Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5375 No. 3: 23 Nov. 2023
Type: Article
Published: 2023-11-23
DOI: 10.11646/zootaxa.5375.3.3
Page range: 349-378
Abstract views: 436
PDF downloaded: 195

How complex is the Naineris setosa species complex? First integrative study of a presumed cosmopolitan and invasive annelid (Sedentaria: Orbiniidae)

Graduate program in Oceanic Coastal Systems (PGSISCO); Federal University of Paraná; Pontal do Paraná; Paraná; Brazil
Department of Natural History; University Museum of Bergen; University of Bergen; Allégaten 41; 5007 Bergen; Norway
Annelida Integrative taxonomy 28S rRNA gene mtDNA COI 16S cosmopolitanism new species

Abstract

We performed a comparative study of the specimens from the Naineris setosa complex from the Pacific and the Atlantic Oceans and re-described the syntype of N. setosa, including the selection of the lectotype. Molecular phylogenetic and species delimitation analyses based on two mitochondrial (COI and 16S) and one nuclear (28S) marker revealed the presence of three species. One clade with wide Amphi-Atlantic distribution was attributed as Naineris setosa s. str. The second Atlantic clade restricted to Southern and Southeastern Brazil was described as a new species, Naineris lanai sp. n. The third clade, reported from the Northwestern Pacific, was identified as a new species but was not formally described due to the presence of only juvenile-sized worms in the studied material. Detailed morphological descriptions of several diagnostic characters in the Naineris setosa complex are provided.

 

References

  1. Amaral, A.C.Z., Nallin, S.A.H., Steneir, T.M., Forroni, T. de O. & Gomes Filho, D. (2006) Catálogo das Espécies de Annelida Polychaeta do Brasil. Available from: http://www.ib.unicamp.br/museu_zoologia/files/lab_museu_zoologia/Catalogo_Polychaeta_Amaral_et_al_2012.pdf (accessed 4 July 2023)
  2. Arduini, D., Borghese, J., Gravina, M. F., Trani, R., Longo, C., Pierri, C. & Giangrande, A. (2022) Biofouling Role in Mariculture Environment Restoration: An Example in the Mar Grande of Taranto (Mediterranean Sea). Frontiers in Marine Science, 9, 842616. https://doi.org/10.3389/fmars.2022.842616
  3. Atzori, G., López, E., Addis, P., Sabatini, A. & Cabiddu, S. (2016) First record of the alien polychaete Naineris setosa (Scolecida; Orbiniidae) in Tyrrhenian Sea (Western Mediterranean). Marine Biodiversity Records, 9 (1), 1–6. https://doi.org/10.1186/s41200-016-0017-6
  4. Blainville, H. (1828) Dictionnaire des Sciences naturelles, dans lequel on traite méthodiquement des différens êtres de la nature, considérés soit en eux-mêmes, d’après l’état actuel de nos connoissances, soit relativement a l’utilité qu’en peuvent retirer la médicine, l’agriculture, le commerce et les arts. Suivi d’une biographie des plus célèbres naturalistes. FG Levrault, Strasbourg and Paris. [unknown pagination]
  5. Blake, J.A. (2000) A new genus and species of polychaete worm (Family Orbiniidae) from methane seeps in the Gulf of Mexico, interrelationships of the genera of Orbiniidae. Cahiers de Biologie Marine, 41 (4), 435–449. https://doi.org/10.21411/CBM.A.84F1D61E
  6. Blake, J.A. (2017) Polychaeta Orbiniidae from Antarctica, the Southern Ocean, the Abyssal Pacific Ocean, and off South America. Zootaxa, 4218 (1), 1–145. https://doi.org/10.11646/zootaxa.4218.1.1
  7. Blake, J.A. (2020) New species and records of deep-water Orbiniidae (Annelida, Polychaeta) from the Eastern Pacific continental slope, abyssal Pacific Ocean, and the South China Sea. Zootaxa, 4730 (1), 1–61. https://doi.org/10.11646/zootaxa.4730.1.1
  8. Blake, J.A. (2021) New species and records of Orbiniidae (Annelida, Polychaeta) from continental shelf and slope depths of the Western North Atlantic Ocean. Zootaxa, 4930 (1), 1–123. https://doi.org/10.11646/zootaxa.4930.1.1
  9. Blake, J.A. & Giangrande, A. (2011) Naineris setosa (Verrill) (Polychaeta, Orbiniidae), an American subtropical-tropical polychaete collected from an aquaculture facility in Brindisi (Adriatic Sea, Italy): A possible alien species. Italian Journal of Zoology, 78 (Supplement), 20–26. https://doi.org/10.1080/11250003.2011.577982
  10. Bleidorn, C. (2005) Phylogenetic relationships and evolution of Orbiniidae (Annelida, Polychaeta) based on molecular data. Zoological Journal of the Linnean Society, 144 (1), 59–73. https://doi.org/10.1111/j.1096-3642.2005.00160.x
  11. Bleidorn, C., Hill, N., Erséus, C. & Tiedemann, R. (2009) On the role of character loss in orbiniid phylogeny (Annelida): Molecules vs. morphology. Molecular Phylogenetics and Evolution, 52 (1), 57–69. https://doi.org/10.1016/j.ympev.2009.03.022
  12. Bleidorn, C. (2017) Phylogenomics: an introduction. Springer, Cham, 217 pp. https://doi.org/10.1007/978-3-319-54064-1
  13. Carr, C.M., Hardy, S.M., Brown, T.M., Macdonald, T.A. & Hebert, P.D.N. (2011) A tri-oceanic perspective: DNA Barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PLoS ONE, 6 (7), e22232. https://doi.org/10.1371/journal.pone.0022232
  14. Çinar, M.E. (2013) Alien polychaete species worldwide: current status and their impacts. Journal of the Marine Biological Association of the United Kingdom, 93 (5), 1257–1278. https://doi.org/10.1017/S0025315412001646
  15. Clement, M., Snell, Q., Walker, P., Posada, D. & Crandall, K. (2002) TCS: estimating gene genealogies. In: Proceedings 16th International Parallel and Distributed Processing Symposium, Fort Lauderdale, Florida, 15–19 April 2002, 0184.
  16. Dávalos, L.M., Cirranello, A.L., Geisler, J.H. & Simmons, N.B. (2012) Understanding phylogenetic incongruence: lessons from phyllostomid bats. Biological Reviews, 87 (4), 991–1024. https://doi.org/10.1111/j.1469-185X.2012.00240.x
  17. Day, J.H. (1961) The polychaet fauna of South Africa. Part 6. Sedentary species dredged off Cape coasts with a few new records from the shore. Zoological Journal of the Linnean Society, 44 (299), 463–560. https://doi.org/10.1111/j.1096-3642.1961.tb01623.x
  18. Day, J.H. (1963) The polychaete fauna of South Africa. Part 8: New species and records from grab samples and dredgings. Bulletin of the British Museum (Natural History), Series Zoology, 10 (7), 381–445. https://doi.org/10.5962/bhl.part.20530
  19. Day, J.H. (1965) Israel South Red Sea Expedition, 1962, Reports no. 7. Some Polychaeta from the Israel South Red Sea Expedition, 1962. Bulletin of the Sea Fisheries Research Station, Haifa, 38, 15–27.
  20. Day, J.H. (1977) A review of the Australian and New Zealand Orbiniidae (Annelida: Polychaeta). In: Essays on Polychaetous Annelids in Memory of Dr. Olga Hartman. Allan Hancock Found, Los Angeles, California, pp. 217–246.
  21. Dean, H.K. & Blake, J.A. (2015) The Orbiniidae (Annelida: Polychaeta) of Pacific Costa Rica. Zootaxa, 3956 (2), 183–198. https://doi.org/10.11646/zootaxa.3956.2.2
  22. DeBiasse, M.B., Nelson, B.J. & Hellberg, M.E. (2014) Evaluating summary statistics used to test for incomplete lineage sorting: mito‐nuclear discordance in the reef sponge Callyspongia vaginalis. Molecular Ecology, 23 (1), 225–238. https://doi.org/10.1111/mec.12584
  23. Degnan, J.H. & Rosenberg, N.A. (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends in ecology & evolution, 24 (6), 332–340. https://doi.org/10.1016/j.tree.2009.01.009
  24. Drennan, R., Wiklund, H., Rouse, G.W., Georgieva, M.N., Wu, X., Kobayashi, G., Yoshino, K. & Glover, A.G. (2019) Taxonomy and phylogeny of mud owls (Annelida: Sternaspidae), including a new synonymy and new records from the Southern Ocean, North East Atlantic Ocean and Pacific Ocean: challenges in morphological delimitation. Marine Biodiversity, 49, 2659–2697. https://doi.org/10.1007/s12526-019-00998-0
  25. Elgetany, A.H., van Rensburg, H., Hektoen, M., Matthee, C., Budaeva, N., Simon, C.A. & Struck, T.H. (2020) Species delineation in the speciation grey zone—The case of Diopatra (Annelida, Onuphidae). Zoologica Scripta, 49 (4), 516–534. https://doi.org/10.1111/zsc.12421
  26. Fabricius, O. (1780) Fauna Groenlandica: systematice sistens animalia Groenlandiae occidentalis hactenus indagata, quoad nomen specificum, triviale, vernaculumque: synonyma auctorum plurium, descriptionem, locum, victum, generationem, mores, usum, capturamque singuli, prout detegendi occasio fuit: maximaque parte secundum proprias observationes. Impensis Ioannis Gottlob Rothe, Hafniae, XIV + 450 pp. https://doi.org/10.5962/bhl.title.13489
  27. Formaggioni, A., Plazzi, F. & Passamonti, M. (2022) Mito-nuclear coevolution and phylogenetic artifacts: the case of bivalve mollusks. Scientific Reports, 12 (1), 11040. https://doi.org/10.1038/s41598-022-15076-y
  28. Gee, H. (2003) Ending incongruence. Nature, 425 (6960), 782–782. https://doi.org/10.1038/425782a
  29. Glasby, C.J., Erséus, C. & Martin, P. (2021) Annelids in extreme aquatic environments: Diversity, adaptations and evolution. Diversity, 13 (2), 1–23. https://doi.org/10.3390/d13020098
  30. Grosse, M., Bakken, T., Nygren, A., Kongsrud, J.A. & Capa, M. (2020) Species delimitation analyses of NE Atlantic Chaetozone (Annelida, Cirratulidae) reveals hidden diversity among a common and abundant marine annelid. Molecular phylogenetics and evolution, 149, 106852. https://doi.org/10.1016/j.ympev.2020.106852
  31. Grube, A.E. (1855) Beschreibungen neuer oder wenig bekannter Anneliden. Archiv fur Naturgeschichte, Berlin, 21, 81–128. https://doi.org/10.5962/bhl.part.13989
  32. Hartman, O. (1942) A review of the types of polychaetous annelids at the Peabody Museum of Natural History, Yale University. Bulletin of the Bingham Oceanographic Collections, 8, 1–98.
  33. Hartman, O. (1951) The littoral marine annelids of the Gulf of Mexico. Publications of the Institute of Marine Science, University of Texas, 2, 7–124.
  34. Hartman, O. (1957) Orbiniidae, Apistobranchidae, Paraonidae and Logosomidae. Allan Hancock Pacific Expeditions, 15 (3), 211–393, pls. 20–44.
  35. Hillis, D.M. & Dixon, M.T. (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. The Quarterly review of biology, 66 (4), 411–453. https://doi.org/10.1086/417338
  36. Hirano, T., Saito, T., Tsunamoto, Y., Koseki, J., Ye, B., Do, V.T, Miura, O., Suyama, Y. & Chiba, S. (2019) Enigmatic incongruence between mtDNA and nDNA revealed by multi-locus phylogenomic analyses in freshwater snails. Scientific Reports, 9 (1), 1–13. https://doi.org/10.1038/s41598-019-42682-0
  37. 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 (2), 518–522. https://doi.org/10.1093/molbev/msx281
  38. Hutchings, P. & Kupriyanova, E. (2018) Cosmopolitan polychaetes—Fact or fiction? Personal and historical perspectives. Invertebrate systematics, 32 (1), 1–9. https://doi.org/10.1071/IS17035
  39. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K., Von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature methods, 14 (6), 587–589. https://doi.org/10.1038/nmeth.4285
  40. Katoh, K., Kuma, K.I., Toh, H. & Miyata, T. (2005) MAFFT version 5: Improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511–518. https://doi.org/10.1093/nar/gki198
  41. Khedhri, I., Lavesque, N., Bonifácio, P., Djabou, H. & Afli, A. (2014) First record of Naineris setosa (Verrill, 1900) (Annelida: Polychaeta: Orbiniidae) in the Western Mediterranean Sea. BioInvasions Records, 3 (2), 83–88. https://doi.org/10.3391/bir.2014.3.2.05
  42. Kinberg, J.G.H. (1867) Annulata nova. Öfversight af Kungliga Vetenskaps-Adakemiens Förhandlingar, Stockholm, 22, 239–258.
  43. Kolbasova, G. & Neretina, T. (2021) A new species of Pelagobia (Lopadorrhynchidae, Annelida), with some notes on literature records of Pelagobia longicirrata Greeff, 1879. Zootaxa, 5023 (1), 77–92. https://doi.org/10.11646/zootaxa.5023.1.4
  44. Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular biology and evolution, 35 (6), 1547. https://doi.org/10.1093/molbev/msy096
  45. Kvist, S. (2016) Does a global DNA barcoding gap exist in Annelida? Mitochondrial DNA Part A, 27 (3), 2241–2252. https://doi.org/10.3109/19401736.2014.984166
  46. Leigh, J.W. & Bryant, D. (2015) POPART: full-feature software for haplotype network construction. Methods in ecology and evolution, 6 (9), 1110–1116. https://doi.org/10.1111/2041-210X.12410
  47. Liò, P. & Goldman, N. (1998) Models of molecular evolution and phylogeny. Genome research, 8 (12), 1233–1244. https://doi.org/10.1101/gr.8.12.1233
  48. Liu, Y., Fend, S. V., Martinsson, S., Luo, X., Ohtaka, A. & Erséus, C. (2017) Multi-locus phylogenetic analysis of the genus Limnodrilus (Annelida: Clitellata: Naididae). Molecular Phylogenetics and Evolution, 112, 244–257. https://doi.org/10.1016/j.ympev.2017.04.019
  49. Liu, P., Xu, L., Xu, S. L., Martínez, A., Chen, H., Cheng, D., Dumont, H., Han, B-P. & Fontaneto, D. (2018) Species and hybrids in the genus Diaphanosoma Fischer, 1850 (Crustacea: Branchiopoda: Cladocera). Molecular phylogenetics and evolution, 118, 369–378. https://doi.org/10.1016/j.ympev.2017.10.016
  50. Martinsson, S., Klinth, M. & Erséus, C. (2020) Testing species hypotheses for Fridericia magna, an enchytraeid worm (Annelida: Clitellata) with great mitochondrial variation. BMC Evolutionary Biology, 20 (1), 1–12. https://doi.org/10.1186/s12862-020-01678-5
  51. Meyer, A., Bleidorn, C., Rouse, G.W. & Hausen, H. (2008) Morphological and molecular data suggest a cosmopolitan distribution of the polychaete Proscoloplos cygnochaetus Day, 1954 (Annelida, Orbiniidae). Marine Biology, 153, 879–889. https://doi.org/10.1007/s00227-007-0860-4
  52. Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., Von Haeseler, A. & Lanfear, R. (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular biology and evolution, 37 (5), 1530–1534. https://doi.org/10.1093/molbev/msaa015
  53. Müller, F. (1858) Einiges über die Annelidenfauna der Insel Santa Catharina an der brasilianischen Küste. Archiv für Naturgeschichte, 24 (1), 211–220.
  54. Nonato, E.F. (1981) Contribuição ao conhecimento dos anelídeos poliquetas bentônicos da Plataforma Continental Brasileira, entre Cabo Frio e o Arroio Chuí. Livre Docência Thesis, Universidade de São Paulo, São Paulo, 246 pp.
  55. Nonato, E.F., Bolívar, G.A. & Lana, P. (1986) Laonice branchiata, a new species of Spionidae (Annelida; Polychaeta) from the southeastern Brazilian coast. Revista Nerítica, 1 (3), 22–25. https://doi.org/10.5380/rn.v1i3.41193
  56. Ortiz, D., Pekár, S., Bilat, J. & Alvarez, N. (2021) Poor performance of DNA barcoding and the impact of RAD loci filtering on the species delimitation of an Iberian ant-eating spider. Molecular phylogenetics and evolution, 154, 106997. https://doi.org/10.1016/j.ympev.2020.106997
  57. Palumbi, S.R., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabowski, G. (1991) The simple fool’s guide to PCR, Special Publication. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, Honolulu, 28 pp.
  58. Qiu, P. L., Liu, S. Y., Bradshaw, M., Rooney-Latham, S., Takamatsu, S., Bulgakov, T. S., Tang, S.R., Feng, J., Aroge, T., Li, Y., Wang, L.L. & Braun, U. (2020) Multi-locus phylogeny and taxonomy of an unresolved, heterogeneous species complex within the genus Golovinomyces (Ascomycota, Erysiphales), including G. ambrosiae, G. circumfusus and G. spadiceus. BMC microbiology, 20, 1–16. https://doi.org/10.1186/s12866-020-01731-9
  59. Radashevsky, V.I. & Lana, P. (2009) Laonice (Annelida: Spionidae) from South and Central America. Zoosymposia, 2, 265–295. https://doi.org/10.11646/zoosymposia.2.1.19
  60. Radashevsky, V.I., Malyar, V.V., Pankova, V.V., Gambi, M.C., Giangrande, A., Keppel, E., Nygren, A., Al-Kandari, M. & Carlton, J.T. (2020) Disentangling invasions in the sea: molecular analysis of a global polychaete species complex (Annelida: Spionidae: Pseudopolydora paucibranchiata). Biological Invasions, 22 (12), 3621–3644. https://doi.org/10.1007/s10530-020-02346-x
  61. Rebai, N., Mosbahi, N., Dauvin, J.C. & Neifar, L. (2022) Ecological Risk Assessment of Heavy Metals and Environmental Quality of Tunisian Harbours. Journal of Marine Science and Engineering, 10 (11), 1625. https://doi.org/10.3390/jmse10111625
  62. Rioja, E. (1960) Estudios anelidologicos. XXIV. Adiciones a la fauna de Anelidos Poliquetos de las costas orientales de México. Anales Del Instituto de Biología, México, 31, 289–316.
  63. Rokas, A., Williams, B.L., King, N. & Carroll, S.B. (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature, 425 (6960), 798–804. https://doi.org/10.1038/nature02053
  64. Salicini, I., Ibáñez, C. & Juste, J. (2011) Multilocus phylogeny and species delimitation within the Natterer’s bat species complex in the Western Palearctic. Molecular Phylogenetics and Evolution, 61 (3), 888–898. https://doi.org/10.1016/j.ympev.2011.08.010
  65. Seixas, V.C., Steiner, T.M., Solé-Cava, A.M., Amaral, A.C.Z. & Paiva, P.C. (2021) Hidden diversity within the Diopatra cuprea complex (Annelida: Onuphidae): Morphological and genetics analyses reveal four new species in the south-west Atlantic. Zoological Journal of The Linnean Society, 191 (3), 637–671. https://doi.org/10.1093/zoolinnean/zlaa032
  66. Solis-Weiss, V. & Fauchald, K. (1989) Orbiniidae (Annelida: Polychaeta) from mangrove root-mats in Belize, with a revision of the protoariciin genera. Proceedings of the Biological Society of Washington, 102 (3), 772–792.
  67. Struck, T. H., Golombek, A., Hoesel, C., Dimitrov, D. & Elgetany, A.H. (2023) Mitochondrial Genome Evolution in Annelida—A Systematic Study on Conservative and Variable Gene Orders and the Factors Influencing its Evolution. Systematic Biology, syad023. https://doi.org/10.1093/sysbio/syad023
  68. Taboada, S., Riesgo, A., Bas, M., Arnedo, M. A., Cristobo, J., Rouse, G.W. & Avila, C. (2015) Bone-eating worms spread: insights into shallow-water Osedax (Annelida, Siboglinidae) from Antarctic, Subantarctic, and Mediterranean waters. PLoS One, 10 (11), e0140341. https://doi.org/10.1371/journal.pone.0140341
  69. Taboada, S., Leiva, C., Bas, M., Schult, N. & McHugh, D. (2017) Cryptic species and colonization processes in Ophryotrocha (Annelida, Dorvilleidae) inhabiting vertebrate remains in the shallow‐water Mediterranean. Zoologica Scripta, 46 (5), 611–624. https://doi.org/10.1111/zsc.12239
  70. Tamura, K., Stecher, G. & Kumar, S. (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38 (7), 3022–3027. https://doi.org/10.1093/molbev/msab120
  71. Toews, D.P. & Brelsford, A. (2012) The biogeography of mitochondrial and nuclear discordance in animals. Molecular ecology, 21 (16), 3907–3930. https://doi.org/10.1111/j.1365-294X.2012.05664.x
  72. Treadwell, A.L. (1901) The polychaetous annelids of Porto Rico. Bulletin of the United States National Fish Commission, 20 (2), 183–210.
  73. Treadwell, A.L. (1936) Polychaetous annelids from the vicinity of Nonsuch Island, Bermuda. Zoologica, 21 (1), 49–68. https://doi.org/10.5962/p.190351
  74. Treadwell, A.L. (1939) Polychaetous annelids from Porto Rico and vicinity. In: Scientific Survey of Porto Rico and the Virgin Islands. Vol. 16. New York Academy of Sciences, New York, New York, pp. 151–319.
  75. Verril, A.E. (1900) Additions to the Turbellaria, Nemertina and Annelida of the Bermudas, with revisions of some New England genera and species. Transactions of the Connecticut Academy of Arts and Sciences, 10, 595–671. https://doi.org/10.5962/bhl.part.7035
  76. Zhadan, A., Stupnikova, A. & Neretina, T. (2015) Orbiniidae (Annelida: Errantia) from Lizard Island, Great Barrier Reef, Australia with notes on orbiniid phylogeny. Zootaxa, 4019 (1), 773–801. https://doi.org/10.11646/zootaxa.4019.1.27
  77. Zhadan, A. (2020) Review of Orbiniidae (Annelida, Sedentaria) from Australia. Zootaxa, 4860 (4), 451–502. https://doi.org/10.11646/zootaxa.4860.4.1
  78. Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29 (22), 2869–2876. https://doi.org/10.1093/bioinformatics/btt499