Male and female Drosophila exhibit aggressive behaviours against same-sex opponents. However, although male and female flies approach an opponent in a similar way, they show different styles of attack: males ‘lunge’ at and tussle with other males, whereas females ‘headbutt’ their opponents. The circuit logic underlying this mix of a sexually monomorphic appetitive behaviour (approach) and a dimorphic consummatory behaviour (attack phase) has not been clear. Now, Chiu et al. characterize neurons that are common to both sexes and regulate aggressive approach, and other, sex-specific neurons that control attack.
The authors used genetic screening methods to identify neurons that, when optogenetically activated, could promote approach and attack in both male and female flies. Males had two such neurons (which the authors dubbed Eb5 neurons) per hemibrain, whereas female flies had one such neuron per hemibrain. Morphological examination revealed that one pair of the Eb5 neurons in males resemble the Eb5 neurons seen in females — and thus these are common aggression-promoting (CAP) neurons. By contrast, the other pair of male Eb5 neurons are a distinct cell type, and were therefore called male-specific aggression-promoting (MAP) neurons.
Low-intensity optogenetic activation of CAP neurons in males or females promoted aggressive approach behaviour. High-intensity activation of these neurons in females also elicited headbutting, whereas such activation in males did not induce lunging. Therefore, CAP neurons promote aggressive approach behaviour and, in females only, attack behaviour.
Photostimulation of CAP neurons and MAP neurons in male flies strongly elicited approach and lunging attacks. However, optogenetic stimulation only of MAP neurons increased lunging behaviour in males, without affecting approach behaviour: lunging attacks were directed at flies that the stimulated flies encountered by chance. Moreover, photoactivation of CAP neurons induced increases in calcium-indicator fluorescence in MAP neurons. Thus, in males, CAP neurons may control approach behaviour and signal to MAP neurons, which promote attack.
A previous study identified a female-specific neuronal subtype that promoted aggression, and so Chiu et al. targeted these cells, which they called fpC1 neurons, for further investigation. Activation and silencing of fpC1 neurons elicited and suppressed headbutting behaviour without affecting approach behaviour, similar to manipulations of MAP neurons in males. The fpC1 neurons showed strong calcium responses to activation of CAP neurons, and silencing fpC1 neurons reduced the aggression induced by high-intensity activation of CAP neurons. Thus, fpC1 neurons in female flies seem to be functionally analogous to MAP neurons in male flies.
Previous work has shown that social isolation increases aggressiveness in flies. Here, suppressing CAP neuron activity in socially isolated (SI) flies of either sex reduced aggressive approaches and attacks compared with control SI flies. Even weak activation of CAP neurons in SI flies of either sex elicited both approach and attack behaviours. Moreover, the responses of MAP neurons or fpC1 neurons to optogenetic activation of CAP neurons were greater in SI flies than in group-housed flies. Therefore, social isolation boosts aggressiveness, potentially by strengthening the functional connection between CAP neurons and downstream MAP or fpC1 neurons.
“weak activation of CAP neurons in SI flies of either sex elicited both approach and attack behaviours”
Overall, this study provides evidence that CAP neurons in both sexes control the appetitive phase of aggressive behaviour (approach), whereas MAP neurons in males, or fpC1 neurons in females, regulate sexually dimorphic consummatory (attack) behaviours.
Chiu, H. et al. A circuit logic for sexually shared and dimorphic aggressive behaviors in Drosophila. Cell https://doi.org/10.1016/j.cell.2020.11.048 (2020)