Publication
Sociability refers to an animal's ease of living amongst members of its own species. This trait is essential for ethologically important social interactions like courtship, mating, and child rearing, as well as collective behaviors like group decision-making, hunting, and colony living. As well, the absence of social interactions (isolation) is known to lead to increased stress, fear, and aggression. Despite an appreciation for the importance of sociability, the degree to which sociability is innate versus learned as well as the underlying neural mechanisms used to switch behaviors driven by the sociability status remains unclear. To address this gap, we investigated sociability in the adult fly, Drosophila melanogaster. We observed that group housed flies are undisturbed by one another, coming into close proximity and engaging in tactile interactions. By contrast, animals raised individually for 5-7 days showed a constellation of fearful reactions toward conspecifics that they encountered for the first time. Remarkably, in single housed animals, sociability can be learned over several hours in the presence of other flies: avoidance behaviors diminish and are replaced by interactions seen in group housed animals. Thus, fear of conspecifics appears to be a default state, and sociability learned through interactions with other animals. Furthermore, in group housed animals sociability can be forgotten in the absence of continued social exposure. We found that learned sociability is specifically tuned to conspecifics and becoming sociable towards conspecifics does not reduce the overall reactivity of flies. Using environmental and genetic manipulations we found that sociability learning requires olfaction and the fearful reactions are driven by vision. To uncover neural circuits that subserve initially fearful reactions of isolated animals as well as those mediating subsequent learning, we next performed a neural silencing screen of 192 brain cell types. Our results show that specific cell types from the a/ß and a'/ß' lobes of the mushroom body subserve both initial fearful reactions as well as learned sociability. Brain connectomic analyses reveal direct synaptic connections between relevant cell types required for learned sociability in our screen and suggest a mechanistic model. We explored this model further by recording neural activity in relevant mushroom body circuits during the learning process over several hours during inter-fly interactions. Taken together, our results reveal that sociability toward conspecifics, an ethologically critical trait, is continuously learned rather than innate and that this learning engages specific subcircuits within a prominent associative learning and memory center in the fly.