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Drosophila Life Span and Physiology Are Modulated by Sexual Perception and Reward

Science  31 Jan 2014:
Vol. 343, Issue 6170, pp. 544-548
DOI: 10.1126/science.1243339

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Battle of the Sexes

In many species, males compete with one another to propagate their own DNA, often to the detriment of females (see the Perspective by Promislow and Kaeberlein). Shi and Murphy (p. 536, published online 19 December) discovered that mating in Caenorhabditis species causes mothers to shrink and die soon after they have ceased producing progeny. Males appear to hijack the longevity and stress resistance pathways normally employed by the mothers to slow reproduction and somatic aging in times of stress. Maures et al. (p. 541, published online 29 November) explored why the presence of abundant mating-competent males causes a decrease in the life span of nematodes of the opposite sex and found that a secreted substance, possibly a pheromone, reproduced the effect of the males when transferred in the culture medium. Detection of pheromones from a female fruit fly is enough to cause changes in metabolism, reduce resistance to starvation, and shorten the life span of male flies. Gendron et al. (p. 544, published online 29 November) report that the signals from the female appear to be recognized by sensory receptors on the legs of male flies.

Abstract

Sensory perception can modulate aging and physiology across taxa. We found that perception of female sexual pheromones through a specific gustatory receptor expressed in a subset of foreleg neurons in male fruit flies, Drosophila melanogaster, rapidly and reversibly decreases fat stores, reduces resistance to starvation, and limits life span. Neurons that express the reward-mediating neuropeptide F are also required for pheromone effects. High-throughput whole-genome RNA sequencing experiments revealed a set of molecular processes that were affected by the activity of the longevity circuit, thereby identifying new candidate cell-nonautonomous aging mechanisms. Mating reversed the effects of pheromone perception; therefore, life span may be modulated through the integrated action of sensory and reward circuits, and healthy aging may be compromised when the expectations defined by sensory perception are discordant with ensuing experience.

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