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

BMC Biol. 2006 Aug 15;4:26. doi: 10.1186/1741-7007-4-26.

Abstract

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.

Conclusion: 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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Caenorhabditis elegans Proteins / physiology
  • Central Nervous System / cytology
  • Central Nervous System / metabolism
  • Central Nervous System / physiology*
  • Copulation / physiology
  • Female
  • Genotype
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Male
  • Models, Biological
  • Motor Neurons / cytology
  • Motor Neurons / metabolism
  • Motor Neurons / physiology
  • Mutation / genetics
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism
  • Phosphoproteins / physiology
  • Sexual Behavior, Animal / physiology*
  • Spermatozoa / physiology
  • Time Factors
  • Vesicular Transport Proteins / genetics
  • Vesicular Transport Proteins / metabolism
  • Vesicular Transport Proteins / physiology

Substances

  • Caenorhabditis elegans Proteins
  • Luminescent Proteins
  • Phosphoproteins
  • Unc-18 protein, C elegans
  • Vesicular Transport Proteins