Social-like responses are inducible in asocial Mexican cavefish despite the exhibition of strong repetitive behavior

  1. Motoko Iwashita
  2. Masato Yoshizawa  Is a corresponding author
  1. School of Life Sciences, the University of Hawai‘i at Manoa, United States
8 figures, 4 videos, 1 table and 3 additional files

Figures

Figure 1 with 1 supplement
Schematics of the behavioral assay.

(A) Schematics of the assay system. The recording tank was back-lighted by an infrared (IR) LED array with a white paper diffuser. The IR camera was set at the top of the tank, and fish movement was …

Figure 1—figure supplement 1
No visual response to the back light emitted from the 850 nm infrared (IR) LED.

(A) Top view of the recording arena. Half of the area was IR illuminated from the bottom, and the other half was not illuminated. The areas of these two regions were exactly the same. (B) No …

Figure 1—figure supplement 1—source data 1

Number of fish found in the infrared-lighted or shaded area within a 5 min period.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig1-figsupp1-data1-v2.csv
Figure 2 with 4 supplements
Detection of social-like nearby interactions.

(A, B) Measurements of nearest neighbour distance (NND) (A) and interindividual distance (IID) (B). Surface fish are shown as black lines, and cavefish are shown as orange lines (N = 18 groups of …

Figure 2—source data 1

Surface fish’s and cavefish’s inter-individual distance (cm) in every 0.05 s.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig2-data1-v2.csv
Figure 2—source data 2

Surface fish’s and cavefish’s inter-individual distance (cm) in every 0.05 s.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig2-data2-v2.csv
Figure 2—source data 3

Event numbers counted under the cut-off distances between pairs of fish in the actual and simulated surface fish data.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig2-data3-v2.csv
Figure 2—source data 4

Nearby event numbers shorter than 5 cm distance counted more than cut-off duration between pairs of fish in the actual and simulated surface fish data.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig2-data4-v2.csv
Figure 2—source data 5

Speed (cm/s) during the nearby interaction events and other periods, and the detected nearby interaction duration (s) comparing between the actual and simulated random data.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig2-data5-v2.csv
Figure 2—figure supplement 1
Determine the cut-off distance and cut-off duration for detecting nearby interactions.

(A, B and D) An example of nearby-interaction profiles in surface fish (a four-fish group). (A) A histogram of inter-individual distance (IID; left) and raster plot for the nearby-interaction events …

Figure 2—figure supplement 1—source data 1

The X-Y coordinates (cm) and distances of each pair (cm) of a four-surface fish group in the dark.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig2-figsupp1-data1-v2.csv
Figure 2—figure supplement 1—source data 2

The X-Y coordinates (cm) and distances of each pair (cm) of a four-cavefish group in the dark.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig2-figsupp1-data2-v2.csv
Figure 2—figure supplement 2
Details of nearby interactions were obtained by classifying them into five categories.

(A) Vector set and their angles for classifying interactions between a fish pair. F1t and F1t-1 are the positions of fish one at times t and t-1, respectively. Similarly, the positions of fish two …

Figure 2—figure supplement 3
Nearby interactions of surface fish in lighted conditions.

(A) An example frame of recorded surface fish video. Coloured lines represent trajectories of each individual fish detected by idTracker software. Trajectories for 1 s (20 frames) are shown. (B) A …

Figure 2—figure supplement 3—source data 1

The X-Y coordinates (cm) and distances of each pair (cm) of a four-surface fish group under the light.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig2-figsupp3-data1-v2.csv
Figure 2—figure supplement 4
Pharmacological ablation of the lateral line by gentamicin antibiotics reduced nearby interactions.

Fish were bath-treated with 0.002% gentamicin for approximately 16 hours before the behavioral assay in an unfamiliar environment. The bath treatment was performed in home trays (15.6 × 15.6 × 5.7 …

Figure 2—figure supplement 4—source data 1

Nearby interaction duration (s) under the gentamicin treatment.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig2-figsupp4-data1-v2.csv
Reduced social-like nearby interactions in cavefish in unfamiliar environments compared with familiar environments.

(A) Schematics of experimental procedure. Fish were acclimated in the home tray for more than 4 days and were transferred to the recording tank in this unfamiliar environment. After the recording, …

Figure 3—source data 1

Position-indices in the recording arena under the familiar or unfamiliar environment.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig3-data1-v2.csv
Figure 3—source data 2

The swimming distances, absolute values of the turning indices, nearby interaction durations, nearby interaction event numbers, and swimming speeds under the familiar or unfamiliar environment.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig3-data2-v2.csv
Figure 4 with 1 supplement
Turning bias index showed strong biased turning in cavefish.

(A) Diagram showing the calculation formula for the turning bias index. The changes in travelling directions were calculated every five frames (every 0.25 s) across all trajectories and were …

Figure 4—source data 1

The turning indices of surface fish and cavefish.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig4-data1-v2.csv
Figure 4—figure supplement 1
Replication test assessing turning bias in cavefish.

(A) Each cavefish was first subjected to the turning assay in the individual recording arena to track their ID. After the initial recording, each cavefish was tattooed with visible implant elastomer …

Figure 4—figure supplement 1—source data 1

Repeated measurement of turning indices.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig4-figsupp1-data1-v2.csv
The relationship between repetitive turning behavior and nearby social-like behavior in cavefish.

(A, B) In the familiar environment, the logarithmic transformed turning bias index and aspects of nearby interactions were significantly negatively correlated, F1,34 = 9.6, adjusted R2 = 0.198, p = …

Figure 5—source data 1

The turning bias indices and nearby interaction under the familiar or unfamiliar environment.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig5-data1-v2.csv
Figure 6 with 2 supplements
The partial agonist of the D2 receptor aripiprazole enhanced nearby interactions and reduced turning bias in cavefish.

The pre-treatment behaviors were recorded for more than four days before the aripiprazole treatment. Aripiprazole and the control DMSO were administered for ~16 hr before the post-treatment …

Figure 6—source data 1

The swimming distances, absolute values of the turning indices, nearby interaction durations, nearby interaction event numbers, and swimming speeds under the aripiprazole treatment.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig6-data1-v2.csv
Figure 6—figure supplement 1
Nearby-interaction durations were significantly longer in the actual fish than in the simulated random data in the aripiprazole treatment.

The plot of the actual data is shown in black and white, and the simulated data are shown in light blue (N = 16 for both actual and simulated surface fish; N = 20 for both actual and simulated …

Figure 6—figure supplement 1—source data 1

The swimming speed and nearby interaction duration in cavefish and surface fish.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig6-figsupp1-data1-v2.csv
Figure 6—figure supplement 2
Swimming speed is not a significant predictor of nearby-interaction durations.

Swimming speeds and nearby-interaction durations before (A) and after (B) treatment with aripiprazole (N = 32 from eight groups: F1,18 = 2.1, p = 0.1622; and F1,18 = 0.1, p = 0.8081, respectively) …

Figure 6—figure supplement 2—source data 1

Nearby-interaction durations were significantly longer in the actual fish than in the simulated random data in the aripiprazole treatment.

https://cdn.elifesciences.org/articles/72463/elife-72463-fig6-figsupp2-data1-v2.csv
Fish 1 and Fish 2 are swimming in velocities of V1 and V2, respectively.

Then, to simplify the calculation, suppose that the two fish swim with the average velocity, V=V1=V2, the average of the relative velocity between two fish is given by V and θ (see above).

By using relative velocity, we can think as that one fish of a pair is still.

Then, while another fish passing by a 5 cm radius of the first fish (circle), this fish travels 5 × 2 × sin(ω) cm (orange arrow).

Videos

Video 1
Swimming patterns of four surface fish in dark conditions (unfamiliar environment).
Video 2
Swimming patterns of four cavefish in dark conditions (unfamiliar environment).
Video 3
Swimming patterns of four surface fish in dark conditions.

The arena was illuminated with infrared light. Fish did not respond to the visual stimulus—a moving object (unfamiliar environment).

Video 4
Swimming patterns of four surface fish in lighted conditions (unfamiliar environment).

Tables

Key resources table
Reagent type (species) or resourceDesignationSource or referenceIdentifiersAdditional information
Strain, strain background (Astyanax mexicanus)Surface (epigean) populationYoshizawa lab descendant of William R Jeffery lab at Univ Maryland College Park USSFe; SFgDOI:10.1126/science.289.5479.631
Strain, strain background (Astyanax mexicanus)Cave (hypogean) populationYoshizawa lab descendant of Richard Borowsky lab at New York Univ. USPAbyDOI:10.1101/pdb.prot5093
Chemical compound, drugAripiprazoleSellek ChemicalsS1975
Chemical compound, drugGentamicinMilliporeSigmaG1914
Software, algorithmMATLABMathWorksR2020a
Software, algorithmPythonPythonPython 3.7.4
Software, algorithmidTrackerPérez-Escudero et al., 2014idTracker-betahttps://github.com/idTracker/idTracker/tree/Beta
Chemical compound, drug4-Di-2-AspMilliporeSigmaD3418

Additional files

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