Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2016-08-10
Page range: 85–92
Abstract views: 100
PDF downloaded: 2

DNA barcodes unite two problematic taxa: the meiobenthic Boreohydra simplex is a life-cycle stage of Plotocnide borealis (Hydrozoa: Aplanulata)

Department of Invertebrate Zoology, Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow, Russia Federal State Budget Institution "Research Center for Obstetrics, Gynecology and Perinatology", Ministry of Healthcare of the Russian Federation, Moscow, Russia
Institute of Marine Science, University of Alaska Fairbanks, Fairbanks AK, USA
Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 237–0061 Yokosuka, Japan
National Systematics Laboratory of NOAA’s Fisheries Service, Smithsonian National Museum of Natural History, Washington DC, USA
Coleoptera polyp medusa metagenesis bipolar distribution meiofauna

Abstract

Genetic barcodes of arctic medusae and meiobenthic cnidarians have uncovered a fortuitous connection between the medusa Plotocnide borealis Wagner, 1885 and the minute, mud-dwelling polyp Boreohydra simplex Westblad, 1937. Little to no sequence differences exist among independently collected samples identified as Boreohydra simplex and Plotocnide borealis, showing that the two different forms represent a single species that is henceforth known by the older name Plotocnide borealis Wagner, 1885. The polyp form has been observed to produce bulges previously hypothesized to be gonophores, and the results here are consistent with that view. Interestingly, the polyp has also been reported to produce egg cells in the epiderm, a surprising phenomenon that we document here for only the second time. Thus, P. borealis produces eggs in two different life stages, polyp and medusa. This is the first documented case of a metagenetic medusozoan species being able to produce gametes in both the medusa and polyp stage. It remains unclear what environmental/ecological conditions modulate the production of eggs and/or medusa buds in the polyp stage. Similarly, sperm production, fertilization and development are unknown, warranting further studies.

 

References

  1. Aisenstadt, T.B. & Polteva, D.G. (1981) Origin of germ cells and early stages of oogenesis in marine hydroid polyp Obelia. Ontogenez, 12 (3), 243–250.

    Alexandrova, O., Schade, M., Böttger, A. & David, C.N. (2005) Oogenesis in Hydra: nurse cells transfer cytoplasm directly to the growing oocyte. Developmental Biology, 281, 91–101.
    http://dx.doi.org/10.1016/j.ydbio.2005.02.015

    Barnett, T.J. (1985) Seasonality of northern New Zealand Hydromedusae and a review of the New Zealand Hydromedusae fauna. Unpublished M.Sc. thesis, Department of Zoology, University of Auckland, New Zealand, 257 pp.

    Bozhenova, O.V., Stepanjants, S.D. & Sheremetevski, A.M. (1989) The first finding of the meiobenthic Cnidaria Boreohydra simplex (Hydrozoa, Athecata) in the White Sea. Zoolgicheskii Zhurnal, 68, 11–16.

    Buecher, E., Goy, J. & Gibbons M.J. (2005) Hydromedusae of the Agulhas Current. African Invertebrates, 46, 27–69.

    Carré, D. & Carré, C. (1990) Complex reproductive cycle in Eucheilota paradoxica (Hydrozoa: Leptomedusae): Medusae, polyps and frustules produced from medusa stage. Marine Biology, 104 (2), 303–310.
    http://dx.doi.org/10.1007/BF01313272

    Collins, A.G., Bentlage, B., Lindner, A., Lindsay, D.J., Haddock, S.H.D., Jarms, G., Norenburg, J.L., Jankowski, T. & Cartwright, P. (2008) Phylogenetics of Trachylina (Cnidaria: Hydrozoa) with new insights on the evolution of some problematic taxa. Journal of the Marine Biological Association of the United Kingdom, 88 (8), 1673–1685.
    http://dx.doi.org/10.1017/S0025315408001732

    Ershova, E.H., Hopcroft, R.R. & Kosobokova, K.N. (2015) Inter-annual variability of summer mesozooplankton communities of the western Chukchi Sea: 2004–2012. Polar Biology, 38, 1461–1481.
    http://dx.doi.org/10.1007/s00300-015-1709-9

    Geller, J.G, Meyer, C., Parker, M. & Hawk, H. (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Molecular Ecology Resources, 13, 851–861.
    http://dx.doi.org/10.1111/1755-0998.12138

    Greeff, R. (1870) Protohydra leuckarti. Eine marine Stammform der Coelenteraten. Zeitschrift für wissenschaftliche Zoologie, 20, 37–54.

    Grossmann, M.M., Collins, A.G. & Lindsay, D.J. (2014) Description of the eudoxid stages of Lensia havock and Lensia leloupi (Cnidaria: Siphonophora: Calycophorae), with a review of all known Lensia eudoxid bracts. Systematics and Biodiversity, 12 (2), 163–180.
    http://dx.doi.org/10.1080/14772000.2014.902867

    Grossmann, M.M., Lindsay, D.J. & Collins, A.G. (2013) The end of an enigmatic taxon: Eudoxia macra is the eudoxid stage of Lensia cossack (Siphonophora, Cnidaria). Systematics and Biodiversity, 11 (3), 381–387.
    http://dx.doi.org/10.1080/14772000.2013.825658

    Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59 (3), 307–321.
    http://dx.doi.org/10.1093/sysbio/syq010

    Honegger, T.G., Zürrer, D. & Tardent, P. (1989) Oogenesis in Hydra carnea: A new model based on light and electron microscopic analyses of oocyte and nurse cell differentiation. Tissue Cell, 21 (3), 381–393.
    http://dx.doi.org/10.1016/0040-8166(89)90052-9

    Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780.
    http://dx.doi.org/10.1093/molbev/mst010

    Kayal, E., Bentlage, B., Cartwright, P., Yanagihara, A.A., Lindsay, D.J., Hopcroft, R.R. & Collins, A.G. (2015) Phylogenetic analysis of higher-level relationships within Hydroidolina (Cnidaria: Hydrozoa) using mitochondrial genome data and insight into their mitochondrial transcription. PeerJ, 3, e1403.
    http://dx.doi.org/10.7717/peerj.1403

    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649.
    http://dx.doi.org/10.1093/bioinformatics/bts199

    Kramp, P.L. (1942) Medusae. In: The ‘Godthaab’ Expedition 1928, Medd. Grønland, 81 (1), pp. 1–168.

    Linko, A. (1900) Observations sur les Méduses de la Mer Blanche. Travaux de la Société Impériale des Naturalistes de St-Pétersbourg, 29, 137–156.

    Lindsay, D.J., Grossmann, M.M., Nishikawa, J., Bentlage, B. & Collins, A.G. (2015) DNA barcoding of pelagic cnidarians: current status and future prospects. Bulletin of the Plankton Society of Japan, 62 (1), 39–43.

    Mayer, A.G. (1900) Some medusae from the Tortugas, Florida. Bulletin of the Museum of Comparative Zoology of Harvard, 37, 13–82.

    McCrady, J. (1859) Gymnopthalmata of Charleston Harbor. Proceedings of the Elliott Society of Natural History, 1, 103–221.

    Miller, M.A., Technau, U., Smith, K.M. & Steele, R.E. (2000) Oocyte development in Hydra involves selection from competent precursor cells. Developmental Biology, 224, 326–338.
    http://dx.doi.org/10.1006/dbio.2000.9790

    Millonig, G. (1964) Study on the factors which influence preservation of fine structure. In: Symposium on electron microscopy Rome, Italy. Consiglio Nazionale delle Ricerche, p. 347.

    Miranda, L.S., Collins, A.G. & Marques, A.C. (2010) Molecules clarify a cnidarian life cycle – the “hydrozoan” Microhydrula limopsicola is an early life stage of the staurozoan Haliclystus antarcticus. PLoS ONE, 5 (4), e10182.

    Nawrocki, A.M., Collins, A.G., Hirano, Y.M., Schuchert, P. & Cartwright, P. (2013) Phylogenetic placement of Hydra and relationships within Aplanulata (Cnidaria: Hydrozoa). Molecular Phylogenetics and Evolution, 67 (1), 60–71.

    Nyholm, K.G. (1951) Egg cells in the ectoderm of Boreohydra simplex. Arkiv för Zoologi, 2 (7), 531–533.

    Sanamyan, K.E. & Sanamyan, N.P. (2012) New records of meiobenthic hydroids (Cnidaria: Hydrozoa) from the Far East Seas of Russia. In: Conservation of biodiversity of Kamchatka and coastal waters: materials of ХIII international scientific conference, dedicated to the 75th anniversary of S.A. Dyrenkov’s birthday. Kamchatpress, Petropavlovsk-Kamchatsky, pp. 102–109.

    Sars, M. (1835) Beskrivelser og iagttagelser over nogle mærkelige eller nye i havet ved den bergenske kyst levende dyr af polypernes, acalephernes, radiaternes, annelidernes og molluskernes classer, med en kort oversigt over de hidtil af forfatteren sammesteds fundne arter og deres forekommen. Thorstein Hallager, Bergen, 81 pp.

    Schuchert, P. (2006) The European athecate hydroids and their medusae (Hydrozoa, Cnidaria): Capitata Part 1. Revue suisse de Zoologie,113 (2), 325–410.
    http://dx.doi.org/10.5962/bhl.part.80356

    Schuchert, P. (2010) The European athecate hydroids and their medusae (Hydrozoa, Cnidaria): Capitata Part 2. Revue suisse de Zoologie, 117 (3), 337–555.

    Schuchert, P. (2015) Capitata incertae sedis. In: Schuchert, P. (2015) World Hydrozoa database. Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=22766 on 2015-08-19.

    Wagner, N. (1885) Die Wirbellosen des Weissen Meeres: Zoologische Forschungen an der Küste des Solowetzkischen Meerbusens in den Sommermonaten der Jahre 1877, 1878, 1879 und 1882. W. Engelmann, Leipzig, 171 pp.

    Werner, B. (1958) Die Verbreitung und das jahreszeitliche Auftreten der Anthomeduse Rathkea octopunctata M. Sars, sowie die Temperaturabhängigkeit ihrer Entwicklung und Fortpflanzung. Helgoländer wissenschaftliche Meeresuntersuchungen, 6, 137–170.
    http://dx.doi.org/10.1007/BF01609131

    Westblad, E. (1937) Boreohydra simplex n. gen., n. sp., ein Solitärpolyp von der norwegischen Küste. Arkiv för Zoologi, 29B (7), 1–6.

    Westblad, E. (1947) Notes on Hydroids. Arkiv för Zoologie, 39A (5), 1–23.

    Westblad, E. (1953) Boreohydra simplex Westblad, a "bipolar" hydroid. Arkiv för Zoologie, 4 (19), 351–354.