Activation of the T1 Neuronal Circuit is Necessary and Sufficient to Induce Sexually Dimorphic Mating Behavior in Drosophila melanogaster

Department of Pharmacology, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9111, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 02/2010; 30(7):2595-9. DOI: 10.1523/JNEUROSCI.4819-09.2010
Source: PubMed


The molecular and cellular events mediating complex behaviors in animals are largely unknown. Elucidating the circuits underlying behaviors in simple model systems may shed light on how these circuits function. In drosophila, courtship behavior provides a tractable model for studying the underlying basis of innate behavior. The male-specific pheromone 11-cis-vaccenyl acetate (cVA) modulates courtship behavior and is detected by T1 neurons, located on the antenna of male and female flies. The T1 neurons express the odorant receptor Or67d and are exquisitely tuned to cVA pheromone. However, cVA-induced changes in mating behavior have also been reported upon manipulation of olfactory neurons expressing odorant receptor Or65a. These findings raise the issue of whether multiple olfactory-driven circuits underlie cVA-induced behavioral responses and what role these circuits play in behavior. Here, we engineered flies in which the Or67d circuit is specifically activated in the absence of cVA to determine the role of this circuit in behavior. We created transgenic flies that express a dominant-active, pheromone-independent variant of the extracellular pheromone receptor, LUSH. We found that, similar to the behaviors elicited by cVA, engineered male flies have dramatically reduced courtship, whereas engineered females showed enhanced courtship. cVA exposure did not enhance the dominant LUSH-triggered effects on behavior in the engineered flies. Finally, we show the effects of both cVA and dominant LUSH on courtship are reversed by genetically removing Or67d. These findings demonstrate that the T1/Or67d circuit is necessary and sufficient to mediate sexually dimorphic courtship behaviors.

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    • "cVA is a semivolatile compound that is stored and synthesized in the ejaculatory bulb of males (Butterworth 1969; Mane et al. 1983; Guiraudie-Capraz et al. 2007), and transferred to females during copulation where it reduces their attractiveness to males (Butterworth 1969; Brieger and Butterworth 1970; Jallon 1984; Ejima et al. 2007). Recently, it has been shown to have effects on both sexual and aggressive behavior (Kurtovic et al. 2007; Datta et al. 2008; Wang and Anderson 2010; Ronderos and Smith 2010). Its effects are sexually dimorphic, since it acts as an antiaphrodisiac for males (Zawistowski and Richmond 1986), while it enhances sexual receptivity in females (Kurtovic et al. 2007). "
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    ABSTRACT: Upon encountering a conspecific in the wild, males have to rapidly detect, integrate and process the most relevant signals to evoke an appropriate behavioral response. Courtship and aggression are the most important social behaviors in nature for procreation and survival: for males, making the right choice between the two depends on the ability to identify the sex of the other individual. In flies as in most species, males court females and attack other males. Although many sensory modalities are involved in sex recognition, chemosensory communication mediated by specific molecules that serve as pheromones plays a key role in helping males distinguish between courtship and aggression targets. The chemosensory signals used by flies include volatile and non-volatile compounds, detected by the olfactory and gustatory systems. Recently, several putative olfactory and gustatory receptors have been identified that play key roles in sex recognition, allowing investigators to begin to map the neuronal circuits that convey this sensory information to higher processing centers in the brain. Here, we describe how Drosophila melanogaster males use taste and smell to make correct behavioral choices.
    Full-text · Article · Sep 2013 · Journal of Comparative Physiology
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    • "The combined effect of olfaction and taste perception of pheromones on Drosophila male sexual behavior may be mediated by several olfactory receptors (Or47b, Or65a, Or67d and Or88a) that respond to fly odors [45], as well as by gustatory receptors (GR32a, Gr33a and GR68a) that are potentially stimulated by CHs [69], [70], [71]. The combined olfactory and gustatory perception of cVA and 7-T (with Or67d- and Gr32a-expressing neurons) may explain their effect on the modulation of male courtship and aggressive behaviors [22], [23], [51], [70], [72], [73]. The gustatory perception of female and male CHs in Gr68a- and Gr32a-expressing neurons, respectively [69], [70], requires the Gr33a co-receptor [71], and may also require Or47b- and Or88a-expressing neurons, to regulate male courtship behavior [45]. "
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    ABSTRACT: Recognition of conspecifics and mates is based on a variety of sensory cues that are specific to the species, sex and social status of each individual. The courtship and mating activity of Drosophila melanogaster flies is thought to depend on the olfactory perception of a male-specific volatile pheromone, cis-vaccenyl acetate (cVA), and the gustatory perception of cuticular hydrocarbons (CHs), some of which are sexually dimorphic. Using two complementary sampling methods (headspace Solid Phase Micro-Extraction [SPME] and solvent extraction) coupled with GC-MS analysis, we measured the dispersion of pheromonal CHs in the air and on the substrate around the fly. We also followed the variations in CHs that were induced by social and sexual interactions. We found that all CHs present on the fly body were deposited as a thin layer on the substrate, whereas only a few of these molecules were also detected in the air. Moreover, social experience during early adult development and in mature flies strongly affected male volatile CHs but not cVA, whereas sexual interaction only had a moderate influence on dispersed CHs. Our study suggests that, in addition to their role as contact cues, CHs can influence fly behavior at a distance and that volatile, deposited and body pheromonal CHs participate in a three-step recognition of the chemical identity and social status of insects.
    Full-text · Article · Jul 2012 · PLoS ONE
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    • "cVA also suppresses courtship towards recently-mated females, as cVA is transferred to the female with the seminal fluid [17]. Or67d, an Or mediating the sensory and behavioral responses to the cVA [15,16,18,19] is expressed in T1 trichoid sensilla [18]. LUSH, an odorant-binding protein (OBP), and SNMP1, a putative membrane bound coreceptor, are also required for cVA sensitivity [15,18,20-22]. "
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    ABSTRACT: Insects respond to the spatial and temporal dynamics of a pheromone plume, which implies not only a strong response to 'odor on', but also to 'odor off'. This requires mechanisms geared toward a fast signal termination. Several mechanisms may contribute to signal termination, among which odorant-degrading enzymes. These enzymes putatively play a role in signal dynamics by a rapid inactivation of odorants in the vicinity of the sensory receptors, although direct in vivo experimental evidences are lacking. Here we verified the role of an extracellular carboxylesterase, esterase-6 (Est-6), in the sensory physiological and behavioral dynamics of Drosophila melanogaster response to its pheromone, cis-vaccenyl acetate (cVA). Est-6 was previously linked to post-mating effects in the reproductive system of females. As Est-6 is also known to hydrolyze cVA in vitro and is expressed in the main olfactory organ, the antenna, we tested here its role in olfaction as a putative odorant-degrading enzyme. We first confirm that Est-6 is highly expressed in olfactory sensilla, including cVA-sensitive sensilla, and we show that expression is likely associated with non-neuronal cells. Our electrophysiological approaches show that the dynamics of olfactory receptor neuron (ORN) responses is strongly influenced by Est-6, as in Est-6° null mutants (lacking the Est-6 gene) cVA-sensitive ORN showed increased firing rate and prolonged activity in response to cVA. Est-6° mutant males had a lower threshold of behavioral response to cVA, as revealed by the analysis of two cVA-induced behaviors. In particular, mutant males exhibited a strong decrease of male-male courtship, in association with a delay in courtship initiation. Our study presents evidence that Est-6 plays a role in the physiological and behavioral dynamics of sex pheromone response in Drosophila males and supports a role of Est-6 as an odorant-degrading enzyme (ODE) in male antennae. Our results also expand the role of Est-6 in Drosophila biology, from reproduction to olfaction, and highlight the role of ODEs in insect olfaction.
    Full-text · Article · Jun 2012 · BMC Biology
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