Molecular and morpho-anatomical assessment of the family Dorididae (Mollusca, Nudibranchia) in the Mediterranean and North-East Atlantic
Abstract
In the present study, a revision of the phylogeny and taxonomy of the family Dorididae is carried out focusing on the genus Doris Linnaeus, 1758. The type species D. verrucosa Linnaeus, 1758 and a blueish and yellow morphotype of D. ocelligera collected in different localities in the Mediterranean Sea and the North-East Atlantic were sequenced, as well as D. bertheloti and the elusive D. marmorata for the first time. The genetic markers include the cytochrome c oxidase subunit I, 16S rRNA, and histone 3. The phylogenetic results suggest that the genus Doris is paraphyletic, and D. ocelligera morphotypes separate into two species, as confirmed with species delimitation tests. To complement the phylogenetic evidence with morphoanatomical data, the dissection of two specimens of each morphotype is conducted. Significant differences in morphological traits such as body shape, colouration patterns, and mantle tubercles come to light, together with anatomical differences in the relative shape and size of the radular teeth and reproductive structures. Considering the modern and old descriptions of D. ocelligera, it is finally concluded that the blueish morphotype belongs to D. ocelligera. In contrast, the yellow morphotype responds to the actual synonym Aldisa berghi (Vayssière, 1901), which is resurrected here as Doris berghi comb. rest. Considering the broad phylogeny of the family, some systematic notes at the genus level are here provided.
References
Altschul S. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389–3402. https://doi.org/10.1093/nar/25.17.3389
Araujo A.K., Pola M., Malaquias M.A.E., Ballesteros M., Vitale F. & Cervera J.L. 2022. Molecular phylogeny of European Runcinida (Gastropoda, Heterobranchia): the discover of an unexpected pool of complex species, 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
Ayres D.L., Cummings M.P., Baele G., Darling A.E., Lewis P.O., Swofford D.L., Huelsenbeck J.P., Lemey P., Rambaut A. & Suchard M.A. 2019. BEAGLE 3: improved performance, scaling, and usability for a high-performance computing library for statistical phylogenetics. Systematic Biology 68: 1052–1061. https://doi.org/10.1093/sysbio/syz020
Azevedo J.M.N. & Gofas S. 1990. Moluscos marinhos litorais da ilha das Flores. Relatórios e Comunicações do Departamento de Biologia 18: 83–87. Available from http://hdl.handle.net/10400.3/856 [accessed 13 May 2024].
Bergh R. 1881. Malacologische untersuchungen. In: Reisen im Archipel der Philippinen von Dr. Carl Gottfried Semper. Zweiter Theil. Wissenschaftliche Resultate 9: 119–181.
Bianchi C.N. & Morri C. 2000. Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Marine Pollution Bulletin 40: 367–376. https://doi.org/10.1016/S0025-326X(00)00027-8
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
Dinapoli A. & Klussmann-Kolb A. 2010. The long way to diversity – Phylogeny and evolution of the Heterobranchia (Mollusca: Gastropoda). Molecular Phylogenetics and Evolution 55: 60–76. https://doi.org/10.1016/j.ympev.2009.09.019
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.
Garzia M., Mariottini P., Salvi D. & Furfaro G. 2021. Variation and diagnostic power of the internal transcribed spacer 2 in Mediterranean and Atlantic eolid nudibranchs (Mollusca, Gastropoda). Frontiers in Marine Science 8: 693093. https://doi.org/10.3389/fmars.2021.693093
Hoang D.T., Chernomor O., von Haeseler A., Minh B.Q. & Vinh L.S. 2018. UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518–522. https://doi.org/ 10.1093/molbev/msx281
ICZN (International Commission on Zoological Nomenclature) 2001. Opinion 1980 (Case 3088). Doris verrucosa Linnaeus, 1758 (Mollusca, Gastropoda): generic and specific names conserved by the designation of a neotype. Bulletin of Zoological Nomenclature 58 (3): 237–238. Available from https://www.biodiversitylibrary.org/page/33818090 [accessed 13 May 2024].
Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A. & Jermiin L.S. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285
Katoh K. & Standley D.M. 2013. MAFFT multiple sequence alignment software Version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120. https://doi.org/10.1007/BF01731581
Korshunova T., Picton B., Furfaro G., Mariottini P., Pontes M., Prkić J., Fletcher K., Malmberg K., Lundin K. & Martynov A. 2019. Multilevel fine-scale diversity challenges the ‘cryptic species’ concept. Scientific Reports 9: 6732. https://doi.org/10.1038/s41598-019-42297-5
Koutsoubas D., Koukouras A. & Thompson T.E. 1993. Sacoglossa and Nudibranchia (Opisthobranchia) from the Aegean Sea: new records for the eastern Mediterranean fauna. Mitteilungen aus dem Zoologischen Museum in Berlin 69: 155–163.
Kurnianda V., Winahyu D.A., Firdaus R., Wahyudi E. & Musman M. 2020. Biological and chemical diversity of the Indonesian marine nudibranchs based on MS/MS molecular networking approach. Depik 9: 83–94. https://doi.org/10.13170/depik.9.1.15126
Le S.Q., Dang C.C. & Gascuel O. 2012. Modeling protein evolution with several amino acid replacement matrices depending on site rates. Molecular Biology and Evolution 29: 2921–2936. https://doi.org/10.1093/molbev/mss112
Lima P.O.V. & Simone L.R.L. 2015. Anatomical review of Doris verrucosa and redescription of Doris januarii (Gastropoda, Nudibranchia) based on comparative morphology. Journal of the Marine Biological Association of the United Kingdom 95: 1203–1220. https://doi.org/10.1017/S0025315415000296
McDonald G.R. & Nybakken J.W. 1997. A worldwide review of the food of nudibranch mollusks. I. Introduction and the suborder Arminacea. The Veliger 40: 157–159. [Supplementary material with details available from e-scholarship – University of California].
McDonald G.R. & Nybakken J.W. 1999. A worldwide review of the food of nudibranch mollusks. II. The suborder Dendronotacea. The Veliger 42: 62–66. [Supplementary material with details available from e-scholarship – University of California].
Moles J. & Giribet G. 2021. A polyvalent and universal tool for genomic studies in gastropod molluscs (Heterobranchia). Molecular Phylogenetics and Evolution 155: 106996. https://doi.org/10.1016/j.ympev.2020.106996
Odhner N.H. 1926. Die Opisthobranchien. In: Odhner T. & Bock S. (eds) Further Zoological Results of the Swedish Antarctic Expedition 1901–1903 under the direction of Dr. Otto Nordenskjold 2: 1–100. Available from https://www.biodiversitylibrary.org/page/62419725 [accessed 13 May 2024].
Ortea J., Moro L., Bacallado J.J. & Caballer M. 2014. Nuevas especies y primeras citas de babosas marinas (Mollusca: Opisthobranchia) en las islas Canarias y en otros archipiélagos de la Macaronesia. Vieraea Folia Scientiarum Biologicarum Canariensium 42: 47–77. https://doi.org/10.31939/vieraea.2014.42.04
Palumbi S.R., Martin A., Romano S., McMillan W.O., Stice L. & Grabowski G. 1991. The Simple Fool’s Guide to PCR, Version 2.0. Privately published document compiled by S. Palumbi, Department of Zoology, University of Hawaii, Honolulu.
Posada D. 2003. Using MODELTEST and PAUP* to select a model of nucleotide substitution. Current Protocols in Bioinformatics 6: unit 6.5. https://doi.org/10.1002/0471250953.bi0605s00
Pruvot-Fol A. 1954. Mollusques opisthobranches. Faune de France 58. P. Lechevalier, Paris.
Puillandre N., Brouillet S. & Achaz G. 2021. ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21: 609–620. https://doi.org/10.1111/1755-0998.13281
Risso A. 1818. Mémoire sur quelques gastéropodes nouveaux, nudibranches et tectibranches observés dans la Mer de Nice. Journal de Physique, de Chimie, d’Histoire naturelle et des Arts, 87: 368–377. Available from https://www.biodiversitylibrary.org/page/6173832 [accessed 13 May 2024].
Risso A. 1826. Histoire naturelle des principales Productions de l’Europe méridionale et particulièrement de celles des Environs de Nice et des Alpes Maritimes Vol. 4. F.-G. Levrault, Paris. https://doi.org/10.5962/bhl.title.58984
Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
Schmekel R.L. 1968a. Ascoglossa, Notaspidea und Nudibranchia im Litoral des Golfes von Neapel. Revue Suisse de Zoologie 75: 103–155. Available from https://www.biodiversitylibrary.org/page/43207505 [accessed 13 May 2024].
Schmekel R.L. 1968b. Die Gattung Doris (Gastr. Nudibranchia) im Golf von Neapel. Pubblicacioni della Stazione Zoologica di Napoli 36: 167–187.
Schmekel L. & Portmann A. 1982. Opisthobranchia des Mittelmeeres. Springer, Berlin. https://doi.org/10.1007/978-3-642-61817-8
Tavaré S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. American Mathematical Society: Lectures on Mathematics in the Life Sciences 17: 57–86.
Urgorri V., Pérez Señarís M., Díaz Agras G., Candás Romero M., Gómez Rodríguez C. 2021. Doris adrianae sp. nov. (Heterobranchia; Nudibranchia; Doridina) from the Galician coasts (NW Iberian Peninsula). Nova Acta Científica Compostelana 28: 1–33. https://doi.org/10.15304/nacc.id7500
Valdés Á. 2002. A phylogenetic analysis and systematic revision of the cryptobranch dorids (Mollusca, Nudibranchia, Anthobranchia). Zoological Journal of the Linnean Society 136: 535–636. https://doi.org/10.1046/j.1096-3642.2002.00039.x
Valdés Á. 2004. Phylogeography and phyloecology of dorid nudibranchs (Mollusca, Gastropoda). Biological Journal of the Linnean Society 83: 551–559. https://doi.org/10.1111/j.1095-8312.2004.00413.x
Valentine J.W. & Jablonski D. 2015. A twofold role for global energy gradients in marine biodiversity trends. Journal of Biogeography 42: 997–1005. https://doi.org/10.1111/jbi.12515
Vayssière A. 1885. Recherches zoologiques et anatomiques sur les Mollusques Opistobranches du Golfe de Marseille. Typ. J. Cayer, Marseille. https://doi.org/10.5962/bhl.title.11753
Vayssière A. 1901. Recherches zoologiques et anatomiques sur les Mollusques Opistobranches du Golfe de Marseille. Troisième partie. Nudibranches (suite et fin). Annales du Musée d’Histoire naturelle de Marseille 6: 1–130. https://doi.org/10.5962/bhl.title.11753
Wägele H. 1990. Revision of the genus Austrodoris Odhner, 1926 (Gastropoda, Opisthobranchia). Journal of Molluscan Studies 56: 163–180. https://doi.org/10.1093/mollus/56.2.163
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. https://doi.org/10.1111/j.1365-294X.2008.04071.x
Wollscheid-Lengeling E., Boore J., Brown W. & Wägele H. 2001. The phylogeny of Nudibranchia (Opisthobranchia, Gastropoda, Mollusca) reconstructed by three molecular markers. Organisms Diversity & Evolution 1: 241–256. https://doi.org/10.1078/1439-6092-00022
WoRMS Editorial Board 2023. World Register of Marine Species. Available from https://www.marinespecies.org/ [accessed 13 May 2024].
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