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
Source: PubMed


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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    • " as CheB proteins ( Xu et al . , 2002 ; Park et al . , 2006 ) , ppk23 , ppk25 and ppk29 DEG / Na channels ( Lu et al . , 2012 ; Pikielny , 2012 ; Thistle et al . , 2012 ; Toda et al . , 2012 ; Vijayan et al . , 2014 ) , gustatory receptors like Gr39a , Gr32a and Gr68a ( Miyamoto and Amrein , 2008 ; Moon et al . , 2009 ; Koganezawa et al . , 2010 ; Wang et al . , 2011 ; Watanabe et al . , 2011 ) , and ionotropic receptors ( Koh et al . , 2014 ) . However , very few studies have considered the wiring of these pheromone - sensitive cells , even though male - to - male detection is affected when ' ' bitter ' ' gustatory receptors such as Gr32a and Gr38a are inactivated ( Miyamoto and Amrein , 2008 ; Moo"
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    ABSTRACT: Most animals possess taste receptors neurons detecting potentially noxious compounds. In humans, the ligands which activate these neurons define a sensory space called “bitter”. By extension, this term has been used in animals and insects to define molecules which induce aversive responses. In this review, based on our observations carried out in Drosophila, we examine how bitter compounds are detected and if bitter-sensitive neurons respond only to molecules bitter to humans. Like most animals, flies detect bitter chemicals through a specific population of taste neurons, distinct from those responding to sugars or to other modalities. Activating bitter-sensitive taste neurons induces aversive reactions and inhibits feeding. Bitter molecules also contribute to the suppression of sugar-neuron responses and can lead to a complete inhibition of the responses to sugar at the periphery. Since some bitter molecules activate bitter-sensitive neurons and some inhibit sugar detection, bitter molecules are represented by two sensory spaces which are only partially congruent. In addition to molecules which impact feeding, we recently discovered that the activation of bitter-sensitive neurons also induces grooming. Bitter-sensitive neurons of the wings and of the legs can sense chemicals from the gram negative bacteria, Escherichia coli, thus adding another biological function to these receptors. Bitter-sensitive neurons of the proboscis also respond to the inhibitory pheromone, 7-tricosene. Activating these neurons by bitter molecules in the context of sexual encounter inhibits courting and sexual reproduction, while activating these neurons with 7-tricosene in a feeding context will inhibit feeding. The picture that emerges from these observations is that the taste system is composed of detectors which monitor different “categories” of ligands, which facilitate or inhibit behaviors depending on the context (feeding, sexual reproduction, hygienic behavior), thus considerably extending the initial definition of “bitter” tasting.
    Full-text · Article · Nov 2015 · Frontiers in Integrative Neuroscience
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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.
    Full-text · Article · Jul 2015
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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.
    Full-text · Article · Jun 2015 · Journal of Comparative Physiology
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