Sensory perception of dead conspecifics induces aversive cues and modulates lifespan through serotonin in Drosophila

Abstract

Sensory perception modulates health and aging across taxa. Understanding the nature of relevant cues and the mechanisms underlying their action may lead to novel interventions that improve the length and quality of life. We found that in the vinegar fly, Drosophila melanogaster , exposure to dead conspecifics in the environment induced cues that were aversive to other flies, modulated physiology, and impaired longevity. The effects of exposure to dead conspecifics on aversiveness and lifespan required visual and olfactory function in the exposed flies. Furthermore, the sight of dead flies was sufficient to produce aversive cues and to induce changes in the head metabolome. Genetic and pharmacologic attenuation of serotonergic signaling eliminated the effects of exposure on aversiveness and lifespan. Our results indicate that Drosophila have an ability to perceive dead conspecifics in their environment and suggest conserved mechanistic links between neural state, health, and aging; the roots of which might be unearthed using invertebrate model systems.

Social behavior and aging: A fly model

“…Recently, Chakraborty et al 100 report that mutants of tryptophan hydroxylase (an enzyme in serotonin synthesis) display an increased longevity, while either null mutants or hyper-activation of neurons expressing the serotonin receptor 5-HT2A cause a reduction in longevity. These authors 100 propose that serotonin is specifically implicated in a form of response to stress, whereby the flies' longevity is negatively affected by the perception of dead conspecifics, through serotonin signaling. 100 Total body serotonin levels do not appear to differ between males and females, 101 but serotonin levels during aging have not been assessed.…”

“…These authors 100 propose that serotonin is specifically implicated in a form of response to stress, whereby the flies' longevity is negatively affected by the perception of dead conspecifics, through serotonin signaling. 100 Total body serotonin levels do not appear to differ between males and females, 101 but serotonin levels during aging have not been assessed. The observed effect on longevity and behavior of serotonin suggests that serotonergic neurons could be also involved in aging related changes to physiology and behavior.…”

Cell non-autonomous regulation of health and longevity

“…Drosophila can visually perceive dead conspecifics in their environment and this perceptive experience induces both short- and long-term effects on health and longevity. Exposure to dead flies decreases resistance to starvation, depletes lipid storage, and shortens lifespan ( Chakraborty et al, 2019 ). As with protein perception, serotonin signaling via receptor 5-HT2A is required for death perception to influence lifespan.…”

Social Perception of Young Adults Prolongs the Lifespan of Aged Drosophila

“…Flies with defective or83b gene are anosmic and live longer, especially in the mutant female flies ( Fig. 4A) (8,18,19). Given the longer lifespan of or83b mutant flies, we included the 60d-old, but not the 40d-old, mutants in the co-housing experiments.…”