Abstract
Pygospio elegans Claparède, 1863, the type species of the genus Pygospio, was originally described from Normandy, France, and later widely reported from boreal waters in the northern hemisphere. Sequence data of four gene fragments (2576 bp in total) of the mitochondrial 16S rDNA, nuclear 18S and 28S rDNA, and Histone 3 have shown that individuals from California and Oregon, USA, Scotland and the White Sea, Russia were genetically similar (the average p-distances for the combined data between the four groups ranged from 0.04 to 0.16%, average p = 0.1%). These individuals are considered to be conspecific and the amphiboreal distribution of P. elegans is here confirmed. Adult morphology of the species is briefly described and illustrated. The molecular analysis revealed two genetically distant populations, Pygospio sp. 1 from the Sea of Okhotsk and Pygospio sp. 2 from Oregon. The morphological differences and high average genetic p-distances for the combined data (ranging from 3.06 to 3.18%, average p = 3.12%) between Pygospio sp. 2 and P. elegans suggest the presence of an undescribed Pygospio species co-occurring with P. elegans in Oregon. High morphological similarity and moderate genetic p-distances for the combined data (ranging from 1 to 1.11%, average p = 1.07%) between Pygospio sp. 1 and P. elegans indicate a comparatively recent genetic divergence of the Pygospio population in the Sea of Okhotsk. Taking into account the high genetic similarity of the remote European and North American populations of P. elegans and medial location of the Pygospio sp. 1 population, we suggest the latter to belong to a separate species. However, this conclusion should be verified in further studies on the morphology, reproductive biology and genetics of this population. The present findings show the need to re-examine Pygospio from the Asian Pacific and elsewhere that have been identified as P. elegans.
References
Anger, V. (1984) Reproduction in Pygospio elegans (Spionidae) in relation to its geographical origin and to environmental conditions: a preliminary report. In: Fischer, A. & Pfannenstiel, H.-D. (Eds.), Polychaete Reproduction: Progress in Comparative Reproductive Biology. Fortschritte der Zoologie, Band 29. Gustav Fischer Verlag, Stuttgart-New York, pp. 45–51.
Annenkova, N.P. (1938) Polychaeta of the North Japan Sea and their horizontal and vertical distribution. In: Reports of the hydrobiological expedition of the Zoological Institute of the Academy of Sciences of the U.S.S.R. in 1934 to the Sea of Japan, 1, pp. 81–230.
Bastrop, R., Jürss, K. & Sturmbauer, C. (1998) Cryptic species in a marine polychaete and their independent introduction from North America to Europe. Molecular Biology and Evolution, 15 (2), 97–103.
Blake, J.A. (1996) Family Spionidae Grube, 1850. Including a review of the genera and species from California and a revision of the genus Polydora Bosc, 1802. In: Blake, J.A., Hilbig, B. & Scott, P.H. (Eds.), Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel. Volume 6. The Annelida Part 3 - Polychaeta: Orbiniidae to Cossuridae. Santa Barbara Museum of Natural History, Santa Barbara, California, pp. 81–223.
Blake, J.A. & Ruff, R.E. (2007) Annelida: Polychaeta. In: Carlton, J.T. (Ed.), The Light & Smith manual: intertidal invertebrates from central California to Oregon. University of California Press, Berkeley, Los Angeles, pp. 309–410.
Blank, M. & Bastrop, R. (2009) Phylogeny of the mud worm genus Marenzelleria (Polychaeta, Spionidae) inferred from mitochondrial DNA sequences. Zoologica Scripta, 38 (3), 313–321.
http://dx.doi.org/10.1111/j.1463-6409.2008.00370.x
Buzhinskaja, G.N. (1985) Polychaeta of the shelf off south Sakhalin and their ecology. Explorations of the Fauna of Seas, 30 (38), 72–224. [in Russian with English Summary].
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17 (4), 540–552.
Claparède, E. (1863) Beobachtungen über Anatomie und Entwicklungsgeschichte wirbelloser Thiere an der Küste von Normandie Angestellt. Wilhelm Engelmann, Leipzig, vii + 120 pp.
Colgan, D.J., Hutchings, P.A. & Braune, M. (2006) A multigene framework for polychaete phylogenetic studies. Organisms, Diversity and Evolution, 6 (3), 220–235.
Dahlgren, T.G., Åkesson, B., Schander, C., Halanych, K.M. & Sundberg, P. (2001) Molecular phylogeny of the model annelid Ophryotrocha. Biological Bulletin, 201 (2), 193–203.
Day, J.H. (1967) A monograph on the Polychaeta of Southern Africa. Part 2. Sedentaria. The British Museum (Natural History), London, xvii + 420 pp. [pp. i–xvii, 459–878 ]
Di Domenico, M., Martínez, A., Lana, P. & Worsaae, K. (2014) Molecular and morphological phylogeny of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat preferences. Molecular Phylogenetics and Evolution, 75, 202–218.
http://dx.doi.org/10.1016/j.ympev.2014.02.003
Ditlevsen, H. (1929) Polychæta. Zoology of the Faroes, 16, 1–83.
Fauvel, P. (1927) Polychètes sédentaires. Addenda aux Errantes, Archiannélides, Myzostomaires. Faune de France, 16, 1–494.
Foster, N.M. (1971) Spionidae (Polychaeta) of the Gulf of Mexico and the Caribbean Sea. Studies on the fauna of Curaçao and other Caribbean Islands, 36 (129), 1–183.
Gibson, G.D. & Harvey, J.M.L. (2000) Morphogenesis during asexual reproduction in Pygospio elegans Claparede (Annelida, Polychaeta). Biological Bulletin, Marine Biological Laboratory, Woods Hole, Mass, 199 (1), 41–49.
Hannerz, L. (1956) Larval development of the polychaete families Spionidae Sars, Disomidae Mesnil, and Poecilochaetidae n. fam. in the Gullmar Fjord (Sweden). Zoologiska bidrag från Uppsala, 31, 1–204.
Hartmann-Schröder, G. (1971) Annelida, Borstenwürmer, Polychaeta. Die Tierwelt Deutschlands und der angrenzenden Meeresteile nach ihren Merkmalen und nach ihrer Lebensweise, 58, 1–594.
Hartmann-Schröder, G. (1974) Zur Kenntnis des Eulitorals der afrikanischen Westküste zwischen Angola und Kap der Guten Hoffnung und der afrikaischen Ostküste von Südafrika und Mocambique unter besonderer Berücksichtigung der Polychaeten und Ostracoden. Teil II. Die Polychaeten des Untersuchungsgebietes. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 69, 95–228.
Hartmann-Schröder, G. (1996) Annelida, Borstenwürmer, Polychaeta. Die Tierwelt Deutschlands und der angrenzenden Meeresteile nach ihren Merkmalen und nach ihrer Lebensweise, 58 (2, neuebearb. Aufl.), 1–645.
Hobson, K.D. & Banse, K. (1981) Sedentariate and archiannelid polychaetes of British Columbia and Washington. Canadian Bulletin of Fisheries and Aquatic Sciences, 209, 1–144.
Hobson, K.D. & Green, R.H. (1968) Asexual and sexual reproduction of Pygospio elegans (Polychaeta) in Barnstable Harbor, Massachusetts. Biological Bulletin, Marine Biological Laboratory, Woods Hole, Mass, 135 (2), 410.
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17 (8), 754–755.
http://dx.doi.org/10.1093/bioinformatics/17.8.754
Hutchings, P. & Rainer, S. (1980) A key to estuarine polychaetes in New South Wales. Proceedings of the Linnean Society of New South Wales, 104 (1), 35–48.
Kesäniemi, J.E., Rawson, P.D., Lindsay, S.M. & Knott, K.E. (2012) Phylogenetic analysis of cryptic speciation in the polychaete Pygospio elegans. Ecology and Evolution, 2 (5), 994–1007.
Kiseleva, M.I. (2004) Polychaetes (Polychaeta) of the Azov and Black Seas. KSC RAS, Apatity, 409 pp. [in Russian].
Lee, J.-H. (1987) The ecological study of benthic polychaetes in the Yellow Sea. BSPE 00097-127-3, Seoul, 153 pp. [in Korean with English Summary].
Light, W.J. (1978) Spionidae (Polychaeta, Annelida). Pacific Grove, California, The Boxwood Press, 211 pp.
McIntosh, W.C. (1909) Notes from the Gatty Marine Laboratory, St. Andrews. No. 31. 1. On a young stage of Gadus luscus with bold transverse bars of pigment. 2. On the British Spionidae. 3. On the Spionidae dredged by H.M.S. 'Porcupine' in 1869 and 1870. The Annals and Magazine of Natural History, Series 8, 3 (14), 153–180.
Mesnil, F. (1896) Études de morphologie externe chez les Annélides. I. Les Spionidiens des côtes de la Manche. Bulletin scientifique de la France et de la Belgique, 29, 110–287.
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010. IEEE, New Orleans, LA, pp. 1–8.
Morgan, T.S., Rogers, A.D., Paterson, G.L.J., Hawkins, L.E. & Sheader, M. (1999) Evidence for poecilogony in Pygospio elegans (Polychaeta: Spionidae). Marine Ecology Progress Series, 178, 121–132.
Nygren, A. & Sundberg, P. (2003) Phylogeny and evolution of reproductive modes in Autolytinae (Syllidae, Annelida). Molecular Phylogenetics and Evolution, 29, 235–249.
http://dx.doi.org/10.1016/S1055-7903(03)00095-2
Oyarzun, F.X., Mahon, A.R., Swalla, B.J. & Halanych, K.M. (2011) Phylogeography and reproductive variation of the poecilogonous polychaete Boccardia proboscidea (Annelida: Spionidae) along the West Coast of North America. Evolution & Development, 13 (6), 489–503.
http://dx.doi.org/10.1111/j.1525-142X.2011.00506.x
Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14 (9), 817–818.
Radashevsky, V.I. (2012) Spionidae (Annelida) from shallow waters around the British Islands: an identification guide for the NMBAQC Scheme with an overview of spionid morphology and biology. Zootaxa, 3152, 1–35.
Radashevsky, V.I., Neretina, T.V., Pankova, V.V., Tzetlin, A.B. & Choi, J.-W. (2014) Molecular identity, morphology and taxonomy of the Rhynchospio glutaea complex with a key to Rhynchospio species (Annelida, Spionidae). Systematics and Biodiversity, 12 (4), 424–433.
http://dx.doi.org/10.1080/14772000.2014.941039
Rasmussen, E. (1973) Systematics and ecology of the Isefjord marine fauna (Denmark). Ophelia, 11 (1-2), 1–495.
http://dx.doi.org/10.1080/00785326.1973.10430115
Rioja, E. (1931) Estudio de los poliquetos de la Península Iberica. Memorias de la Academia de Ciencias Exactas, Físicas y Naturales de Madrid, 2, 1–471.
Ronquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574.
http://dx.doi.org/10.1093/bioinformatics/btg180
Rousset, V., Pleijel, F., Rouse, G.W., Erséus, C. & Siddall, M.E. (2007) A molecular phylogeny of annelids. Cladistics, 23 (1), 41–63.
http://dx.doi.org/10.1111/j.1096-0031.2006.00128.x
Rullier, F. (1963) Les Annélides Polychètes du Bosphore, de la Mer de Marmara et de la Mer Noire, en relation avec celles de la Méditerranée. Rapports et Procès-Verbaux des Réunions Commission Internationale pour l'Exploration Scientifique de la Mer Mediterranée, Monaco, 17 (2), 161–260.
Sikorski, A.V. (2001) Spionidae Grube, 1850. In: Zhirkov, I.A. (Ed.), Polychaeta of the Arctic Ocean. Yanus-K, Moscow, pp. 271–332.
Söderström, A. (1920) Studien über die Polychätenfamilie Spionidae. Inaugural-Dissertation. Almquist & Wicksells, Uppsala, 286 pp.
Sun, D.Y. (1994) Annelida: Polychaeta. In: Zong-guo, H. (Ed.), Marine species and their distributions in China's seas. China Ocean Press, Beijing, pp. 343–377.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28 (10), 2731–2739.
http://dx.doi.org/10.1093/molbev/msr121
Thorson, G. (1946) Reproduction and larval development of Danish marine bottom invertebrates, with special reference to the planktonic larvae in the Sound (Øresund). Meddelelser fra Kommissionen for Danmarks Fiskeri- og Havundersøgelser, Serie Plankton, 4 (1), 1–523.
Uschakov, P.V. (1955) Polychaeta of the Far Eastern Seas of the USSR. Keys to the fauna of the USSR, 56, 1–445. [in Russian]
Wesenberg-Lund, E. (1950) The Polychæta of West Greenland, with special reference to the fauna of Nordre Strømfjord, Kvane- and Bredefjord. Meddelelser om Grønland, 151 (2), 1–171.
Wu, B.L., Sun, R.P. & Chen, M. (1980) Zoogeographical studies on Polychaeta from the Xisha Islands and its adjacent waters. Acta Oceanologica Sinica, 2 (1), 111–130. [in Chinese with English Summary]
Xia, X. & Lemey, P. (2009) Assessing substitution saturation with DAMBE In: Lemey, P., Salemi, M. & Vandamme, A.-M. (Eds.), The Phylogenetic Handbook: a Practical Approach to Phylogenetic Analysis and Hypothesis Testing. Cambridge University Press, Cambridge, pp. 611–626.
Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26 (1), 1–7.
http://dx.doi.org/10.1016/s1055-7903(02)00326-3