Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 4193 No. 2: 16 Nov. 2016
Type: Article
Published: 2016-11-15
DOI: 10.11646/zootaxa.4193.2.6
Page range: 304–316
Abstract views: 114
PDF downloaded: 11

Diaphorodoris alba Portmann & Sandmeier, 1960 is a valid species: molecular and morphological comparison with D. luteocincta (M. Sars, 1870) (Gastropoda: Nudibranchia)

Department of Science, University of “Roma Tre”, Viale G. Marconi 446, I-00146 Rome, Italy
National Museums Northern Ireland, 153 Bangor Road, Cultra, Holywood, BT18 0PE, UK
Zoological Museum Moscow State University Bolshaya Nikitskaya Str. 6, 125009, Russia
Department of Science, University of “Roma Tre”, Viale G. Marconi 446, I-00146 Rome, Italy
Mollusca DNA-Barcoding 3D RNA-Barcoding Integrative taxonomy Nudibranchs Diaphorodoris

Abstract

The nudibranch Diaphorodoris luteocincta (M. Sars, 1870) shows two colour morphotypes defined as D. luteocincta var. alba and D. luteocincta var. reticulata, which are easy to identify and which share an overlapping distribution in the Mediterranean Sea and the North-Eastern Atlantic Ocean. Their systematics has long been discussed by several authors until recently when a molecular study proposed the two varieties as intraspecific colour variability occurring within D. luteocincta species. In order to solve their ranking status, we have carried out a morphological study on anatomical characters and molecular analyses on the mitochondrial markers (COI and 16S rDNA) and the nuclear H3 gene. Results proved the usefulness of the integrative taxonomy approach in assessing species delimitation; in fact Diaphorodoris alba stat. nov. and D. luteocincta were revealed to be two different species. D. luteocincta var. reticulata is confirmed as synonym of D. luteocincta s.str. A hypothesis on phylogenetic relationship among most of the currently recognised species of the genus Diaphorodoris Iredale & O'Donoghue, 1923 is also here presented.

 

References

  1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403−410.
    http://dx.doi.org/10.1016/s0022-2836(05)80360-2

    Bonfield, J.K., Smith, K.F. & Staden, R. (1995) A new DNA sequence assembly program. Nucleic Acids Res, 23, 4992−4999.
    http://dx.doi.org/10.1093/nar/23.24.4992

    Coleman, A.W., (2009) Is there a molecular key to the level of ‘‘biological species’’ in eukaryotes? A DNA guide. Molecular Phylogenetics and Evolution, 50, 197–203.
    http://dx.doi.org/10.1016/j.ympev.2008.10.008

    Colgan, D.J., McLauchlan, A., Wilson, G.D.F., Livingston, S.P., Edgecombe, G.D., Macaranas, J., Cassis G. & Gray, M.R. (1998) Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology, 46 (5), 419–437.
    http://dx.doi.org/10.1071/ZO98048

    Fahey, S.J. & Valdés, A. (2005) Review of Acanthodoris Gray, 1850 with a phylogenetic analysis of Onchidorididae Alder and Hancock, 1845 (Mollusca, Nudibranchia). Proceedings of the California Academy of Sciences, 56, 20, 213−273.

    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 and Biotechnology, 3, 294−299.

    Furfaro, G., Modica, M.V., Oliverio, M. & Mariottini, P. (2016.a) A DNA-barcoding approach to the phenotypic diversity of Mediterranean species of Felimare Ev. Marcus & Er. Marcus, 1967 (Mollusca: Gastropoda), with a preliminary phylogenetic analysis. Italian Journal of Zoology, 83 (2), 195−207.

    Furfaro, G., Modica, M.V., Oliverio, O., Cervera, J.L. & Mariottini, M. (2014) Phenotypic diversity of Thuridilla hopei (Vérany, 1853) (Gastropoda Heterobranchia Sacoglossa). A DNA-barcoding approach. Biodiversity Journal, 5, 117−130.

    Furfaro, G., Oliverio, M. & Mariottini, P. (2016b) The southernmost record of Felimida elegantula (Philippi, 1844) (Gastropoda: Nudibranchia). Marine Biodiversity, 6 pp.

    Gutell, R.R. & Fox, G.E. (1988) A compilation of large subunit RNA sequences presented in a structural format. Nucleic Acids Res, 16, 175−313.
    http://dx.doi.org/10.1093/nar/16.suppl.r175

    Gutell, R.R., Gray, M.W. & Schnare, M.N. (1993) Compilation of large subunit (23S and 23S-like) ribosomal RNA structures. Nucleic Acids Res, 21, 3055−3074.

    Hallas, J.M. & Gosliner, T.M. (2015) Family matters: The first molecular phylogeny of the Onchidorididae Gray, 1827 (Mollusca, Gastropoda, Nudibranchia). Molecular Phylogenetics and Evolution, 88, 16–27.
    http://dx.doi.org/10.1016/j.ympev.2015.03.015

    Hirose, M., Hirose, E. & Kiyomoto, M. (2015) Identification of five species of Dendrodoris (Mollusca: Nudibranchia) from Japan, using DNA barcode and larval characters. Marine Biodiversity, 45, 769–780.
    http://dx.doi.org/10.1007/s12526-014-0288-2

    Horovitz, I. & Meyer, A. (1995) Systematics of New World monkeys (Platyrrhini, Primates) based on 16S mitochondrial DNA sequences: a comparative analysis of different weighting methods in cladistic analysis. Molecular Phylogenetics and Evolution, 4, 448–456.
    http://dx.doi.org/10.1006/mpev.1995.1041

    Ihering, H. (1880) Beiträge zur Kenntniss der Nudibranchien des Mittelmeeres. Part 1. (1. Chromodoris, 2. Doriopsis, 3. Cadlina.) Malakozoologische Blätter, N.F., 2, 57–112

    Iredale, T. & O’Donoghue, C. (1923) List of British nudibranchiate Mollusca. Proceedings of the Malacological Society of London, 15, 115–226.

    Jörger, K.M., Norenburg, J.L., Wilson, N.G. & Schrödl, M. (2012) Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs. BMC Evolutionary Biology, 12, 1–245.
    http://dx.doi.org/10.1186/1471-2148-12-245

    Librado, P. & Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451−1452.
    http://dx.doi.org/10.1093/bioinformatics/btp187

    Lydeard, C., Holznagel, W.E., Schnare M.N. & Gutell, R.R. (2000) Phylogenetic analysis of molluscan mitochondrial LSU rDNA sequences and secondary structures. Molecular Phylogenetics and Evolution, 15, 83−102.
    http://dx.doi.org/10.1006/mpev.1999.0719

    Oliverio, M. & Mariottini, P. (2001) A molecular framework for the phylogeny of Coralliophila and related muricoids. Journal of Molluscan Studies, 67, 215−224.
    http://dx.doi.org/10.1093/mollus/67.2.215

    Padula, V., Araujo, A.K., Matthews-Cascon, H. & Schrödl, M. (2014) Is the Mediterranean nudibranch Cratena peregrina (Gmelin, 1791) present on the Brazilian coast? Integrative species delimitation and description of Cratena minor n. sp. Journal of Molluscan Studies.
    http://dx.doi.org/10.1093/mollus/eyu052

    Padula, V., Bahia, J., Stöger, I., Camacho-García, Y., Malaquias, M.A.E., Cervera, J.L. & Schrödl, M. (2016) A test of color-based taxonomy in nudibranchs: Molecular phylogeny and species delimitation of the Felimida clenchi (Mollusca: Chromodorididae) species complex. Molecular Phylogenetics and Evolution, 103, 215–229.
    http://dx.doi.org/10.1016/j.ympev.2016.07.019

    Palumbi, S., Martin, A., Romano, S., Mc Millan, W.O., Stice, L. & Grabowski, G. (2001) The simple fool's guide to PCR Version 2.0 Honolulu: Department of Zoology and Kewalo Marine Laboratory, University of Hawaii.

    Pola, M., Camacho-Garía, Y.E. & Gosliner, T.M. (2012) Molecular data illuminate cryptic nudibranch species: the evolution of the Scyllaeidae (Nudibranchia: Dendronotina) with a revision of Notobryon. Zoological Journal of the Linnean Society, 165, 311–336.
    http://dx.doi.org/10.1111/j.1096-3642.2012.00816.x

    Pola, M., Cervera, J.L. & Gosliner, T.M. (2007) Phylogenetic relationships of Nembrothinae (Mollusca: Doridacea: Polyceridae) inferred from morphology and mitochondrial DNA. Molecular Phylogenetics and Evolution, 43, 726–742.
    http://dx.doi.org/10.1016/j.ympev.2007.02.003

    Pola, M., Valles, Y., Cervera, J.L., Medina, M. & Gosliner, T. (2006) Taxonomic status of Tambja abdere and Tambja fusca based on morphological and molecular evidence, with comments on the phylogeny of the subfamily Nembrothinae (Nudibranchia, Polyceridae). Annales Zoologici Fennici, 43, 52–64.

    Popenda, M., Szachniuk, M., Antczak, M., Purzycka, K.J., Lukasiak, P., Bartol, N., Blazewicz, J. & Adamiak, R.W. (2012) Automated 3D structure composition for large RNAs. Nucleic Acids Research, 40, e112.
    http://dx.doi.org/10.1093/nar/gks339

    Portmann, A. & Sandmeier, E. (1960) Zur kenntnis von Diaphorodoris (Gastropoda, Nudibranchia) und ihrer mediterranen Formen. Verhandelungen der Naturforschenden Gesellschaft in Basel, 71, 174–183.

    Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 7, 1253–6.
    http://dx.doi.org/10.1093/molbev/msn083

    Pruvot-Fol, A. (1932) Notes de systématique sur les Opisthobranches. Bulletin du museum, 2 Série, 4, 3, 323–329.

    Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012.a) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21, 1864−1877.

    Puillandre, N., Modica, M.V., Zhang, Y., Sirovich, L., Boisselier, M.C., Cruaud, C., Holford, M. & Samadi, S. (2012.b) Large-scale species delimitation method for hyperdiverse groups. Molecular Ecology, 21, 2671−2691.

    Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2011) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539−542.

    Salvi, D. & Mariottini, P. (2012) Molecular phylogenetics in 2D: ITS2 rRNA evolution and sequence-structure barcode from Veneridae to Bivalvia. Molecular Phylogenetics and Evolution, 65, 792–798.
    http://dx.doi.org/10.1016/j.ympev.2012.07.017

    Salvi, D., Bellavia, G., Cervelli, M. & Mariottini, P. (2010) The analysis of rRNA Sequence-Structure in phylogenetics: an application to the family Pectinidae (Mollusca, Bivalvia). Molecular Phylogenetics and Evolution, 56, 1059−1067.
    http://dx.doi.org/10.1016/j.ympev.2010.04.025

    Salvi, D., Macali, A. & Mariottini, P. (2014) Molecular phylogenetics and systematics of the bivalve family Ostreidae based on rRNA sequence-structure models and multilocus species tree. PLoS ONE, 9, e108696.
    http://dx.doi.org/10.1371/journal.pone.0108696

    Sars, M. (1870) Bidrag til Kundskab om Christianiafjordens Fauna. 2 NYT Magazin for Naturividenskaberne, 17, 113–232.

    Schmekel, R.L. & Portmann, A. (1982) Opisthobranchia des Mittelmeeres, Nudibranchia und Saccoglossa. Fauna e flora del Golfo di Napoli, Monografia della Stazione Zoologica di Napoli, 40, 1–410.

    Seibel, P.N., Müller, T., Dandekar, T., Schultz, J. & Wolf, M. (2006) 4SALE–a tool for synchronous RNA sequence and secondary structure alignment and editing BMC. Bioinformatics, 7, 1–11.

    Seibel, P.N., Müller, T., Dandekar, T. & Wolf, M. (2008) Synchronous visual analysis and editing of RNA sequence and secondary structure alignments using 4SALE. BMC Research Notes, 1, 1–91.
    http://dx.doi.org/10.1186/1756-0500-1-91

    Swofford, D.L. (1998) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4 Laboratory of Molecular Systematics Smithsonian Institution Sinauer Associates, Sunderland, Massachusetts.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725−2729.
    http://dx.doi.org/10.1093/molbev/mst197

    The Sea Slug Forum. Australian Museum, Sydney. Available from: http://www.seaslugforum.net (Accessed 15 Nov. 2016)

    Thompson, T.E. & Brown, G.H. (1984) Biology of Opisthobranch Molluscs, vol. 2. The Ray Society, London, UK, 280 pp.

    Trainito, E. & Doneddu, M. (2014) Nudibranchi del Mediterraneo. Edizione Il Castello, Milano, Italy, 192 pp.

    Wilson, N.G., Schrödl, M. & Halanych, K.M. (2009) Ocean barriers and glaciation: evidence for explosive radiation of mitochondrial lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia). Molecular Ecology, 18, 965–984.
    http://dx.doi.org/10.1111/j.1365-294X.2008.04071.x

    Zhang, J.J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A General Species Delimitation Method with Applications to Phylogenetic Placements. Bioinformatics (Oxford, England), 29 (22), 2869–2876.
    http://dx.doi.org/10.1093/bioinformatics/btt499

    Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31, 3406–3415.
    http://dx.doi.org/10.1093/nar/gkg595