Discovery of a new song mode in Drosophila reveals hidden structure in the sensory and neural drivers of behavior

Abstract

SummaryDeciphering how brains generate behavior depends critically on an accurate description of behavior. If distinct behaviors are lumped together, separate modes of brain activity can be wrongly attributed to the same behavior. Alternatively, if a single behavior is split into two, the same neural activity can appear to produce different behaviors [1]. Here, we address this issue in the context of acoustic communication in Drosophila. During courtship, males utilize wing vibration to generate time-varying songs, and females evaluate songs to inform mating decisions [2-4]. Drosophila melanogaster song was thought for 50 years to consist of only two modes, sine and pulse, but using new unsupervised classification methods on large datasets of song recordings, we now establish the existence of at least three song modes: two distinct, evolutionary conserved pulse types, along with a single sine mode. We show how this seemingly subtle distinction profoundly affects our interpretation of the mechanisms underlying song production, perception and evolution. Specifically, we show that sensory feedback from the female influences the probability of producing each song mode and that male song mode choice affects female responses and contributes to modulating his song amplitude with distance [5]. At the neural level, we demonstrate how the activity of three separate neuron types within the fly’s song pathway differentially affect the probability of producing each song mode. Our results highlight the importance of carefully segmenting behavior to accurately map the underlying sensory, neural, and genetic mechanisms.

Shared Song Detector Neurons in Drosophila Male and Female Brains Drive Sex-Specific Behaviors

“…S3A). The sex-specific sign and shape of the IPI tuning curves of 278 flies from these two strains matches acoustic tuning measured in other playback assays: 279 females slow for pulse song (Clemens et al, 2017;Crossley et al, 1995;280 F. Von Schilcher, 1976) and copulate most when exposed to conspecific IPIs and less for 281 shorter or longer IPIs (Bennet-Clark and Ewing, 1969;Li et al, 2018); males in groups 282 increase their speed (Crossley et al, 1995;F. Von Schilcher, 1976;Vaughan et al, 2014) 283 and court other females or males most when exposed to pulse song with the conspecific IPI 284 (Crossley et al, 1995;Yoon et al, 2013;Zhou et al, 2015).…”

“…496 S3). Using a naturalistic courtship assay, previous studies show that these same strains 497 exhibit similar behaviors -males pattern their song in response to the female behavior and 498 females change their locomotor speed to the natural courtship song similarly across all 499 strains (Clemens et al, 2017;Coen et al, 2016;2014). 500…”

“…http://dx.doi.org/10.1101/366765 doi: bioRxiv preprint first posted online Jul. 10, 2018; pIP10 activation (Clemens et al, 2017) -pIP10 is a sex-specific descending neuron 576 (Philipsborn et al, 2011), but we don't yet know if it directly connects with pC2 neurons. The 577 fact that song responses are bi-directional -pulse song can induce both slowing and 578 acceleration within each sex ( Fig.…”

“…2A) and do not change their speed or may even 481 accelerate for deviant pulse parameters (Fig. S2E) (Clemens et al, 2017;Riabinina et al, 2011). 487…”

“…Interestingly, the behavioral tuning for 287 IPI in seven additional wild type strains is still sex-specific but deviates from the species-288 typical tuning (Fig. S3B) when assayed in FLyTRAP, even though the same wild type strains 289 -including NM91 -display virtually identical responses to song in a courtship assay in 290 which a male courts a female (Clemens et al, 2017;Coen et al, 2016;2014). This 291 indicates that these strains require additional cues (e.g., pheromones or visual cues) to fully 292 express their preference for conspecific song features.…”