Sex, behavior and receptors

The mating of the fruit fly Drosophila melanogaster has been studied by geneticists and neurobiologists as a model for animal behavior. Drosophila courtship consists largely of the male exhibiting a stereotypical series of behaviors in pursuit of a female. The male first pursues the female by following her. If he is not rejected, he woos her by song, one that is sung by the rapid beatings of one of his wings. If still not rejected, the male will then lick the female's genitals and ultimately, mate. At any point in the courtship, the female may decide the suitor is unworthy, and frequently terminates the whole affair by kicking him in the face.

If the couple mates, the female now exhibits two important behaviors: she loses interest in additional matings and she starts to lay eggs. The post-mating behavior is regulated by a peptide in seminal fluid referred to as Sex Peptide (SP). This peptide controls behavior by transiting from the reproductive organs to the hemolymph, where SP can bind to specific receptors on neurons. Recently, Yapici et al. identified a receptor for SP by using an RNAi screen to identify small RNAs that would block the post-mating behavior, particularly by reducing egg laying. One RNAi inhibited egg laying and yielded females that continued to be receptive to sex despite a prior mating. The target gene of this RNAi encodes a receptor belonging to the family of guanine nucleotide binding protein (G-protein) coupled receptors. When SPR was expressed in a hamster cell line, the cells became responsive to Drosophila sex-peptide confirming that SP specifically activates SPR.

Immunofluroescent staining using an antibody against SPR revealed receptor protein in the female spermathecae (a site for long term sperm storage), the lower portion of the oviduct and in the central nervous system. In males, SPR expression was detected in the nervous system, but was absent from the male reproductive tract. Within the nervous system a portion of the SPR expression overlapped with neurons that also express the fruitless gene. When SPR protein was expressed only in those neurons expressing fruitless, complete wild-type post-mating behavior, and partial egg laying behavior, was restored. Curiously, fruitless is a transcription regulatory factor that plays a central role in controlling male courtship behavior, although it is expressed in both males and females. Fruitless mutant males fail to complete courtship behavior of females, and frequently court other males.

The importance of the paper by Yapici et al. is that it completes the circuitry between the male specific peptide and the receptor that modulates female behavior. As pointed out by the authors, this will provide insight into behavior regulation at several levels, including determining how SP interacts with SPR, how SPR controls neuronal activity, and how those neurons interact to manifest the female specific behaviors. In addition, the studies raise the question: what is the function of SPR in male neurons? If SPR expression in male neurons also overlaps with fruitless gene expression, perhaps SP also plays a role in controlling male specific courtship behaviors.

Another important point lies in the evolution of this receptor. Similar receptors can be identified in other insects; including mosquitoes, moths, and beetles by database searching using BLAST. It also turns out that the Drosophila Sex Peptide can activate receptors cloned from other insect species and direct injection of fruit fly SP into moths can stimulate post-mating behavior. The broad conservation across insect species of the behavior mediated by this receptor may provide new avenues for insect control. A common concern for any chemical that might control insect populations is the specificity of the agent. The conservation of the receptor across these genera suggests that it will be difficult to develop agents that target individual species
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A receptor that mediates the post-mating switch in Drosophila reproductive behavior
Nilay Yapici, Young-Joon Kim, Carlos Ribeiro & Barry J. Dickson
Nature doi:10.1038/nature06483

Biological Overview of Fruitless

Common functional elements of Drosophila melanogaster seminal peptides involved in reproduction of Drosophila melanogaster and Helicoverpa armigera females.