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Connected across the ocean: taxonomy and biogeography of deep-water Nudibranchia from the Northwest Pacific reveal trans-Pacific links and two undescribed species

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Abstract

In this paper, we investigate a collection of Northwest Pacific nudibranch molluscs by means of integrative taxonomy, including morphological analyses, molecular data from the cytochrome c oxidase subunit I, 16S rRNA, histone H3, 28S rRNA, 18S rRNA markers, and ecological data. Two new species, Bathydoris antoni sp. nov. and Dendronotus kurilensis sp. nov., are described, and their phylogenetic relationships reconstructed. We also document two potentially new species of the genera Cadlina (Cadlinidae) and Cuthona (Fionidae s.l.). For the first time, we report molecular data for the Northwest Pacific specimens of Colga pacifica (Polyceridae), Dendronotus patricki (Dendronotidae), Ziminella vrijenhoeki (Paracoryphellidae), and Zeusia herculea (Aeolidiidae). Our molecular data supports the existence of biogeographic connections between the shallow water nudibranch fauna and their continental slope counterparts and communities on both sides of the North Pacific with possible ongoing gene exchange between fauna of both regions. We found two general types of deep shelf and bathyal communities inhabited by nudibranchs in the Northwest Pacific, each characterized by a certain type of fauna and a connectivity with different bathymetric and geographic areas.

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Availability of data and material

All studied specimens were deposited to the official collection of the National Scientific Center of Marine Biology, Far Eastern Branch RAS. All newly obtained sequences were submitted to GenBank. Unedited trees are provided as Supplementary material.

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Not applicable.

References

  • Afonso, P., McGinty, N., Graça, G., Fontes, J., Inácio, M., Totland, A., & Menezes, G. (2014). Vertical migrations of a deep-sea fish and its prey. PLoS ONE, 9(5), e97884. https://doi.org/10.1371/journal.pone.0097884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410.

    Article  CAS  PubMed  Google Scholar 

  • Baco, A. R., Smith, C. R., Peek, A. S., Roderick, G. K., & Vrijenhoek, R. C. (1999). The phylogenetic relationships of whale-fall vesicomyid clams based on mitochondrial COI DNA sequences. Marine Ecology Progress Series, 182, 137–147. https://doi.org/10.3354/meps182137

    Article  Google Scholar 

  • Bergh, R. (1894). Die Opisthobranchien. Reports on the dredging operations off the west coast of Central America to the Galapagos, to the west coast of Mexico, and in the Gulf of California, in charge of Alexander Agassiz, carried on by the U. S. Fish Commission steamer “Albatross”, during 1891, Lieut. Commander Z.L. Tanner, U.S.N., commanding. Bulletin of the Museum of Comparative Zoology, 25 (10), 125–233.

  • Borisanova, A. O., Chernyshev, A. V., & Ekimova, I. A. (2018). Deep-sea Entoprocta from the Sea of Okhotsk and the adjacent open Pacific abyssal area: New species and new taxa of host animals. Deep Sea Research Part II: Topical Studies in Oceanography, 154, 87–98.

    Article  CAS  Google Scholar 

  • Brandt, A., Gooday, A. J., Brandao, S. N., Brix, S., Brökeland, W., Cedhagen, T., Choudhury, M., Cornelius, N., Danis, B., De Mesel, I., Diaz, R. J., Gillan, D. C., Ebbe, B., Howe, J. A., Janussen, D., Kaiser, S., Linse, K., Malyutina, M., Pawlowski, J., Raupach, M. & Vanreusel, A. (2007a). First insights into the biodiversity and biogeography of the Southern Ocean deep sea. Nature, 447(7142), 307–311.

    Article  CAS  PubMed  Google Scholar 

  • Brandt, A., Brix, S., Brökeland, W., Choudhury, M., Kaiser, S., & Malyutina, M. (2007b). Deep-sea isopod biodiversity, abundance, and endemism in the Atlantic sector of the Southern Ocean—results from the ANDEEP I-III expeditions. Deep Sea Research Part II: Topical Studies in Oceanography, 54(16–17), 1760–1775.

    Article  Google Scholar 

  • Brandt, A., & Malyutina, M. V. (2015). The German-Russian deep-sea expedition KuramBio (Kurile Kamchatka biodiversity studies) on board of the RV Sonne in 2012 following the footsteps of the legendary expeditions with RV Vityaz. Deep Sea Research Part II: Topical Studies in Oceanography, 111, 1–9.

    Article  CAS  Google Scholar 

  • Brandt, A., Elsner, N. O., Malyutina, M. V., Brenke, N., Golovan, O. A., Lavrenteva, A. V., & Riehl, T. (2015). Abyssal macrofauna of the Kuril-Kamchatka Trench area (Northwest Pacific) collected by means of a camera–epibenthic sledge. Deep Sea Research Part II: Topical Studies in Oceanography, 111, 175–187.

    Article  Google Scholar 

  • Brandt, A., Alalykina, I., Brix, S., Brenke, N., Błażewicz, M., Golovan, O. A., & Lins, L. (2019). Depth zonation of Northwest Pacific deep-sea macrofauna. Progress in Oceanography, 176, 102–131.

    Article  Google Scholar 

  • Briggs, J. C. (1995). Global biogeography. Elsevier.

    Google Scholar 

  • Briggs, J. C. (2003). Marine centers of origin as evolutionary engines. Journal of Biogeography, 30, 1–18.

    Article  Google Scholar 

  • Cannon, J. T., Rychel, A. L., Eccleston, H., Halanych, K. M., & Swalla, B. J. (2009). Molecular phylogeny of hemichordata, with updated status of deep-sea enteropneusts. Molecular Phylogenetics and Evolution, 52(1), 17–24.

    Article  CAS  PubMed  Google Scholar 

  • Cella, K., Carmona, L., Ekimova, I., Chichvarkhin, A., Schepetov, D., & Gosliner, T. M. (2016). A radical solution: The phylogeny of the nudibranch family Fionidae. PloS ONE, 11(12), e0167800.

  • Chaban, E. M., Ekimova, I. A., Schepetov, D. M., & Chernyshev, A. V. (2019a). Meloscaphander grandis (Heterobranchia: Cephalaspidea), a deep-water species from the North Pacific: Redescription and taxonomic remarks. Zootaxa, 4646(2), 385–400.

    Article  Google Scholar 

  • Chaban, E. M., Ekimova, I. A., Schepetov, D. M., Kohnert, P. C., Schrödl, M., & Chernyshev, A. V. (2019b). Euopisthobranch mollusks of the order Cephalaspidea (Gastropoda: Heterobranchia) of the Kuril-Kamchatka Trench and the adjacent Pacific abyssal plain with descriptions of three new species of the genus Spiraphiline (Philinidae). Progress in Oceanography, 178, 102–185.

    Article  Google Scholar 

  • Chichvarkhin, A. (2016). Shallow water sea slugs (Gastropoda: Heterobranchia) from the northwestern coast of the Sea of Japan, north of Peter the Great Bay, Russia. PeerJ, 4, e2774.

  • Chichvarkhin, A. Y., Ekimova, I. A., Egorova, E. L., & Chichvarkhina, O. V. (2016). Identity of nudibranch mollusk of the genus Cuthona (Gastropoda: Tergipedidae), associated with hermit crabs in the Sea of Japan. Russian Journal of Marine Biology, 42(6), 449–457.

    Google Scholar 

  • Clement, M., Snell, Q., Walker, P., Posada, D., & Crandall, K. (2002). TCS: Estimating gene genealogies. Parallel and Distributed Processing Symposium, International, 3, 0184–0184.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Darriba, D., Posada, D., Kozlov, A.M., Stamatakis, A., Morel, B., & Flouri, T. (2020). ModelTest-NG: A new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution, 37(1), 291–294. https://doi.org/10.1093/molbev/msz189

  • Do, T. D., Jung, D. W., Kil, H. J., & Kim, C. B. (2020). A report of a new species and new record of Cadlina (Nudibranchia, Cadlinidae) from South Korea. Zookeys, 996, 1–18. https://doi.org/10.3897/zookeys.996.54602

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ekimova, I., Korshunova, T., Schepetov, D., Neretina, T., Sanamyan, N., & Martynov, A. (2015). Integrative systematics of northern and Arctic nudibranchs of the genus Dendronotus (Mollusca, Gastropoda), with descriptions of three new species. Zoological Journal of the Linnean Society, 173(4), 841–886.

    Article  Google Scholar 

  • Ekimova, I. A., Schepetov, D. M., Chichvarkhina, O. V., & Chichvarkhin, A. Y. (2016a). Nudibranch molluscs of the genus Dendronotus Alder et Hancock, 1845 (Heterobranchia: Dendronotina) from Northwestern Sea of Japan with description of a new species. Invertebrate Zoology, 13(1), 15–42.

    Article  Google Scholar 

  • Ekimova, I., Valdés, Á., Schepetov, D., & Chichvarkhin, A. (2016b). Was Gordon Robilliard right? Integrative systematics suggest that Dendronotus diversicolor (multicolor frond-aeolis) is a valid species. Canadian Journal of Zoology, 94(11), 793–799.

    Article  Google Scholar 

  • Ekimova, I. A., & Malakhov, V. V. (2016). Progenesis in the evolution of the nudibranch mollusks genus Dendronotus (Gastropoda: Nudibranchia). Doklady Biological Sciences, 467(1), 86–88.

    Article  CAS  PubMed  Google Scholar 

  • Ekimova, I., Valdés, Á., Chichvarkhin, A., Antokhina, T., Lindsay, T., & Schepetov, D. (2019). Diet-driven ecological radiation and allopatric speciation result in high species diversity in a temperate-cold water marine genus Dendronotus (Gastropoda: Nudibranchia). Molecular Phylogenetics and Evolution, 141, 106609. https://doi.org/10.1016/j.ympev.2019.106609

    Article  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Flouri, T., Izquierdo-Carrasco, F., Darriba, D., Aberer, A. J., Nguyen, L. T., Minh, B. Q., von Haeseler, A., & Stamatakis, A. (2014). The Phylogenetic Likelihood Library. Systematic Biology, 64(2), 356–362. https://doi.org/10.1093/sysbio/syu084

    Article  PubMed  PubMed Central  Google Scholar 

  • Giribet, G., Carranza, S., Baguñà, J., Riutort, M., & Ribera, C. (1996). First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution, 13(1), 76–84.

    Article  CAS  PubMed  Google Scholar 

  • Gordeeva, N. V. (2014). Phylogeography, genetic isolation, and migration of deep-sea fishes in the South Atlantic. Journal of Ichthyology, 54(9), 642–659.

    Article  Google Scholar 

  • 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.

  • Hamatani, I., & Kubodera, T. (2010). A new species of abyssal opisthobranch belonging to the genus Bathydoris Bergh, 1884 (Opisthobranchia: Nudibranchia: Doridoidea) from Japan. Venus, 68(3–4), 113–120.

    Google Scholar 

  • Horne, D. J. (1999). Ocean circulation modes of the phanerozoic: Implications for the antiquity of deep-sea benthonic invertebrates. Crustaceana, 72, 999–1018. https://doi.org/10.1163/156854099503906

    Article  Google Scholar 

  • Ivanova, N. V., deWaard, J., & Hebert, P. D. N. (2006). An inexpensive, automation-friendly proto-col for recovering high-quality DNA. Molecular Ecology Notes, 6, 998–1002.

    Article  CAS  Google Scholar 

  • Jablonski, D., & Bottjer, D. J. (1991). Environmental patterns in the origins of higher taxa: The post-Palaeozoic fossil record. Science, 252, 251–253. https://doi.org/10.1126/science.252.5014.1831

    Article  Google Scholar 

  • Jablonski, D., Sepkoski, J. J., Jr., Bottjer, D. J., & Sheehan, P. M. (1983). Onshore-offshore patterns in evolution of Phanaerozoic shelf communities. Science, 22, 1123–1125. https://doi.org/10.1126/science.222.4628.1123

    Article  Google Scholar 

  • Jacobs, D. K., & Lindberg, D. R. (1998). Oxygen and evolutionary patterns in the sea: Onshore/offshore trends and recent recruitment of deep-sea faunas. Proceedings of the National Academy of Sciences of the United States of America, 95, 9396–9401. https://doi.org/10.1073/pnas.95.16.9396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeppsson, L. (1990). An oceanic mode for lithological and faunal changes tested on the Silurian record. Journal of the Geological Society, 147, 663–674. https://doi.org/10.1144/gsjgs.147.4.0663

    Article  Google Scholar 

  • Jumars, P. A., Mayer, L. M., Deming, J. W., Baross, J. A., & Wheatcroft, R. A. (1990). Deep-sea deposit-feeding strategies suggested by environmental and feeding constraints. Philosophical Transactions of the Royal Society of London. Series A, Mathematical and Physical Sciences, 331, 85–101. https://doi.org/10.1098/rsta.1990.0058

    Article  Google Scholar 

  • Kano, Y. (2008). Vetigastropod phylogeny and a new concept of Seguenzioidea: Independent evolution of copulatory organs in the deep-sea habitats. Zoologica Scripta, 37(1), 1–21.

    Article  Google Scholar 

  • Kano, Y., Brenzinger, B., Nützel, A., Wilson, N. G., & Schrödl, M. (2016). Ringiculid bubble snails recovered as the sister group to sea slugs (Nudipleura). Scientific Reports, 6(1), 1–11.

    Article  Google Scholar 

  • Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., & Drummond, A. (2012). Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647–1649.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kiel, S., & Goedert, J. L. (2006). Deep-sea food bonanzas: Early Cenozoic whale-fall communities resemble wood-fall rather than seep communities. Proceedings of the Royal Society B: Biological Sciences, 273, 2625–2631. https://doi.org/10.1098/rspb.2006.3620

    Article  PubMed  PubMed Central  Google Scholar 

  • Korshunova, T., & Martynov, A. (2020). Consolidated data on the phylogeny and evolution of the family Tritoniidae (Gastropoda: Nudibranchia) contribute to genera reassessment and clarify the taxonomic status of the neuroscience models Tritonia and Tochuina. PLoS ONE, 15(11), e0242103.

  • Korshunova, T., Sanamyan, N., Zimina, O., Fletcher, K., & Martynov, A. (2016). Two new species and a remarkable record of the genus Dendronotus from the North Pacific and Arctic oceans (Nudibranchia). ZooKeys, 630, 19.

    Article  Google Scholar 

  • Korshunova, T., Martynov, A., Bakken, T., Evertsen, J., Fletcher, K., Mudianta, W. I., Saito, H., Lundin, K., Schrödl, M., & Picton, B. (2017a). Polyphyly of the traditional family Flabellinidae affects a major group of Nudibranchia: Aeolidacean taxonomic reassessment with descriptions of several new families, genera, and species (Mollusca, Gastropoda). ZooKeys, 717, 1–139.

    Article  Google Scholar 

  • Korshunova, T., Zimina, O., & Martynov, A. (2017b). Unique pleuroproctic taxa of the nudibranch family Aeolidiidae from the Atlantic and Pacific Oceans, with description of a new genus and species. Journal of Molluscan Studies, 83(4), 409–421.

    Article  Google Scholar 

  • Korshunova, T., Martynov, A., Bakken, T., & Picton, B. (2017c). External diversity is restrained by internal conservatism: New nudibranch mollusc contributes to the cryptic species problem. Zoologica Scripta, 46(6), 683–692.

    Article  Google Scholar 

  • Korshunova, T., Martynov, A., & Picton, B. (2017d). 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.

    Article  Google Scholar 

  • Korshunova, T., Lundin, K., Malmberg, K., Picton, B., & Martynov, A. (2018). First true brackish-water nudibranch mollusc provides new insights for phylogeny and biogeography and reveals paedomorphosis-driven evolution. PLoS ONE, 13(3), e0192177.

  • Korshunova, T., Fletcher, K., Picton, B., Lundin, K., Kashio, S., Sanamyan, N., & Martynov, A. (2020a). 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.

    Article  Google Scholar 

  • Korshunova, T., Bakken, T., Grøtan, V. V., Johnson, K. B., Lundin, K., & Martynov, A. (2020b). A synoptic review of the family Dendronotidae (Mollusca: Nudibranchia): A multilevel organismal diversity approach. Contributions to Zoology, 90(1), 93–153.

    Article  Google Scholar 

  • 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.

  • Lê, H. L., Lecointre, G., & Perasso, R. (1993). A 28S rRNA-based phylogeny of the gnathostomes: First steps in the analysis of conflict and congruence with morphologically based cladograms. Molecular Phylogenetics and Evolution, 2(1), 31–51.

    Article  PubMed  Google Scholar 

  • Leduc, D., Zhao, Z. Q., Verdon, V., & Xu, Y. (2018). Phylogenetic position of the enigmatic deep-sea nematode order Rhaptothyreida: A molecular analysis. Molecular Phylogenetics and Evolution, 122, 29–36.

    Article  PubMed  Google Scholar 

  • Leigh, J. W., & Bryant, D. (2015). Popart: Full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6(9), 1110–1116.

    Article  Google Scholar 

  • Linder, A., Cairns, S. D., & Cunningham, C. W. (2008). From offshore to onshore: Multiple origins of shallow-water corals from deep-sea ancestors. PLoS ONE, 3(6), e2429. https://doi.org/10.1371/journal.pone.0002429

    Article  CAS  Google Scholar 

  • Mahguib, J., & Valdés, Á. (2015). Molecular investigation of the phylogenetic position of the polar nudibranch Doridoxa (Mollusca, Gastropoda, Heterobranchia). Polar Biology, 38(9), 1369–1377.

    Article  Google Scholar 

  • Malyutina, M. V., & Brandt, A. (2012). The joint Russian-German deep-sea research projects SoJaBio (Sea of Japan Biodiversity Studies) and KuramBio (Kurile Kamchatka Deep-Sea Biodiversity). Marine Ecosystems under the Global Change in the Northwestern Pacific, 11.

  • Malyutina, M. V., & Brandt, A. (2013). Introduction to SoJaBio (Sea of Japan biodiversity studies). Deep Sea Research Part II: Topical Studies in Oceanography, 86, 1–9.

    Article  Google Scholar 

  • Malyutina, M. V., Chernyshev, A. V., & Brandt, A. (2018). Introduction to the SokhoBio (Sea of Okhotsk Biodiversity Studies) expedition 2015. Deep Sea Research Part II: Topical Studies in Oceanography, 154, 1–9.

    Article  Google Scholar 

  • Martynov, A. V. (1993). Subclassis Opisthobranchia. In: B. I. Sirenko (Ed.), List of species of the fauna of invertebrates of continental slope of the Kurile Islands String. Issledovaniya Fauny Morei, 46(54), 198.

  • Martynov, A. V. (2013). Morphology, taxonomic status and distribution of the opisthobranch mollusc Coryphella (s. l.) japonica from the central deep water basin of the Sea of Japan. Deep-Sea Research, Part II: Topical Studies in Oceanography, 86–87, 111–118. https://doi.org/10.1016/j.dsr2.2012.08.012

    Article  Google Scholar 

  • Martynov, A. V., & Baranets, O. N. (2002). A revision of the genus Colga Bergh (Opisthobranchia, Polyceridae), with description of a new species from the North Pacific. Ruthenica, 12(1), 23–43.

    Google Scholar 

  • Martynov, A. V., & Roginskaya, I. S. (2005). A new species of the genus Doridunculus G.O. Sars. (1878). (Mollusca, Nudibranchia): A hydroid-feeding dorid from the abyssal depths of the Sea of Japan. Ruthenica, 14(2), 135–145.

    Google Scholar 

  • Martynov, A. V., Sanamyan, N. P., Korshunova, T. A. (2015). New data on the opisthobranch molluscs (Gastropoda: Opisthobranchia) of waters of Commander Islands and Far-Eastern seas of Russia. In: Conservation of biodiversity of Kamchatka and coastal waters. Proceedings of XV international scientific conference Petropavlovsk-Kamchatsky. Kamchat Press, Petropavlovsk-Kamchatsky, 55–69.

  • Martynov, A. V., Sanamyan, N. P., & Korshunova, T. A. (2016). Review of the opisthobranch mollusc fauna of Russian Far Eastern seas: Pleurobranchomorpha, Doridida and Nudibranchia. Bulletin of Kamchatka State Technical University, 34, 62–87.

    Google Scholar 

  • Martynov, A., Fujiwara, Y., Tsuchida, S., Nakano, R., Sanamyan, N., Sanamyan, K., Fletcher, K., & Korshunova, T. (2020). Three new species of the genus Dendronotus from Japan and Russia (Mollusca, Nudibranchia). Zootaxa, 4747(3), 495–513.

    Article  Google Scholar 

  • McClain, C. R. (2007). Guest editorial: Seamounts: Identity crisis or split personality? Journal of Biogeography, 34, 2001–2008. https://doi.org/10.1111/j.1365-2699.2007.01783.x

    Article  Google Scholar 

  • McClain, C. R., Rex, M. A., & Etter, R. J. (2009). Deep-sea macroecology. In J. D. Witman & K. Roy (Eds.), Marine macroecology (pp. 65–100). University of Chicago Press.

    Chapter  Google Scholar 

  • McClain, C. R., & Hardy, S. M. (2010). The dynamics of biogeographic ranges in the deep sea. Proceedings of the Royal Society B: Biological Sciences, 277(1700), 3533–3546.

    Article  PubMed  PubMed Central  Google Scholar 

  • Menzies, R. J., & Imbrie, J. (1958). On the antiquity of the deep-sea bottom fauna. Oikos, 9, 192–210. https://doi.org/10.2307/3564764

    Article  Google Scholar 

  • Milligan, R. J., Scott, E. M., Jones, D. O., Bett, B. J., Jamieson, A. J., & O’brien, R., & Bailey, D. M. (2020). Evidence for seasonal cycles in deep-sea fish abundances: A great migration in the deep SE Atlantic? Journal of Animal Ecology, 89(7), 1593–1603.

    Article  PubMed  Google Scholar 

  • Moles, J., Berning, M. I., Hooker, Y., Padula, V., Wilson, N. G., & Schrödl, M. (2021). Due South: The evolutionary history of sub-Antarctic and Antarctic Tritoniidae nudibranchs. Molecular Phylogenetics and Evolution, 107209.

  • Orlov, A. M., Rabazanov, N. I., & Nikiforov, A. I. (2020). Transoceanic migrations of fishlike animals and fish: Norm or exclusion? Journal of Ichthyology, 60, 242–262.

    Article  Google Scholar 

  • Orlova, S. Y., Schepetov, D. M., Mugue, N. S., Smirnova, M. A., Senou, H., Baitaliuk, A. A., & Orlov, A. M. (2019). Evolutionary history told by mitochondrial markers of large teleost deep-sea predators of family Anoplopomatidae Jordan & Gilbert 1883, endemic to the North Pacific. Journal of the Marine Biological Association of the UK, 99(7), 1683–1691. https://doi.org/10.1017/S0025315419000572

    Article  Google Scholar 

  • Osterburg, H. H., Allen, J. K., & Finch, C. E. (1975). The use of ammonium acetate in the precipitation of ribonucleic acid. Biochemical Journal, 147(2), 367–368. https://doi.org/10.1042/bj1470367

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Palumbi, S. R. (1996). Nucleic acids II: The polymerase chain reaction. In D. M. Hillis, C. Moritz, & B. K. Mable (Eds.), Molecular systematics (pp. 205–247). Sinauer & Associates Inc.

    Google Scholar 

  • Pearse, J. S., & Lockhart, S. J. (2004). Reproduction in cold water: Paradigm changes in the 20th century and a role for cidaroid sea urchins. Deep Sea Research Part II: Topical Studies in Oceanography, 51(14–16), 1533–1549. https://doi.org/10.1016/j.dsr2.2004.06.023

    Article  Google Scholar 

  • Pradillon, F., & Gaill, F. (2007). Pressure and life: Some biological strategies. Reviews in Environmental Science and Bio/technology, 6, 181–195. https://doi.org/10.1007/s11157-006-9111-2

    Article  Google Scholar 

  • Puslednik, L., & Serb, J. M. (2008). Molecular phylogenetics of the Pectinidae (Mollusca: Bivalvia) and effect of increased taxon sampling and outgroup selection on tree topology. Molecular Phylogenetics and Evolution, 48(3), 1178–1188.

    Article  CAS  PubMed  Google Scholar 

  • Raupach, M. J., Mayer, C., Malyutina, M., & Wagele, J.-W. (2009). Multiple origins of deep-sea Asellota (Crustacea: Isopoda) from shallow waters revealed by molecular data. Proceedings of the Royal Society B: Biological Sciences, 276(1658), 799–808. https://doi.org/10.1098/rspb.2008.1063

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rogers, A. D. (2000). The role of the oceanic oxygen minima in generating biodiversity in the deep sea. Deep Sea Research Part II: Topical Studies in Oceanography, 47(1–2), 119–148. https://doi.org/10.1016/S0967-0645(99)00107-1

    Article  Google Scholar 

  • Saeedi, H., Simões, M., & Brandt, A. (2020). Biodiversity and distribution patterns of deep-sea fauna along the temperate NW Pacific. Progress in Oceanography, 183, 102296.

  • Shank, T. M. (1998). Miocene radiation of deep-sea hydrothermal vent shrimp (Caridea: Bresiliidae): Evidence from mitochondrial cytochrome oxidase subunit I. Molecular Phylogenetics and Evolution, 13(2), 244–254. https://doi.org/10.1006/mpev.1999.0642

    Article  Google Scholar 

  • Sibuet, M., & Olu, K. (1998). Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins. Deep Sea Research Part II: Topical Studies in Oceanography, 45(1–3), 517–567. https://doi.org/10.1016/S0967-0645(97)00074-X

    Article  Google Scholar 

  • Smith, A. B., & Stockley, B. (2005). The geological history of deep-sea colonization by echinoids: Roles of surface productivity and deep-water ventilation. Proceedings of the Royal Society B: Biological Sciences, 272, 865–869. https://doi.org/10.1098/rspb.2004.2996

    Article  PubMed  PubMed Central  Google Scholar 

  • Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stout, C. C., Wilson, N. G., & Valdés, Á. (2011). A new species of deep-sea Dendronotus Alder & Hancock (Mollusca: Nudibranchia) from California, with an expanded phylogeny of the genus. Invertebrate Systematics, 25(1), 60–69.

    Article  Google Scholar 

  • Sukumaran, J., & Holder, M. T. (2010). DendroPy: A Python library for phylogenetic computing. Bioinformatics, 26(12), 1569–1571.

    Article  CAS  PubMed  Google Scholar 

  • Talavera, G., & Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology., 56(4), 564–577.

    Article  CAS  PubMed  Google Scholar 

  • Tittensor, D. P., Schlacher, T., Smith, C. R., & Susko, E. (2010). Endemism at low sampling effort: Real or artifact. International Deep-Sea Biology Symposium, 12th, Reykjavik, Iceland (pp. 84–85). Southhampton, UK: InterRidge.

  • Valdés, Á. (2002). Phylogenetic systematics of “Bathydoris” sl Bergh, 1884 (Mollusca, Nudibranchia), with the description of a new species from New Caledonian deep waters. Canadian Journal of Zoology, 80(6), 1084–1099.

    Article  Google Scholar 

  • Valdés, Á., & Bertsch, H. (2000). Redescription and range extension of Bathydoris aioca Marcus, & Marcus, 1962 (Nudibranchia: Gnathodoridoidea). Veliger, 43(2), 172–178.

    Google Scholar 

  • Valdés, Á., Lundsten, L., & Wilson, N. G. (2018). Five new deep-sea species of nudibranchs (Gastropoda: Heterobranchia: Cladobranchia) from the Northeast Pacific. Zootaxa, 4526(4), 401–433.

    Article  PubMed  Google Scholar 

  • Van Dover, C. L. (2000). The ecology of deep-sea hydrothermal vents. Princeton University Press.

    Book  Google Scholar 

  • Vinogradova, N. G. (1997). Zoogeography of the abyssal and hadal zones. Advances in Marine Biology, 32, 325–387. https://doi.org/10.1016/S0065-2881(08)60019-X

    Article  Google Scholar 

  • Volodchenko, N. I. (1941). New nudibranchiate molluscs from seas of the far-east of the U.S.S.R. Investigations of the Far Eastern Seas of the USSR, 1, 53–72.

    Google Scholar 

  • Waelbroeck, C., Labeyrie, L., Michel, E., Duplessy, J. C., McManus, J. F., Lambeck, K., Balbon, E., & Labracherie, M. (2001). Sea-level and deep water temperature changes derived from benthic foraminifera isotopic records. Quaternary Science Reviews, 21, 295–305. https://doi.org/10.1016/S0277-3791(01)00101-9

    Article  Google Scholar 

  • Watling, L., Guinotte, J., Clark, M. R., & Smith, C. R. (2013). A proposed biogeography of the deep ocean floor. Progress in Oceanography, 111, 91–112.

    Article  Google Scholar 

  • Whiting, M. F., Carpenter, J. M., Wheeler, Q. D., & Wheeler, W. C. (1997). The Strepsiptera problem: Phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology, 46, 1–68.

    CAS  PubMed  Google Scholar 

  • Wilson, G. (1999). Some of the deep-sea fauna is ancient. Crustaceana, 72(8), 1019–1030. https://doi.org/10.1163/156854099503915

    Article  Google Scholar 

  • Zardus, J. D., Etter, R. J., Chase, M. R., Rex, M. A., & Boyle, E. E. (2006). Bathymetric and geographic population structure in the pan-Atlantic deep-sea bivalve Deminucula atacellana (Schenck, 1939). Molecular Ecology, 15(3), 639–651. https://doi.org/10.1111/j.1365-294X.2005.02832.x

    Article  CAS  PubMed  Google Scholar 

  • Zenkevitch, L. A., & Birstein, J. A. (1953). On the problem of the antiquity of the deep-sea fauna. Deep Sea Research, 7(1), 10–23.

    Article  Google Scholar 

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Acknowledgements

We are deeply grateful to all friends and colleagues who kindly collected and supplied specimens for this study: Dr. Anastassya Maiorova (NSCMB RAS), and team of 82nd cruise of R/V “Akademik M.A. Lavrentyev, including Dr. Vladimir Mordukhovich (NSCMB RAS) and Dr. Elena Krylova (IO RAS). The authors gratefully acknowledge the National Scientific Center of Marine Biology FEBRAS for providing nudibranch molluscs collection for this study and the Team of ROV “Komanch” and Dr. Nadezhda Sanamyan for providing photos of nudibranchs collected from seeps. We thank Valentina Tambovceva for assistance with Sanger sequencing. We also want to thank the staff of Joint Usage Center “Instrumental methods in ecology at the A.N. Severtsov Institute of Ecology and Evolution RAS” and the staff of the scanning electron microscopic laboratory of the Moscow State University for providing SEM facilities. Sanger sequencing was conducted using equipment of the Core Centrum of Institute of Developmental Biology RAS.

Funding

This study is uniting proceeding made during research on the nudibranch families Fionidae, Dendronotidae, Flabellinidae, and Doridina in frame of scientific project of the State Order of the Russian Federation Government to Lomonosov Moscow State University No. 121032300121-0 with financial support of Russian Science Foundation (grant no. 19-74-00144 for the family Fionidae to DS and grant no. 20-74-10012 for the families Flabellinidae and Dendronotidae to IE, AM, MS, TA and DS). Depository of specimens used in this study was supported by the Moscow State University Grant for Leading Scientific Schools “Depository of the Living Systems” in the frame of the MSU Development Program. Specimen collection and fixation was supported by the Grant of the Ministry of Science and Higher Education of the Russian Federation (agreement number 075-15-2020-796, grant number 13.1902.21.0012).

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Authors and Affiliations

  1. Lomonosov Moscow State University, Moscow, Russia

    Irina Ekimova, Maria Stanovova, Anna Mikhlina, Tatiana Neretina & Dimitry Schepetov

  2. Department of Biological Sciences, California State Polytechnic University, Pomona, CA, USA

    Ángel Valdés

  3. A.N. Severtsov Institute of Ecology and Evolution, Moscow, Russia

    Tatiana Antokhina

  4. National Scientific Center of Marine Biology, Far Eastern Branch RAS, Vladivostok, Russia

    Olga Chichvarkhina

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  1. Irina Ekimova
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  2. Ángel Valdés
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  8. Dimitry Schepetov
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Contributions

Conceptualization: IE, DS. Investigation: IE, AV, DS. Methodology: IE. Software: IE, DS. Validation: IE, DS. Formal analysis: IE, MS, AM, TA, TN, OC, DS. Resources: IE. Data curation: IE. Writing — original draft: IE, AV, DS. Writing — review and editing: IE, AV, MS, AM, TA, TN, OC, DS. Visualization: IE, AM, TA, DS. Supervision: IE. Project administration: IE, DS. Funding acquisition: IE, DS.

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Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 Data S1. Unedited Maximum likelihood and Bayesian phylogenetic trees. (RAR 57 KB)

13127_2021_526_MOESM2_ESM.docx

Supplementary file2 Table S1. List of specimens used in this study. Voucher numbers, collection data and collectors are given. (DOCX 20 KB)

13127_2021_526_MOESM3_ESM.xlsx

Supplementary file3 Table S2. Specimens used for molecular analyses. Voucher numbers, collection localities and GenBank accession numbers are given (sequences obtained for this study are pending accession numbers). Sequences obtained for this study are highlighted in bold. (XLSX 55 KB)

Supplementary file4 Table S3. Dataset length and respective DNA substitution model. (DOCX 15 KB)

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Ekimova, I., Valdés, Á., Stanovova, M. et al. Connected across the ocean: taxonomy and biogeography of deep-water Nudibranchia from the Northwest Pacific reveal trans-Pacific links and two undescribed species. Org Divers Evol 21, 753–782 (2021). https://doi.org/10.1007/s13127-021-00526-8

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