Skip to main content Skip to main navigation menu Skip to site footer
Type: Articles
Published: 2007-04-25
Page range: 45–62
Abstract views: 85
PDF downloaded: 32

Comparison of the cryptic nematode species Caenorhabditis brenneri sp. n. and C. remanei (Nematoda: Rhabditidae) with the stem species pattern of  the Caenorhabditis Elegans group

Institut für Biologie/Zoologie, AG Evolutionsbiologie, Freie Universität Berlin, Königin-Luise Straße 1-3, 14195 Berlin, Germany
Department of Biology, New York University, 100 Washington Square E., New York, NY10003, USA
Nematoda Caenorhabditis biogeography biological species concept circumtropical mating tests remanei stem species pattern

Abstract

The new gonochoristic member of the Caenorhabditis Elegans group, C. brenneri sp. n., is described. This species is reproductively isolated at the postmating level from its sibling species, C. remanei. Between these species, only minute morphological differences are found, but there are substantial genetic differences. The stem species pattern of the Elegans group is reconstructed. C. brenneri sp. n. deviates from this character pattern only in small diagnostic characters. In mating tests of C. brenneri sp. n. females with C. remanei males, fertilization takes place and juveniles occasionally hatch. In the reverse combination, no offspring were observed. Individuals from widely separated populations of each species can be crossed successfully (e.g. C. brenneri sp. n. populations from Guadeloupe and Sumatra, or C. remanei populations from Japan and Germany). Both species have been isolated only from anthropogenic habitats, rich in decomposing organic material. C. brenneri sp. n. is distributed circumtropically, C. remanei is only found in northern temperate regions. To date, no overlap of the ranges was found. Hypotheses to explain the allopatric distribution of the two species are discussed. One suggests that the speciation center for the Elegans group was in East Asia, and globally distributed members dispersed from there.

References

  1. Andrássy, I. (2005) Free-living nematodes from Hungary (Nematoda errantia), I. Pedozoologica Hungarica 3. Hungarian Natural History Museum and Systematic Zoology Research Group of the Hungarian Academy of Sciences, Budapest, 518 pp.

    Baird, S.E. (1999) Natural and experimental associations of Caenorhabditis remanei with Trachelipus rathkii and other terrestrial isopods. Nematology, 1, 471–475.

    Baird, S.E., Fitch, D.H.A. & Emmons, S.W. (1994) Caenorhabditis vulgaris n. sp. (Nematoda: Rhabditidae): a necromenic associate of pill bugs and snails. Nematologica, 40, 1–11.

    Baird, S.E., Sutherlin, M.E., Fitch, D.H.A. & Emmons, S.W. (1990) Strange bedfellows. Worm Breeder's Gazette, 11 (4), 89.

    Baird, S.E., Sutherlin, M.E. & Emmons, S.W. (1992) Reproductive isolation in Rhabditidae (Nematoda: Secernentea): mechanisms that isolate six species of three genera. Evolution, 46, 585–594.

    Baird, S.E. & Yen, W.C. (2000) Reproductive isolation in Caenorhabditis: terminal phenotypes of hybrid embryos. Evolution & Development, 2, 9–15.

    Binder, B.F., Demilo, A.B., Kochansky, J.P.J. & Chitwood, D. (1992) Inhibition of development in Caenorhabditis elegans (Nematoda) by a reduced aromatic schiff base and related compounds. Journal of Agricultural and Food Chemistry, 40, 1475–1477.

    Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics, 77, 71–94.

    Cangiano, G. & La Volpe, A. (1993) Repetitive DNA sequences located in the terminal portion of the Caenorhabditis elegans chromosomes. Nucleic Acids Research, 21, 1133–1139.

    Cho, S., Jin, S.W., Cohen, A. & Ellis, R.E. (2004) A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Research, 14, 1207–1220.

    Cutter, A.D. (2006) Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans. Genetics, 172, 171–184.

    Cutter, A.D., Baird, S.E. & Charlesworth, D. (2006) High nucleotide polymorphism and rapid decay of linkage disequilibrium in wild populations of Caenorhabditis remanei. Genetics, 174, 901–913.

    Dougherty, E.C. & Nigon, V. (1949) A new species of the free-living nematode genus Rhabditis of interest in comparative physiology and genetics. Journal of Parasitology, 35 (Suppl.), 11.

    Felsenstein, K.M. & Emmons, S.W. (1988) Nematode repetitive DNA with ARS and segregation function in Saccharomyces cerevisiae. Molecular and Cellular Biology, 8, 875–883.

    Fitch, D.H.A., Bugaj-Gaweda, B. & Emmons, S.W. (1995) 18S ribosomal RNA gene phylogeny for some Rhabditidae related to Caenorhabditis. Molecular Biology & Evolution, 12, 346–358.

    Fodor, A. (1986) A newly isolated wild type strain of the bisexual Caenorhabditis remanei from the soil of India. Worm Breeder's Gazette, 9 (3), 121.

    Fodor, A. & Timar, T. (1989) Effects of precocene analogs on the nematode Caenorhabditis remanei (var. Bangaloreiensis). II. Competitions with a juvenile hormone analog (Methoprene). General and Comparative Endocrinology, 74, 32–44.

    Fodor, A., Timar, T., Kiss, I., Hosztafi, S., Varga, E., Soos, J. & Sebok, P. (1989) Effects of precocene analogs on the nematode Caenorhabditis remanei (var. Bangaloreiensis). I. Structure/activity relations. General and Comparative Endocrinology, 74, 18–31.

    Friedman, P.A., Platzer, E.G. & Eby, J.E. (1977) Species differentiation in Caenorhabditis briggsae and Caenorhabditis elegans. Journal of Nematology, 9, 197–203.

    Graustein, A., Gaspar, J.M., Walters, J.R. & Palopoli, M.F. (2002) Levels of DNA polymorphism vary with mating system in the nematode genus Caenorhabditis. Genetics, 161, 99–107.

    Hekimi, S. (1990) A neuron-specific antigen in C. elegans allows visualization of the entire nervous system. Neuron, 4, 855–865.

    Hodgkin, J. (1984) Switch genes and sex determination in the nematode C. elegans. Journal of Embryology and Experimental Morphology, 83 Suppl, 103–117.

    Jones, A.R. & Schedl, T.B. (1995) Mutations in gld-1, a female germ cell-specific tumor suppressor gene in Caenorhabditis elegans, affect a conserved domain also found in Src-associated protein Sam68. Genes & Development, 9, 1491–1504.

    Kiontke, K., Gavin, N.P., Raynes, Y., Roehrig, C., Piano, F. & Fitch, D.H.A. (2004) Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proceedings of the National Academy of Sciences of the United States of America, 101, 9003–9008.

    Kiontke, K., Hironaka, M. & Sudhaus, W. (2002) Description of Caenorhabditis japonica n. sp. (Nematoda: Rhabditida) associated with the burrower bug Parastrachia japonensis (Heteroptera: Cydnidae) in Japan. Nematology, 4, 933–941.

    Kiontke, K. & Sudhaus, W. (2006) Ecology of Caenorhabditis. In: The C. elegans Community (Ed.) WormBook. Available from http://www.wormbook.org/chapters/www_ecolCaenorhabditis/ecolCaenorhabditis.html (accessed 15 April 2007)

    Kloek, A.P., McCarter, J.P., Setterquist, R.A., Schedl, T. & Goldberg, D.E. (1996) Caenorhabditis globin genes: rapid intronic divergence contrasts with conservation of silent exonic sites. Journal of Molecular Evolution, 43, 101–108.

    Kreis, H.A. & Faust, E.C. (1933) Two new species of Rhabditis (Rhabditis macrocerca and R. clavopapillata) associated with dogs and monkeys in experimental Strongyloides studies. Transactions of the American Microscopical Society, 52, 162–172.

    Lee, R.C., Feinbaum, R.L. & Ambros, V.R. (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843–854.

    Llopart, A., Comeron, J.M., Brunet, F.G., Lachaise, D. & Long, M. (2002) Intron presence-absence polymorphism in Drosophila driven by positive Darwinian selection. Proceedings of the National Academy of Sciences of the United States of America, 99, 8121–8126.

    Maupas, E. (1899) La mue et l'enkystement chez les nématodes. Archive de Zoologie expérimentale et génerale, 7, 563–628.

    Moss, E.G., Lee, R.C. & Ambros, V. (1997) The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell, 88, 637–646.

    Nigon, V. & Dougherty, E.C. (1949) Reproductive patterns and attempts at reciprocal crossing of Rhabditis elegans Maupas, 1900, and Rhabditis briggsae Dougherty and Nigon, 1949 (Nematoda: Rhabditidae). Journal of Experimental Zoology, 112, 485–503.

    Nigon, V. & Dougherty, E.C. (1950) A dwarf mutation in a nematode. A morphological mutant of Rhabditis briggsae, a free-living soil nematode. Journal of Heredity, 41, 103–109.

    Okabe, K. & Shiraishi, S. (1971) Experimental infection of Oncomelania hupensis nosophora with Rhabditis oncomelaniae Yokoo et Okabe. The Kurume Medical Journal, 18, 195–199.

    Roy, S.W. & Penny, D. (2006) Smoke without fire: most reported cases of intron gain in nematodes instead reflect intron losses. Molecular Biology & Evolution, 23, 2259–2262.

    Schuurmans Stekhoven, J. (1951) Nématodes saprozoaires et libres du Congo belge. Mémoire de l'Institut Royale des Sciences Naturelles de Belgique, 39, 1–79.

    Sedensky, M.M., Hudson, S.J., Everson, B. & Morgan, P.G. (1994) Identification of a mariner-like repetitive sequence in C. elegans. Nucleic Acids Research, 22, 1719–1723.

    Stothard, P. & Pilgrim, D. (2006) Conspecific and interspecific interactions between the FEM-2 and the FEM-3 sex-determining proteins despite rapid sequence divergence. Journal of Molecular Evolution, 62, 281–291.

    Sulston, J.E., Albertson, D.G. & Thomson, J.N. (1980) The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Developmental Biology, 78, 542–576.

    Sudhaus, W. (1974) Zur Systematik, Verbreitung, Ökologie und Biologie neuer und wenig bekannter Rhabditiden (Nematoda). 2. Teil. Zoologische Jahrbücher (Systematik), 101, 417–465.

    Sudhaus, W. (1976) Vergleichende Untersuchungen zur Phylogenie, Systematik, Ökologie, Biologie und Ethologie der Rhabditidae (Nematoda). Zoologica, 43, 1–229.

    Sudhaus, W. & Fitch, D.H.A. (2001) Comparative studies on the phylogeny and systematics of the Rhabditidae (Nematoda). Journal of Nematology, 33, 1–70.

    Sudhaus, W. & Kiontke, K. (1996) Phylogeny of Rhabditis subgenus Caenorhabditis (Rhabditidae, Nematoda). Journal of Zoological Systematics & Evolutionary Research, 34, 217–233.

    Thomas, W.K. & Wilson, A.C. (1991) Mode and tempo of molecular evolution in the nematode Caenorhabditis: cytochrome oxidase II and calmodulin sequences. Genetics, 128, 269–279.

    Weber, A. (1995) Ökosystem Komposthaufen: Phoretisch gebundene Nematoden an Landasseln (Oniscoidea). Diplom Thesis Freie Universität Berlin, Berlin, 46p.

    Yokoo, T. & Okabe, K. (1968) Two new species of genus Rhabditis (Nematoda: Rhabditidae) found in the intermediate host of Schistosoma japonica, Oncomelania hupensis nosophora and Oncomelania hupensis formosana. Saga daigaku nogakubu iho, 25, 69–78.

    Youngman, S., van Luenen, H.G. & Plasterk, R.H. (1996) Rte-1, a retrotransposon-like element in Caenorhabditis elegans. FEBS Letters, 380, 1–7.