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Type: Article
Published: 2019-02-03
Page range: 415–431
Abstract views: 86
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Morphological and molecular diversity of rissoellids (Mollusca, Gastropoda, Heterobranchia) from the Northwest Pacific island of Hokkaido, Japan

Department of Natural History Sciences, Hokkaido University, Sapporo 060-0810, Japan
Institute for International Collaboration, Hokkaido University, Sapporo 060-0810, Japan
Cawthron Institute, Nelson 7042, New Zealand
Department of Zoology, National Museum of Nature and Science, Tokyo, Japan
Department of Natural History Sciences, Hokkaido University, Sapporo 060-0810, Japan
Mollusca COI gene Rissoelidae Rissoella morphospecies integrative taxonomy ABGD

Abstract

This study deals with four species of marine microgastropods of the family Rissoellidae. Rissoella elatior (Golikov, Gulbin & Sirenko, 1987), R. golikovi (Gulbin, 1979), R. japonica n. sp., and Rissoella sp. 1 were collected in different locations around the island of Hokkaido, Japan. Light and scanning electron microscopy (SEM) were used to study the general morphology of the shell and radula, and a region of the mitochondrial cytochrome c oxidase subunit I (COI) gene was amplified for 26 specimens. Rissoella elatior is morphologically characterized by a highly asymmetrical radula with a deep notch encircled by 10–13 minute secondary cusps on the left dorsal margin of the central tooth. Rissoella golikovi is characterized by a skeneiform shell and possession of three teeth per row on the radula. Rissoella japonica n. sp. shows five teeth per row on the radula; central tooth higher than wide; lateral and marginal teeth narrow with an outer lateral projection at the base; all teeth presenting numerous small cusps on the cutting edge. Rissoella sp. 1 is distinguished from R. japonica n. sp. in having i) very short oral lobes, ii) a mantle with a large, black patch and whitish blotches inside, and iii) different color patterns associated with the visceral mass. Although Rissoella sp. 1 probably represents an undescribed species, additional specimens are needed to complete its description. This study represents a first molecular approach to the family Rissoellidae. Studies of traditional morphological characters indicated four species, the addition of COI data raised the count to eight potential species, suggesting the occurrence of cryptic species among rissoellids.

 

References

  1. Caballer, M., Ortea, J. & Narciso, S. (2011) Description of two new species of Rissoella Gray, 1847 (Mollusca, Gastropoda, Heterobranchia) from Venezuela, with a key to the Caribbean species known for the genus. ZooKeys, 115, 1–18.

    https://doi.org/10.3897/zookeys.115.1163

    Caballer, M., Ortea, J. & Redfern, C. (2014) On the Genus Rissoella Gray, 1847 (Gastropoda: Heterobranchia: Rissoellidae) in the Bahamas. American Malacological Bulletin, 32 (1), 104–121.

    https://doi.org/10.4003/006.032.0109

    Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.

    https://doi.org/10.1046/j.1365-294x.2000.01020.x

    Dinapoli, A. & Klussmann-Kolb, A. (2010) The long way to diversity—phylogeny and evolution of the Heterobranchia (Mollusca: Gastropoda). Molecular Phylogenetics and Evolution, 55 (1), 60–76.

    https://doi.org/10.1016/j.ympev.2009.09.019

    Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32 (5), 1792–1797.

    https://doi.org/10.1093/nar/gkh340

    Espinosa, J. & Ortea, J. (2009) Nueva especie de Rissoella J.E. Gray, 1847 (Gastropoda: Heterobranchia) de la Península de Guanahacabibes, Pinar del Río, Cuba. Revista de la Academia Canaria de Ciencias, XX (4), 15–17. [in Spanish]

    Felsenstein, J. (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17 (6), 368–376.

    https://doi.org/10.1007/BF01734359

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology Biotechnology, 3 (5), 294–299.

    Fretter, V. (1948) The structure and life history of some minute prosobranchs of rock pools: Skeneopsis planorbis (Fabricius), Omalogyra atomus (Philippi), Rissoella diaphana (Alder) and Rissoella opalina (Jeffreys). Journal of the Marine Biological Association of the United Kingdom, 27 (3), 597–632.

    https://doi.org/10.1017/S0025315400056058

    Galindo, L.A., Puillandre, N., Strong, E.E. & Bouchet, P. (2014) Using microwaves to prepare gastropods for DNA barcoding. Molecular Ecology Resources, 14 (4), 700–705.

    https://doi.org/10.1111/1755-0998.12231

    Golikov, A.N., Gulbin, V.V. & Sirenko, B.I. (1987) Prosobranch from Moneron Island shelf (Sea of Japan). I. Orders Patelliformes—Calyptraeiformes. In: Fauna and Distribution of Molluscs, North Pacific and Polar Basin, edited by A. Kafanov. Far Eastern Science Center of the USSR Academy of Science, Moscow, pp. 20–40.

    Gulbin, V.V. (1979) A new species of the littoral gastropod Rissoellidae from the Far-eastern seas. Academy of Sciences of the USSR, Vladivostok. Far East Science Center. Marine Biology, 3, 88–89. [in Russian]

    Hasegawa, K. (2000) Rissoellidae. In: Okutani, T. (Ed.), Marine Mollusks in Japan. Tokai University Press, Tokyo, pp. 700–701.

    Hasegawa, K. (2017) Rissoellidae. In: Okutani, T. (Ed.), Marine Mollusks in Japan. 2nd Edition. Tokai University Press, Tokyo, pp. 398 + 1063.

    Hebert, P.D.N., Cywinska, A., Ball, S.L. & Dewaard, J.R. (2003a) Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences, 270 (1512), 313–321.

    https://doi.org/10.1098/rspb.2002.2218

    Hebert, P.D.N., Ratnasingham, S. & Dewaard, J.R. (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B: Biological Sciences, 270 (Supplement 1), 96–99. [S96–S99]

    https://doi.org/10.1098/rsbl.2003.0025

    Kano, Y., Chikyu, E. & Warén, A. (2009) Morphological, ecological and molecular characterization of the enigmatic planispiral snail Genus Adeuomphalus (Vetigastropoda: Seguenzioidea). Journal of Molluscan Studies, 75 (4), 397–418.

    https://doi.org/10.1093/mollus/eyp037

    Kantor, Y.I. & Sysoev, A.V. (2006) Marine and Brackish Water Gastropoda of Russia and Adjacent Countries: An Illustrated Catalogue. KMK Scientific Pres Ltd., Moscow, 371 pp., 140 pls.

    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. & Meintjes, P. (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649.

    https://doi.org/10.1093/bioinformatics/bts199

    Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16 (2), 111–120.

    https://doi.org/10.1007/BF01731581

    Kristof, A., De Oliveira, A.L., Kolbin, K.G. & Wanninger, A. (2016) A putative species complex in the Sea of Japan revealed by DNA sequence data: a study on Lottia cf. kogamogai (Gastropoda: Patellogastropoda). Journal of Zoological Systematics and Evolutionary Research, 54 (3), 177–181.

    https://doi.org/10.1111/jzs.12120

    Maturana, C.S., Moreno, R.A., Labra, F.A., González-Wevar, C.A., Rozbaczylo, N., Carrasco, F.D. & Poulin, E. (2011) DNA barcoding of marine polychaetes species of southern Patagonian fjords. Revista de Biologia Marina Y Oceanografia, 46 (1), 35–42.

    https://doi.org/10.4067/S0718-19572011000100005

    Olabarria, C. (2002) Role of colonization in spatio-temporal patchiness of microgastropods in coralline turf habitat. Journal of Experimental Marine Biology and Ecology, 274 (2), 121–140.

    https://doi.org/10.1016/S0022-0981(02)00201-0

    Ortea, J. & Espinosa, J. (2004) Una combinación de ciencia, arte y naturaleza: Especies nuevas del género Rissoella J. E. Gray, 1847 (Gastropoda, Heterobranchia) descritas en homenaje a las artistas de la plástica cubana. Avicennia, 17, 77–94. [in Spanish]

    Ortea, J., Espinosa, J. & Magaña, J. (2004) Descripción de una nueva especie del género Rissoella J. E. Gray, 1847 (Mollusca, Gastropoda, Heterobranchia) del Pacifico de Costa Rica. Avicennia, 17, 95–100. [in Spanish]

    Ponder, W.F. & Yoo, E.K. (1977) A revision of the Australian species of Rissoellidae (Mollusca: Gastropoda). Records of The Australian Museum, 31 (4), 133–185.

    https://doi.org/10.3853/j.0067-1975.31.1977.208

    Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology, 21 (8), 1864–1877.

    https://doi.org/10.1111/j.1365-294X.2011.05239.x

    Rolán, E. & Hernández, J.M. (2004) Dos nuevas especies de Rissoella (Mollusca: Rissoellidae) de las islas Canarias y Senegal. Revista de la Academia Canaria de Ciencias, XV (3–4), 229–235. [in Spanish]

    Sars, G.O. (1878) Mollusca regionis Arcticae Norvegiae. In: Bidrag til Kundskaben om Norges Arktiske Fauna. Chritiania, Brøgger, 466 pp.

    Simone, L. (1995) Rissoella ornata, a new species of Rissoellidae (Mollusca: Gastropoda: Rissoelloidea) from the southeastern coast of Brazil. Proceedings of the Biological Society of Washington, 108 (4), 560–567.

    Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22 (21), 2688–2690.

    https://doi.org/10.1093/bioinformatics/btl446

    Sun Y., Li Q., Kong, L. & Zheng, X. (2012) DNA barcoding of Caenogastropoda along coast of China based on the COI gene. Molecular Ecology Resources, 12 (2), 209–218.

    https://doi.org/10.1111/j.1755-0998.2011.03085.x

    Syromyatnikov, M.Y., Golub, V.B., Kokina, A.V., Soboleva, V.A. & Popov, V.N. (2017) DNA barcoding and morphological analysis for rapid identification of most economically important crop-infesting Sunn pests belonging to Eurygaster Laporte, 1833 (Hemiptera, Scutelleridae). Zookeys, 706, 51–71.

    https://doi.org/10.3897/zookeys.706.13888

    Thiele, J. (1929–1935) Handbuch der systematischen Weichtierkunde. Gustav Fischer, Jena, 1154 pp.

    Weigand, A.M., Jochum, A., Pfenninger, M., Steinke, D. & Klussmann-Kolb, A. (2011) A new approach to an old conundrum—DNA barcoding sheds new light on phenotypic plasticity and morphological stasis in microsnails (Gastropoda, Pulmonata, Carychiidae). Molecular Ecology Resources, 11 (2), 255–265.

    https://doi.org/10.1111/j.1755-0998.2010.02937.x

    Weigand, A.M., Jochum, A., Slapnik, R., Schnitzler, J., Zarza, E. & Klussmann-Kolb, A. (2013) Evolution of microgastropods (Ellobioidea, Carychiidae): integrating taxonomic, phylogenetic and evolutionary hypotheses. BMC Evolutionary Biology, 13 (1), 1–24.

    https://doi.org/10.1186/1471-2148-13-18

    Wise, J.B. (1998) Morphology and systematic position of Rissoella caribaea Rehder, 1943 (Gastropoda: Heterobranchia: Rissoellidae). The Nautilus, 111 (1), 13–21.

    Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29 (22), 2869–2876.

    https://doi.org/10.1093/bioinformatics/btt499