Genetic Regulation of Mating Behavior in C. elegan Males

Summary

Principal Investigator: LUIS R GARCIA
Abstract: DESCRIPTION (provided by applicant): The goal of this project is to understand how a step in a complex behavior is genetically specified. This fundamental problem will be addressed by studying C. elegans male mating behavior. During mating, the male executes a series of stereotyped sub-behaviors that result in the insertion of his copulatory spicules into his mate and the subsequent transfer of sperm. Although C. elegans male mating behavior consists of many steps, this project will focus on dissecting how the male inserts his spicules into his mate's vulva. Spicule insertion behavior is a simple reflex;however, the male nervous system and musculature must regulate many factors. The neurons and muscles must compute when to initiate the behavior and monitor if the behavioral outcome was successful. If an insertion attempt fails, the circuitry must re-initiate the behavior. If penetration is successful, the circuitry keeps the spicules inserted while the next behavioral step proceeds. Males display spicule insertion behavior only during mating. However, mutations can be generated that will cause males to display this behavior abnormally in the absence of mating cues. One of these mutations disrupts the C. elegans unc-103 gene. Unc-103 is the C. elegans homolog of the human h-erg-encoded voltage-gated delayed rectifying K+ channel. In humans, HERG channels regulate cardiac rhythm. Mutations in h-erg that reduce ion channel function can increase the probability of spontaneous lethal heart arrhythmias, a condition called long QT syndrome. Spicule insertion behavior requires coordination between different neurons and muscles. Mutations in unc-103 disrupt that regulation and result in spontaneous seizures of male-specific muscles that are used for copulation. To understand how unc-103 is used to regulate behavior, this project will identify where unc-103 is acting in the behavioral circuitry of males. The project will also determine the identities of mutations that affect candidate genes that may act with or in parallel to unc-103 to regulate behavior. Additionally, this project will identify components of activating pathways that must be attenuated by unc-103 during periods between mating.
Funding Period: 2003-09-15 - 2010-06-30
more information: NIH RePORT

Top Publications

  1. pmc A cholinergic-regulated circuit coordinates the maintenance and bi-stable states of a sensory-motor behavior during Caenorhabditis elegans male copulation
    Yishi Liu
    Department of Biology, Texas A and M University, College Station, Texas, United States of America
    PLoS Genet 7:e1001326. 2011
  2. pmc The effects of transient starvation persist through direct interactions between CaMKII and ether-a-go-go K+ channels in C. elegans males
    B Leboeuf
    Department of Biology, Texas A and M University, College Station, TX 77843 3258, USA
    Neuroscience 175:1-17. 2011
  3. pmc Sensory perception of food and insulin-like signals influence seizure susceptibility
    Todd R Gruninger
    Department of Biology, Texas A and M University, College Station, Texas, United States of America
    PLoS Genet 4:e1000117. 2008
  4. pmc Food deprivation attenuates seizures through CaMKII and EAG K+ channels
    Brigitte LeBoeuf
    Department of Biology, Texas A and M University, College Station, Texas, USA
    PLoS Genet 3:1622-32. 2007
  5. ncbi Molecular signaling involved in regulating feeding and other motivated behaviors
    Todd R Gruninger
    Department of Biology, Texas A and M University, TAMU 3258, College Station, TX, USA
    Mol Neurobiol 35:1-20. 2007
  6. ncbi G alpha(q)-coupled muscarinic acetylcholine receptors enhance nicotinic acetylcholine receptor signaling in Caenorhabditis elegans mating behavior
    Yishi Liu
    Department of Biology, Texas A and M University, College Station, Texas 77843 3258, USA
    J Neurosci 27:1411-21. 2007
  7. pmc Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes
    L Rene Garcia
    Department of Biology, Texas A and M University, College Station, Texas 77843 3258, USA
    Genetics 175:1761-71. 2007
  8. ncbi Behavioral genetics of caenorhabditis elegans unc-103-encoded erg-like K(+) channel
    David J Reiner
    Department of Genome Sciences, University of Washington, Seattle, WA, USA
    J Neurogenet 20:41-66. 2006
  9. ncbi Integration of male mating and feeding behaviors in Caenorhabditis elegans
    Todd R Gruninger
    Department of Biology, Texas A and M University, College Station, Texas 77843 3258, USA
    J Neurosci 26:169-79. 2006

Scientific Experts

  • LUIS R GARCIA
  • Todd R Gruninger
  • Brigitte LeBoeuf
  • Yishi Liu
  • Daisy G Gualberto
  • B Leboeuf
  • David J Reiner
  • Brigitte Lebeouf
  • Xiaoyan Guo
  • Robyn Lints
  • Paola A Correa
  • X Guo
  • Todd Gruninger
  • David Weinshenker
  • Hong Tian
  • Kiyoji Nishiwaki
  • Johji Miwa
  • James H Thomas

Detail Information

Publications10

  1. pmc A cholinergic-regulated circuit coordinates the maintenance and bi-stable states of a sensory-motor behavior during Caenorhabditis elegans male copulation
    Yishi Liu
    Department of Biology, Texas A and M University, College Station, Texas, United States of America
    PLoS Genet 7:e1001326. 2011
    ..We demonstrate that coordination of sensory inputs and motor outputs used to initiate, maintain, self-monitor, and complete an innate behavior is accomplished via the coupling of a few circuit components...
  2. pmc The effects of transient starvation persist through direct interactions between CaMKII and ether-a-go-go K+ channels in C. elegans males
    B Leboeuf
    Department of Biology, Texas A and M University, College Station, TX 77843 3258, USA
    Neuroscience 175:1-17. 2011
    ....
  3. pmc Sensory perception of food and insulin-like signals influence seizure susceptibility
    Todd R Gruninger
    Department of Biology, Texas A and M University, College Station, Texas, United States of America
    PLoS Genet 4:e1000117. 2008
    ..Insulin-like receptor signaling in the sex muscles then reduces cell excitability via activation of downstream molecules, including PLC-gamma and CaMKII...
  4. pmc Food deprivation attenuates seizures through CaMKII and EAG K+ channels
    Brigitte LeBoeuf
    Department of Biology, Texas A and M University, College Station, Texas, USA
    PLoS Genet 3:1622-32. 2007
    ..Our work suggests that upregulating mechanisms used by food deprivation can suppress muscle seizures...
  5. ncbi Molecular signaling involved in regulating feeding and other motivated behaviors
    Todd R Gruninger
    Department of Biology, Texas A and M University, TAMU 3258, College Station, TX, USA
    Mol Neurobiol 35:1-20. 2007
    ..These three molecules work to ensure that the proper behaviors are executed in response to the feeding state of an organism...
  6. ncbi G alpha(q)-coupled muscarinic acetylcholine receptors enhance nicotinic acetylcholine receptor signaling in Caenorhabditis elegans mating behavior
    Yishi Liu
    Department of Biology, Texas A and M University, College Station, Texas 77843 3258, USA
    J Neurosci 27:1411-21. 2007
    ..We propose that the GAR-3(mAChR)/G alpha(q) pathway sensitizes the spicule neurons and muscles before and during mating so that the male can respond to hermaphrodite vulva efficiently...
  7. pmc Diversity in mating behavior of hermaphroditic and male-female Caenorhabditis nematodes
    L Rene Garcia
    Department of Biology, Texas A and M University, College Station, Texas 77843 3258, USA
    Genetics 175:1761-71. 2007
    ....
  8. ncbi Behavioral genetics of caenorhabditis elegans unc-103-encoded erg-like K(+) channel
    David J Reiner
    Department of Genome Sciences, University of Washington, Seattle, WA, USA
    J Neurogenet 20:41-66. 2006
    ..In the egg-laying circuit, unc-103 is expressed in vulval muscles and the HSN neurons from different promoters. Supplying the proper UNC-103 isoform to the vulval muscles is sufficient to restore regulation to egg-laying behavior...
  9. ncbi Integration of male mating and feeding behaviors in Caenorhabditis elegans
    Todd R Gruninger
    Department of Biology, Texas A and M University, College Station, Texas 77843 3258, USA
    J Neurosci 26:169-79. 2006
    ..Additionally, unc-103-induced spicule protraction can be suppressed by reducing a pharyngeal-specific troponin T. These observations demonstrate that non-genitalia cells involved in feeding also mediate male sexual behaviors...