Skip to main content
SpringerLink
Log in

The behavioral genetics ofCaenorhabditis elegans

  • Articles
  • Published:
Behavior Genetics Aims and scope Submit manuscript

Abstract

Caenorhabditis elegans, a small free-living soil nematode, is an ideal organism for the genetic dissection of simple behaviors. Over 150 genes required for normal behavior have been identified. We review here the neural and genetic pathways underlying four of the best-studiedC. elegans behaviors: locomotion, response to gentle touch, egg-laying, and chemotaxis. Mutations affecting these behaviors have identified genes which specify neuronal cell lineage, neuronal cell fate, and the formation of cell matrix cues involved in axonal guidance. Molecular analysis of genes required for normal behavior offers the prospect of characterizing functionally important nervous system proteins, regardless of their abundance or biochemical role.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Albertson, D. G., and Thomson, J. N. (1976). The pharynx ofCaenorhabditis elegans.Phil. Trans. R. Soc. Lond. B 275:299–325.

    Google Scholar 

  • Boucaut, J.-C., Danibere, T., Poole, T. J., Aoyama, H., Yamada, K., and Thiery, J. P. (1984). Biologically active synthetic peptides as probes of embryonic development: A competitive peptide inhibitor of fibronectin function inhibits gastrulation in amphibian embryos and neural crest cell migration in avian embryos.J. Cell Biol. 99:18822–1830.

    Google Scholar 

  • Brenner, S. (1974). The genetics ofCaenorhabditis elegans.Genetics 77:71–94.

    Google Scholar 

  • Caddy, K. W. T., and Biscoe, T. J. (1979). Structural and quantitative studies on the normal C3H andLurcher mutant mouse.Phil. Trans. Roy. Soc. B 287:167–201.

    Google Scholar 

  • Cassada, R. C., and Russell, R. L. (1975). The dauer larva, a post-embryonic developmental variant of the nematodeCaenorhabditis elegans.Dev. Biol. 46:326–342.

    Google Scholar 

  • Chalfie, M. (1982). Microtubule structure inCaenorhabditis elegans neurons.Cold Spring Harbor Symp. Quant. Biol. 46:255–261.

    Google Scholar 

  • Chalfie, M., and Au, M. (1988). Genetic control of differentiation of theCaenorhabditis elegans touch receptor neurons.Science 243:1027–1033.

    Google Scholar 

  • Chalfie, M., and Sulston, J. (1981). Developmental genetics of the mechanosensory neurons ofCaenorhabditis elegans.Dev. Biol. 82:358–370.

    Google Scholar 

  • Chalfie, M., and Thomson, J. N. (1979). Organization of neuronal microtubules in the nematodeCaenorhabditis elegans.J. Cell Biol. 82:278–289.

    Google Scholar 

  • Chalfie, M., and White, J. (1988). The nervous system. In Wood, W. (ed.),The Nematode Caenorhabditis elegans, Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp. 337–391.

    Google Scholar 

  • Chalfie, M., Horvitz, H. R., and Sulston, J. E. (1981). Mutations that lead to reiterations in the cell lineages ofC. elegans.Cell 24:59–69.

    Google Scholar 

  • Chalfie, M., Sulston, J. E., White, J. G., Southgate, E., Thomson, J. N., and Brenner, S. (1984). The neural circuits for touch sensitivity inCaenorhabditis elegans.J. Neurosci 5: 956–964.

    Google Scholar 

  • Coulson, A., Sulston, J., Brenner, S., and Karn, J. (1986). Towards a physical map of the genome of the nematodeCaenorhabditis elegans.Proc. Natl. Acad. Sci. USA 83:7821–7825.

    Google Scholar 

  • Coulson, A., Waterston, R., Kiff, J., Sulston, J., and Kohara, Y. (1988). Genome linking with yeast artificial chromosomes.Nature 335:184–186.

    Google Scholar 

  • Culotti, J. G., and Russell, R. L. (1978). Osmotic avoidance defective mutants of the nematodeCaenorhabditis elegans.Genetics 90:243–256.

    Google Scholar 

  • Desai, C., Garriga, G., McIntire, S. L., and Horvitz, H. R. (1988). A genetic pathway for the development of theCaenorhabditis elegans HSN motorneurons.Nature 336:638–646.

    Google Scholar 

  • Duband, J. L., Tucker, G. C., Poole, T. J., Vincent, M., Aoyama, H., and Thiery, J. P. (1985). How do the migratory and adhesive properties of the neural crest govern ganglia formation in the avian peripheral nervous system?J. Cell. Biochem. 27:189–203.

    Google Scholar 

  • Dusenberry, D. B., Sheridan, R. E., and Russell, R. L. (1975). Chemotaxis defective mutants of the nematodeCaenorhabditis elegans.Genetics 80:297–309.

    Google Scholar 

  • Ferguson, E. L., and Horvitz, H. R. (1985). Identification and characterization of 22 genes that affect the vulval cell lineages of the nematodeCaenorhabditis elegans.Genetics 110:17–72.

    Google Scholar 

  • Fire, A. (1986). Integrative transformation ofCaenorhabditis elegans.EMBO J. 5:2673–2680.

    Google Scholar 

  • Garcia-Bellido, A. (1975). Genetic control of wing development inDrosophila.Ciba Found. Symp. 29:161–182.

    Google Scholar 

  • Gehring, W. J. (1987). Homeo boxes in the study of development.Science 236:1245–1252.

    Google Scholar 

  • Golden, J. W., and Riddle, D. L. (1982). A pheromone influences larval development in the nematodeCaenorhabditis elegans.Science 218:578–580.

    Google Scholar 

  • Greenwald, I. S., Sternberg, P. W., and Horvitz, H. R. (1983). Thelin-12 locus specifies cell fate inCaenorhabditis elegans.Cell 34:435–444.

    Google Scholar 

  • Gundersen, R. W. (1987). Response of sensory neurites and growth cones to patterned substrata of laminin and fibronectinin vitro.Dev. Biol. 121:423–431.

    Google Scholar 

  • Hall, D. (1977).The Posterior Nervous System of Caenorhabditis elegans, Ph.D. thesis, California Institute of Technology, Pasadena.

    Google Scholar 

  • Hammarback, J. A., McArthy, J. B., Palm, S. L., Furcht, L. T., and Letorneau, P. C. (1988). Growth cone guidance by substrate-bound laminin pathways is correlated with neuron-to-pathway adhesivity.Dev. Biol. 126:29–39.

    Google Scholar 

  • Hedgecock, E. M., and Russell, R. L. (1975). Normal and mutant thermotaxis in the nematode,Caenorhabditis elegans.Proc. Natl. Acad. Sci. USA 72:4061–4065.

    Google Scholar 

  • Hedgecock, E. M., Culotti, J. G., Thomson, J. N., and Perkins, L. A. (1985). Axonal guidance mutants ofCaenorhabditis elegans identified by filling neurons with fluorescein dyes.Dev. Biol. 111:158–170.

    Google Scholar 

  • Hedgecock, E., Culotti, J., Hall, D., and Stern, B. (1987). Genetics of cell and axon migration inCaenorhabditis elegans.Development 100:365–382.

    Google Scholar 

  • Hodgkin, J. (1983). Male phenotypes and mating efficiency inCaenorhabditis elegans.Genetics 103:43–64.

    Google Scholar 

  • Horvitz, H. R., Chalfie, M., Trent, C., Sulston, J. E., and Evans, P. D. (1982). Serotonin and octopamine in the nematodeCaenorhabditis elegans.Science 216:1012–1014.

    Google Scholar 

  • Johnson, C. D., and Stretton, A. O. W. (1980). Neural control of locomotion inAscaris: Anatomy, electrophysiology and biochemistry. In Zukerman, B. (ed.),Nematodes as Biological Models, Academic Press, New York.

    Google Scholar 

  • Lewis, J. A., and Hodgkin, J. A. (1977). Specific neuroanatomical changes in chemosensory mutants of the nematodeCaenorhabditis elegans.J. Comp. Neurol. 172:489–510.

    Google Scholar 

  • Lewis, J. A., Wu, C. H., and Berg, H. (1980a). The genetics of levamisole resistance in the nematodeCaenorhabditis elegans.Genetics 95:905–928.

    Google Scholar 

  • Lewis, J. A., Wu, C. H., Levine, J. H., and Berg, H. (1980b). Levamisole resistant mutants of the nematodeCaenorhabditis elegans appear to lack pharmacological acetylcholine receptors.Neuroscience 5:967–989.

    Google Scholar 

  • Lewis, J. A., Elmer, J. S., Skimming, J., McLafferty, S., Fleming, J., and McGee, T. (1987). Cholinergic receptor mutants of the nematodeCaenorhabditis elegans.J. Neurosci. 7: 3059–3071.

    Google Scholar 

  • Ma, J., and Ptashne, M. (1987a). Deletion analysis of GAL4 defines two transcriptional activating segments.Cell 48:847–853.

    Google Scholar 

  • Ma, J., and Ptashne, M. (1987b). A new class of yeast transcriptional activators.Cell 51:113–119.

    Google Scholar 

  • MacLeod, A. R., Karn, J., and Brenner, S. (1981). Molecular analysis of theunc-54 myosin heavy chain gene ofCaenorhabditis elegans.Nature 291:386–390.

    Google Scholar 

  • Moerman, D. G., Plurad, S., Waterston, R. H., and Baillie, D. L. (1982). Mutations in theunc-54 myosin heavy chain gene ofCaenorhabditis elegans that alter contractility but not muscle structure.Cell 29:773–781.

    Google Scholar 

  • Moerman, D. G., Benian, G. M., and Waterston, R. H. (1986). Molecular cloning of the muscle geneunc-22 inCaenorhabditis elegans by Tc1 transposon tagging.Proc. Natl. Acad. Sci. 83:2579–2583.

    Google Scholar 

  • Perkins, L. A., Hedgecock, E. M., Thomson, J. N., and Culotti, J. G. (1986). Mutant sensory cilia in the nematodeCaenorhabditis elegans.Dev. Biol. 117:456–487.

    Google Scholar 

  • Rand, J. B., and Russell, R. L. (1984). Choline acetyltransferase-deficient mutants of the nematodeCaenorhabditis elegans.Genetics 106:227–248.

    Google Scholar 

  • Riddle, D. L. (1977). A genetic pathway for dauer larva formation inCaenorhabditis elegans.Stadler Genet. Symp. 9:101–120.

    Google Scholar 

  • Riddle, D. L. (1988). The dauer larva. In Wood, W. (ed.),The Nematode Caenorhabditis elegans, Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.

    Google Scholar 

  • Riddle, D. L., Swanson, M. M., and Albert, P. S. (1981). Interacting genes in dauer nematode dauer larva formation.Nature 290:668–671.

    Google Scholar 

  • Savage, C., Hamelin, M., Culotti, J., Coulson, A., Albertson, D. G., and Chalfie, M. (1989).mec-7 is a beta tubulin gene required for the production of 15 protofilament microtubules inC. elegans.Genes Dev. 3:870–881.

    Google Scholar 

  • Sulston, J., and Brenner, S. (1974). The DNA ofCaenorhabditis elegans.Genetics 77:95–104.

    Google Scholar 

  • Sulston, J. E., and Horvitz, H. R. (1981). Abnormal cell lineages in mutants of the nematodeCaenorhabditis elegans.Dev. Biol. 82:41–55.

    Google Scholar 

  • Trent, C. (1983). Ph.D. thesis, Massachusetts Institute of Technology, Cambridge.

  • Trent, C., Tsung, N., and Horvitz, H. R. (1984). Egg-laying defective mutants of the nematodeCaenorhabditis elegans.Genetics 104:619–647.

    Google Scholar 

  • Walrond, J. P., and Stretton, A. O. W. (1985). Excitatory and inhibitory activity in the dorsal musculature of the nematodeAscaris evoked by single dorsal excitatory motoneurons.J. Neurosci. 5:16–23.

    Google Scholar 

  • Walrond, J. P., Kass, I. S., Stretton, A. O. W., and Donmeyer, J. E. (1985). Identification of excitatory and inhibitory motoneurons in the nematodeAscaris by electrophysiological techniques.J. Neurosci. 5:1–8.

    Google Scholar 

  • Ward, S. (1973). Chemotaxis by the nematodeCaenorhabditis elegans: Identification of attractants and analysis of the response by the use of mutants.Proc. Natl. Acad. Sci. USA 70:817–821.

    Google Scholar 

  • Ward, S., Thomson, N., White, J. G., and Brenner, S. (1975). Electron microscopical reconstruction of the anterior sensory anatomy of the nematode,Caenorhabditis elegans.J. Comp. Neurol. 160:313–338.

    Google Scholar 

  • Ware, R. W., Clark, C., Crossland, K., and Russell, R. L. (1975). The nerve ring of the nematode,Caenorhabditis elegans.J. Comp. Neurol. 162:71–110.

    Google Scholar 

  • Waterston, R. H., Fishpool, R. M., and Brenner, S. (1977). Mutations affecting paramyosin inCaenorhabditis elegans.J. Mol. Biol. 117:679–697.

    Google Scholar 

  • Waterston, R. H., Thomson, J. N., and Brenner, S. (1980). Mutants with altered muscle structure inCaenorhabditis elegans.Dev. Biol. 77:271–302.

    Google Scholar 

  • Way, J., and Chalfie, M. (1988).mec-3, a homeobox-containing gene that specifies differentiation of the touch receptor neurons inC. elegans.Cell 54:5–16.

    Google Scholar 

  • White, J. G., Southgate, E., Thomson, J. N., and Brenner, S. (1976). The structure of the ventral nerve cord ofCaenorhabditis elegans.Phil. Trans. R. Soc. Lond. B 275:327–348.

    Google Scholar 

  • White, J. G., Southgate, E., Thomson, J. N., and Brenner, S. (1988). The structure of the nervous system of the nematode.Phil. Trans. R. Soc. Lond. B 314:1–340.

    Google Scholar 

Download references

Author information

Author notes

  1. Eve Wolinsky

    Present address: Department of Biochemistry, New York University Medical School, 550 First Avenue, MSB 359, 10016, New York, New York

Authors and Affiliations

  1. Department of Biology, Nelson Labs, Rutgers University (Piscataway), 08855-1059, Piscataway, NJ

    Jeffrey Way

Authors
  1. Eve Wolinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeffrey Way
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

E. Wolinsky was supported by the Huntington's Disease Society of America and J. Way was supported by National Institutes of Health Post-doctoral Fellowship HD06983 during the preparation of the manuscript.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wolinsky, E., Way, J. The behavioral genetics ofCaenorhabditis elegans . Behav Genet 20, 169–189 (1990). https://doi.org/10.1007/BF01067789

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01067789

Key Words

Search

Navigation