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Type: Article
Published: 2017-09-26
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Ontogeny as an important part of integrative taxonomy in tergipedid aeolidaceans (Gastropoda: Nudibranchia) with a description of a new genus and species from the Barents Sea

Koltzov Institute of Developmental Biology RAS, 26 Vavilova Str., 119334 Moscow, Russia Zoological Museum, Moscow State University, Bolshaya Nikitskaya Str. 6, 125009 Moscow, Russia
Zoological Museum, Moscow State University, Bolshaya Nikitskaya Str. 6, 125009 Moscow, Russia
National Museums Northern Ireland, Holywood, Northern Ireland, United Kingdom
Mollusca morphological and molecular data ontogenetic systematics nudibranchs

Abstract

The taxonomy of aeolidacean nudibranchs of the traditional group previously known as Tergipedidae is discussed. To integrate the diverse molecular phylogenetic pattern and morphological disparity in a broadly ontogenetic context a revised classification at the family level is presented. The families Calmidae Iredale & O'Donoghue, 1923, Eubranchidae Odhner, 1934, Fionidae Gray, 1857 s. str. (restricted, with the genus Fiona only), and Tergipedidae Bergh, 1889 s.str. (restricted, with inclusion of the genus Tergipes only) are restored. The families Cuthonidae Odhner, 1934 s.str. (restricted, with only single genus Cuthona), Cuthonellidae Miller, 1971, stat. nov., and Trinchesiidae Nordsieck, 1972 (with inclusion of the genera Catriona, Diaphoreolis, Phestilla, Tenellia, Trinchesia) are reinstated. At the genus level, the family Trinchesiidae appears as a most diverse assemblage that needs to be further divided. In the present study, the “Eolis pustulata species complex is particularly investigated, including description of a new ontogenetically different species Zelentia ninel sp. nov. “Eolis” pustulata Alder & Hancock, 1854 and two closely related species are morphologically well separated from Trinchesia s. str. (absence of foot corners, narrow radular teeth) and form a distinct molecular phylogenetic clade basal to all the other Trinchesiidae. Therefore, this group is a distinct unit according to both morphological and molecular data and is separated here as a new genus, Zelentia gen. nov. The genus Catriona is also briefly discussed and the valid status of the species Catriona aurantia (Alder et Hancock, 1842) stat. nov. is confirmed.

 

References

  1. Albert, V.A., Gustafsson, M.H.G. & Di Laurenzio, L. (1998) Ontogenetic systematics, molecular developmental genetics, and the angiosperm petal. In: Soltis, P.S., Soltis, D.E. & Doyle, J.J. (Eds.), Molecular systematics of plants II: Kluwer Academic Publishers, Boston, MA, pp. 349–374.
    https://doi.org/10.1007/978-1-4615-5419-6_12

    Anton, R.F., Schories, D., Wilson, N.G., Wolf, M., Abad, M. & Schrödl, M. (2016) Host specificity versus plasticity: testing the morphology-based taxonomy of the endoparasitic copepod family Splanchnotrophidae with COI barcoding. Journal of the Marine Biological Association of the United Kingdom. [published online]
    https://doi.org/10.1017/S002531541600120X

    Alder, J. & Hancock, A. (1842) Descriptions of several new species of nudibranchous Mollusca found on the coast of Northumberland. Annals & Magazine of Natural History, 9, 31–36.

    Alder, J. & Hancock, A. (1854) Notice of some new species of British Nudibranchiata. Annals & Magazine of Natural History, Series 2, 14, 102–105.
    https://doi.org/10.1080/037454809494312

    Alder, J. & Hancock, A. (1845–1855) A monograph of the British nudibranchiate Mollusca: with figures of all the species. Pt. 1–7. Ray Society, London, 48 pls., 54 pp. + xl pp. [Appendix]

    Baba, K. (1961) Three new species of the genus Catriona from Japan (Nudibranchia - Eolidacea). Publications of the Seto Marine Biological Laboratory, 9, 367–372.
    https://doi.org/10.5134/175287

    Baba, K. (1962) Anatomical review of Subcuthona pallida Baba (Nudibranchia - Eolidacea). Publications of the Seto Marine Biological Laboratory, 10, 241–243.
    https://doi.org/10.5134/175312

    Baba, K. (1975) Description of Trinchesia diversicolor spec. nov. from the Japan Sea coast of Middle Japan (Nudibranchia: Eolidoidea: Cuthonidae). Veliger, 17, 251–254.

    Behrens, D.W. (1980) Pacific coast nudibranchs, a guide to the opisthobranchs of the northeastern Pacific. Sea Challengers, Los Osos, 112 pp.

    Behrens, D.W. (1991) Pacific coast nudibranchs: a guide to the opisthobranchs, Alaska to Baja California. 2nd Edition. Sea Challengers, Monterey, California,107 pp.

    Bergh, R. (1874) Neue Nacktschnecken der Südsee, malacologische Untersuchungen II. Journal des Museum Godeffroy, 2, 91–116.

    Bergh, R. (1884) Report on the Nudibranchiata dredged by H.M.S. Challenger during the years 1873-1876. Report of the Scientific Results of the Voyage of H.M.S. Challenger during the years 1873–76, Zoology, 10, 1–154.

    Bergh, R. (1889) Carus, J.V. (1889–1893) Prodromus Faunae Mediterraneae sive descriptio animalium Maris Mediterranei. Vol. II. Brachiostomata, Mollusca, Tunicata, Vertebrata. E. Schweizerbarfsche Verlagsliandhing (E. Koch), Stuttgart, 854 pp. [854S]

    Bocak, L., Kundata, R., Andujar Fernandez, C. & Vogler, A.P. (2016) The discovery of Iberobaeniidae (Coleoptera: Elateroidea): a new family of beetles from Spain, with immatures detected by environmental DNA sequencing. Proceedings of the Royal Society B: Biological Sciences, 283, 20152350.
    https://doi.org/10.1098/rspb.2015.2350

    Carmona, L., Pola, M., Gosliner, T.M. & Cervera, J.L. (2013) A tale that morphology fails to tell: A molecular phylogeny of Aeolidiidae (Aeolidida, Nudibranchia, Gastropoda). PLoS ONE, 8, e63000.
    https://doi.org/10.1371/journal.pone.0063000

    Cella, K., Carmona, L., Schepetov, D. & Gosliner, T.M. (2016) A Radical Solution: The phylogeny of the nudibranch family Fionidae. PLoS ONE, 11 (12), e0167800.
    https://doi.org/10.1371/journal.pone.0167800

    Costa, A. (1866) Saggio sui molluschi eolididei del Golfo di Napoli. Annuario del Museo Zoologico della Universita di Napoli, 3, 59–80.

    Couthouy, J.P. (1838) Descriptions of new species of Mollusca and shells, and remarks on several Polypi found in Massachusetts Bay. Boston Journal of Natural History, 2, 53–111

    Cuvier, G. (1805) Mémoire sur la Scyllee, l'Eolide et le Glaucus, avec des additions au mémoire sur la Tritonie. Annales de Museum National d'Histoire Naturelle, 6, 416–436.

    Danchin, E., Charmantier, A. & Champagne, F.C., Mesoudi, A., Pujol, B. & Blanchet, S. (2011) Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nature Revue Genetics, 12, 475–486.
    https://doi.org/10.1038/nrg3028

    Debelius, H. & Kuiter, R.H. (2007) Nudibranchs of the World. Hollywood Import & Export, Inc., 360 pp.

    Dias, B.G. & Ressler, K.J. (2013) Parental olfactory experience influences behavior and neural structure in subsequent generations. Nature Neuroscience, 17, 89–96.
    https://doi.org/10.1038/nn.3594

    Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
    https://doi.org/10.1093/nar/gkh340

    Edmunds, M. (1970) Opisthobranchiate Mollusca from Tanzania. II. Eolidacea (Cuthonidae, Piseinotecidae and Facelinidae). Proceedings of the Malacological Society of London, 39, 15–57.

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

    Forbes, E. & Hanley, S. (1850–1851) [1853] A history of the British Mollusca, and their shells, vol. III. Including the families of Gasteropoda from Neritidae to Elysiadae. John Van Voorst, London, 616 pp.

    Ihering, H. von (1879) Einiges neue über Mollusken. Zoologische Anzeiger, 2, 136–138.

    Gosliner, T.M. (1979) The systematics of the Aeolidacea (Nudibranchia: Mollusca) of the Hawaiian Islands, with descriptions of two new species. Pacific Science, 33, 37–77.

    Gosliner, T.M., Behrens, D.W. & Valdés, Á. (2008) Indo-Pacific nudibranchs and sea slugs, afield guide to the world’s most diverse fauna. Sea Challengers & California Academy of Sciences, San Francisco, CA, 426 pp.

    Iredale, T. & O'Donoghue, C.H. (1923) List of British nudibranchiate Mollusca. Proceedings of the Malacological Society of London, 15, 195–200.

    Irie, N. & Kuratani, S. (2011) Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nature Communications, 2, 248.
    https://doi.org/10.1038/ncomms1248

    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
    https://doi.org/10.1093/molbev/msw054

    Layton, K., Martel, A. & Hebert, P. (2014) Patterns of DNA barcode variation in Canadian marine molluscs. PLoS ONE, 9 (4), e95003.
    https://doi.org/10.1371/journal.pone.0095003

    Levin, M., Anavy, L., Cole, A.G., Winter, E., Mostov, N., Khair, S., Senderovich, N., Kovalev, E., Silver, D.H., Feder, M., Fernandez-Valverde, S.L., Nakanishi, N., Simmons, D., Simakov, O., Larsson, T., Liu, S.Y., Jerafi-Vider, A., Yaniv, K., Ryan, J.F., Martindale, M.Q., Rink, J.C., Arendt, D., Degnan, S.M., Degnan, B.M., Hashimshony, T. & Yanai, I. (2016) The mid-developmental transition and the evolution of animal body plans. Nature, 531, 637–641.
    https://doi.org/10.1038/nature16994

    MacFarland, F.M. (1966) Studies of opisthobranchiate mollusks of the Pacific coast of North America. Memoirs of the California Academy of Sciences, 6, 1–546.

    Martynov, A.V. (1992) A new species of nudibranch molluscs of the Sea of Japan with notes on the genus Cuthonella (Gastropoda, Opisthobranchia). Zoologicheskij Zhurnal, 71, 18–24.

    Martynov, A.V. (2002) Two new species of the genus Trinchesia Ihering, 1879 from Peter the Great Bay, Japan Sea (Nudibranchia, Tergipedidae), with notes on the taxonomy of the family. Ruthenica, 12, 45–54.

    Martynov, A.V. (2006) Archaic Tergipedidae of the Arctic and Antarctic: Murmania antiqua gen. et sp. nov. from the Barents Sea and a revision of the genus Guyvalvoria Vayssière with descriptions of two new species. Ruthenica, 16, 73–88.

    Martynov, A.V. (2011) From “tree-thinking” to “cycle-thinking”: ontogenetic systematics of nudibranch molluscs. Thalassas, 27, 193–224.

    Martynov, A.V. & Korshunova, T.A. (2015) A new deep-sea genus of the family Polyceridae (Nudibranchia) possesses a gill cavity, with implications for the cryptobranch condition and a ‘Periodic Table’ approach to taxonomy. Journal of Molluscan Studies, 81, 365–379.
    https://doi.org/10.1093/mollus/eyv003

    Martynov, A.V., Korshunova, T.A. & Savinkin, O.V. (2006) Shallow-water opisthobranch molluscs of the Murman coast of the Barents Sea, with new distributional data and remarks on biology. Ruthenica, 16, 59–72.

    Martynov, A., Ishida, Y., Irimura, S., Tajiri, R., O’Hara, T. & Fujita, T. (2015) When ontogeny matters: A new Japanese species of brittle star illustrates the importance of considering both adult and juvenile characters in taxonomic practice. PLoS ONE, 10 (10), e0139463.
    https://doi.org/10.1371/journal.pone.0139463

    Martynov, A. & Schrödl, M. (2011) Phylogeny and evolution of corambid nudibranchs (Mollusca: Gastropoda). Zoological Journal of the Linnean Society, 163, 585–604.
    https://doi.org/10.1111/j.1096-3642.2011.00720.x

    Millen, S.V. (1986) Northern, primitive tergipedid nudibranchs, with a description of a new species from the Canadian Pacific. Canadian Journal of Zoology, 64, 1356–1362.
    https://doi.org/10.1139/z86-202

    Miller, M.C. (1977) Aeolid nudibranchs (Gastropoda: Opisthobranchia) of the family Tergipedidae from New Zealand waters. Zoological Journal of the Linnean Society, 60, 197–222.
    https://doi.org/10.1111/j.1096-3642.1977.tb01027.x

    Miller, M.C. (2004) An appraisal of the identity of the New Zealand species of the aeolid nudibranch family Tergipedidae (Gastropoda: Opisthobranchia). Journal of Natural History, 38, 1183–1192.
    https://doi.org/10.1080/0022293031000077699

    Moles, J., Wägele, H., Cutignano, A., Fontana, A., Ballesteros, M. & Avila, C. (2017) Giant embryos and hatchlings of Antarctic nudibranchs (Mollusca: Gastropoda: Heterobranchia). Marine Biology, 164, 1–13.
    https://doi.org/10.1007/s00227-017-3143-8

    Nordmann, A. von (1845) Versuch einer Natur- und Entwicklungsgeschichte des Tergipes Edwardsii. VI. Serie. Memoires, presentes parr Divers Savants. Memoires de l'Accademie Imperiale des Sciences de St. Petersbourg, Series 6, 4, 497–602.

    Nordsieck, F. (1972) Die europäischen Meeresschnecken (Opisthobranchia mit Pyramidellidae; Rissoacea), Vom Eismeer bis Kapverden, Mittelmeer und Schwarzes Meer. Gustav Fischer Verlag, Stuttgart, 327 pp. [327S]

    Odhner, N.H. (1934) The Nudibranchiata. British Antarctic (“Terra Nova”) Expedition, 1910. British Museum (Natural History) Natural History Report, Zoology, 7, 229–310.

    O'Donoghue, C.H. (1922) Notes on the nudibranchiate Mollusca from the Vancouver Island region. III. Records of species and distribution. Transactions of the Royal Canadian Institute, 14, 145–167.

    Padial, J.M., Miralles, A., De La Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, 16.
    https://doi.org/10.1186/1742-9994-7-16

    Padula, V., Araújo, A.K., Mathews-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, 80, 575–584.
    https://doi.org/10.1093/mollus/eyu052

    Picton, B.E. & Brown, G.H. (1978) A new species of Cuthona (Gastropoda: Opisthobranchia) from the British Isles. Journal of Conchology, 29, 345–348.

    Pievani, T. (2016) How to rethink evolutionary theory: a plurality of evolutionary patterns. Evolutionary Biology, 43, 446–455.
    https://doi.org/10.1007/s11692-015-9338-3

    Putz, A., König, G.M. & Wägele, H. (2010) Defensive strategies of Cladobranchia (Gastropoda, Opisthobranchia). Natural Product Reports, 27, 1386–1402.
    https://doi.org/10.1039/b923849m

    Rudman, W.B. (1981) Further studies on the anatomy and ecology of opisthobranch molluscs feeding on the scleractinian coral Porites. Zoological Journal of the Linnean Society, 71, 373–412.
    https://doi.org/10.1111/j.1096-3642.1981.tb01136.x

    Rudman, W.B. (1998) Suborder Aeolidina. In: Pamela, L., Beesley, G., Ross, J.B. & Wells, A. (Eds.), Mollusca: the southern synthesis. Fauna of Australia. Vol. 5. Part B. CSIRO Publishing, Melbourne, pp. 1011–1017.

    Rudman, W.B. (2007) Comment on Phestilla melanobrachia from Bali by Mike Krampf. Message in Sea Slug Forum, Australian Museum, Sydney. Available from: http://www.seaslugforum.net/find/20365 (accessed 13 September 2017)

    Sharma, A. (2017) Transgenerational epigenetics: Integrating soma to germline communication with gametic inheritance. Mechanisms of Ageing and Development, 163, 15–22.
    https://doi.org/10.1016/j.mad.2016.12.015

    Stöhr, S. & Martynov, A. (2016) Paedomorphosis as an evolutionary driving force: Insights from deep-dea brittle stars. PLoS ONE, 11 (11), e0164562.
    https://doi.org/10.1371/journal.pone.0164562

    Tardy, J.P. (1970) Contribution a l'étude des métamorphoses chez les nudibranches. Annales des Sciences Naturelles (Zoologie), 12, 299–370.

    Thompson, T.E. & Brown, G.H. (1984) Biology of opisthobranch molluscs. Vol. 2. No. 156. Ray Society, London, 229 pp.

    Trickey, J.S., Thiel, M. & Waters, J.M. (2016) Transoceanic dispersal and cryptic diversity in a cosmopolitan rafting nudibranch. Invertebrate Systematics, 30, 290–301.
    https://doi.org/10.1071/IS15052

    Winckworth, R. (1941) The name Cratena. Proceedings of the Malacological Society of London, 24, 146–149.
    https://doi.org/10.1093/oxfordjournals.mollus.a064404