Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord.
BACKGROUND
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 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.


RESULTS
Based 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.


CONCLUSIONS
Our 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.
Schindelman
Gary
G
Howard Hughes Medical Institute and Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA. garys@caltech.edu
Whittaker
Allyson J
AJ
Thum
Jian Yuan
JY
Gharib
Shahla
S
Sternberg
Paul W
PW
D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D002490:Central Nervous System / Q000166:cytology / Q000378:metabolism / Q000502:physiology*; D003307:Copulation / Q000502:physiology; D005260:Female; D005838:Genotype; D008164:Luminescent Proteins / Q000235:genetics / Q000378:metabolism; D008297:Male; D008954:Models, Biological; D009046:Motor Neurons / Q000166:cytology / Q000378:metabolism / Q000502:physiology; D009154:Mutation / Q000235:genetics; D010750:Phosphoproteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D012726:Sexual Behavior, Animal / Q000502:physiology*; D013094:Spermatozoa / Q000502:physiology; D013997:Time Factors; D033921:Vesicular Transport Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology
D029742:Caenorhabditis elegans Proteins; D008164:Luminescent Proteins; D010750:Phosphoproteins; C082636:Unc-18 protein, C elegans; D033921:Vesicular Transport Proteins