Ascending SAG Neurons Control Sexual Receptivity of Drosophila Females

Feng, Kai; Palfreyman, Mark T.; Häsemeyer, Martin; Talsma, Aaron D; Dickson, Barry J.

doi:10.1016/j.neuron.2014.05.017

Cited by 155 publications

(240 citation statements)

References 57 publications

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“…Other recent studies have also examined the abdominal ganglion neurons necessary for female reproductive behavior in Drosophila (18,19,(33)(34)(35). One question is whether the neurons we report here are the same or different from those previously reported.…”

Section: Resultssupporting

confidence: 41%

“…One question is whether the neurons we report here are the same or different from those previously reported. Gou et al (33) focused on ascending neurons from the reproductive tract, and both Feng et al (34) and Bussell et al (35) reported stimulation of neurons favoring receptivity. In contrast, we observed that stimulation of R17H01-GAL4 neurons inhibits receptivity, suggesting the neurons examined here differ from the ones reported above.…”

Section: Resultsmentioning

confidence: 99%

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Sex-specific regulation of Lgr3 in Drosophila neurons

Meissner

Luo

Dias

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The development of sexually dimorphic morphology and the potential for sexually dimorphic behavior in Drosophila are regulated by the Fruitless (Fru) and Doublesex (Dsx) transcription factors. Several direct targets of Dsx have been identified, but direct Fru targets have not been definitively identified. We show that Drosophila leucine-rich repeat G protein-coupled receptor 3 (Lgr3) is regulated by Fru and Dsx in separate populations of neurons. Lgr3 is a member of the relaxin-receptor family and a receptor for Dilp8, necessary for control of organ growth. Lgr3 expression in the anterior central brain of males is inhibited by the B isoform of Fru, whose DNA binding domain interacts with a short region of an Lgr3 intron. Fru A and C isoform mutants had no observed effect on Lgr3 expression. The female form of Dsx (Dsx F ) separately up-and down-regulates Lgr3 expression in distinct neurons in the abdominal ganglion through female-and male-specific Lgr3 enhancers. Excitation of neural activity in the Dsx F -up-regulated abdominal ganglion neurons inhibits female receptivity, indicating the importance of these neurons for sexual behavior. Coordinated regulation of Lgr3 by Fru and Dsx marks a point of convergence of the two branches of the sex-determination hierarchy.M ost animal species are comprised of female and male individuals, in which sex differences in form and behavior are specified by their genetic makeup. The developmental processes by which genes build sex-specific differences into the nervous system, and hence encode the potential for sex-specific behavior, have long been of interest (1).In Drosophila melanogaster the assessment of the number of X chromosomes leads to sex-differential splicing of transcripts from genes making up the sex-determination hierarchy, in particular the terminal genes of that hierarchy, fruitless (fru) and doublesex [dsx (2), reviewed in ref. 3]. fru and dsx encode sexspecific Zn-finger transcription factors that alter, either directly or indirectly, the expression of downstream genes to produce the sexually dimorphic elements of flies. The male-specific forms of Fru (Fru M ) act in a subset of the neurons within the male's nervous system to establish the potential for social interactions such as courtship behavior and aggression (reviewed in ref.3). In contrast, Dsx acts in subsets of both neural and nonneural tissues of males and females to regulate behavioral and nonbehavioral aspects of sexual development (reviewed in ref.3).Although the mechanisms regulating the production of the sexspecific isoforms of the Fru and Dsx proteins are well-established (4), how these proteins in turn function is only beginning to be elucidated. Several direct Dsx targets and a well-conserved 13-bp Dsx binding site have been identified (5-13). Many Dsx target genes encode well-known transcription factors and cell-cell signaling molecules that function sex-nonspecifically in most tissues in which they are expressed. However, in other tissues, Dsx directs the sexspecific expression of these gene...

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Section: Resultssupporting

confidence: 41%

Section: Resultsmentioning

confidence: 99%

Sex-specific regulation of Lgr3 in Drosophila neurons

Meissner

Luo

Dias

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…For example, virgins are receptive to male courtship and lay very few eggs, whereas mated females are unreceptive to courtship, lay eggs frequently, and preferentially consume proteins over sugars (Carvalho et al, 2006; Kubli, 2003; Ribeiro and Dickson, 2010). Much progress has been made in recent years in elucidating the molecular and circuit basis by which the experience of mating modifies physiologies and behaviors of female flies (Bussell et al; Feng et al, 2014; Häsemeyer et al, 2009; Rezával et al, 2012; Yang et al, 2009; Zhou et al, 2014). In contrast, whether and how egg-laying need influences how female flies interpret the valence of external stimuli – so as to guide their decision of whether to move towards or away from specific stimuli – remains little explored, despite the fact that female flies are known to be highly selective about where to lay eggs (Azanchi et al, 2013; Dweck et al, 2013; Joseph et al, 2009; Joseph and Heberlein, 2012; Rockwell and Grossfield, 1978; Schwartz et al, 2012; Yang et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Mechanosensitive Neurons on the Internal Reproductive Tract Contribute to Egg-Laying-Induced Acetic Acid Attraction in Drosophila

et al. 2014

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Selecting a suitable site to deposit their eggs is an important reproductive need of Drosophila females. While their choosiness towards egg-laying sites is well documented, the specific neural mechanism that activates females’ search for attractive egg-laying sites is not known. Here we show that distention/contraction of females’ internal reproductive tract triggered by egg-delivery through the tract plays a critical role in activating such search. We found that females start to exhibit acetic acid attraction prior to depositing each egg but no attraction when they are not laying eggs. Artificially distending the reproductive tract triggers acetic acid attraction in non-egg-laying females whereas silencing the mechanosensitive neurons we identified that can sense the contractile status of the tract eliminates such attraction. Our work uncovers the circuit basis of an important reproductive need of Drosophila females and provides a simple model to dissect the neural mechanism that underlies a reproductive need-induced behavioral modification.

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“…Behavioral genetic studies of Drosophila have identified critical brain neurons that regulate female sexual behavior (Ferveur, 2010). Electrical silencing of SAG neurons of the abdominal ganglion inhibits female sexual receptivity (Feng et al, 2014). Similarly, inactivation of subsets of doublesex-expressing brain neurons (pCd and pC1) also inhibits female sexual receptivity (Zhou et al, 2014).…”

mentioning

confidence: 99%

Knockout mutations of insulin-like peptide genes enhance sexual receptivity in <i>Drosophila</i> virgin females

Watanabe

Sakai

2015

Genes Genet. Syst.

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In the fruitfly Drosophila melanogaster, females take the initiative to mate successfully because they decide whether to mate or not. However, little is known about the molecular and neuronal mechanisms regulating sexual receptivity in virgin females. Genetic tools available in Drosophila are useful for identifying molecules and neural circuits involved in the regulation of sexual receptivity. We previously demonstrated that insulin-producing cells (IPCs) in the female brain are critical to the regulation of female sexual receptivity. Ablation and inactivation of IPCs enhance female sexual receptivity, suggesting that neurosecretion from IPCs inhibits female sexual receptivity. IPCs produce and release insulinlike peptides (Ilps) that modulate various biological processes such as metabolism, growth, lifespan and behaviors. Here, we report a novel role of the Ilps in sexual behavior in Drosophila virgin females. Compared with wild-type females, females with knockout mutations of Ilps showed a high mating success rate toward wild-type males, whereas wild-type males courted wild-type and Ilp-knockout females to the same extent. Wild-type receptive females retard their movement during male courtship and this reduced female mobility allows males to copulate. Thus, it was anticipated that knockout mutations of Ilps would reduce general locomotion. However, the locomotor activity in Ilp-knockout females was significantly higher than that in wild-type females. Thus, our findings indicate that the high mating success rate in Ilp-knockout females is caused by their enhanced sexual receptivity, but not by improvement of their sex appeal or by general sluggishness.

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Ascending SAG Neurons Control Sexual Receptivity of Drosophila Females

Cited by 155 publications

References 57 publications

Sex-specific regulation of Lgr3 in Drosophila neurons

Sex-specific regulation of Lgr3 in Drosophila neurons

Mechanosensitive Neurons on the Internal Reproductive Tract Contribute to Egg-Laying-Induced Acetic Acid Attraction in Drosophila

Knockout mutations of insulin-like peptide genes enhance sexual receptivity in <i>Drosophila</i> virgin females

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