Evolutionary conservation and diversification of auditory neural circuits that process courtship songs in Drosophila

Abstract

Acoustic communication signals diversify even on short evolutionary time scales. To understand how the auditory system underlying acoustic communication could evolve, we conducted a systematic comparison of the early stages of the auditory neural circuit involved in song information processing between closely-related fruit-fly species. Male Drosophila melanogaster and D. simulans produce different sound signals during mating rituals, known as courtship songs. Female flies from these species selectively increase their receptivity when they hear songs with conspecific temporal patterns. Here, we firstly confirmed interspecific differences in temporal pattern preferences; D. simulans preferred pulse songs with longer intervals than D. melanogaster. Primary and secondary song-relay neurons, JO neurons and AMMC-B1 neurons, shared similar morphology and neurotransmitters between species. The temporal pattern preferences of AMMC-B1 neurons were also relatively similar between species, with slight but significant differences in their band-pass properties. Although the shift direction of the response property matched that of the behavior, these differences are not large enough to explain behavioral differences in song preferences. This study enhances our understanding of the conservation and diversification of the architecture of the early-stage neural circuit which processes acoustic communication signals.

Neural-circuit basis of song preference learning in fruit flies

“…We used restricted mean time lost (RMTL) as an indicator of the cumulative copulation rate to evaluate this change, where a larger RMTL reflects higher copulation acceptance (Fig. 4 E ; See Materials and Methods for details) (15). We found that the response of experienced females to the conspecific song, but not to the heterospecific song, was significantly reduced in the Dop1R2 knockdown group when compared to that of the control group (conspecific song: p = 1.62e -12 ; heterospecific song: p = 0.32; restricted mean survival time adjusted by Bonferroni).…”

“…Fly pairs were recorded for 35 min at 15 fps with a web camera (Logicool HD Webcam C270, Tokyo, Japan). Copulation was defined as the following criteria: (1) the male mounts the female for more than 5 min, (2) the mounted female decreases locomotor activity, and (3) opens her wings during the mounting (15).…”

“…Briefly, a lack of song preference learning results in a LI of 1, whereas LI > 1 indicates that flies demonstrate the learning phenotype (See SI Appendix, Supporting Information Text). To evaluate the cumulative copulation rate and copulation latency of each group, we also utilized restricted mean time lost (RMLT) (71) calculations using the survRM2 package (version 2.2.1) of R (15). Calculated p-values were adjusted by Bonferroni corrections.…”

“…The major component of the courtship song of D. melanogaster is the pulse song, i.e., a repetition of sound pulses (14). The inter-pulse interval (IPI) of the pulse song differs among sibling Drosophila species and significantly affects female mate choice, with increased mating receptivity to conspecific courtship songs rather than heterospecific songs (13,15). The auditory pathways from sensory neurons to higher-order brain neurons are organized to tune selectively to the conspecific song and thus facilitate mating acceptance in female flies (16)(17)(18).…”

The females' response to male attractiveness: Mate choice, larvae production and differential brain protein expression

“…Previous research in Poecilia reticulata has revealed differential gene expression in the brains of females in response to male attractiveness (i.e., colorful vs. dull males; Bloch et al, 2018). Similarly, studies on Drosophila have explored the neural circuits and differential gene expression in females' brains related to male courtship and/or female receptivity (Baker et al, 2022; Immonen & Ritchie, 2012; Kohl et al, 2013; Mezzera et al, 2020; Ning et al, 2022; Ohashi et al, 2023; Pacheco et al, 2021; Wang et al, 2020; Yang et al, 2023). However, much investigation is still needed to understand how male attractiveness affects the underlying mechanisms in female brains and their association with mate rejection and offspring production.…”