Abstract
This paper describes four new Chromodoris species: Chromodoris balat sp. nov., Chromodoris baqe sp. nov., Chromodoris kalawakan sp. nov., and Chromodoris quagga sp. nov. We were able to distinguish 44 species level lineages within Chromodoris, expanding the Indo-Pacific species from 39 species. The phylogeny presented here provides slightly greater resolution of species relationships than do previous studies of this genus. Layton et al. (2018), determined that variable color patterns made it difficult to differentiate in living specimens of distinct species, but we provide some additional stable color characters that potentially help resolve this issue, as well as additional internal features that are useful in species delimitation and correlate with the molecular phylogenetic analysis.
References
Alder, J. & Hancock, A. (1855) A monograph of the British Nudibranchiate Mollusca. Part VII. Ray Society, London, 54 pp.
Alfaro, M.E., Zoller, S. & Lutzoni, F. (2003) Bayes or Bootstrap? A simulation study comparing the performance of Bayesian Markov Chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Molecular Biology and Evolution, 20, 255–266.
https://doi.org/10.1093/molbev/msg028
Almada, F., Levy, A. & Robalo, J.I. (2016) Not so sluggish: the success of the Felimare picta complex (Gastropoda, Nudibranchia) crossing Atlantic biogeographic barriers. PeerJ, 4, e1561.
https://doi.org/10.7717/peerj.1561
Bergh, L.S.R. (1874) Malacologische Untersuchungen 6. Reisen im Archipel Philippinen. Wissenschaftliche Resultate, 2, 247–285.
Bergh, L.S.R. (1877) Malacologische Untersuchungen 11. Reisen im Archipel Philippinen. Wissenschaftliche Resultate, 2, 429–546.
Bergh, L.S.R. (1891) Die cryptobranchiaten Dorididen. Zoologische Jahrbücher, Abtheilung für Systematik Geographie und Biologie der Thiere, 6, 103–144.
Edmunds, M. (1981) Opisthobranchiate Mollusca from Ghana: Chromodorididae. Zoological Journal of the Linnean Society, 72, 175–201.
https://doi.org/10.1111/j.1096-3642.1981.tb01657.x
Eliot, C.N.E. (1904) On some nudibranchs from East Africa and Zanzibar. Part IV. Proceedings of the Zoological Society of London, 1904, 380–406.
https://doi.org/10.1111/j.1469-7998.1904.tb08295.x
Eliot, C.N.E. (1906) On the nudibranchs of Southern India and Ceylon, with special reference to the drawings by Kelaart and the collections belonging to Alder & Hancock preserved in the Hancock Museum at Newcastle-on-Tyne. Proceedings of the Zoological Society of London, 1906, 636–691.
Epstein, H.E., Hallas, J.M., Johnson, R.F., Lopez, A. & Gosliner, T.M. (2019) Reading between the lines: revealing cryptic species diversity and colour patterns in Hypselodoris nudibranchs (Mollusca: Heterobranchia: Chromodorididae). Zoological Journal of the Linnean Society, 186, 116–189.
https://doi.org/10.1093/zoolinnean/zly048
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.
Gohar, H. & Soliman, G.N. (1967) The biology and development of Chromodoris inornata Pease (Gastropoda, Nudibranchia). Publications of the Marine Biological Station, Ghardaqa, 14, 77–94.
Gosliner, T.M. (1994) New species of Chromodoris and Noumea (Nudibranchia: Chromodorididae) from the Western Indian Ocean and Southern Africa. Proceedings of the California Academy of Sciences, 48, 239–252.
Gosliner, T.M. (2006) Marine Gastropoda collected by the Steamer Albatross from the Philippines in 1908. Records of the Western Australian Museum, 69, 83–93.
https://doi.org/10.18195/issn.0313-122x.69.2006.083-093
Gosliner, T.M. & Behrens, D.W. (1998) Five new species of Chromodoris (Mollusca: Nudibranchia: Chromodorididae) from the tropical Indo-Pacific Ocean. Proceedings of the California Academy of Sciences, 50, 139–165.
Gosliner, T., Behrens, D. & Valdés, Á. (2015) Indo-Pacific nudibranchs and sea slugs: A field guide to the world’s most diverse fauna. New World Publications, Inc., Jacksonville, Florida, 426 pp.
Gosliner, T., Valdeìz, A. & Behrens, D.W. (2018) Indo-Pacific nudibranchs and sea slugs: A field guide to the world’s most diverse fauna. New World Publications, Inc., Jacksonville, Florida, 451 pp. Available from: https://www.kogan.com/au/buy/nudibranch-and-sea-slug-identification-indo-pacific-terrence-gosliner-9781878348678/ (accessed 19 July 2019)
Gould, A.A. (1852) In United States exploring expedition during the years 1839–1842 under the command of Charles Wilkens U.S.N. In: Mollusca and Shells. Gould & Lincoln, Boston, pp. 510.
https://doi.org/10.5962/bhl.title.61454
van Hasselt, J.C. (1824) Extrait d’une lettre du Dr. J. C. van Hasselt auf Prof. van Swinderen sur mollusques de Java. Bulletin des Sciences naturelles et de Geologie, 3, 237–248.
Hoover, C.A., Padula, V., Schrödl, M., Hooker, Y. & Valdés, Á. (2017) Integrative taxonomy of the Felimare californiensis and F. ghiselini species complex (Nudibranchia: Chromodorididae), with description of a new species from Peru. Journal of Molluscan Studies, 83, 461–475.
https://doi.org/10.1093/mollus/eyx035
Johnson, R.F. & Gosliner, T.M. (2012) Traditional taxonomic groupings mask evolutionary history: A molecular phylogeny and new classification of the Chromodorid Nudibranchs J. H. Badger (Ed). PLoS ONE, 7, e33479.
https://doi.org/10.1371/journal.pone.0033479
Kay, E.A. & Young, D.K. (1969) The Doridacea (Opisthobranchia; Mollusca) of the Hawaiian Islands! Pacific Science, 23, 172–231.
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. & Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.
https://doi.org/10.1093/bioinformatics/bts199
Kelaart, E.F. (1859) Descriptions of new and little known species of Ceylonese nudibranchiate molluscs. Annals and Magazine of Natural History, 3, 291–304.
Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
https://doi.org/10.1093/molbev/mss020
Lanfear, R., Calcott, B., Kainer, D., Mayer, C. & Stamatakis, A. (2014) Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evolutionary Biology, 14, 82.
https://doi.org/10.1186/1471-2148-14-82
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2016) PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, msw260.
https://doi.org/10.1093/molbev/msw260
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948.
https://doi.org/10.1093/bioinformatics/btm404
Layton, K.K.S., 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
Maddison, W.P. & Maddison, D.R. (2018) Mesquite: a modular system for evolutionary anaysis.
Matsuda, S.B. & Gosliner, T.M. (2018a) Glossing over cryptic species: Descriptions of four new species of Glossodoris and three new species of Doriprismatica (Nudibranchia: Chromodorididae). Zootaxa 4444 (5), 501–529.
https://doi.org/10.11646/zootaxa.4444.5.1
Matsuda, S.B. & Gosliner, T.M. (2018b) Molecular phylogeny of Glossodoris (Ehrenberg, 1831) nudibranchs and related genera reveals cryptic and pseudocryptic species complexes. Cladistics, 34, 41–56.
https://doi.org/10.1111/cla.12194
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.
https://doi.org/10.1016/J.YMPEV.2016.07.019
Palumbi, S., Martin, A., Romano, S., McMillan, W.O., Stice, I. & Grabowski, G. (1991) The simple fool’s guide to PCR. Version 2.0. University of Hawaii, Honolulu, 40 pp.
Pease, W.H. (1866) Remarks on Nudibranchiata inhabiting the Pacific islands, with descriptions of two new genera. American Journal of Conchology, 2, 204–208.
Pease, W.H. (1871) Descriptions of new species of nudibranchiate Mollusca inhabiting Polynesia. No. 2. American Journal of Conchology, 7, 11–19.
Platt, A.R., Woodhall, R.W. & George, A.L. (2007) Improved DNA sequencing quality and efficiency using an optimized fast cycle sequencing protocol. BioTechniques, 43, 58–62.
https://doi.org/10.2144/000112499
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
Quoy, J.C.R. & Gaimard, P. (1832) Voyage de découvertes de l’Astrolabe, exécuté par ordre du Roi pendant les années 1826–1829, sous le commandement de M. Dumont D’Urville. Zoologie, Tome 2, Mollusques 2, 1–686.
Risbec, J. (1928) Contribution a l’etude des nudibranches Neo-Caledoniens. Faune Colon. Franc., 1–328.
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180
Rudman, W.B. (1973) Chromodorid opisthobranch Mollusca from the Indo-West Pacific. Zoological Journal of the Linnean Society, 52, 175–199.
https://doi.org/10.1111/j.1096-3642.1973.tb01880.x
Rudman, W.B. (1977) Chromodorid opisthobranch Mollusca from East Africa and the tropical West Pacific. Zoological Journal of the Linnean Society, 61, 351–397.
https://doi.org/10.1111/j.1096-3642.1977.tb01033.x
Rudman, W.B. (1982) The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: Chromodoris quadricolor, C. lineolata and Hypselodoris nigrolineata colour groups. Zoological Journal of the Linnean Society, 76, 183–241.
https://doi.org/10.1111/j.1096-3642.1982.tb02182.x
Rudman, W.B. (1983) The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: Chromodoris splendida, C. aspersa and Hypselodoris placida colour groups. Zoological Journal of the Linnean Society, 78, 105–173.
https://doi.org/10.1111/j.1096-3642.1983.tb00864.x
Rudman, W.B. (1984) The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: a review of the genera. Zoological Journal of the Linnean Society, 81, 115–273.
https://doi.org/10.1111/j.1096-3642.1984.tb01174.x
Rüppell, E. & Leuckart, F.S. (1830) Neue wirbellose Thiere des Rothen meeres. Atlas zu der Reise im nordlichen Afrika von Eduard Ruppell, 1830, 15–47.
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
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.
https://doi.org/10.1093/nar/22.22.4673
Tibiriçá, Y., Pola, M., Ortigosa, D. & Cervera, J.L. (2020) Systematic review of the “Chromodoris quadricolor group” of East Africa, with descriptions of two new species of the genus Chromodoris Alder & Hancock, 1855 (Heterobranchia, Nudibranchia). Journal of Zoological Systematics and Evolutionary Research, 58 (1), 230–261.
https://doi.org/10.1111/jzs.12334
Turner, L.M. & Wilson, N.G. (2008) Polyphyly across oceans: A molecular phylogeny of the Chromodorididae (Mollusca, Nudibranchia). Zoologica Scripta, 37, 23–42.
https://doi.org/10.1111/j.1463-6409.2007.00310.x
Valdés, Á., Mollo, E. & Ortea, J. (1999) Two new species of Chromodoris (Mollusca, Nudibranchia, Chromodorididae) from Southern India, with a redescription of Chromodoris trimarginata (Winckworth, 1946). Proceedings of the California Academy of Sciences, 51, 461–472.
Wilson, N.G. & Lee, M.S.Y. (2005) Molecular phylogeny of Chromodoris (Mollusca, Nudibranchia) and the identification of a planar spawning clade. Molecular Phylogenetics and Evolution, 36, 722–727.
https://doi.org/10.1016/j.ympev.2005.04.003
Yonow, N. (2008) Sea Slugs of the Red Sea. Pensoft, Sofia-Moscow, 304 pp.
Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29, 2869–2876.