Sex and Death: Identification of Feedback Neuromodulation Balancing Reproduction and Survival

Abstract

Some semelparous organisms in nature mate as many times as they can in a single reproductive episode before death, while most iteroparous species including humans avoid such suicidal reproductive behavior. Animals naturally pursue more sex and the possible fatal consequence of excessive sex must be orchestrated by negative feedback signals in iteroparous species, yet very little is known about the regulatory mechanisms. Here we used Drosophila male sexual behavior as a model system to study how excessive sex may kill males and how the nervous system reacts to prevent death by sex. We found that continuous sexual activity by activating the fruitlessexpressing neurons induced a fixed multi-step behavioral pattern ending with male death. We further found negative feedback in the fly brain to prevent suicidal sexual behavior by expression changes of the neurotransmitters acetylcholine and gamma-aminobutyric acid, and neuropeptide F. These findings are crucial to understand the molecular underpinnings of how different organisms choose reproductive strategies and balance reproduction and survival.

Hormonal control of motivational circuitry orchestrates the transition to sexuality in Drosophila

“…In work from the Montell laboratory, male-specific NPF neurons were reported to decrease sexual motivation generally and to prevent male-male courtship in particular (55). These conclusions appear to be in direct contrast with the courtship-promoting roles for these same NPF neurons we described here and previously (14), as well as with earlier findings from the Park laboratory (56), although they are in line with recent results from the Pan laboratory (57). The results obtained across these four laboratories are derived from a variety of assays and genetic manipulations, complicating direct comparisons, although they clearly point to multiple roles for NPF in courtship target selection and motivation.…”

“…The results obtained across these four laboratories are derived from a variety of assays and genetic manipulations, complicating direct comparisons, although they clearly point to multiple roles for NPF in courtship target selection and motivation. While several experiments have argued for various forms of hypersexuality resulting from decreased NPF signaling ( 55 , 57 ), the lone NPF neuronal stimulation experiment to yield a reduction in courtship behavior assessed courtship toward decapitated females and the effect was modest [figure 4B in ( 55 )]. The robust effects we see [ Fig.…”

Neural Control of Action Selection Among Innate Behaviors

“…Furthermore, mating increases NPF expression in male flies [ 138 ]. Interestingly, while NPF serves as a reward signal of sex, it also prevents further courtship in frequently-mated males [ 75 , 139 ], suggesting that NPF may be a modulator to switch behavior between sex and rest.…”

Serotonin Signaling Modulates Sexual Receptivity of Virgin Female Drosophila

“…Drosophila sexual behaviors include stereotypic male courtship rituals such as orienting to a female, extending an ipsilateral wing to produce courtship songs, tapping and licking the female, attempting copulation, and finally copulation [6,7]. The neural circuit involved in male courtship behavior has been dissected in recent years owing to advances in genetic technology [8][9][10][11]. However, studies on female sexual behavior are far fewer than those on males.…”