Threat induces changes in cardiac activity and metabolism negatively impacting survival in flies

Abstract

Adjusting to a dynamic environment involves fast changes in the bodys internal state, characterized by coordinated alterations in brain activity, physiological and motor responses. Threat-induced defensive states are a classic example of coordinated adjustment of bodily responses, being cardiac regulation one of the best characterized in vertebrates. A great deal is known regarding the neural basis of invertebrate defensive behaviours, mainly in Drosophila melanogaster. However, whether physiological changes accompany these remains unknown. Here, we set out to describe the internal bodily state of fruit flies upon an inescapable threat and found cardiac acceleration during running and deceleration during freezing. In addition, we found that freezing leads to increased cardiac pumping from the abdomen towards the head-thorax, suggesting mobilization of energy resources. Concordantly, threat-triggered freezing reduces sugar levels in the hemolymph and renders flies less resistant to starvation. The cardiac responses observed during freezing were absent during spontaneous immobility, underscoring the active nature of freezing response. Finally, we show that baseline cardiac activity predicts the amount of freezing upon threat. This work reveals a remarkable similarity with the cardiac responses of vertebrates, suggesting an evolutionarily convergent defensive state in flies. Our findings are at odds with the widespread view that cardiac deceleration while freezing has first evolved in vertebrates and that it is energy sparing. Investigating the physiological changes coupled to defensive behaviours in the fruit fly has revealed that freezing is costly, yet accompanied by cardiac deceleration, and points to heart activity as a key modulator of defensive behaviours.