Integrative taxonomic methods reveal an incorrect synonymisation of the South African Pseudonereis podocirra (Schmarda) as the widespread Pseudonereis variegata (Grube) from Chile
Jyothi Kara
A , Angus H. H. Macdonald B and Carol A. Simon A C
+ Author Affiliations
- Author Affiliations
A Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland Stellenbosch, 7602, South Africa.
B School of Life Sciences, University of KwaZulu-Natal, Private Bag X54001, Durban, 4000, South Africa.
C Corresponding author. Email: csimon@sun.ac.za
Invertebrate Systematics 32(6) 1282-1297 https://doi.org/10.1071/IS18016
Submitted: 26 February 2018 Accepted: 12 June 2018 Published: 29 November 2018
Abstract
The nereidid Pseudonereis variegata (Grube, 1866) described from Chile includes 14 synonymised species from 10 type localities with a discontinuous distribution, but no taxonomic or molecular studies have investigated the status of this species outside Chile. Two synonymised species, Mastigonereis podocirra Schmarda, 1861 and Nereis (Nereilepas) stimpsonis Grube, 1866, were described from South Africa and investigated here using morphological examination. MtCOI species delimitation analyses and morphology were used to determine the status of P. variegata in South Africa. Morphological examination revealed that museum and freshly collected specimens from South Africa that conform to the general description of P. variegata are similar to M. podocirra and N. stimpsonis with respect to the consistent absence of homogomph spinigers in the inferior neuropodial fascicle, expanded notopodial ligules and the subterminal attachment of dorsal cirri in posterior parapodia. The synonymy of M. podocirra and N. stimpsonis as P. variegata are rejected and P. podocirra, comb. nov. is reinstated. Morphologically, Pseudonereis podocirra differed from specimens from Chile with regard to the numbers of paragnaths, the absence of homogomph spinigers and changes in parapodial morphology along the body. Independence of these species was further supported by genetic distances, automatic barcode gap discovery and multi-rate Poisson tree process species delimitation analyses of 77 mtCOI sequences. Haplotype network revealed no genetic structuring within the South African populations.
http://zoobank.org/urn:lsid:zoobank.org:pub:F0B1A5AF-9CE9-4A43-ACCF-17117E1C2F21
References
Arias, A., Richter, A., Anadón, N., and Glasby, C. J. (2013). Revealing polychaetes invasion patterns: identification, reproduction and potential risks of the Korean ragworm, Perinereis linea (Treadwell), in the western Mediterranean. Estuarine, Coastal and Shelf Science 131, 117–128.| Revealing polychaetes invasion patterns: identification, reproduction and potential risks of the Korean ragworm, Perinereis linea (Treadwell), in the western Mediterranean.Crossref | GoogleScholarGoogle Scholar |
Augener, H. (1934). Polychaeten aus den Zoologischen Museen von Leiden und Amsterdam. – IV. (Schluss). Zoölogische Mededeelingen 17, 67–167.
Bakken, T. (2007). Revision of Pseudonereis (Polychaeta, Nereididae). Zoological Journal of the Linnean Society 150, 145–176.
| Revision of Pseudonereis (Polychaeta, Nereididae).Crossref | GoogleScholarGoogle Scholar |
Bakken, T., Glasby, C. J., and Wilson, R. S. (2009). A review of paragnath morphology in Nereididae (Polychaeta). Zoosymposia 2, 305–316.
Brett, C. D. (2006). ‘Testing the Effectiveness of the mtDNA Cytochrome c Oxidase Subunit 1 (COI) Gene Locus for Identifying Species of Polychaete Worm (Polychaeta : Annelida) in New Zealand.’ (The University of Waikato: Hamilton, New Zealand.)
Carlton, J. T. (2009). Deep invasion ecology and the assembly of communities in historical time. In ‘Biological Invasions in Marine Ecosystems: Ecological, Management, and Geographic Perspectives’. (Eds G. Rilov and J. A. Crooks.) pp. 13–56. (Springer Berlin Heidelberg: Berlin, Heidelberg, Germany.)
Carr, C. M., Hardy, S. M., Brown, T. M., Macdonald, T. A., and Hebert, P. D. N. (2011). A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PLoS One 6, .
| A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes.Crossref | GoogleScholarGoogle Scholar |
Chen, C. A., Chen, C.-P., Fan, T.-Y., Yu, J.-K., and Hsieh, H.-L. (2002). Nucleotide sequences of ribosomal internal transcribed spacers and their utility in distinguishing closely related Perinereis Polychaets (Annelida; Polychaeta; Nereididae). Marine Biotechnology 4, 0017–0029.
| Nucleotide sequences of ribosomal internal transcribed spacers and their utility in distinguishing closely related Perinereis Polychaets (Annelida; Polychaeta; Nereididae).Crossref | GoogleScholarGoogle Scholar |
Day, J. H. (1967). ‘A Monograph on the Polychaeta of Southern Africa.’ (The British Museum of Natural History: London.)
de Jong, M. A., Wahlberg, N., van Eijk, M., Brakefield, P. M., and Zwaan, B. J. (2011). Mitochondrial DNA signature for range-wide populations of Bicyclus anynana suggests a rapid expansion from recent refugia. PLoS One 6, e21385–5.
| Mitochondrial DNA signature for range-wide populations of Bicyclus anynana suggests a rapid expansion from recent refugia.Crossref | GoogleScholarGoogle Scholar |
Ehlers, E. (1901). Die Polychaeten des magellanischen und chilenischen Strandes. Ein faunistischer Versuch. Festschrift zur Feier des Hundertfünfzigjährigen Bestehens des Königlichen Gesellschaft der Wissenschaften zu Göttingen, Abhandlungen der Mathematisch-Physikalischen. Available at: http://www.annelida.net/docs/Ehlers1901_PolychaetenMagellanischenChilenischenStrandes.pdf [verified 29 January 2016].
Ehlers, E. (1920). Polychaeten von Java und Amboina. Ein Beitrag zur Kenntnis der malaiischen Strandfauna. Abhandlungen der Königlichen Gesellschaft der Wissenschaften zu Göttingen. Mathematisch-Physikalische Klasse 10, 1–73.
Fauvel, P. (1918). Annélides polychètes nouvelles de l’Afrique Orientale. Bulletin du Muséum d’Histoire Naturelle, Paris 24, 503–509.
Fauvel, P. (1921). Annélides polychètes de Madagascar, du Muséum R. d’Histoire Naturelle recueillies par M. le Dr. W. Kaudern en 1912. Arkiv för Zoologi. Available at: http://www.biodiversitylibrary.org/item/30139#page/597/mode/1up [verified 31 July 2018].
Fernández, R., Lemer, S., Mcintyre, E., and Giribet, G. (2015). Comparative phylogeography and population genetic structure of three widespread mollusc species in the Mediterranean and near Atlantic. Marine Ecology (Berlin) 36, 701–715.
| Comparative phylogeography and population genetic structure of three widespread mollusc species in the Mediterranean and near Atlantic.Crossref | GoogleScholarGoogle Scholar |
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates.Crossref | GoogleScholarGoogle Scholar |
Glasby, C. J., Wilson, R. S., and Bakken, T. (2011). Redescription of the Indo-Pacific polychaete Neanthes pachychaeta (Fauvel, 1918) n. comb. (Annelida, Phyllodocida, Nereididae) and its synonyms. Zoosystema 33, 361–375.
| Redescription of the Indo-Pacific polychaete Neanthes pachychaeta (Fauvel, 1918) n. comb. (Annelida, Phyllodocida, Nereididae) and its synonyms.Crossref | GoogleScholarGoogle Scholar |
Glasby, J. C., Wei, N. V., and Gibb, K. S. (2013). Cryptic species of Nereididae (Annelida : Polychaeta) on Australian coral reefs. Invertebrate Systematics 27, 245–264.
| Cryptic species of Nereididae (Annelida : Polychaeta) on Australian coral reefs.Crossref | GoogleScholarGoogle Scholar |
Grube, A. (1857). ‘Annulata Örstediana. Enumeratio Annulatorum, quac in itinere per Indiam occidentalem et Americam centralem annis 1845–1848 suscepto legit cl. A. S. Örsted, adjectis speciebus nonnullis a cl. H. Kröyero in itinere ad Americam meridionalem collection.’ Vidensk Meddr Dansk Naturh Foren, 158–166.
Grube, A. (1866). ‘Beschreibungen neuer von der Novara-Expedition mitgebrachter Anneliden und einer neuen Landplanarie. Verhandlungen der kaiserlich-königlichen zoologisch-botanischen Gesellschaft in Wien.’
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
| New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar |
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
Hamdy, R., Dorgham, M. M., El-Rashid, H. H., and Atta, M. M. (2014). Biometry and reproductive biology of Pseudonereis anomala Gravier 1901 (Polychaeta: Nereididae) on the Alexandria coast, Egypt. Oceanologia 56, 41–58.
| Biometry and reproductive biology of Pseudonereis anomala Gravier 1901 (Polychaeta: Nereididae) on the Alexandria coast, Egypt.Crossref | GoogleScholarGoogle Scholar |
Hart, M. W., and Marko, P. B. (2010). It’s about time: divergence, demography, and the evolution of developmental modes in marine invertebrates. Integrative and Comparative Biology 50, 643–661.
| It’s about time: divergence, demography, and the evolution of developmental modes in marine invertebrates.Crossref | GoogleScholarGoogle Scholar |
Hartman, O. (1959). Catalogue of the polychaetous annelids of the world. Parts 1 and 2. Allan Hancock Foundation Occasional Paper 23, 1–628.
Hebert, P. D. N., Ratnasingham, S., and Waard, J. (2003). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings. Biological Sciences 270, S96–S99.
| Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species.Crossref | GoogleScholarGoogle Scholar |
Hutchings, P., and Kupriyanova, E. (2018). Cosmopolitan polychaetes – fact or fiction? Personal and historical perspectives. Invertebrate Systematics 32, 1–9.
| Cosmopolitan polychaetes – fact or fiction? Personal and historical perspectives.Crossref | GoogleScholarGoogle Scholar |
Iannotta, M. A., Patti, F. P., Ambrosino, M., Procaccini, G., and Gambi, M. C. (2007). Phylogeography of two species of Lysidice (Polychaeta, Eunicidae) associated to the seagrass Posidonia oceanica in the Mediterranean Sea. Marine Biology 150, 1115–1126.
| Phylogeography of two species of Lysidice (Polychaeta, Eunicidae) associated to the seagrass Posidonia oceanica in the Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar |
Kinberg, J. G. H. (1865). Annulata nova. [Continuatio.]. Öfversigt af Königlich Vetenskapsakademiens Förhandlingar, Stockholm 22, 167–179.
Knowlton, N. (1993). Sibling species in the sea. Annual Review of Ecology and Systematics 24, 189–216.
| Sibling species in the sea.Crossref | GoogleScholarGoogle Scholar |
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar |
Kvist, S. (2014). Does a global DNA barcoding gap exist in Annelida? Mitochondrial DNA 27, 1–12.
| Does a global DNA barcoding gap exist in Annelida?Crossref | GoogleScholarGoogle Scholar |
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., and Calcott, B. (2017). Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
| Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |
Leigh, J. W., and Bryant, D. (2015). POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.
| POPART: full-feature software for haplotype network construction.Crossref | GoogleScholarGoogle Scholar |
Leliaert, F., Verbruggen, H., Vanormelingen, P., Steen, F., López-Bautista, J. M., Zuccarello, G. C., and De Clerck, O. (2014). DNA-based species delimitation in algae. European Journal of Phycology 49, 179–196.
| DNA-based species delimitation in algae.Crossref | GoogleScholarGoogle Scholar |
Librado, P., and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.
| DnaSP v5: a software for comprehensive analysis of DNA polymorphism data.Crossref | GoogleScholarGoogle Scholar |
Linnaeus, C. (1758). ‘Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio decima, reformata.’ (Holmiae: Impensis Direct. Laurentii Salvii 1758–1759)
Maggs, C. A., Castilho, R., Foltz, D., Henzler, C., Taimour, M., Olsen, J., Perez, K. E., Stam, W., Risto, V., and Wares, J. (2008). Evaluating signatures of glacial refugia for north Atlantic benthic marine taxa. Ecology 89, S108–122.
Malmgren, A. J. (1867). Annulata Polychaeta Spetsbergiae, Groelanlandiae, Islandiae et Scandinaviae hactenus cognita. Cum xiv. tabulis.
Marko, P. B., and Hart, M. W. (2011). The complex analytical landscape of gene flow inference. Trends in Ecology & Evolution 26, 448–456.
| The complex analytical landscape of gene flow inference.Crossref | GoogleScholarGoogle Scholar |
Muths, D., Jollivet, D., Gentil, F., and Davoult, D. (2009). Large-scale genetic patchiness among NE Atlantic populations of the brittle star Ophiothrix fragilis. Aquatic Biology 5, 117–132.
| Large-scale genetic patchiness among NE Atlantic populations of the brittle star Ophiothrix fragilis.Crossref | GoogleScholarGoogle Scholar |
Pons, J., Barraclough, T. G., Gomez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., Kamoun, S., Sumlin, W. D., and Vogler, A. P. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.
| Sequence-based species delimitation for the DNA taxonomy of undescribed insects.Crossref | GoogleScholarGoogle Scholar |
Rambaut, A., and Drummond, A. J. (2013). Tracer v1.6. Available from http://tree.bio.ed.ac.uk/software/tracer/.
Read, G. (2018). Pseudonereis variegata. In ‘World Polychaeta Database’. (Eds G. Read and K. Fauchald.) Available online at: http://www.marinespecies.org/polychaeta/aphia.php?p=taxdetails&id=209792 [verified 17 January 2018].
Read, G., and Fauchald, K. (2018). Nereididae Blainville, 1818. (Ed.) (2018). World Polychaeta database. Available at: http://www.marinespecies.org/polychaeta/aphia.php?p=taxdetails&id=22496 [verified 15 February 2018].
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |
Rozbaczylo, N., and Bolados, J. (1980). Nereidos de Iquique, Chile. (Polychaeta, Nereidae). Boletín del Museo Nacional de Historia Natural 37, 205–224.
Salazar-Vallejo, S. I., Gillet, P., and Surugiu, V. (2017). How false is Nereis falsa (Annelida, Phyllodocida, Nereididae)? Revista de Biología Tropical 65, 847–857.
| How false is Nereis falsa (Annelida, Phyllodocida, Nereididae)?Crossref | GoogleScholarGoogle Scholar |
Sampertegui, S., Rozbaczylo, N., Canales-Aguirre, C. B., Carrasco, F., Hernandez, C. E., and Rodriguez-Serrano, E. (2013). Morphological and molecular characterization of Perinereis gualpensis (Polychaeta: Nereididae) and its phylogenetic relationships with other species of the genus off the Chilean coast, Southeast Pacific. Cahiers de Biologie Marine 54, 27–40.
Schmarda, L. K. (1861). ‘Neue wirbellose thiere beobachtet und gesammelt auf einer reise um die erde 1853 bis 1857. In Turbellarien, Rotatorien und Anneliden’. (W. Engelmann: Leipzig.) Available at: https://www.biodiversitylibrary.org/item/50342 [verified 22 January 2018].
Sikorski, A., and Pavlova, L. (2016). Three new species of Laonice (Polychaete: Spionidae) from west and southwest Africa. Zootaxa 4097, 353–368.
| Three new species of Laonice (Polychaete: Spionidae) from west and southwest Africa.Crossref | GoogleScholarGoogle Scholar |
Simon, C. A., Sato-Okoshi, W., and Abe, H. (2017). Hidden diversity within the cosmopolitan species Pseudopolydora antennata (Claparède, 1869) (Spionidae: Annelida). Marine Biodiversity , .
| Hidden diversity within the cosmopolitan species Pseudopolydora antennata (Claparède, 1869) (Spionidae: Annelida).Crossref | GoogleScholarGoogle Scholar |
Simon, C. A., Williams, L.-G., and Henninger, T. (2018). A new species of Rhynchospio (Annelida: Spionidae) in South Africa. Marine Biodiversity , .
| A new species of Rhynchospio (Annelida: Spionidae) in South Africa.Crossref | GoogleScholarGoogle Scholar |
Stimpson, W. (1856). Description of some new marine invertebrates. Proceedings. Academy of Natural Sciences of Philadelphia 7, 385–394.
Teske, P. R., Papadopoulos, I., Zardi, G. I., McQuaid, C. D., Edkins, M. T., Griffiths, C. L., and Barker, N. P. (2007). Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development. Marine Biology 152, 697–711.
| Implications of life history for genetic structure and migration rates of southern African coastal invertebrates: planktonic, abbreviated and direct development.Crossref | GoogleScholarGoogle Scholar |
Van Herwerden, L. (1989). Collection of mussel worms Pseudonereis variegata for bait – a legislative anachronism. South African Journal of Marine Science 8, 363–366.
| Collection of mussel worms Pseudonereis variegata for bait – a legislative anachronism.Crossref | GoogleScholarGoogle Scholar |
Villalobos-Guerrero, T. F., and Carrera-Parra, L. F. (2015). Redescription of Alitta succinea (Leuckart, 1847) and reinstatement of A. acutifolia (Ehlers, 1901) n. comb. based upon morphological and molecular data (Polychaeta: Nereididae). Zootaxa 3919, 157–178.
| Redescription of Alitta succinea (Leuckart, 1847) and reinstatement of A. acutifolia (Ehlers, 1901) n. comb. based upon morphological and molecular data (Polychaeta: Nereididae).Crossref | GoogleScholarGoogle Scholar |
Wäge, J., Valvassori, G., Hardege, J. D., Schulze, A., and Gambi, M. C. (2017). The sibling polychaetes Platynereis dumerilii and Platynereis massiliensis in the Mediterranean Sea: are phylogeographic patterns related to exposure to ocean acidification? Marine Biology 164, 199.
| The sibling polychaetes Platynereis dumerilii and Platynereis massiliensis in the Mediterranean Sea: are phylogeographic patterns related to exposure to ocean acidification?Crossref | GoogleScholarGoogle Scholar |
Wilson, R. S., and Glasby, C. J. (1993). A revision of the Perinereis nuntia species group (Polychaeta: Nereididae). Records of the Australian Museum 45, 253–277.
| A revision of the Perinereis nuntia species group (Polychaeta: Nereididae).Crossref | GoogleScholarGoogle Scholar |
Zhang, Y., Pham, N. K., Zhang, H., Lin, J., and Lin, Q. (2014). Genetic variations in two seahorse species Hippocampus mohnikei and Hippocampus trimaculatus: evidence for middle pleistocene population expansion. PLoS One 9, 1–10.
| Genetic variations in two seahorse species Hippocampus mohnikei and Hippocampus trimaculatus: evidence for middle pleistocene population expansion.Crossref | GoogleScholarGoogle Scholar |
