Sleep deprivation suppresses aggression in Drosophila
- Perelman School of Medicine at the University of Pennsylvania, United States
- Howard Hughes Medical Institute, Perelman School of Medicine at the University of Pennsylvania, United States
Figures
Figure 1 with 4 supplements
Acute sleep deprivation suppresses aggressive behaviors.
(A) Quantification of aggression (lunge count) in control or sleep deprived male CS flies. ‘Between conditions’ indicates fights between a control fly and a sleep-deprived fly; ‘within condition’ is a fight between 2 sleep-deprived or 2 control flies. ‘Daytime deprivation’ and ‘recovery’ refers to fights between conditions (n = 16, 16, 9, 10, 10, 8, 14, 9 from left to right). (B) Percentage of flies in each condition establishing dominance (fights between conditions). (C) Latency to first lunge following first social encounter (fights are within condition; n = 9 control, 7 deprived). (D) Lunging follow sleep deprivation during the final 1, 3 or 6 hr(s) of the night (fights within condition; n = 8, 8, 13, 9, 12, 12 from left to right). (E) Lunging following 6 hr of mechanical stimulation during the final 3 hr of night and first 3 hr of day (fights within condition; n = 11 for both). (F) Recovery of aggression following prior sleep deprivation for 12 hr (fights within condition; n = 10, 10, 18, 17, 19, 18, 15, 12 from left to right). Box plots in this figure and all others represent median value (horizontal line inside box), interquartile range (height of the box, 50% of the data within this range), and minimum and maximum value (whiskers). Bar graphs in this figure and all others are presented as mean ± s.e.m. *p < 0.05; 1 way ANOVA with Tukey's (A, D) or Sidak's (F) post-hoc test; unpaired two-tailed Student's t-test (C, E). SD = sleep deprivation.
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Figure 1—source data 1
Quantification of lunging following mechanical sleep deprivation.
- https://doi.org/10.7554/eLife.07643.004
Figure 1—figure supplement 1
Quantification of percentage of time pairs of flies spent interacting, with or without prior sleep deprivation (n = 12 pairs for control and deprived).
Unpaired two-tailed Student's t-test.
Figure 1—figure supplement 2
Sleep trace of CS male, showing high sleep amounts during both day and night (n = 22 flies).
https://doi.org/10.7554/eLife.07643.006
Figure 1—figure supplement 3
Quantification of aggression following 12 hr of high temperature (31°C) -induced sleep deprivation (fights within condition at 25°C; n = 21 control, 28 deprived).
*p < 0.05; Unpaired two-tailed Student's t-test.
Figure 1—figure supplement 4
Courtship index and copulation frequency of control or mechanically sleep-deprived males (n = 15 control and deprived).
Unpaired two-tailed Student's t-test (courtship index); Fischer's exact test (copulation frequency).
Figure 2 with 4 supplements
Octopamine agonist CDM rescues reduced aggression following sleep deprivation.
Quantification of aggression at 23°C in Tdc2-GAL4>UAS-TrpA1 or TH-GAL4>UAS-TrpA1 males that were thermogenetically sleep-deprived the prior night at 29°C (SD, red bars) or remained at 21°C (Ctrl, white/gray bars) (n = 10, 16, 10, 12 from left to right). (B, C) Rescue of suppressed aggression in Tdc2-GAL4>UAS-TrpA1 (B) or TH-GAL4>UAS-TrpA1 (C) males fed either CDM or L-DOPA and thermogenetically sleep-deprived (B, n = 12, 10, 10; C, n = 12, 12, 12 from left to right). (D) Rescue of suppressed aggression in group-housed CS males fed either CDM or L-DOPA compared to males reared in isolation (Control) (n = 9, 9, 12, 12 from left to right). (E) Locomotor activity over 1 hr following exposure to 29°C the prior night (n = 16, 16, 32, 32 from left to right). All fights are within condition. *p < 0.05; 1 way ANOVA with Sidak's (A) or Tukey's (B–E) post-hoc test.
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Figure 2—source data 1
Quantification of lunging following thermogenetic sleep deprivation and pharmacologic rescue.
- https://doi.org/10.7554/eLife.07643.012
Figure 2—figure supplement 1
Sleep traces in TH-GAL4>UAS-TrpA1 (n = 24 red, 20 black) or Tdc2-GAL4>UAS-TrpA1 (n = 10 red, 10 black) flies loaded at ZT6 with temperature shift (red trace) to 29°C at ZT12, compared to controls (black trace) remaining at 21°C.
https://doi.org/10.7554/eLife.07643.013
Figure 2—figure supplement 2
(Left) Sleep traces in Tdc2-GAL4>UAS-TrpA1 (black) and GAL4 (red) and UAS (blue) controls loaded at ZT6 with temperature shift (pink box) to 29°C at ZT12.
(Right) Quantification of aggression at 23°C in GAL4 and UAS controls exposed to 29°C during the prior night (n = 13, 14, 8, 8, 9 from left to right). *p < 0.05; 1 way ANOVA with Tukey's post-hoc test.
Figure 2—figure supplement 3
Quantification of aggression in CS males fed either CDM or L-DOPA and mechanically sleep-deprived (n = 17, 20, 24 from left to right).
*p < 0.05; 1 way ANOVA with Tukey's post-hoc test.
Figure 2—figure supplement 4
Quantification of aggression following 1 days or 3 days of drug exposure in isolated males.
1 way ANOVA with Tukey's post-hoc test.
Figure 3
Sleep loss is required for suppressed aggression following octopaminergic activation.
(A) Images of Tdc2+ Cha- neurons in brains from Tdc2-GAL4;Cha-GAL80>UAS-CD8::GFP flies immunostained for GFP (green) and nc82 (magenta). Arrows indicate 2–4 VUM neuron cluster in posterior brain. Scale bar = 100 µm. (B) Sleep traces in Tdc2-GAL4;Cha-GAL80>UAS-TrpA1 (red), Tdc2-GAL4>UAS-TrpA1 (black), and UAS-TrpA1;Cha-GAL80 (blue) flies with temperature shift (pink box) to 29°C at ZT12 (n = 12 flies for all conditions). (C) Quantification of aggression in Tdc2-GAL4>UAS-TrpA1 males exposed to elevated temperature (and sleep deprived) overnight compared to Tdc2-GAL4;Cha-GAL80>UAS-TrpA1 males, and temperature controls (fights within condition; n = 14, 15, 16, 15 flies, from left to right). *p < 0.05; 1 way ANOVA with Sidak's post-hoc test.
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Figure 3—source data 1
Quantification of lunging following thermogenetic activation of Tdc2+Cha- neurons.
- https://doi.org/10.7554/eLife.07643.018
Figure 4 with 1 supplement
Suppressed aggression following sleep deprivation impairs reproductive fitness.
Courtship index towards the female target (A) or male (B) in control (white, n = 32) or sleep-deprived (gray, n = 31) flies during a competitive courtship assay (within condition). (C) Percentage of time spent in chains/clusters during the competitive courtship assay with control (n = 29) or sleep-deprived (n = 30) flies (within condition). (D) Percentage of assays in which the control or sleep-deprived male first copulates with (‘wins’) the female target in a competitive courtship assay between conditions (n = 116 assays, 5 independent experiments). (E) As in (D) but with control vs sleep-deprived ± drug rescue males (control vs SD + no drug, n = 20 assays; control vs SD + L-DOPA, n = 28 assays; control vs SD + CDM n = 27 assays; 3 independent experiments). **p < 0.01, *p < 0.05; Unpaired two-tailed Student's t-test (A–C) or two-tailed Binomial test (D, E).
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Figure 4—source data 1
Courtship and competitive copulations measures following sleep deprivation.
- https://doi.org/10.7554/eLife.07643.020
Figure 4—figure supplement 1
Percentage of assays in which the control or drug condition male first copulates with the female target in a competitive courtship assay between conditions (control vs L-DOPA, n = 30 assays; control vs CDM n = 30 assays; 3 independent experiments).
p = 0.36 for control vs L-DOPA, p = 0.86 for control vs CDM; two-tailed Binomial test.
Videos
Video 1
Aggression assay between two control flies (on regular food with a drop of yeast paste in the center).
https://doi.org/10.7554/eLife.07643.009
Video 2
Aggression assay between two sleep-deprived flies.
https://doi.org/10.7554/eLife.07643.010
Video 3
Competitive courtship assay between 2 control males (white or red painted dot) and a virgin female.
https://doi.org/10.7554/eLife.07643.022
Video 4
Competitive courtship assay between 2 sleep-deprived males (white or red painted dot) and a virgin female.
https://doi.org/10.7554/eLife.07643.023Download links
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Sleep deprivation suppresses aggression in Drosophila
eLife 4:e07643.
https://doi.org/10.7554/eLife.07643
