Ophryotrocha (Dorvilleidae, Polychaeta, Annelida) from deep-sea hydrothermal vents, with the description of five new species
Abstract
Dorvilleids belonging to Ophryotrocha Claparède & Mecznikow, 1869 are known from deep-sea hydrothermal vents in the Pacific, Atlantic, Indian and Southern Oceans. However, how they colonized and diversified in these ecosystems has not been assessed in detail. Here, a collection of Pacific hydrothermal vent Ophryotrocha was examined using morphology and DNA markers (COI, 16S and H3). Five new species were revealed, largely expanding the diversity of the group at this habitat type. They are Ophryotrocha charlottae sp. nov., O. kailae sp. nov., O. marinae sp. nov., O. pruittae sp. nov. from eastern Pacific, and O. bohnorum sp. nov. from the western Pacific. Phylogenetic analyses based on the concatenated alignments of all three genes suggest vent habitants have been colonized several times independently within Ophryotrocha. One clade of six vent species was recovered, indicative of diversification following a colonization of hydrothermal vents, likely in the eastern Pacific. An Indian Ocean species, O. jiaolongi, was nested inside this clade and was closely related to one of the new species from the Gulf of California, diverging from it by less than 4% on COI.
References
Åkesson 1974. Reproduction and larval morphology of five Ophryotrocha species (Polychaeta, Dorvilleidae). Zoologica Scripta 2: 145–155. https://doi.org/10.1111/j.1463-6409.1974.tb00746.x
Blake J.A. 1985. Polychaeta from the vicinity of deep-sea geothermal vents in the eastern Pacific. I. Euphrosinidae, Phyllodocidae, Hesionidae, Nereididae, Glyceridae, Dorvilleidae, Orbiniidae, and Maldanidae. Bulletin of the Biological Society of Washington 6: 67–101.
Blake J.A. & Hilbig B. 1990. Polychaeta from the vicinity of deep-sea hydrothermal vents in the eastern Pacific. II. New species and records from the Juan de Fuca and Explorer Ridge systems. Pacific Science 44: 219–253.
Borda E., Kudenov J.D., Chevaldonné P., Blake J.A., Desbruyères D., Fabri M.-C., Hourdez S., Pleijel F., Shank T.M., Wilson N.G., Schulze A. & Rouse G.W. 2013. Cryptic species of Archinome (Annelida: Amphinomida) from vents and seeps. Proceedings. Biological sciences / The Royal Society 280 (1770): 20131876. https://doi.org/10.1098/rspb.2013.1876
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: e22232. https://doi.org/10.1371/journal.pone.0022232
Clement M., Posada D. & Crandall K.A. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x
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: 419–437. https://doi.org/10.1071/zo98048
Dahlgren T.G., Akesson B., Schander C., Halanych K.M. & Sundberg P. 2001. Molecular phylogeny of the model annelid Ophryotrocha. The Biological Bulletin 201: 193–203. https://doi.org/10.2307/1543334
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: 291–294. https://doi.org/10.1093/molbev/msz189
Desbruyères D., Segonzac M. & Bright M. 2006. Handbook of Deep-Sea Hydrothermal Vent Fauna. Denisia 2006: 1–565.
Edgar R.C. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797. https://doi.org/10.1093/nar/gkh340
Edler D., Klein J., Antonelli A. & Silvestro D. 2021. raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution 12: 373–377. https://doi.org/10.1111/2041-210x.13512
Eibye-Jacobsen D. & Kristensen R. 1994. A new genus and species of Dorvilleidae (Annelida, Polychaeta) from Bermuda, with a phylogenetic analysis of Dorvilleidae, Iphitimidae and Dinophilidae. Zoologica Scripta 23: 107–131. https://doi.org/10.1111/j.1463-6409.1994.tb00379.x
Folmer O., Black M., Hoeh W.R., Lutz R.A. & Vrijenhoek R.C. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
Goffredi S.K., Johnson S., Tunnicliffe V., Caress D., Clague D., Escobar E., Lundsten L., Paduan J.B., Rouse G., Salcedo D.L., Soto L.A., Spelz-Madero R., Zierenberg R. & Vrijenhoek R. 2017. Hydrothermal vent fields discovered in the southern Gulf of California clarify role of habitat in augmenting regional diversity. Proceedings. Biological Sciences / The Royal Society 284: 20170817. https://doi.org/10.1098/rspb.2017.0817
Han Y., Zhang D., Wang C. & Zhou Y. 2021. Out of the Pacific: A new alvinellid worm (Annelida: Terebellida) from the northern Indian Oocean hydrothermal vents. Frontiers in Marine Science 8: 543. https://doi.org/10.3389/fmars.2021.669918
Heggøy K.K., Schander C. & Åkesson B. 2007. The phylogeny of the annelid genus Ophryotrocha (Dorvilleidae). Marine biology research 3: 412–420. https://doi.org/10.1080/17451000701695361
Jimi N., Chen C. & Hiroshi K. 2019. New record of the hydrothermal vent-endemic polychaete Archinome jasoni Borda et al., 2013 (Annelida, Amphinomidae) from the Northwest Pacific. Check List 15 (3): 523–526. https://doi.org/10.15560/15.3.523
Katoh K. & Standley D.M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
Kozlov A.M., Darriba D., Flouri T., Morel B. & Stamatakis A. 2019. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35: 4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Leigh J.W. & Bryant D. 2015. POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution / British Ecological Society 6: 1110–1116. https://doi.org/10.1111/2041-210x.12410
Levin L.A., Ziebis W., Mendoza G.F., Growney V.A., Tryon M.D., Brown K.M., Mahn C., Gieskes J.M. & Rathburn A.E. 2003. Spatial heterogeneity of macrofauna at northern California methane seeps: influence of sulfide concentration and fluid flow. Marine Ecology Progress Series 265: 123–139. https://doi.org/10.3354/meps265123
Macnaughton M.O., Worsaae K. & Eibye-Jacobsen D. 2010. Jaw morphology and ontogeny in five species of Ophryotrocha. Journal of Morphology 271: 324–339. https://doi.org/10.1002/jmor.10800
Miura 1997. Two new species of the genus Ophryotrocha (Polychaeta, Iphitimiidae) from Kagoshima Bay. Bulletin of Marine Science 60: 300–305.
Orensanz J.M. 1990. The eunicemorph polychaete annelids from Antarctic and Subantarctic Seas. Antarctic Research Series 52: 1–183.
Palumbi S.R. 1996. Nucleic acids II: The polymerase chain reaction. In: Hillis D.M., Moritz C. & Mable B.K. (eds) Molecular Systematics. 2nd Edition: 205–247. Sinauer Associates, Sunderland, Massachusetts.
Paxton H. 2004. Jaw growth and replacement in Ophryotrocha labronica (Polychaeta, Dorvilleidae). Zoomorphology 123: 147–154. https://doi.org/10.1007/s00435-004-0097-4
Paxton H. & Morineaux M. 2009. Three species of Dorvilleidae (Annelida: Polychaeta) associated with Atlantic deep-sea reducing habitats, with the description of Ophryotrocha fabriae, new species. Proceedings of the Biological Society of Washington 122: 14–25. https://doi.org/10.2988/08-22.1
Pleijel F. & Eide R. 1996. The phylogeny of Ophryotrocha (Dorvilleidae, Eunicida, Polychaeta). Journal of Natural History 30: 647–659. https://doi.org/10.1080/00222939600770361
Premoli M.C. & Sella G. 1995. Sex economy in benthic polychaetes. Ethology Ecology & Evolution 7: 27–48. https://doi.org/10.1080/08927014.1995.9522968
Rambaut A. & Drummond A.J. 2003. FigTree 1.1.2. Available form http://tree.bio.ed.ac.uk/software/figtree/ [accessed 28 Mar. 2023].
Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904. https://doi.org/10.1093/sysbio/syy032
Ravara A., Wiklund H. & Cunha M.R. 2021. Four new species and further records of Dorvilleidae (Annelida, Polychaeta) from deep-sea organic substrata, NE Atlantic. European Journal of Taxonomy 736: 44–81. https://doi.org/10.5852/ejt.2021.736.1251
Read G. & Fauchald K. 2022. World Polychaeta Database. Dorvilleidae Chamberlin, 1919. Available from Accessed through: World Register of Marine Species. Available from https://www.marinespecies.org/aphia.php?p=taxdetails&id=971 [accessed 14 Jun. 2022].
Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model
choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
Rouse G.W., Pleijel F. & Tilic E. 2022. Annelida. Oxford University Press, London / New York. https://doi.org/10.1093/oso/9780199692309.001.000
Salcedo D.L., Soto L.A. & Paduan J.B. 2019. Trophic structure of the macrofauna associated to deep-vents of the southern Gulf of California: Pescadero Basin and Pescadero Transform Fault. PloS One 14: e0224698. https://doi.org/10.1371/journal.pone.0224698
Salvo F., Wiklund H., Dufour S.C., Hamoutene D., Pohle G. & Worsaae K. 2014. A new annelid species from whalebones in Greenland and aquaculture sites in Newfoundland: Ophryotrocha cyclops, sp. nov. (Eunicida: Dorvilleidae). Zootaxa 3887: 555–514. https://doi.org/10.11646/Zootaxa.3887.5.3
Solis Weiss V. & Hilbig B. 1992. Redescription of Ophryotrocha platykephale Blake (Polychaeta, Dorvilleidae) from the Guaymas Basin hydrothermal vents. Bulletin of the Southern California Academy of Sciences 91: 92–96.
Swofford D.L. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
Taboada S., Bas M., Leiva C., Garriga M., Sarda R. & Avila C. 2016. Life after death: shallow-water Mediterranean invertebrate communities associated with mammal bones. Marine Ecology – an Evolutionary Perspective 37: 164–178. https://doi.org/10.1111/maec.12257
Taboada S., Wiklund H., Glover A.G., Dahlgren T.G., Cristobo J. & Avila C. 2013. Two new Antarctic Ophryotrocha (Annelida: Dorvilleidae) described from shallow-water whale bones. Polar Biology 36: 1031–1045. https://doi.org/10.1007/s00300-013-1326-4
Templeton A.R., Crandall K.A. & Sing C.F. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132: 619–633. https://doi.org/10.1093/genetics/132.2.619
Thornhill D.J., Dahlgren T.G. & Halanych K.M. 2009. Evolution and Ecology of Ophryotrocha (Dorvilleidae, Eunicida). In: Shain D.H. (ed.) Annelids in Modern Biology: 242–256. Wiley & Blackwell.
Thornhill D.J., Struck T.H., Ebbe B., Lee R.W., Mendoza G.F., Levin L.A. & Halanych K.M. 2012. Adaptive radiation in extremophilic Dorvilleidae (Annelida): diversification of a single colonizer or multiple independent lineages? Ecology and Evolution 2: 1958–1970. https://doi.org/10.1002/ece3.314
Wang Z., Xu T., Zhang Y., Zhou Y., Liu Z., Chen C., Watanabe H.K. & Qiu J.-W. 2020. Molecular phylogenetic and morphological analyses of the ‘monospecific’ Hesiolyra (Annelida: Hesionidae) reveal two new species. Deep Sea Research Part I: Oceanographic Research Papers 166: 103401. https://doi.org/10.1016/j.dsr.2020.103401
Watanabe H. & Kojima S. 2015. Vent Fauna in the Okinawa Trough. In: Ishibashi J.-I., Okino K. & Sunamura M. (eds) Subseafloor Biosphere Linked to Hydrothermal Systems: TAIGA Concept: 449–459. Springer Japan, Tokyo.
Wiklund H., Altamira I.V., Glover A.G., Smith C.R., Baco A.R. & Dahlgren T.G. 2012. Systematics and biodiversity of Ophryotrocha (Annelida, Dorvilleidae) with descriptions of six new species from deep-sea whale-fall and wood-fall habitats in the north-east Pacific. Systematics and Biodiversity 10: 243–259. https://doi.org/10.1080/14772000.2012.693970
Wiklund H., Glover A.G. & Dahlgren T.G. 2009. Three new species of Ophryotrocha (Annelida: Dorvilleidae) from a whale-fall in the North-East Atlantic. Zootaxa 2228: 43–56. https://doi.org/10.11646/zootaxa.2228.1.3
Wiklund H., Purschke G. & Ravara A. 2021. 7.12.2 Dorvilleidae Chamberlin, 1919. In: Purschke G., Böggemann M. & Wilfried W. (eds) Handbook of Zoology, Annelida Volume 1: Annelida Basal Groups and Pleistoannelida, Sedentaria III and Errantia I.: 361–382.
Yen N.K. & Rouse G.W. 2020. Phylogeny, biogeography and systematics of Pacific vent, methane seep, and whale-fall Parougia (Dorvilleidae : Annelida), with eight new species. Invertebrate Systematics 34: 200. https://doi.org/10.1071/is19042
Zhang D., Zhou Y., Wang C. & Rouse G.W. 2017. A new species of Ophryotrocha (Annelida, Eunicida, Dorvilleidae) from hydrothermal vents on the Southwest Indian Ridge. ZooKeys 686:1–9. https://doi.org/10.3897/zookeys.687.13046
Zhou Y., Chen C., Sun Y., Watanabe H.K., Zhang R. & Wang C. 2019. Amphisamytha (Annelida: Ampharetidae) from Indian Ocean hydrothermal vents: Biogeographic implications. Deep Sea Research Part I: Oceanographic Research Papers 154: 103148. https://doi.org/10.1016/j.dsr.2019.103148
Zhou Y., Chen C., Zhang D., Wang Y., Watanabe H.K., Sun J., Bissessur D., Zhang R., Han Y., Sun D., Xu P., Lu B., Zhai H., Han X., Tao C., Qiu Z., Sun Y., Liu Z., Qiu J.-W. & Wang C. 2022. Delineating biogeographic regions in Indian Ocean deep-sea vents and implications for conservation. Diversity & Distributions 28: 2858–2870. https://doi.org/10.1111/ddi.13535
Copyright (c) 2023 Dongsheng Zhang, Yadong Zhou, Nicole Yen, Avery S. Hiley, Greg W. Rouse
This work is licensed under a Creative Commons Attribution 4.0 International License.
Creative Commons Copyright Notices
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are NOT ALLOWED TO post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to taxonomic issues.
