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Ferreira, C. H.

Publications and source records attributed to Ferreira, C. H..

3 recordsLinked to original sources

Neuronal sex identity shapes social buffering of defensive freezing behaviour in fruit flies

Sex differences are pervasive across the animal kingdom1,2, shaped by reproductive strategies, ecological roles, and physiological demands. Neurobiological studies have largely focused on sex differences in reproduction and aggression3,4, leaving understudied how sex shapes other survival-relevant behaviours such as responses to predatory threats. Previous work in vertebrates uncovered sex differences in individual defence responses deployed by rats5 and in social modulation of freezing responses in zebrafish6. The origin of these differences and their potential underlying neuronal circuitry remain however unknown. Here we characterise defensive responses to a visual threat of female and male fruit flies tested alone and in groups. Individually, defensive responses are comparable across sex, with similar freezing levels and moderately increased escape responses in males. In groups, however, we uncovered strong sex differences in freezing as males show consistently shorter freezing bouts, reflecting a stronger social buffering effect than in females. Using a generalised linear mixed model, we demonstrate that the shorter freezes of male flies, when tested in groups, are not explained by well-known locomotor differences between sexes7,8. Although males move more and faster, generating stronger social motion cues that mediate the "safety in numbers" effect in female flies9,10, their response to the surrounding motion is not increased. We further identify the nervous system as the source of this sex-dimorphic behaviour by feminising males through pan-neuronal ectopic expression of transformer, a key regulator of the cell-autonomous sex-differentiation pathway. Finally, we ruled out the visual projection neurons, lobula columnar neurons 11 (LC11), detectors of social motion10, as the source of the neuronal-sex differences observed. This study identifies a neuronal origin of sex differences in socially modulated behaviour that extends beyond sex-specific behavioural modules or locomotor function, important to understand differential impact on survival upon threat across sexes.

neuroscience↗

Social cues of safety can override differences in threat level

Animals in groups integrate social information with that directly-gathered about the environment to guide decisions regarding reproduction, foraging and defense against predatory threats. In the context of predation, usage of social information has acute fitness benefits, aiding the detection of predators, the mounting of concerted defensive responses, or allowing the inference of safety, permitting other beneficial behaviors such as foraging for food. Individual and group defense responses to predatory threats can vary in modality and vigor depending on the perceived threat level. Moreover, predation level has been shown to modulate the use of social cues about foraging sites. Whether and how different threat levels affect the use of social cues to guide defense responses, is currently unknown. We previously showed that Drosophila melanogaster display a graded decrease in freezing behavior, triggered by an inescapable visual threat, with increasing group sizes. Crucially, we identified the movement of others as a cue of safety and its cessation a cue of threat and found the group responses to be primarily guided by the safety cues, resulting in a net social buffering effect. Here, we investigated how threat level impacts the use of social cues by exposing flies individually and in groups to two threat imminences using looms of different speeds. We show that freezing responses are stronger to the faster looms regardless of social condition. However, social buffering was stronger for groups exposed to the fast looms, such that the increase in freezing caused by the higher threat was less prominent in flies tested in groups than those tested individually. Through artificial control of behavior, we created different group compositions, titrating the motion cues that were maintained across threat levels. We, found that the same level of safety motion cues had a bigger weight on the flies decisions when these were exposed to the higher threat, thus overriding differences in perceived threat levels. These findings shed light on the safety in numbers effect, revealing the modulation of the saliency of social safety cues across threat intensities, a possible mechanism to regulate costly defensive responses.

neuroscience↗

Safety in numbers is mediated by motion cues and depends on lobula columnar neurons in Drosophila melanogaster

Living in a group allows individuals to decrease their defenses enabling other beneficial behaviors such as foraging. The detection of a threat through social cues is widely reported, however the safety cues that guide animals to break away from a defensive behavior and resume alternate activities remain elusive. Here we show that fruit flies displayed a graded decrease in freezing behavior, triggered by an inescapable threat, with increasing group sizes. Furthermore, flies used the cessation of movement of other flies as a cue of threat and its resumption as a cue of safety. Finally, we found that lobula columnar neurons, LC11, mediate the propensity for freezing flies to resume moving in response to the movement of others. By identifying visual motion cues, and the neurons involved in their processing, as the basis of a social safety cue this study brings new insights into the neuronal basis of safety in numbers.

neuroscience↗