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Auditory experience controls the maturation of song discrimination and sexual response in Drosophila

  1. Xiaodong Li
  2. Hiroshi Ishimoto
  3. Azusa Kamikouchi  Is a corresponding author
  1. Nagoya University, Japan
Research Article
Cite this article as: eLife 2018;7:e34348 doi: 10.7554/eLife.34348
7 figures, 1 table and 3 additional files

Figures

Social interaction shapes the preference to the song.

Chaining response of naïve male flies that were housed in different experimental conditions, grouped without wings (A), grouped with intact wings (B), and single-reared with intact wings (C). The time-courses of the chain index in response to playback of conspecific song (red) and heterospecific song (blue) are shown. Sound playback starts at 5 min. The bold line and ribbon represent the average value and standard error, respectively. The box plot shows the summed chain index between 5 min and 11.5 min. Boxplots display the median of each group with the 25th and 75th percentiles and whiskers denote 1.5x the inter-quartile range. N.S., not significant, p>0.05; **p<0.01; Mann-Whitney U test. n, number of behavioral chambers examined.

https://doi.org/10.7554/eLife.34348.003
Fine-tuned song response of males after the training.

(A) Protocol for the training and test sessions. (B) Setup for the training and chaining test. In the training session, single-housed male flies were exposed to a training song for the first 6 days after eclosion. In the test session, song was delivered from a loudspeaker. Appropriate song typically drove the male flies to form male-male chains (chaining). Males in a chain are marked with red dots. (C, D) Chaining response to the conspecific song (C) or heterospecific song (D) after training. N, naïve group with no sound training (blue); E, experienced group with conspecific song training (red) or heterospecific song training (orange). The way to show the time courses of chaining behavior and the boxplot is similar to that depicted in Figure 1. N.S., not significant, p>0.05; ***p<0.001; Mann-Whitney U test versus naïve group.

https://doi.org/10.7554/eLife.34348.004
Playback of pulse song promotes copulation in wild-type fly pairs.

(A) Setup for song-induced copulation test. (B) Cumulative copulation rate and copulation latency with playback of artificial pulse songs of different inter-pulse interval (IPI). Copulation latency represents the latency to accept copulation in the 30 min observation period. Boxplots display the median of each group with the 25th and 75th percentiles and whiskers denote 1.5x the inter-quartile range. N.S., not significant, p>0.05; ***p<0.001; Log rank test versus no sound group (left panel); Kruskal–Wallis test followed by Scheffe’s test (right panel). n, number of fly pairs examined.

https://doi.org/10.7554/eLife.34348.005
Fine-tuned song response of females after the training.

(A, B) Cumulative copulation rate in the conspecific song test (A) or heterospecific song test (B) after training females. Naïve group (no sound during training) and experienced groups (trained with conspecific song or heterospecific song) are shown. The color code is the same with that in Figure 2. N, naïve; E, experienced. (C) Copulation latencies of females under playback of conspecific song (green bars) or heterospecific song (purple bars). Nc and Nh, naïve flies tested with conspecific and heterospecific songs, respectively. Ec and Eh, experienced flies tested with conspecific and heterospecific songs, respectively. (D) Inhibition index under playback of conspecific song (green bars) or heterospecific song (purple bars) after training of conspecific song or heterospecific song. Inhibition index = (copulation ratioNaïve - copulation ratioExperienced)/copulation ratioNaive. N.S., not significant, p>0.05; ***p<0.001; Log rank test versus naïve group (A, B); Kruskal–Wallis test versus naïve group (C).

https://doi.org/10.7554/eLife.34348.006
Figure 5 with 1 supplement
Involvement of Gad1 in the experience-dependent song preference in females.

(A, B) Cumulative copulation rate in the conspecific song test (A) or heterospecific song test (B) after training Gad1 knockdown (left) and control (right) females. Naïve group (no sound training) and experienced groups (conspecific song training and heterospecific song training) are shown. The color code is the same with that in Figure 2. N, naïve; E, experienced. N.S., not significant, p>0.05; *p<0.05; ***p<0.001; Log rank test versus naïve group.

https://doi.org/10.7554/eLife.34348.007
Figure 5—figure supplement 1
Male Gad1 knockdown flies responded normally to conspecific courtship song.

The time-courses of the chain index in response to playback of conspecific song in Gad1 knockdown group (red, Gad1-GAL4/+; UAS-Gad1 RNAi/+) and control group (blue, Gad1-GAL4/+; +/+) are shown. The way to perform chaining test is similar to that described in the Method part. Sound playback starts at 5 min and lasts until 60 min. Error bars denotes s.e.m. n, number of behavioral chambers examined.

https://doi.org/10.7554/eLife.34348.008
Rdl receptors in pC1 neurons modulate the experience-dependent song preference in females.

(A, B) Cumulative copulation rate in the conspecific song test (A) or heterospecific song test (B) after training Rdl knockdown (left) and control (right) females. Naïve group (no sound training) and experienced groups (conspecific song training or heterospecific song training) are shown. The color code is the same with that in Figure 2. N, naïve; E, experienced. N.S., not significant, p>0.05; *p<0.05; Log rank test versus naïve group.

https://doi.org/10.7554/eLife.34348.009
A model for experience-dependent tuning of IPI perception in Drosophila.
https://doi.org/10.7554/eLife.34348.010

Tables

Key resources table
Reagent type (species) or resourceDesignationSource or referenceIdentifiersAdditional information
gene (Drosophila melanogaster)RdlNAFLYB: FBgn0004244
gene (Drosophila melanogaster)GAD1NAFLYB: FBgn0004516
strain, strain background
(Drosophila melanogaster)
Canton-Sothergift from K. Ito
strain, strain background
(Drosophila melanogaster)
Gad1-GAL4PMID: 12408848gift from K. Ito
strain, strain background
(Drosophila melanogaster)
UAS-Gad1 RNAiVienna Drosophila
Resource Center
VDRC ID: 32344;
RRID: Fly-Base_FBst0459538
strain, strain background
(Drosophila melanogaster)
w1118Vienna Drosophila
Resource Center
VDRC ID: 60000
strain, strain background
(Drosophila melanogaster)
UAS-Rdl RNAiBloomington Drosophila
Stock Center
BDRC: 52903;
RRID: BDSC_52903
strain, strain background
(Drosophila melanogaster)
TRiP RNAiBloomington Drosophila
Stock Center
BDRC: 36304;
RRID: BDSC_36304
strain, strain background
(Drosophila melanogaster)
tubP>GAL80>;
NP2631-GAL4/CyO;
dsxFLP/TM2
PMID: 27185554gift from D. Yamamoto
software, algorithmChaIN (ver. 3)PMID: 28701929

Additional files

Supplementary file 1

Genotypes.

The genotypes used in figures are as follows. In Figures 5 and 6, the genotypes of females are listed, while the paired males are always wild type.

https://doi.org/10.7554/eLife.34348.011
Supplementary file 2

Statistical results.

The detailed statistical results in each figure are listed. N.S., not significant, p>0.05; *p<0.05; **p<0.01; ***p<0.001.

https://doi.org/10.7554/eLife.34348.012
Transparent reporting form
https://doi.org/10.7554/eLife.34348.013

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