Selectivity and Plasticity in a Sound-Evoked Male-Male Interaction in Drosophila

Abstract

During courtship, many animals, including insects, birds, fish, and mammals, utilize acoustic signals to transmit information about species identity. Although auditory communication is crucial across phyla, the neuronal and physiologic processes are poorly understood. Sound-evoked chaining behavior, a display of homosexual courtship behavior in Drosophila males, has long been used as an excellent model for analyzing auditory behavior responses, outcomes of acoustic perception and higher-order brain functions. Here we developed a new method, termed ChaIN (Chain Index Numerator), in which we use a computer-based auto detection system for chaining behavior. The ChaIN system can systematically detect the chaining behavior induced by a series of modified courtship song playbacks. Two evolutionarily related Drosophila species, Drosophila melanogaster and Drosophila simulans, exhibited dramatic selective increases in chaining behavior when exposed to specific auditory cues, suggesting that auditory discrimination processes are involved in the acceleration of chaining behavior. Prolonged monotonous pulse sounds containing courtship song components also induced high intense chaining behavior. Interestingly, the chaining behavior was gradually suppressed over time when song playback continued. This behavioral change is likely to be a plastic behavior and not a simple sensory adaptation or fatigue, because the suppression was released by applying a different pulse pattern. This behavioral plasticity is not a form of habituation because different modality stimuli did not recover the behavioral suppression. Intriguingly, this plastic behavior partially depended on the cAMP signaling pathway controlled by the rutabaga adenylyl cyclase gene that is important for learning and memory. Taken together, this study demonstrates the selectivity and behavioral kinetics of the sound-induced interacting behavior of Drosophila males, and provides a basis for the systematic analysis of genes and neural circuits underlying complex acoustic behavior.

Hearing regulates Drosophila aggression

“…Previous reports described courtship song-induced chaining behavior between males (36)(37)(38). In our assay, we did not observe this behavior.…”

Neuroligins Nlg2 and Nlg4 Affect Social Behavior in Drosophila melanogaster

“…Dnlg2-deficient flies showed a significantly lower chance of male–male courtship, which might be caused by their larger interindividual distance (Figure 6). It has been shown that CSs stimulate the formation of courtship chains (92, 93) and especially the inter-pulse interval of CSs has been identified as a critical factor for species recognition and attractiveness (20, 94), an alteration in song production might also lead to the chaining phenotype. Since dnlg2 KO17 -mutant males produced songs with significantly prolonged inter-pulse intervals (Figure 6C), complete absence of chaining behavior could also have been a consequence of less attractive songs.…”

Organization of projection neurons and local neurons of the primary auditory center in the fruit flyDrosophila melanogaster

“…Previous studies have demonstrated that artificial courtship songs dramatically accelerate the chaining behavior of male flies, a typical homosexual courtship behavior in a single‐sex group situation (Eberl et al, ; Yoon et al, ). Female flies, in contrast, gradually decrease their locomotor activity and finally accept a courting male upon exposure to a courtship song (Crossley et al, ).…”