Here, we identify two ion channel genes belonging to the degenerin/epithelial sodium channel/pickpocket (ppk) family, ppk23 and ppk29, which are expressed in fruitless-positive neurons on the legs and are essential for courtship. Gene loss-of-function, cell-inactivation, and cell-activation experiments demonstrate that these genes and neurons are necessary and sufficient to inhibit courtship toward males and promote courtship toward females. Moreover, these cells respond to cuticular hydrocarbons, with different cells selectively responding to male or female pheromones. These studies identify a large population of pheromone-sensing neurons and demonstrate the essential role of contact chemosensation in the early courtship steps of mate selection and courtship initiation.
    Cell 05/2012; 149(5):1140-51. DOI:10.1016/j.cell.2012.03.045 · 33.12 Impact Factor
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