Abstract
Nereididae is one of Annelida’s most diverse and well-studied families; despite this, only recently have molecular approaches been used to access phylogenetic hypotheses within the family. At least two nereidid groups can be identified based on mitochondrial gene order; however, this type of molecular information is not available for most taxa, and relationships of subfamilies are still poorly understood. In the present study, we used nuclear and mitochondrial markers to evaluate relationships within Nereididae and verified hypotheses on subfamilies delineation and relationship. Our results suggest the paraphyletic status of Gymnonereidinae and Nereidinae, as well as some genera within these subfamilies. Despite this, a revision of these subfamilies delineation and diagnoses was presented to match current phylogenetic understanding of the group. We suggest reverting to the original definition of Gymnonereidinae to include only the genera originally proposed by Banse in 1977. Our results also support monophyly of a large group that can be defined by mitochondrial gene order. This group includes most taxa identified as Nereidinae, and therefore, we suggest that this feature should be used as diagnostic of the subfamily.
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Data availability
Data from the sequences used in this study are available on Genbank. Other data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Alves, P. R., Glasby, C. J., & Santos, C. S. G. (2018). On the use of troglomorphic characters in Namanereidinae (Annelida; Nereididae) systematics. Zootaxa, 4531(2), 195. https://doi.org/10.11646/zootaxa.4531.2.2
Alves, P. R., Halanych, K. M., & Santos, C. S. G. (2020). The phylogeny of Nereididae (Annelida) based on mitochondrial genomes. Zoologica Scripta, 49(3), 366–378. https://doi.org/10.1111/zsc.12413
Bakken, T., Glasby, C. J., Santos, C. S. G., & Wilson, R. S. (2022). Nereididae Blainville, 1818. In Handbook of Zoology Online. Volume 4 Pleistoannelida, Errantia II (pp. 259–307). Berlin: De Gruyter.
Bakken, T., Glasby, C. J., & Wilson, R. (2009). A review of paragnath morphology in Nereididae (Polychaeta). Zoosymposia, 2, 305–316.
Bakken, T., & Wilson, R. S. (2005). Phylogeny of nereidids (Polychaeta, Nereididae) with paragnaths. Zoologica Scripta, 34(5), 507–547. https://doi.org/10.1111/j.1463-6409.2005.00200.x
Banse, K. (1977). Gymnonereidinae new subfamily: The Nereididae (Polychaeta) with bifid parapodial neurocirri. Journal of Natural History, 11(6), 609–628. https://doi.org/10.1080/00222937700770541
Böggemann, M. (2009). Polychaetes (Annelida) of the abyssal SE Atlantic, 178.
Bolotov, I. N., Aksenova, O. V., Bakken, T., Glasby, C. J., Gofarov, MYu., Kondakov, A. V., et al. (2018). Discovery of a silicate rock-boring organism and macrobioerosion in fresh water. Nature Communications, 9(1), 2882. https://doi.org/10.1038/s41467-018-05133-4
Boore, J. L., & Brown, W. M. (2000). Mitochondrial Genomes of Galathealinum, Helobdella, and Platynereis: Sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Molecular Biology and Evolution, 17(1), 87–106. https://doi.org/10.1093/oxfordjournals.molbev.a026241
Chen, X., Li, M., Liu, H., Li, B., Guo, L., Meng, Z., & Lin, H. (2016). Mitochondrial genome of the polychaete Tylorrhynchus heterochaetus (Phyllodocida, Nereididae). Mitochondrial DNA Part A, 27(5), 3372–3373. https://doi.org/10.3109/19401736.2015.1018226
Colgan, D., Hutchings, P., & Braune, M. (2006). A multigene framework for polychaete phylogenetic studies. Organisms Diversity & Evolution, 6(3), 220–235. https://doi.org/10.1016/j.ode.2005.11.002
Conde-Vela, V. M. (2021). Revision of Laeonereis Hartman, 1945 (Annelida: Phyllodocida: Gymnonereidinae), with a review of shaft morphology in nereidids. Journal of Natural History, 55(7–8), 381–455. https://doi.org/10.1080/00222933.2021.1903601
Conde-Vela, V. M. (2017). The troglomorphic adaptations of Namanereidinae (Annelida, Nereididae) revisited, including a redescription of Namanereis cavernicola (Solís-Weiss & Espinasa, 1991), and a new Caribbean species of Namanereis Chamberlin, 1919. Subterranean Biology, 23, 19–28. https://doi.org/10.3897/subtbiol.23.13701
Dahlgren, T. G., Lundberg, J., Pleijel, F., & Sundberg, P. (2000). Morphological and molecular evidence of the phylogeny of Nereidiform polychaetes (Annelida). Journal of Zoological Systematics and Evolutionary Research, 38(4), 249–253. https://doi.org/10.1046/j.1439-0469.2000.384150.x
Drennan, R., Wiklund, H., Rabone, M., Georgieva, M. N., Dahlgren, T. G., & Glover, A. G. (2021). Neanthes goodayi sp. nov. (Annelida, Nereididae), a remarkable new annelid species living inside deep-sea polymetallic nodules. European Journal of Taxonomy, 760, 160–185. https://doi.org/10.5852/ejt.2021.760.1447
Fischer, A., & Dorresteijn, A. (2004). The polychaete Platynereis dumerilii (Annelida): A laboratory animal with spiralian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle. BioEssays, 26(3), 314–325. https://doi.org/10.1002/bies.10409
Fitzhugh, K. (1987). Phylogenetic relationships within the Nereididae (Polychaeta): Implications at the subfamily level. Proceedings of the Biological Society of Washington, 7, 174–183.
Gallardo, V. A. (1968). Polychaeta from the Bay of Nha Trang. South Vietnam. Naga Report, 4(3), 35–279.
Glasby, C. J. (1991). Phylogenetic relationships in the Nereididae (Annelida: Polychaeta), chiefly in the subfamily Gymnonereidinae, and the monophyly of the Namanereidinae. Bulletin of Marine Science, 48(2), 559–573.
Glasby, C. J. (1999). The Namanereidinae (Polychaeta: Nereididae). Part 1, taxonomy and phylogeny. Records of the Australian Museum, 25, 129–129.
Glasby, C. J. (1993). Family revision and cladistic analysis of the Nereidoidea (Polychaeta: Phyllodocida). Invertebrate Taxonomy, 7, 1551–1573.
Hall, K. A., Hutchings, P. A., & Colgan, D. J. (2004). Further phylogenetic studies of the Polychaeta using 18S rDNA sequence data. Journal of the Marine Biological Association of the United Kingdom, 84(5), 949–960. https://doi.org/10.1017/S0025315404010240h
Hartman, O. (1959). Capitellidae and Nereidae (Marine Annelids) from the Gulf side of Florida, with a review of Freshwater Nereidae, 16.
Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q., & Le, S. V. (2007). UFBoot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution, 35(2), 518–522. https://doi.org/10.5281/zenodo.854445
Hylleberg, J., & Nateewathana, A. (1988). Polychaetes of Thailand. Nereididae (Part 2): Ceratocephale and Gymnonereis, with description of two new species and notes on the subfamily Gymnonereis (p. 20). Phuket Marine Biological Center Research Bulletin No 49.
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., 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
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772–780. https://doi.org/10.1093/molbev/mst010
Kim, H., Choi, H. K., Kim, H. J., & Min, G. S. (2017). The complete mitochondrial genome of epitokous Nereis species (Phyllodocida, Nereididae) from Dok-do. Korea. Mitochondrial DNA Part B: Resources, 2(2), 751–752. https://doi.org/10.1080/23802359.2017.1390419
Kim, H., Jung, G., Lee, Y.-C., Pae, S.-J., Kim, C.-G., & Lee, Y.-H. (2015). The complete mitochondrial genome of the marine polychaete: Perinereis aibuhitensis (Phyllodocida, Nereididae). Mitochondrial DNA, 26(6), 869–870. https://doi.org/10.3109/19401736.2013.861435
Kim, H., Kim, H. J., & Lee, Y.-H. (2016). The complete mitochondrial genome of the marine polychaete: Hediste diadroma (Phyllodocida, Nereididae). Mitochondrial DNA Part B, 1(1), 822–823. https://doi.org/10.1080/23802359.2016.1247663
Kück, P., & Meusemann, K. (2010). FASconCAT: Convenient handling of data matrices. Molecular Phylogenetics and Evolution, 56(3), 1115–1118. https://doi.org/10.1016/j.ympev.2010.04.024
Lin, G.-M., Audira, G., & Hsiao, C.-D. (2017). The complete mitogenome of nereid worm, Neanthes glandicincta (Annelida: Nereididae). Mitochondrial DNA Part B, 2(2), 471–472. https://doi.org/10.1080/23802359.2017.1361346
Lin, G.-M., Shen, K.-N., & Hsiao, C.-D. (2016). Next generation sequencing yields the complete mitogenome of nereid worm, Namalycastis abiuma (Annelida: Nereididae). Mitochondrial DNA Part B, 1(1), 103–104. https://doi.org/10.1080/23802359.2015.1137845
Liu, M., Liu, H., Wang, Q., Guan, S., & Ge, S. (2012). Phylogenetic relationships of twenty-one nereids species inferring two different evolutionary origins? Aquatic Science and Technology, 1(1), 167–180. https://doi.org/10.5296/ast.v1i1.2980
Magesh, M., Kvist, S., & Glasby, C. (2012). Description and phylogeny of Namalycastis jaya sp. n. (Polychaeta, Nereididae, Namanereidinae) from the southwest coast of India. ZooKeys, 238, 31–43. https://doi.org/10.3897/zookeys.238.4014
Metcalfe, K. N., & Glasby, C. J. (2008). Diversity of Polychaeta (Annelida) and other worm taxa in mangrove habitats of Darwin Harbour, northern Australia. Journal of Sea Research, 59(1–2), 70–82. https://doi.org/10.1016/j.seares.2007.06.002
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
Olive, P. J. W. (1999). Polychaete aquaculture and polychaete science: A mutual synergism. Reproductive Strategies and Developmental Patterns in Annelids, 175–183. https://doi.org/10.1007/978-94-017-2887-4_9
Özpolat, B. D., Randel, N., Williams, E. A., Bezares-Calderón, L. A., Andreatta, G., Balavoine, G., et al. (2021). The Nereid on the rise: Platynereis as a model system. EvoDevo, 12(1), 10. https://doi.org/10.1186/s13227-021-00180-3
Paiva, P. C., Mutaquilha, B. F., Coutinho, M. C. L., & Santos, C. S. G. (2019). Comparative phylogeography of two coastal species of Perinereis Kinberg, 1865 (Annelida, Polychaeta) in the South Atlantic. Marine Biodiversity, 49(3), 1537–1551. https://doi.org/10.1007/s12526-018-0927-0
Park, T., Lee, S. H., & Kim, W. (2016). Complete mitochondrial genome sequence of the giant mud worm Paraleonnates uschakovi Khlebovich & Wu, 1962 (Polychaeta: Nereididae). Mitochondrial DNA Part B: Resources, 1(1), 640–642. https://doi.org/10.1080/23802359.2016.1214552
Park, T., Lee, S.-H., Shin, M.-H., & Kim, W. (2017). Determination of complete mitogenome sequence for Eastern Asian population of Cheilonereis cyclurus (Harrington, 1897) (Polychaeta: Nereididae). Mitochondrial DNA Part B, 2(2), 669–671. https://doi.org/10.1080/23802359.2017.1372717
Pettibone, M. H. (1970). Polychaeta erranta of the Siboga expedition 4: Some additional Polychetes of the Polynoidae, Hesionidae, Nereidae, Goniadidae, Eunicidae, and Onuphidae, selected as new species by the late Dr. Hermann Augener with remarks on other related species. In M. Weber, L. F. Beaufort, & J. H. Stock (Eds.), Siboga-Expeditie Uitkomsten op Zoologisch, Bonatisch, Oceanographisch en Geol ogischgebied verzameld in Nederlandsch Oost-Indië 1899–1900, (pp. 199–270). Leiden: EJ Brill.
Pleijel, F., & Dahlgren, T. (1998). Position and delineation of Chrysopetalidae and Hesionidae (Annelida, Polychaeta, Phyllodocida). Cladistics, 14(2), 129–150. https://doi.org/10.1111/j.1096-0031.1998.tb00327.x
Purschke, G., Hessling, R., & Westheide, W. (2000). The phylogenetic position of the Clitellata and the Echiura - On the problematic assessment of absent characters. Journal of Zoological Systematics and Evolutionary Research, 38(3), 165–173. https://doi.org/10.1046/j.1439-0469.2000.383146.x
Reish, D. J., & Gerlinger, T. V. (1997). A review of the toxicological studies with polychaetous annelids. Bulletin of Marine Science, 60(2), 584–607.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542. https://doi.org/10.1093/sysbio/sys029
Rousset, V., Pleijel, F., Rouse, G. W., Erséus, C., & Siddall, M. E. (2007). A molecular phylogeny of annelids. Cladistics, 23(1), 41–63. https://doi.org/10.1111/j.1096-0031.2006.00128.x
Ruta, C., Nygren, A., Rousset, V., Sundberg, P., Tillier, A., Wiklund, H., & Pleijel, F. (2007). Phylogeny of Hesionidae (Aciculata, Polychaeta), assessed from morphology, 18S rDNA, 28S rDNA, 16S rDNA and COI. Zoologica Scripta, 36(1), 99–107. https://doi.org/10.1111/j.1463-6409.2006.00255.x
Sampieri, B. R., Vieira, P. E., Teixeira, M. A. L, Seixas, V. C, Pagliosa, P. R, Amaral, A. C. Z., & Costa F. O. (2021). Molecular diversity within the genus Laeonereis (Annelida, Nereididae) along the west Atlantic coast: Paving the way for integrative taxonomy. PeerJ, 9:e11364. https://doi.org/10.7717/peerj.11364
Santos, C. S. G., Pleijel, F., Lana, P., & Rouse, G. W. (2005). Phylogenetic relationships within Nereididae (Annelida: Phyllodocida). Invertebrate Systematics, 19(6), 557. https://doi.org/10.1071/IS05001
Sato, M., & Nakashima, A. (2003). A review of Asian Hediste species complex (Nereididae, Polychaeta) with descriptions of two new species and a redescription of Hediste japonica (Izuka, 1908). Zoological Journal of the Linnean Society, 137, 403–445.
Seixas, V. C., Paiva, P. C., & Russo, C. A. M. (2016). Complete mitochondrial genomes are not necessarily more informative than individual mitochondrial genes to recover a well-established annelid phylogeny. Gene Reports, 5, 10–17. https://doi.org/10.1016/j.genrep.2016.07.011
Shimodaira, H. (2002). An approximately unbiased test of phylogenetic tree selection. Systematic Biology, 51(3), 492–508. https://doi.org/10.1080/10635150290069913
Shoobs, N. F., Schmidt, R. E., & McMullin, E. R. (2016). A new record of the freshwater polychaete Namanereis hummelincki (Polychaeta: Nereididae) from epigean waters of Montserrat. Zootaxa, 4061(2), 157. https://doi.org/10.11646/zootaxa.4061.2.5
Tosuji, H., Bastrop, R., Götting, M., Park, T., Hong, J.-S., & Sato, M. (2019). Worldwide molecular phylogeny of common estuarine polychaetes of the genus Hediste (Annelida: Nereididae), with special reference to interspecific common haplotypes found in southern Japan. Marine Biodiversity, 49(3), 1385–1402. https://doi.org/10.1007/s12526-018-0917-2
Vijapure, T., Sukumaran, S., & Manohar, C. S. (2019). Molecular characterization and phylogenetics of Indian polychaete fauna: Scope for implementation in ecological monitoring. Aquatic Ecology, 53(4), 665–677. https://doi.org/10.1007/s10452-019-09717-0
Westheide, W., McHugh, D., Purschke, G., & Rouse, G. (1999). Systematization of the Annelida: Different approaches. Hydrobiologia, 402, 291–307. https://doi.org/10.1023/A:1003713230485
Won, E.-J., Rhee, J.-S., Shin, K.-H., & Lee, J.-S. (2013). Complete mitochondrial genome of the marine polychaete, Perinereis nuntia (Polychaeta, Nereididae). Mitochondrial DNA, 24(4), 342–343. https://doi.org/10.3109/19401736.2012.760082
Zhong, M. Hansen, B., Nesnidal, M., Golombek, A., Halanych, K. M., &. Struck, T. H. (2011). Escaping the symplesiomorphy trap: A multigene phylogenetic analysis for terebelliform annelids. BMC Evolutionary Biology, 11(369), 1–15. https://doi.org/10.1186/1471-2148-11-369
Acknowledgements
The authors are grateful for Orlemir Carrete, Karla Paresque, Nicolas Lavesque, Andrew Mackie, and Sandra Sampertegui who provided samples for this study. We are also grateful to Dr. Torkild Bakken and an anonymous reviewer for comments in previous versions of the manuscript.
Funding
P.R.A. and C.S.G.S. thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for financial support (process: PDSE 88881.188038/2018–01 and EST-SENIOR 99999.001299/2015–08). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior—Brasil (CAPES)—Finance Code 001. This work was funded by USA National Science Foundation grant EAR-0120646 to K.M.H.
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Alves, P.R., Halanych, K.M., Silva, E.P. et al. Nereididae (Annelida) phylogeny based on molecular data. Org Divers Evol 23, 529–541 (2023). https://doi.org/10.1007/s13127-023-00608-9
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DOI: https://doi.org/10.1007/s13127-023-00608-9