A neural circuit encoding mating states tunes defensive behavior in Drosophila

Abstract

Social context can dampen or amplify the perception of touch, and touch in turn conveys nuanced social information. However, the neural mechanism behind social regulation of mechanosensation is largely elusive. Here we report that fruit flies exhibit a strong defensive response to mechanical stimuli to their wings. In contrast, virgin female flies being courted by a male show a compromised defensive response to the stimuli, but following mating the response is enhanced. This state-dependent switch is mediated by a functional reconfiguration of a neural circuit labelled with the Tmc-L gene in the ventral nerve cord. The circuit receives excitatory inputs from peripheral mechanoreceptors and coordinates the defensive response. While male cues suppress it via a doublesex (dsx) neuronal pathway, mating sensitizes it by stimulating a group of uterine neurons and consequently activating a leucokinin-dependent pathway. Such a modulation is crucial for the balance between defense against body contacts and sexual receptivity.

Leucokinin and Associated Neuropeptides Regulate Multiple Aspects of Physiology and Behavior in Drosophila

“…LK and these other peptide hormones are also likely to be part of a more global orchestration of nutritional- and osmotic state-dependent physiology and behaviors. The recent finding that ABLKs partake in a circuit that changes the behavior of female flies after mating is interesting [ 118 ]. The phenotype described in that study is the result of LK acting within circuits of the CNS.…”

“…A recent paper described a very different and somewhat surprising role of ABLKs in female Drosophila [ 118 ]. The ABLKs in adult female flies serve as an interface between sensory neurons of the oviduct and interneurons in the thoracic ganglia that regulates a defensive wing retraction response ( Figure 9 ).…”

“…Since the touch of the wings by male flies is important in courtship, virgin female flies do not display this wing defense response. This is ensured by a pathway where sensory inputs (courtship song and pheromones) to female-specific neurons that express the gene doublesex use γ-aminobutyric acid (GABA) to inhibit the CTNs ( Figure 9 ) [ 118 ]. In recently mated flies, however, the defensive response is strengthened by activation of the CTNs as part of the post-mating response.…”

“…A set of sensory neurons (UNs) in the uterus that express the gustatory receptor Gr32a and the gene pickpocket synapse onto ABLKs [ 118 ]. The UNs receive signals from the semen and activate the ABLKs, which signal with LK to stimulate the CTNs and thus strengthen the defensive response ( Figure 9 ) [ 118 ]. These authors demonstrated that the signal that triggered the UNs was not sex peptide, but rather some other chemical signal in the semen.…”

“…In female flies, ABLKs receive inputs from sensory cells in the uterus (UNs). When the UNs are activated by mating, ABLKs act on a set of neurons (CTNs) in the metathoracic ganglion that modulate a circuit that regulates wing retraction as a defense response [ 118 ]. ALK/ITPn are neurosecretory cells that use ITP to systemically regulate water homeostasis via the intestine and hindgut and also to regulate feeding and drinking [ 45 ].…”