Our research focuses on cell fate specification, nervous system development, evolution of developmental programs, and sexual behavior. These related studies have utilized the C. elegans male to investigate universal problems in animal biology.  Genetic analysis of the male is facilitated by the fact that male-defective strains can be propagated through self-fertilization of the hermaphrodite.  Our primary approach has been to isolate mutations that cause abnormal development or aberrant behavior of the C. elegans male and to study them to identify the genes that specify the male phenotype and to understand how these genes work.

Cell Fate Specification

Specification of correct cell fates is a central process in the development of differentiated structures. Many mutations we identified causing abnormality in development of the C. elegans male affected the specification of cell fates in the cell lineages leading to male-specific structures. We have focused specifically on those mutations affecting the male rays, sensory structures projecting out on both sides of the male tail. We have studied the functions of the genes defined by these mutations to understand how cell fates are allocated in a cell lineage.
c. elegans mating
The male C. elegans uses his tail to locate the vulva of the hermaphrodite.
Key Findings
  • A cell fate specification program occurring during postembryonic cell lineages, involving, in part, the regulated expression of Hox genes, is the central developmental process that determines the identities of sensory structures and the morphology of the tail.
c. elegans male tail
The fan and rays of the C. elegans male tail.
Baird, S.E., Fitch, D.H.A., Kassem, I.A.A., and Emmons, S.W. (1991) Pattern formation in the nematode epidermis: determination of the spatial arrangement of peripheral sense organs in the C. elegans male tail. Development, 113, 515-526.
Chow, K.L., and Emmons, S.W. (1994) HOM-C/Hox genes and four interacting loci determine the morphogenetic properties of single cells in the nematode male tail. Development 120, 2579-2593.
Ferreira, H.B., Zhang, Y., Zhao, C., and Emmons, S.W. (1999) Patterning of Caenorhabditis elegans posterior structures by the Abdominal-B homolog, egl-5. Dev. Biol. 207, 215-228. 90 [PDF]
  • Specification of the neuroblast cell fate as well as the properties of differentiated neurons requires transcription factors of the bHLH family related to atonal and daughterless of Drosophila and similar transcription factors in vertebrates.
Zhao, C., and Emmons, S.W. (1995) A transcription factor controlling development of peripheral sense organs in C. elegans. Nature 373, 74-78.
Portman, D.S., and Emmons, S.W. (2000) The basic helix-loop-helix transcription factors LIN-32 and HLH-2 function together in multiple steps of a C. elegans neuronal sublineage. Development 127, 5415-5426. [PDF]
  • A Pax6 gene, noted in other species for its role in eye development, specifies sensory organ identity in the male tail.
Zhang, Y., and Emmons, S.W. (1995) Specification of sense-organ identity by a Caenorhabditis elegans Pax6 homologue. Nature 377, 55-59.
  • Components of the Mediator Complex, a multiprotein complex that acts with the core RNA polymerase in transcription, are essential elements of a regulatory mechanism for directing Hox gene transcription to specific branches of postembryonic cell lineages.
Zhang, H., and Emmons, S.W. (2000) A C. elegans Mediator protein confers regulatory selectivity on lineage-specific expression of a transcription factor gene. Genes and Development 14, 2161-2172. [PDF]
Zhang, H., and Emmons, S. W. (2001) The novel C. elegans gene sop-3 modulates Wnt signaling to regulate Hox gene expression. Development 128, 767-777. [PDF]
  • In C. elegans, a novel protein (SOP-2) appears to have taken over the function of one type of Polycomb gene in limiting Hox gene transcription to specific body regions.
Zhang, H., Azevedo, R. B. R., Lints, R., Doyle, C., Teng, Y., Haber, D., and Emmons, S. W. (2003) Global regulation of Hox gene expression in C. elegans by a SAM-domain protein. Dev. Cell 4, 903-915. [PDF] (Commentaries: Pires-daSilva, A., and Sommer, R. J. (2003) Dev. Cell 4, 770-772; Baxter, C. (2003) Nature Reviews, Genetics, 4, 491.)
Zhang, H., Cristoforou, A., Aravind, L., Emmons, S. W., van den Heuvel, S., and Haber, D. A. (2004) Polycomb group proteins directly bind to RNA. Mol. Cell 14, 841-847. [PDF]

Nervous System Development

Once their fates are correctly specified, cells differentiate to provide the specialized functions of organs and tissues. These two connected processes, cell fate specification and cell differentiation, are particularly crucial in the nervous system, where each of the many individual neurons may have distinct properties. The sensory nervous system of the C. elegans male tail has provided an opportunity to explore how patterning genes define the properties of neurons and for identifying downstream target genes.
Key Findings
  • The combined activities of Hox genes and a TGFβ signal specify the spatial patterning of neuron subtype identity. Subtype identity governs multiple neuronal properties including expression of dopamine, serotonin, and multiple neuropeptide neurotransmitters.
Lints, R., and Emmons, S.W. (1999) Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFβ family signaling pathway and a Hox gene. Development 126, 5819-5831. [PDF]
Lints, R., Jia, L., Kim, K., Li, C., and Emmons, S. W. (2004) Axial patterning of C. elegans male sensilla identities by selector genes. Dev. Biol. 269, 137-151. [PDF]
  • Conserved ephrin and semaphorin proteins, which are essential for patterning in the vertebrate nervous system, are required for specifying the morphogenesis of individual C. elegans sensory structures.
Hahn, A., and Emmons, S. W. (2003) The roles of an ephrin and a semaphorin in patterning cell-cell contacts in C. elegans sensory organ development. Dev. Biol. 256, 379-388. [PDF]
  • A DM domain transcription factor, possibly representing an ancient, conserved sex-determination gene family, is required for multiple aspects of differentiation of the male nervous system. Transcription factors of this family also appear to be required for male development in mammals.
Lints, R., and Emmons, S. W. (2002) Regulation of sex-specific differentiation and mating behavior in C. elegans by a new member of the DM domain transcription factor family. Genes and Dev. 16, 2390-2402. [PDF]
(Commentary: Hodgkin, J (2002) Genes and Dev. 16, 2322-2326.)
  • Microarray studies have allowed the identification of new genes required for the differentiation of the ray sensory structures.
Portman, D. S., and Emmons, S. W. (2004) Identification of C. elegans sensory ray genes using whole-genome expression profiling. Dev. Biol. 270, 499-512. [PDF]
  • Previously known genes as well as novel genes are both required for axon pathfinding by the ray neurons.
Jia, L., and Emmons, S. W. (2006) Genes that control ray sensory neuron axon development in the Caenorhabditis elegans male. Genetics 173, 1241-1258.
Nematodes, though they comprise an enormous and ancient phylum, are by and large morphologically conservative. An exception to this rule is the highly differentiated male tail. The morphology of the male genital structures varies widely and often serves as a key feature in discriminating between similar species. Combined with our studies of male tail development, this variability provides an opportunity to explore the evolution of a genetic program.
Key Findings
  • This laboratory has contributed to the collection of nematode species in laboratory culture, including the strain of C. remanei whose genome has been sequenced.
Baird, S.E., Fitch, D.H.A., and Emmons, S.W. (1994) Caenorhabditis vulgaris SP.N. (Nematoda:Rhabditidae): a necromenic associate of pill bugs and snails. Nematologica, 40, 1-11.
Fitch, D.H.A., Bugaj-Gaweda, B., and Emmons, S.W. (1995) 18S Ribosomal RNA gene phylogeny for some Rhabditidae related to Caenorhabditis. Mol. Biol. Evol. 12, 346-358.

  • Evolutionary changes in the positions of cells in the larval epidermis underlie changes in adult morphology affecting the rays
Fitch, D.H.A., and Emmons, S.W. (1995) Variable cell positions and cell contacts underlie morphological evolution of the rays in the male tails of nematodes related to Caenorhabditis elegans. Dev. Biol. 170, 564-582.
  • A key Hox gene regulatory gene (sop-2), which is essential for viability in C. elegans, cannot be identified in the available genome sequences of any of the related Caenorhabditis species or in any available nematode or other DNA sequence (April, 2007, J. Thomas, personal communication). This unexpected and surprising discovery is a current interest.
Sexual behavior is an essential aspect of the male phenotype, allowing the male to transmit his genes. Behavior emerges after the developmental program has constructed the animal body, including the complex connections and cellular activities within the nervous system. Many of the mutants we isolated that result in abnormal males also affect male behavior. We seek to connect the structural and behavioral phenotypes to understand how genes determine behavior.
Key Findings
  • In addition to copulatory behavior, C. elegans males exhibit a mate-searching behavior. Using a novel, quantitative behavioral assay, we have demonstrated how this behavior is regulated by environmental signals from hermaphrodites and physiological signals reflecting nutritional and reproductive status. This novel behavioral paradigm represents a model for dissecting the genetic and physiological basis of sex drive.
Lipton, J., Kleemann, G., Ghosh, R., Lints, R., and Emmons, S. W. (2004)  Mate searching in Caenorhabditis elegans: A genetic model for sex drive in a simple invertebrate. J. Neurosci. 24, 7427-7434. [PDF]
  • The nuclear hormone receptor DAF-12 acts downstream of a gonadal signal to regulate male mate searching behavior.
Kleemann, G., Jia, L., and Emmons, S. W.  Hormonal control of reproductive behavior in C. elegans. (submitted)
  • C. elegans swimming is interrupted at regular intervals by bouts of quiescence.
Ghosh, R., and Emmons, S. W.  Episodic swimming behavior in the nematode C. elegans. (submitted)