Genetics and neurobiology of aggression in Drosophila

Figures & data

Table 1. Modules of aggressive behavior in male and female Drosophila

Male	Female
Retreat
Walking, flying or running away	Walking or flying away
Approach/turn toward
Walk toward the opponent while lowering body	Turn/walk toward the opponent
Wing threat
Raise both wings to a 45° angle toward opponent (> 1s) Flicks wings at 45° angle while facing away from opponent	Raise one or both wings to a 45–90° angle toward opponent (< 1s)
Lunge
Rear up on hind legs and collapse on opponent	Rear up on hind legs and collapse on opponent
Shove
Not observed	Thrust the torso toward the opponent with both forelegs extended without recoil
Thrust with a wing threat
Not observed	Thrust and lift one or both wings to a 45–90° angle (< 1s)
Head butt
Not observed	Thrust the torso toward the opponent and strike the opponent with the head; usually followed by recoiling of the torso
Fencing
Fencing (low): extend one leg and tap opponent’s leg Fencing (high): extend leg forward and push opponent facing each other	Fencing (low): Extend leg and contact the opponent in a normal standing posture Fencing (high): Stand tall on the middle and rear legs and contact the opponent with the forelegs (can be combined with a wing threat < 1s) Fencing and feeding: Extend the middle or rear legs and contact the opponent while feeding Fencing threat: Extend the middle legs without contacting the opponent
Chasing
Run after opponent	Not observed
Holding
Grasp opponent with forelegs and try to immobilize	Not observed
Tussling
Tumble over each other, sometimes leaving food surface	Not observed
Boxing
Rear both up on hind legs and strike the opponent with forelegs	Not observed

Ethogram describing the observed modules of aggressive behavior in male and female Drosophila. The listed modules include threat, attack and retreat behaviors. Some of these modules are used by both sexes or show only subtle differences, while others are sex-specific.

Figure 1. Different set-ups to study aggression in Drosophila. (A) Arena with a centrally placed food cup that can contain yeast paste or a virgin female, allowing the videotaping of aggressive behavior.⁶⁸ (B) Set-up allowing the simultaneous recording of 35 arenas, usually during a 15 min period.⁷² (C) Scheme of a set-up compatible with CADABRA software allowing automated scoring of lunging, tussling, wing threats and chasing of two pairs of flies simultaneously. This set-up can be expanded to analyze eight pairs of flies simultaneously.⁶⁷ (D) Set-up allowing the instant analysis of the aggressive encounters between groups of eight flies over a 2 min period.^6,12,73

Figure 2. (A–C) Schematic representation of adult central brain cells reported to be serotonergic, dopaminergic or octopaminergic. Cholinergic cells were reported to be widespread throughout the entire brain making it difficult to present a schematic overview.^140-143 PB, protocerebral bridge; FB, fan-shaped body; EB, ellipsoid body; NO, noduli; MB, mushroom bodies; P, mushroom body peduncle; CA, mushroom body calyx; AL, antennal lobe; SOG, subesophageal ganglion; LC, lobula complex; ME, medulla; LA, lamina. (A) Serotonergic cells. LLP1, posterior lateral protocerebrum; LP2a, between the medulla and the lateral protocerebrum; LP2b, between the medulla and the lateral protocerebrum; DP, dorsal protocerebrum; SP1, posterior to superior median protocerebrum; SP2, posterior median protocerebrum; IP, posterior inferior median protocerebrum; PLP, posterior lateral protocerebrum; SLP, superior lateral protocerebrum; AMP, anterior median protocerebrum; ALP, anterior lateral protocerebrum; AVP, anterior ventral protocerebrum; PAL, posterior to antennal lobe; DLS, dorsal lateral subesophageal ganglion; AS, anterior subesophageal ganglion; SE1, lateral subesophageal ganglion; SE2, anterior lateral subesophageal ganglion; SE3, most ventral subesophageal ganglion.^144-146 (B) Dopaminergic cells. PAM, dorsomedial anterior protocerebral; PAL, dorsolateral anterior protocerebral; PPM, dorsomedial posterior protocerebral; PPL1, dorsolateral posterior protocerebral; PPL2, lateral posterior protocerebral; PPD, protocerebral posterial dorsal; T1, tritocerebrum; VUM, ventral unpaired medial neurons.^76,147,148 (C) Octopaminergic cells (nomenclature according to Sinakevitch and Strausfeld, 2006; nomenclature between brackets according to Monastirioti et al., 1995). Cluster G0a, Cluster G0b (LP, lateral protocerebrum cell), Cluster G1 (DMC, dorsal medial cluster), Cluster G2a (~DAC, dorsal anterior cluster?), Cluster G2b (~DAC, dorsal anterior cluster?), Cluster G3a (AL, antennal lobe cluster), Cluster G3b, Cluster G4a (DPC, dorsal posterior cluster), Cluster G4b (DPC, dorsal posterior cluster), Cluster G5a, Cluster G5b,c, Cluster G6, VUM, Ventral unpaired median neurons 1–3 (SM, subesophageal medial). (D-F) Diagrams representing the biosynthetic pathways of acetylcholine and the monoaminergic neurotransmitters: serotonin, dopamine and octopamine. (D) Serotonin synthesis. TPH, Tryptophan hydroxylase; DDC, DOPA decarboxylase. (E) Dopamine/octopamine synthesis. TH, Tyrosine hydroxylase; TDC, Tyrosine decarboxylase; DDC, DOPA decarboxylase; TβH, Dopamine β hydroxylase (F) Acetylcholine synthesis. ChAT, Choline acetyltransferase

Figure 3. Scheme representing the flow of information provided by external stimuli to integration centers in the central brain. This central integration results in interpretation and integration of the different inputs and the generation of an appropriate response. The role of stimuli or neuronal structures marked with an asterisk (*) in aggression has been more closely analyzed. Visual information is received by the retinal ommatidia and travels through the different layers of the optic lobes, lamina, medulla and lobula complexes, to the central brain.¹⁴⁹ The described higher integration centers of this visual information include the mushroom bodies, the central complex and different neurons in the lateral protocerebrum.^97-99,150 Olfactory information is sensed by olfactory neurons expressing olfactory receptors located on the third antennal segments and the maxillary palps. Odorant cues travel via these neurons to the glomeruli in the antennal lobe from where projection neurons send this information to higher integration centers, including the mushroom bodies and the lateral horn.^93,151-155 Gustatory signals are sensed by gustatory receptors expressing gustatory receptors located on the proboscis, wings, legs and vaginal plate. These neurons all project to the SOG. The SOG has been shown to project toward multiple other brain regions including the antennal lobe, the lateral horn and the mushroom bodies.^96,155,156 Mechanosensory information is sensed by a variety of receptors, located all over the body, which can be subdivided into a ciliated and a non-ciliated group. Non-ciliated mechanosensory receptors include nociceptors and muscle and visceral stretch receptors. Ciliated mechanosensory receptors include: bristles responsible for touch perception, campaniform sensilla on wings and haltere providing info on flight parameters and chordotonal organs including scolopidial organs providing proprioceptive and gravireceptive information.^157,158 The fly's largest chordotonal organ, Johnston’s organ, is located in the second antennal segment and represents the flies ear. Part of these neurons have been shown to innervate the antennal mechanosensory and motor center of the brain, a neuropil lateral to the SOG and the antennal lobes, further higher integration is mainly unknown.^100,157,158

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