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Revealing the diversity of the green Eulalia (Annelida, Phyllodocidae) species complex along the European coast, with description of three new species

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Abstract

The green phyllodocids Eulalia clavigera and E. viridis are a known European pseudo-cryptic complex, but questions about its distribution and evidence of additional lineages in previous studies call for an investigation of the real diversity within the complex.

We analyze DNA sequences (mtCOI-5P, ITS, and 28S rRNA) of different populations of E. clavigera from intertidal and subtidal marine waters along the North East Atlantic, Mediterranean Sea,  the Azores and Webbnesia (Madeira, Savage islands and Canaries), and populations of E. viridis from the Scandinavia. This provided compelling evidence for the existence of six additional divergent evolutionary lineages, three of the most abundant being described here as new species: Eulalia feliciae sp. nov., intertidal and unique to the Western Mediterranean, Eulalia madeirensis sp. nov., subtidal and unique to the Madeira Island (Portugal), and Eulalia xanthomucosa sp. nov., mostly subtidal and occurring in the British Isles and southern France. Complementary morphometric analyses showed that E. feliciae sp. nov. and E. madeirensis sp. nov. formed two independent morphometric clusters, while E. xanthomucosa sp. nov. often overlapped with E. clavigera sensu stricto (s. s.), although being unique in showing a yellow coloration and parapodial cirri on median segments larger in relation to its body size.

Recent biotechnological findings based on “E. clavigera” specimens highlight the importance of formally describing cryptic complexes, since each lineage chemistry might be unique and may have a range of distinct effects and applications.

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Availability of data and materials

New sequence data and specimen metadata were uploaded in the project “Eulalia species complex” (DS-MTE) within BOLD (https://v4.boldsystems.org/) and in the following link: https://doi.org/10.5883/DS-MTEC. The alignments (FASTA and NEXUS formats) for each marker (mtCOI-5P, ITS and 28S) and the concatenated one (mtCOI-5P + ITS + 28S) are all publicly available online at Figshare (DOI: https://doi.org/10.6084/m9.figshare.2165741). GenBank accession numbers: OP898309-OP898427 (mtCOI-5P), OP897856-OP897897 (ITS), and OP897898-OP897939 (28S)). See online supplemental Table S1 for more details. The new biological material is deposited at the Biological Research Collection (Marine Invertebrates) of the Department of Biology of the University of Aveiro (CoBI at DBUA), Portugal. The specimen from Banyuls (France) belonging to E. xanthomucosa sp. nov was donated to SCRIPPS Oceanography Institution (SIO), one specimen from the Savage islands was kindly loaned by the National Museum of Science and Natural History (MUHNAC, Portugal), while the two specimens from Corsica are deposited at the Muséum national d’Histoire naturelle (MNHN). All specimens available upon request, including the ones from Arne Nygren’s personal collection (ANPC, tagged with the BOLD Process ID: "MTE").

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Acknowledgements

The authors wish to thank Sofia Duarte for the Portuguese Eulalia specimens, Ana Costa for the specimens from the Azores, Nicolas Lavesque and Felicia Ulltin for the northern and southern French samples, respectively and Julio Parapar for the northern Spanish specimens, Additionally, to Jorge Núñez and Beatriz Alfonso for all the assistance and knowledge provided during the Canary islands sampling campaign. Moreover, we would like to thank the reviewer for taking the time reviewing and improving upon the original version of our manuscript.

Thanks are due to the Corsica program. The CORSICABENTHOS expeditions (PI: Line Le Gall), with a focus on the small benthic biota, are the marine component of the “Our Planet Reviewed” program. The Corsica program is run by Muséum National d’Histoire Naturelle in partnership with Université de Corse Pasquale Paoli and Office de l’Environnement de la Corse (OEC), with the support of Office Français de la Biodiversité (OFB) and Collectivité Territoriale de Corse (CTC). CORSICABENTHOS 2 took place in October 2020 in collaboration with Réserve Naturelle des Bouches de Bonifacio. The organizers are grateful to Medeleine Cancemi, Jean-François Cubells, Jean-Michel Culioli, and Jean-Michel Palazzi for their support.

Funding

This study was supported by the project ATLANTIDA–Platform for the monitoring of the North Atlantic Ocean and tools for the sustainable exploitation of the marine resources, with the reference NORTE-01–0145-FEDER-000040, co-financed by the European Regional Development Fund (ERDF), through Programa Operacional Regional do Norte (NORTE 2020). Thanks are due, for the financial support to CESAM (UIDB/50017/2020 + UIDP/50017/2020), to Portuguese Foundation for Science and Technology and Ministry of Education and Science (FCT/MEC) through national funds, and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020. Marcos A. L. Teixeira was supported by a PhD grant from FCT co-financed by ESF (SFRH/BD/131527/2017) and from the DNAqua-Net STSM grant “Rich and hidden biodiversity not yet barcoded in the Canary archipelago (Spain) as an opportunity to enrich the DNA barcode reference library for European polychaetes,” under the EU Cost action CA15219–Developing new genetic tools for bio-assessment of aquatic ecosystems in Europe. Pedro E. Vieira was supported by national funds through the Portuguese Foundation for Science and Technology (FCT, I.P.) in the scope of the project (early detection and monitoring of non-indigenous species in coastal ecosystems based on high-throughput sequencing tools, PTDC/BIA-BMA/29754/2017). Ascensão Ravara was supported by national funds, through FCT, I.P., in the scope of the framework contract foreseen in the numbers 4, 5, and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19. Arne Nygren was supported by the Norwegian Taxonomy Initiative [https://www.biodiversity.no/Pages/135523] (Cryptic polychaete species in Norwegian waters, knr 49–13, pnr 70184228), the Swedish Taxonomy Initiative [https://www.artdatabanken.se/en/the-swedish-taxonomy-initiative/] (Polychaete species complexes in Swedish waters, dnr 140/07 1.4 and 166/08 1.4), and Kungliga Fysiografiska sällskapet Nilsson-Ehle donationerna [https://www.fysiografen.se/sv/].

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Authors and Affiliations

  1. Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus de Gualtar, Braga, 4710-057, Portugal

    Marcos A. L. Teixeira, Pedro E. Vieira & Filipe O. Costa

  2. Institute of Science and Innovation for Bio-Sustainability (IB-S), University of Minho, Campus de Gualtar, Braga, 4710-057, Portugal

    Marcos A. L. Teixeira, Pedro E. Vieira & Filipe O. Costa

  3. Myrtles Court, Saltash, Cornwall, UK

    David Fenwick

  4. Consorzio Nazionale Interuniversitario per Le Scienze del Mare (CoNISMa), U.L.R. Di Lecce, via provinciale Lecce-Monteroni, Campus Ecotekne, 73100, Lecce, Italy

    Joachim Langeneck

  5. Institutionen for marina vetenskaper, Göteborgs Universitet, Strömstad, Tjärnö, Sweden

    Fredrik Pleijel & Arne Nygren

  6. Museu de Zoologia da Universidade Estadual de Campinas–IB/UNICAMP, Instituto de Biologia, Rua Charles Darwin, Bloco N, Cidade Universitária, Campinas, SP, Brasil

    Bruno R. Sampieri

  7. Biología Animal, Edafología Y Geología, Universidad de La Laguna, Tenerife, Spain

    José Carlos Hernández

  8. Centre for Environmental and Marine Studies (CESAM), Department of Biology, University of Aveiro, Campus de Santiago, Aveiro, 3810-193, Portugal

    Ascensão Ravara

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  1. Marcos A. L. Teixeira
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Contributions

All authors contributed to the study conception and design. Material preparation and data collection were performed by Marcos A. L. Teixeira, Pedro E. Vieira, Joachim Langeneck, José Carlos Hernández, David Fenwick, Fredrik Pleijel, Ascensão Ravara, and Arne Nygren. Analyses were performed by Marcos A. L. Teixeira. The first draft of the manuscript was written by Marcos A. L. Teixeira, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Marcos A. L. Teixeira.

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Supplementary Information

Below is the link to the electronic supplementary material.

13127_2022_597_MOESM1_ESM.xlsx

Supplementary file1: Voucher data, origin of the specimens and GenBank accession numbers for each of the analyzed genetic markers original to this study and molecular metadata used for comparison purposes or as outgroups. (XLSX 21 KB)

13127_2022_597_MOESM2_ESM.xlsx

Supplementary file2: Measurements for all the specimens used in morphometry belonging to Eulalia clavigera with populations from the Macaronesia islands and mainland Europe, Eulalia feliciae sp. nov., Eulalia madeirensis sp. nov. and Eulalia xanthomucosa sp. nov. (XLSX 50 KB)

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Teixeira, M.A.L., Vieira, P.E., Fenwick, D. et al. Revealing the diversity of the green Eulalia (Annelida, Phyllodocidae) species complex along the European coast, with description of three new species. Org Divers Evol 23, 477–503 (2023). https://doi.org/10.1007/s13127-022-00597-1

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