Neuroendocrine control of a sexually dimorphic behavior by a few neurons of the pars intercerebralis in Drosophila

Abstract

In Drosophila, locomotor activity is sexually dimorphic and the brain area controlling this dimorphism has been mapped. The neurons of the pars intercerebralis (PI) have been suggested to participate in such differences between males and females. However, the precise physical nature of the dimorphism, the identity of the PI neurons involved, and the nature of the neuronal signal coding the dimorphism remain unknown. In this study, we used a video-tracking paradigm to characterize further the pattern of locomotor activity in Drosophila. We show that the number of activity͞inactivity periods (start͞stop bouts) is also sexually dimorphic, and that it can be genetically feminized in males. Moreover, the transplantation of PI neurons from a female, or of feminized PI neurons from a donor male into a receiver wild-type male is sufficient to induce the feminization of locomotor behavior, confirming that this tiny cluster of Ϸ10 neurons is directly responsible for the sexual dimorphism in locomotor activity. Finally, feeding males with fluvastatin, a juvenile hormone (JH) inhibitor, also led to start͞stop feminization, and this effect is reversible by the simultaneous application of methoprene, a JH analog, suggesting the existence of a neuroendocrine control, by JH, of such behavioral dimorphism. Invertebrates and vertebrates show sexually dimorphic behaviors, and it has been suggested that males and females differ in the brain structures controlling such behavioral differences (1-4). Such sex differences have often been used as a way of studying how brain structure contributes to brain function. However, although many sexually dimorphic neural structures have been described (2-4), very few studies have yet demonstrated the direct involvement of a brain structure in a sexually dimorphic behavior (5, 6) and still less a behavior expressed in a nonsexual context. We recently showed that Drosophila locomotor activity is sexually dimorphic (7) outside any sexual context. We could abolish this behavioral dimorphism and create males with a female-like activity profile by genetic manipulations (8). Briefly, we used a UAS-transformer transgene (UAS-tra; ref. 9), the feminizing action of which has been shown to be cell-autonomous (10-12), under the control of different brainspecific enhancer trap P[Gal4] lines. This first study suggested strongly that a few neurons located in the mid-anterior part of the pars intercerebralis (PI) might participate in the control of this sexually dimorphic behavior (8). However, because in this previous study the fly was observed in a small tube, the locomotor activity was indirectly quantified when the fly crossed an infra-red light-gate. As a result, the precise locomotor parameters that accounted for the sexual difference could not be elucidated. Furthermore, the involvement of the PI neurons was indirectly deduced on the basis of a genetic ablation, and the molecular mechanisms linking those few PI neurons to the sexually dimorphic behavior remained to be identified. In this study, we develo...

In the monarch butterfly the juvenile hormone effect upon immune response depends on the immune marker and is sex dependent

“…On the other hand, in insects, JH is expressed in both sexes [34] and differentially affects male and female behavior [38], morphology [39], development and locomotion [38], but the novelty of our results is that the effect of JH upon immune response seems to be sex dependent at least in the monarch butterfly. In females two out of three immune parameters were affected by the JH while in males only PO was affected.…”

Insulin signalling in mushroom body neurons regulates feeding behaviour inDrosophilalarvae

“…In Drosophila, insulin signalling has been implicated in ethanol sensitivity (Corl et al, 2005), sexually dimorphic locomotor activity (Belgacem and Martin, 2002;Belgacem and Martin, 2006) and age-related locomotor impairment (Jones et al, 2009), and in a Drosophila model of -amyloid-induced neurotoxicity (Chiang et al, 2010). Here, we report that inhibition but not activation of insulin signalling in mushroom body neurons throughout larval development disrupts starvation-induced food intake and growth of foraging third instar larvae.…”

“…It has served as a model to study the function of insulin signalling in a variety of processes (e.g. Broughton et al, 2005;Belgacem and Martin, 2002;Belgacem and Martin, 2006;Corl et al, 2005) (reviewed by Teleman, 2010). Increased levels of insulin suppress starvation-dependent feeding behaviour (Wu et al, 2005a).…”

Regulation of feeding behaviour and locomotor activity bytakeoutinDrosophila

“…It has been previously suggested that TO could act as a juvenile hormone (JH) carrier protein based on its protein sequence similarity with JH binding proteins (JHBPs) (Lerro and Prestwich, 1990). Moreover, we have previously found that JH level is involved in sexual dimorphism of locomotor activity (Belgacem and Martin, 2002). to 1 flies lack such sexual dimorphism and this could be rescued both genetically, by expressing to under the timeless (tim) driver, and pharmacologically, using methoprene, a JH analog.…”