Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2022-05-05
Page range: 383-406
Abstract views: 1330
PDF downloaded: 56

Attack on crypsis: Molecular and morphological study of Dendrodoris Ehrenberg, 1831 (Mollusca: Gastropoda: Nudibranchia) from the Mediterranean Sea and Northern Atlantic Ocean reinstates Dendrodoris temarana Pruvot-Fol, 1953

Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Universitat de Barcelona, Avda. Diagonal, 643, 08028 Barcelona, Spain 2Departament de Genètica, Microbiologia i Estadística, Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Avinguda Diagonal 643 CP 08028, Barcelona, Spain
Departamento de Biología, Facultad de Ciencias del Mar y Ambientales, Campus de Excelencia Internacional del Mar (CEIMAR), Universidad de Cádiz, Av. República Saharaui, s/n, P.O. Box 40, 11510 Puerto Real (Cádiz), Spain.
Department of Biological Sciences, California State Polytechnic University Pomona, 3801 West Temple Avenue, Pomona, California 91768, USA
Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Universitat de Barcelona, Avda. Diagonal, 643, 08028 Barcelona, Spain
Mollusca Species complex radula-less dorid Dendrodorididae chromatic pattern biodiversity Heterobranchia

Abstract

The genus Dendrodoris is ascribed to the family Dendrodorididae, whose members are characterized lacking spicules in the dorsum as well as a radula, one of the most important taxonomic traits to distinguish and define nudibranch species. The absence of this taxonomic character makes difficult to delineate species based on morphologic traits, and consequently, several cryptic species may remain unreported resulting in a potential underestimation of the real diversity of the genus. Species delimitation analyses based on molecular data constitute an important tool to unveil cryptic species, especially when morphology may be misleading. However, for the genus Dendrodoris, only two molecular studies have been performed to date, both based on Indo-pacific species and the molecular marker COI. In the present study, we performed a multilocus approach using the molecular markers COI, 16S and H3 based on 47 Dendrodoris specimens from the North Atlantic Ocean and Mediterranean Sea. As a result, we detected monophyly for five of the previously accepted species plus the presence of an unidentified one. Using morphological and anatomical data from 14 additional individuals and a review of the literature, we verified this unidentified species is the previously synonymized species Dendrodoris temarana Pruvot-Fol, 1953, and we redescribe it morphologically (chromatic pattern, gills, rhinophores and anal papilla), anatomically (neural, circulatory, digestive and reproductive systems), and biologically herein. D. temarana is differentiated by its chromatic pattern, previously thought to be intraspecific variation of D. grandiflora (Rapp, 1827), D. limbata (Cuvier, 1804) and D. herytra Valdés & Ortea in Valdés, Ortea, Avila & Ballesteros, 1996, and therefore it is considered a pseudocryptic species. This study increases the number of valid species in the North Atlantic and Mediterranean to nine and confirms the importance of integrative taxonomic approaches to resolve the identification of cryptic species in complex groups.

 

References

  1. Appeltans, W., Ahyong, S.T., Anderson, G., Angel, M.V., Artois, T., Bailly, N., Bamber, R., Barber, A., Bartsch, I., Berta, A., Błażewicz-Paszkowycz, M., Bock, P., Boxshall, G., Boyko, C.B., Brandão, S.N., Bray, R.A., Bruce, N.L., Cairns, S.D., Chan, T., Cheng, L., Collins, A.G., Cribb, T., Curini-Galletti, M., Gordon, D.P., Guiry, M.D., Hernandez, F., Hoeksema, B.W., Hopcroft, R.R., Jaume, D., Kirk, P., Koedam, N., Koenemann, S., Kolb, J.B., Kristensen, R.M., Kroh, A., Lambert, G., Lazarus, D.B., Lamaitre, R., Longshaw, M., Lowry, J., Macpherson, E., Madin, L.P., Mah, C., Mapstone, G., McLaughlin, P.A., Mees, J., Meland, K., Messing, C.G., Mills, C.E., Molodtsova, T.N., Mooi, R., Nehaus, B., Ng, P.K., Nielsen, C., Norenburg, J., Opresko, D.M., Osawa, M., Paulay, G., Perrin, W., Pilger, J.F., Poore, G.C., Pugh, P., Read, G.B., Reimer, J.D., Rius, M., Roch, R.M., Saiz-Salinas, J.I., Scarabino, V., Schierwater, B., Schmidt-Rhaesa, A., Schnabel, K.E., Schotte, M., Schuchert, P., Schwabe, E., Segers, H., Self-Sullivan, C., Shenkar, N., Siegel, V., Sterrer, W., Stöhr, S., Swalla, B., Tasker, M.L., Theusen, E.V., Timm, T., Todaro, M.A., Turon, X., Tyler, S., Uetz, P., van der Land, J., Vanhoorne, B., van Ofwegen, L.P., van Soest, R.W., Vanaverbeke, J., Walker-Smith, G., Walter, T.C., Warren, A., Williams, G.C., Wilson, S.P., Costello, M.J. (2012) The magnitude of global marine species diversity. Current Biology, 22, 1–14. https://doi.org/10.1016/j.cub.2012.09.036
    Araujo, A.K., Pola, M., Malaquias, M.A.E. & Cervera, J.L. (2019) To be or not to be? What molecules say about Runcina brenkoae Thompson, 1980 (Gastropoda: Heterobranchia: Runcinida). Scientia marina, 83 (3), 223–235. https://doi.org/10.3989/scimar.04907.07A
    Araujo, A.K., Pola, M., Malaquias, M.A.E., Ballesteros, M., Vitale, F. & Cervera, J.L. (2021) Molecular phylogeny of European Runcinida (Gastropoda, Heterobranchia): the discovery of an unexpected pool of species complex, with special reference to the case of Runcina coronata. Zoological Journal of the Linnean Society, 194, 761–788. https://doi.org/10.1093/zoolinnean/zlab041
    Ballesteros, M. (1978) Contribución al conocimiento de la fauna bentónica de Cubellas. Publicaciones del Departamento de Zoología, III, 11–23.
    Ballesteros, M. (1984) Adición a la fauna de Opistobranquios de Cubellas. Miscelánea Zoológica, VIII, 41–49.
    Ballesteros, M. (1985) Contribución al conocimiento de los Ascoglosos y Nudibranquios. Publicaciones Ediciones Universidad de Barcelona, 1985, 1–46.
    Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution, 22 (3), 148–155. https://doi.org/10.1016/j.tree.2006.11.004
    Bouchet, P. (1975) Nudibranches nouveaux des côtes du Senegal. Vie et Milieu, 25, 119–132.
    Brodie, G. & Calado, G. (2006) Dendrodoris arborescens (Collingwood, 1881) (Mollusca: Nudibranchia): larval characteristics reveal a masked porostome species. Records of the Western Australian Museum Supplement No. 69, 119–126.
    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, 419–437. https://doi.org/10.1071/ZO98048
    Cuvier, G. (1804) Mémorie sur le genre Doris. Annales du Muséum National d’Historie Naturelle, Paris, 4, 447–473.
    Cyrne, R., Rosa, I.C., Faleiro, F., Dionísio, G., Baptista, M., Couto, A., Pola, M. & Rosa, R. (2018) Nudibranchs out of water: Long-term temporal variations in the abundance of two Dendrodoris species under emersion. Helgoland Marine Research, 72 (14). [published online] https://doi.org/10.1186/s10152-018-0516-4
    Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. (2015) jModelTest 2: more models, new heuristics and high- performance computing. Nature Methods, 9 (8), 772. https://doi.org/10.1038/nmeth.2109
    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
    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 (5), 294–299.
    Galià-Camps, C., Carmona, L., Cabrito, A. & Ballesteros, M. (2020) Double trouble. A cryptic first record of Berghia marinae Carmona, Pola, Gosliner, & Cervera 2014 in the Mediterranean Sea. Mediterranean Marine Science, 21 (1), 191–200. https://doi.org/10.12681/mms.20026
    García-Gómez, J.C. (1984) Bulomorfos, ascoglosos y nudibranquios (Mollusca: Opisthobranchia) del estrecho de Gibraltar con algunas referencias al litoral onubense: estudio morfoanatómico, sistemático, faunístico y zoogeográfico. Unpublished PhD Thesis, Universidad de Sevilla, Sevilla. [unknown pagination]
    Goddard, J.H. (2005) Ametamorphic direct development in Dendrodoris behrensi (Nudibranchia: Dendrodorididae), with a review of developmental mode in the family. Proceedings of the California Academy of Sciences, Series 4, 56 (19), 201–211.
    Golestani, H., Crocetta, F., Padula, V., Camacho-García, Y., Langeneck, J., Poursanidis, D., Pola, M., Yokeş, M.B., Cervera, J.L., Jung, D.-W., Gosliner, T.M., Araya F., Hooker, Y., Schrödl, M. & Valdés, Á. (2019). The little Aplysia’s coming of age: From one species to a complex of species complexes in Aplysia parvula Mörch, 1863 (Mollusca, Gastropoda, Heterobranchia). Zoological Journal of the Linnean Society, 187 (2), 279–330. https://doi.org/10.1093/zoolinnean/zlz028
    Gómez-Álvarez, G. (2017) Guía de moluscos marinos de Huelva y del Golfo de Cádiz: con más de 250 espécies. Diputación Provincial de Huelva. Servicio de Publicaciones, Huelva, 300 pp.
    Goodheart, J., Camacho-García, Y., Padula, V., Schrödl, M., Cervera, J.L., Gosliner, T.M. & Valdés, Á. (2015) Systematics and biogeography of Pleurobranchus Cuvier,1804 sea slugs (Mollusca: Gastropoda: Heterobranchia: Nudipleura: Pleurobranchidae). Zoological Journal of the Linnean society, 174, 322–362. https://doi.org/10.1111/zoj.12237
    Hallas, J.M., Chichvarkhin, A. & Gosliner, T.M. (2017) Aligning evidence: concerns regarding multiple sequence alignments in estimating the phylogeny of the Nudibranchia suborder Doridina. Royal Society Open Science, 4 (10), 171095. https://doi.org/10.1098/rsos.171095
    Hillis, D.M. & Bull, J.J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42,182–192. https://doi.org/10.1093/sysbio/42.2.182
    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.
    Hoover, C., Lindsay, T., Goddard, J.H.R. & Valdés, A. (2015) Seeing double: pseudocryptic diversity in the Doriopsilla albopunctata-Doriopsilla gemela species complex of the north-eastern Pacific. Zoological Scripta, 44 (6), 612–631. https://doi.org/10.1111/zsc.12123
    Huelsenbeck, J.P. & Rannala, B. (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology, 53, 904–913. https://doi.org/10.1080/10635150490522629
    Korshunova, T., Fletcher, K., Picton, B., Lundin, K., Kashio, S., Sanamyan, N., Sanamyan, K., Padula, V., Schrödl, M. & Martynov, A. (2020) The Emperor’s Cadlina, hidden diversity and gill cavity evolution: new insights for the taxonomy and phylogeny of dorid nudibranchs (Mollusca: Gastropoda). Zoological Journal of the Linnean Society, 189 (3), 762–827. https://doi.org/10.1093/zoolinnean/zlz126
    Korshunova, T., Martynov, A. & Picton, B. (2017) 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. Zootaxa, 4324(1), 1–22. https://doi:10.11646/zootaxa.4324.1.1
    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33 (7), 1870–1874. https://doi.org/10.1093/molbev/msw054
    Layton, K.K., Gosliner, T.M. & Wilson, N.G. (2018) Flexible colour patterns obscure identification and mimicry in Indo-Pacific Chromodoris nudibranchs (Gastropoda: Chromodorididae). Molecular Phylogenetics and Evolution, 124, 27–36. https://doi.org/10.1016/j.ympev.2018.02.008
    Marcus, E. & Gallagher, S.B. (1976) A new species of Dendrodoris from Florida. Veliger, 18, 353–356.
    Marsh, A.C., Ribbink, A.J. & Marsh, B.A. (1981) Sibling species complexes in sympatric populations of Petrotilapia Trewavas (Cichlidae, Lake Malawi). Zoological Journal of the Linnean Society, 71 (3), 253–264. https://doi.org/10.1111/j.1096-3642.1981.tb01132.x
    Martín-Hervás, M.R., Carmona, L., Jensen, K.R., Licchelli, C., Vitale, F. & Cervera, J.L. (2020) Description of a new pseudocryptic species of Elysia Risso, 1818 (Heterobranchia, Sacoglossa) in the Mediterranean Sea. Bulletin of Marine Science, 96 (1), 127–143. https://doi.org/10.5343/bms.2018.0087
    McCarthy, J.B., Krug, P.J. & Valdés, Á. (2019) Integrative systematics of Placida cremoniana (Trinchese, 1892) (Gastropoda, Heterobranchia, Sacoglossa) reveals multiple pseudocryptic species. Marine Biodiversity, 49, 357–371. https://doi.org/10.1007/s12526-017-0812-2
    MolluscaBase (Eds.) (2022) MolluscaBase. Dendrodoris Ehrenberg, 1831. Accessed through: World Register of Marine Species. Available from: http://www.marinespecies.org/aphia.php?p=taxdetails&id=137883 (accessed 23 August 2021)
    Mörch, O.A.L. (1863) Contributions à la faune malacologique des Antilles Danoises. Journal de Conchyhology, 11, 21–43.
    Ortea, J. & Espinosa, J. (2001) Descripción de una nueva especie de Dendrodoris Ehrenberg, 1831. A new species of Dendrodoris Ehrenberg, 1831. Avicennia, (Supplement 4), 52–53.
    Padula, V., Bahia, J., Stöger, I., Camacho-García, Y., Malaquías, M.A.E., Cervera, J.L. & Schrödl, M. (2016) A test of color-based taxonomy in nudibranchs: molecular phylogeny and species delimitation of Felimida clenchi (Mollusca: Chromodorididae) species complex. Molecular Phylogenetics and Evolution, 103, 215–229. https://doi.org/10.1016/j.ympev.2016.07.019
    Palumbi, S., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabowski, G. (2002) The Simple Fool’s guide to PCR. Version 2.0. Department of Zoology and Kewalo Marine Laboratory, Honolulu, 45 pp.
    Park, J., Lee, Y., Shin, Y., Kim, T. & Park, J. (2019) Dendrodoris guttata (Nudibranchia: Dendrodorididae) from Korean Waters. Animal Systematics, Evolution and Diversity, 35 (1), 6–9. https://doi.org/10.5635/ASED.2019.35.1.039
    Pfenninger, M. & Schwenk, K. (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology, 7, 121. https://doi.org/10.1186/1471-2148-7-121
    Pola, M., Paz-Sedano, S., Macali, A., Minchin, D., Marchini, A., Vitale, F., Licchelli, C. & Crocetta, F. (2019) What is really out there? Review of the genus Okenia Menke, 1830 (Nudibranchia: Goniodorididae) in the Mediterranean Sea with description of two new species. PLoS ONE, 14 (5), e0215037. https://doi.org/10.1371/journal.pone.0215037
    Pruvot-Fol, A. (1951) Étude des Nudibranches de la Méditerranée. Archives de Zoologie Experimentale et Generale, 88,1–80.
    Pruvot-Fol, A. (1953) Étude de quelques Opisthobranches de la Côte Atlantique du Maroc et du Sénégal. Travaux de l´Institut Scientifique Chérifien, 5, 1–93.
    Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21, 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
    Rambaut, A. (2014) FigTree. Version 1.4.2. Institute of Evolutionary Biology, The University of Edinburgh, Edinburgh. [software]
    Rapp, W. (1827) Über das Molluskengeschlecht Doris und Beschreibung einiger neuen Arten desselben. Nova Acta Physico-Medica Academiae Caesareae Leopoldino-Carolinae Naturae Curiosorum, 13, 515–522.
    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
    Rose, R.A. (1985) The spawn and embryonic development of colour variants of Dendrodoris nigra Stimpson (Mollusca: Nudibranchia). Journal of the Malacological Society of Australia, 7 (1–2), 75–88. https://doi.org/10.1080/00852988.1985.10673977
    Rüppell, E. & Leuckart, F.S. (1830) s.n .In: Atlas zu der Reise im nordlichen Afrika van Eduard Rüppell. Zoology Neue wirbellose Thiere des Rothen Meers. Gedruckt und in Commission bei Heinr. Ludw. Brönner, Frankfurt am Main, pp. 15–47.
    Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and Phylogenetic Utility of Mitochondrial Gene Sequences and a complitation of Conserved Polymerase Chain Reaction Primers. Annals of the Entomological Society of America, 87 (6), 651–701. https://doi.org/10.1093/aesa/87.6.651
    Stamatakis A. (2014) RAxML version 8: a tool for phylogenetic analysis and post–analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
    Swindell, S.R. & Plasterer, T.N. (1997) SEQMAN. Contig assembly. Methods in Molecular Biology, 70, 75–89.
    Valdés, A., Ortea, J.A., Ávila, C. & Ballesteros, M. (1996) Review of the genus Dendrodoris Ehrenberg, 1831 (Gastropoda: Nudibranchia) in the Atlantic Ocean. Journal of Molluscan Studies, 62 (1), 1–31. https://doi.org/10.1093/mollus/62.1.1
    Valdés, A. & Behrens, D.W. (1998) A new species of Doriopsilla (Mollusca, Nudibranchia, Dendrodorididae) from the Pacific coast of North America. Proceedings-California Academy of Sciences, 50, 307–314.
    Valdés, Á. & Gosliner, T.M. (1999) Phylogeny of the radula-less dorids (Mollusca, Nudibranchia), with the description of a new genus and a new family. Zoologica Scripta, 28 (3–4), 315–360. https://doi.org/10.1046/j.1463-6409.1999.00014.x
    Wirtz, P. (1995) Unterwasserführer Madeira, Kanaren/Azoren. Delius Klasing, Edition Naglschmid. [unknown pagination]
    Wirtz, P. (1998) Opisthobranch molluscs from the Azores. Vita Marina, 45, 1–16.
    Zenetos, A., Çinar, M.E., Crocetta, F., Golani, D., Rosso, A., Servello, G., Shenkar, N., Turon, X., Verlaque, M. (2017) Uncertainties and validation of alien species catalogues: the Mediterranean as an example. Estuarine, Coastal and Shelf Science, 191, 171–187. https://doi.org/10.1016/j.ecss.2017.03.031
    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

  2.  

  3.