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Disentangling invasions in the sea: molecular analysis of a global polychaete species complex (Annelida: Spionidae: Pseudopolydora paucibranchiata)

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Abstract

The spionid polychaete Pseudopolydora paucibranchiata (Okuda, 1937) was originally described from Japan and has since been reported as a non-indigenous species in soft bottom communities in the Northeast Pacific, the Mediterranean Sea, around Europe, Australia, Brazil, and Florida. The diagnostic features of the adults are palps with ramified yellow chromatophores, prostomium rounded anteriorly, short occipital antenna on the caruncle, and a small disc-like pygidium. We collected Pseudopolydora with these features from locations worldwide and compared them by a molecular analysis. The Bayesian analysis of the combined dataset of three genetic markers (mitochondrial 16S rDNA, nuclear 28S rDNA and Histone 3; 811 bp in total) showed that the worms form a monophyletic group comprising four genetically different clades. We name this group the P. paucibranchiata complex and consider the clades as four pseudocryptic species. The largest examined clade comprises individuals from the Pacific Canada (British Columbia), Russia (Sea of Japan), South Korea (East Sea), Italy (Tyrrhenian and Ionian Seas), Australia (Victoria), Netherlands, and Japan, which we identify as P. paucibranchiata. The morphology, reproductive biology and ecology of P. paucibranchiata are briefly reviewed. The other three clades are referred to as Pseudopolydora vexillosa Radashevsky and Hsieh, 2000 (Vietnam, Nha Trang Bay), Pseudopolydora sp. A (Australia, Northern Territory), and Pseudopolydora sp. B (Kuwait, Arabian Gulf). We explain the occurrence of P. paucibranchiata outside of the Northwest Pacific by unintentional human-mediated transportation in ballast water and/or with commercial oyster movements in aquaculture operations, followed by successful invasions.

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Acknowledgements

Our sincere thanks to Robin S. Wilson (Australia), Christopher J. Glasby (Australia), Graham E. Gillespie (Canada), Céline Houbin (France), Hwey-Lian Hsieh (Taiwan), Jin-Woo Choi (South Korea), Marco Lezzi (Italy), Marco Faasse (Netherlands), and Temir A. Britayev (Russia) for providing material for molecular analysis or help in the field. Ertan Dağli (Turkey), Elianne P. Omena (Brazil) and Barbara Mikac (Croatia) provided specimens for morphological examination. Vyatcheslav V. Potin (Russia), Leslie H. Harris (USA), Christina Piotrowski (USA), Linda Ward (USA) and Xin-zheng Li (China) helped with museum collections. We thank Seungshic Yum for help with sequencing the material and James Blake for clarifying early records for some California localities. Vitaly O. Pois and Eugene Shvetsov helped with VIR database and the QGIS software. We thank two anonymous reviewers for their important comments. To all these colleagues, we express our sincere gratitude.

Funding

This study was funded by the Kuwait Institute for Scientific Research (KISR) and Kuwait Petroleum Corporation (KPC) for the Project “Biodiversity, distribution and abundance of intertidal macrofauna in Kuwait” (EM075C), Norwegian Research Council (Project 233635/H30 “Environmental management of petroleum activities in the Barents Sea: Norwegian-Russian collaboration”), and the Far Eastern Branch of the Russian Academy of Sciences (Grant 18-4-040).

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Authors and Affiliations

  1. National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, 17 Palchevsky Street, Vladivostok, 690041, Russia

    Vasily I. Radashevsky, Vasily V. Malyar & Victoria V. Pankova

  2. Department of Marine Integrative Ecology, Ischia Marine Center, Stazione Zoologica “Anton Dohrn” di Napoli, 80070, Ischia, Napoli, Italy

    Maria Cristina Gambi & Adriana Giangrande

  3. Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento, CONISMA, Via Prov. le Lecce Monteroni, 73100, Lecce, Italy

    Adriana Giangrande

  4. Smithsonian Environmental Research Center (SERC), Smithsonian Institution, 647 Contees Wharf Road, Edgewater, MD, 21037, USA

    Erica Keppel

  5. Department of Marine Science, The Faculty of Science, University of Gothenburg, Tjärnö, Strömstad, Sweden

    Arne Nygren

  6. Kuwait Institute for Scientific Research, 22107, Salmiya, Kuwait

    Manal Al-Kandari

  7. Maritime Studies Program, Williams College-Mystic Seaport, Mystic, CT, 06355, USA

    James T. Carlton

  8. Department of Biology, Williams College, Williamstown, MA, USA

    James T. Carlton

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  1. Vasily I. Radashevsky
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  2. Vasily V. Malyar
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  3. Victoria V. Pankova
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  4. Maria Cristina Gambi
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  9. James T. Carlton
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Contributions

VIR formulated the idea, collected and examined most of the material, wrote the first draft of the manuscript. VVM and VVP sequenced material and analyzed molecular data. MCG, AG and EK collected and examined material in Italy. AN collected and sequenced material from Norway. MAK organised sampling in the Arabian Gulf and financial support for this study. JTC provided additional records, new insights on the biogeography and final editing of the manuscript.

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Correspondence to Vasily I. Radashevsky.

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Radashevsky, V.I., Malyar, V.V., Pankova, V.V. et al. Disentangling invasions in the sea: molecular analysis of a global polychaete species complex (Annelida: Spionidae: Pseudopolydora paucibranchiata). Biol Invasions 22, 3621–3644 (2020). https://doi.org/10.1007/s10530-020-02346-x

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