Abstract
BackgroundThe Caenorhabditis elegans male exhibits a stereotypic behavioral pattern when attempting to mate. This behavior has been divided into the following steps: response, backing, turning, vulva location, spicule insertion, and sperm transfer. We and others have begun in-depth analyses of all these steps in order to understand how complex behaviors are generated. Here we extend our understanding of the sperm-transfer step of male mating behavior.ResultsBased on observation of wild-type males and on genetic analysis, we have divided the sperm-transfer step of mating behavior into four sub-steps: initiation, release, continued transfer, and cessation. To begin to understand how these sub-steps of sperm transfer are regulated, we screened for ethylmethanesulfonate (EMS)-induced mutations that cause males to transfer sperm aberrantly. We isolated an allele of unc-18, a previously reported member of the Sec1/Munc-18 (SM) family of proteins that is necessary for regulated exocytosis in C. elegans motor neurons. Our allele, sy671, is defective in two distinct sub-steps of sperm transfer: initiation and continued transfer. By a series of transgenic site-of-action experiments, we found that motor neurons in the ventral nerve cord require UNC-18 for the initiation of sperm transfer, and that UNC-18 acts downstream or in parallel to the SPV sensory neurons in this process. In addition to this neuronal requirement, we found that non-neuronal expression of UNC-18, in the male gonad, is necessary for the continuation of sperm transfer.ConclusionOur division of sperm-transfer behavior into sub-steps has provided a framework for the further detailed analysis of sperm transfer and its integration with other aspects of mating behavior. By determining the site of action of UNC-18 in sperm-transfer behavior, and its relation to the SPV sensory neurons, we have further defined the cells and tissues involved in the generation of this behavior. We have shown both a neuronal and non-neuronal requirement for UNC-18 in distinct sub-steps of sperm-transfer behavior. The definition of circuit components is a crucial first step toward understanding how genes specify the neural circuit and hence the behavior.
Highlights
The Caenorhabditis elegans male exhibits a stereotypic behavioral pattern when attempting to mate
No gross changes in morphology were observed, except for the exit of sperm from the seminal vesicle, through the 'valve region', and into the tube formed by the vas deferens
The expression in the rays appears to be in the A-type ray neurons, as acr-5 expression in the tail does not overlap with pkd-2::GFP, which is expressed in the B-type ray neurons [10]. acr-5 shows expression in a cell in the right preanal ganglion, which we have tentatively identified as PGA or PVZ
Summary
The Caenorhabditis elegans male exhibits a stereotypic behavioral pattern when attempting to mate. This behavior has been divided into the following steps: response, backing, turning, vulva location, spicule insertion, and sperm transfer. We extend our understanding of the sperm-transfer step of male mating behavior. Male mating behavior in C. elegans affords the opportunity to study a complex multistep behavior in an organism with a relatively simple nervous system. If the male's tail reaches the end of the hermaphrodite before encountering the vulva, the male turns and continues scanning the other side. When the vulva is located, the male ceases backward motion, prods with his copulatory spicules, inserts them into the vulva, and transfers sperm into the uterus [3,4,5,6]. The steps of reproductive behavior have been described in many organisms, relatively little is known about the genes that control these behaviors [7]
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