Hearing regulates Drosophila aggression

Abstract

Aggression is a universal social behavior important for the acquisition of food, mates, territory, and social status. Aggression in Drosophila is context-dependent and can thus be expected to involve inputs from multiple sensory modalities. Here, we use mechanical disruption and genetic approaches in Drosophila melanogaster to identify hearing as an important sensory modality in the context of intermale aggressive behavior. We demonstrate that neuronal silencing and targeted knockdown of hearing genes in the fly's auditory organ elicit abnormal aggression. Further, we show that exposure to courtship or aggression song has opposite effects on aggression. Our data define the importance of hearing in the control of Drosophila intermale aggression and open perspectives to decipher how hearing and other sensory modalities are integrated at the neural circuit level.A ggression is one of the most important social behaviors in nature, ensuring reproduction and survival when competing for food, territory, or mating partners (1). Aggression is a complex behavior shaped by many factors, including a complex genetic architecture, the integration of various neurotransmitter and hormone systems, and a range of environmental factors (2).Correct integration and processing of sensory information are crucial to evoke an appropriate behavioral response. Previous studies have implicated different sensory modalities in the regulation of aggressive behavior in Drosophila melanogaster, including the olfactory, gustatory, and visual systems (3-6).Another important sensory modality in Drosophila is hearing. Stereotypic sound patterns generated by wing vibration and their behavioral significance have been extensively studied in the context of Drosophila courtship (7-12). On the contrary, nothing is known about the impact of hearing on aggressive behavior. Furthermore, although agonistic sound pulses are known to be generated during aggressive encounters, it is unknown whether they serve as acoustic communication signals to modulate behavior (13).The Drosophila auditory organ, Johnston's organ (JO), is situated in the fly's antenna (Fig. 1A) (14-17). Antennal displacement leads to activation of ∼500 chordotonal stretch-receptor neurons in the JO, which contains AB neurons responsive to sound-evoked vibrations and CE neurons sensitive to sustained antennal deflections caused by gravity and wind (Fig. 1A) (18). The sensory neuron subclasses each innervates a particular region of the antennal mechanosensory and motor center (AMMC), the primary processing center for auditory input in the fly brain (18).In this study, we use mechanical disruption and genetic approaches in D. melanogaster to identify hearing as an important sensory modality in the context of intermale aggressive behavior. We show that neuronal silencing and targeted knockdown of hearing genes in the fly's auditory organ induce abnormal aggression. Further, we show that exposure to courtship or aggression song has opposite effects on aggression. Our data provide evidence on the r...

Neuroligins Nlg2 and Nlg4 Affect Social Behavior in Drosophila melanogaster

“…A recent study (76) further reported that AS promote aggression, while CSs inhibit aggressive interactions between Drosophila males. In order to test whether Dnlg2- and Dnlg4-deficient flies react appropriately to sound signals, we extended the competitive courtship paradigm by continuous stimulation with WN, CS, or aggression sounds.…”

Multisensory neural integration of chemical and mechanical signals

“…Although the precise mechanism by which this polymodal information is integrated is still unclear, anatomical and functional studies point to the P1 neurons in the brain as candidates for mediating sensory integration and behavioral action selection . A related, sexually‐dimorphic social behavior, aggression, is also modulated by chemical and auditory signals . Interestingly, integration of these cues may also occur in P1 neurons , raising the question of how these central neurons are differentially regulated to trigger alternative behaviors.…”

Asip(Agouti-signaling protein) aggression gene regulate auditory processing genes in mice

“…These reports indicate that aggression and hearing are possibly interlinked. Previous reports have shown various sensory modalities in mediating of aggressive behavior in Drosophila melanogaster including olfactory, gustatory, as well as visual neural networks [6]. Furthermore it was found that, neuronal silencing and targeted knockdown of hearing genes such as d trpl (transient receptor potential-like) and the Ca2+ signaling-related genes Arr2 and inaD in the fly's auditory organ elicit abnormal aggression [6].…”

“…Hearing as a sensory modality in the context of aggressive behavior has been shown to play a major role in controlling behavior [6]. Precise integration and processing of sensory inputs are crucial to evoke a suitable behavioral response [7].…”