Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-10T09:13:19.574Z Has data issue: false hasContentIssue false

The enigmatic bivalve genus Paramya (Myoidea: Myidae): symbiotic association of an East Asian species with spoon worms (Echiura) and its transfer to the family Basterotiidae (Galeommatoidea)

Published online by Cambridge University Press:  20 June 2016

Ryutaro Goto*
Affiliation:
Museum of Zoology and Department of Ecology and Evolutionary Biology, University of Michigan, 1109 Geddes Avenue, Ann Arbor, MI 48109-1079, USA Department of Marine Ecosystem Dynamics, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwa-no-ha, Kashiwa, Chiba 277-8564, Japan
Hiroshi Ishikawa
Affiliation:
965-1 Kawachi-ko, Uwajima, Ehime 798-0075, Japan
Yoichi Hamamura
Affiliation:
14-16 Yakeyama-Hibarigaoka-cho, Kure, Hiroshima 737-0901, Japan
*
Correspondence should be addressed to: R. Goto, Museum of Zoology and Department of Ecology and Evolutionary Biology, University of Michigan, 1109 Geddes Avenue, Ann Arbor, MI 48109-1079, USA email: gotoryutaro@gmail.com

Abstract

Paramya is an enigmatic genus of Myidae (Bivalvia: Heterodonta: Myoidea) that includes three uncommon species: Paramya subovata (Conrad, 1845), Paramya recluzi (A. Adams, 1864) and Paramya africana Cosel, 1995. Paramya subovata is known as a commensal living in the burrow of the spoon worm Thalassema hartmani Fisher, 1947 (Annelida: Echiura: Thalassematidae), in North American coastal waters. However, the biology of the other two species remains unknown. In this study, we found P. recluzi living in the burrows of the two thalassematid echiuran species, Ikedosoma gogoshimense (Ikeda, 1904) and Arhynchite hayaoi Tanaka & Nishikawa, 2013, in intertidal flats in the Seto Inland Sea, Japan. Paramya recluzi was embedded in the burrow wall with its short siphons protruding into the host burrow lumen for respiration and filter feeding. To determine the phylogenetic position of P. recluzi, we performed a molecular phylogenetic analysis using the 18S, 28S, COI and H3 genes. Molecular analysis showed that P. recluzi belongs not to the family Myidae, but to the genus Basterotia (Galeommatoidea: Basterotiidae). Morphological examination of P. recluzi revealed that this species has many similarities with Basterotia (e.g. a single cardinal tooth on each valve and short siphons surrounded by tentacles). Thus, we propose that this species should be transferred from the genus Paramya to Basterotia. In addition, we also suggest that the other two species of Paramya (P. subovata and P. africana) should be transferred to the family Basterotiidae based on their shell morphology, anatomy and ecological characteristics.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abbott, R.T. (1974) American seashells: the marine mollusks of the Atlantic and Pacific Coasts of North America, 2nd edition. New York, NY: Van Nostrand Reinhold Company.Google Scholar
Adams, A. (1864) On some new genera and species of Mollusca from the sea of China and Japan. Annals and Magazine of Natural History, 3rd Series 13, 307310.CrossRefGoogle Scholar
Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403410.CrossRefGoogle ScholarPubMed
Anker, A., Murina, G.V., Lira, C., Vera Caripe, J.A., Palmer, A.R. and Jeng, M.S. (2005) Macrofauna associated with echiuran burrows: a review with new observations of the innkeeper worm, Ochetostoma erythrogrammon Leuckart and Rüppel, in Venezuela. Zoological Studies 44, 157190.Google Scholar
Campbell, L.D. (1993) Pliocene molluscs from the Yorktown and Chowan River formations in Virginia. Virginia Division of Natural Resources, Publication 127. Charlottesville, VA: Department of Mines, Minerals, and Energy, Division of Mineral Resources, 259 pp.Google Scholar
Coan, E.V. (1999a) The Eastern Pacific Sportellidae (Bivalvia). The Veliger 42, 131151.Google Scholar
Coan, E.V. (1999b) The eastern Pacfic species of Sphenia (Bivalvia: Myidae). The Nautilus 113, 103120.Google Scholar
Colgan, D.J., Mclauchlan, A., Wilson, G.D.F., Livingston, S., Macaranas, J., Edgecombe, G.D., Cassis, G. and Gray, M.R. (1998) Molecular phylogenetics of the Arthropoda: relationships based on histone H3 and U2 snRNA DNA sequences. Australian Journal of Zoology 46, 419437.CrossRefGoogle Scholar
Colgan, D.J., Ponder, W.F., Beacham, E. and Macaranas, J.M. (2003) Gastropod phylogeny based on six segments from four genes representing coding or non-coding and mitochondrial or nuclear DNA. Molluscan Research 23, 123148.CrossRefGoogle Scholar
Cosel, R.V. (1995) Fifty-one new species of marine bivalves from tropical West Africa. Iberus 13, 1115.Google Scholar
Dayrat, B., Tillier, A., Lecointre, G. and Tillier, S. (2001) New clades of euthyneuran gastropods (Mollusca) from 28S rRNA sequences. Molecular Phylogenetics and Evolution 19, 225235.CrossRefGoogle ScholarPubMed
Deshayes, G.P. (1860) Description des animaux sans vertèbres découverts dans le bassin de Paris, Volume 1, Paris: Baillières.Google Scholar
Edgar, R.C. (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 17921797.CrossRefGoogle ScholarPubMed
Folmer, O., Black, M., Hoeh, W., Lutz, R.A. 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, 294299.Google ScholarPubMed
Fox, T.H. (1979) Reproductive adaptations and life histories of the commensal leptonacean bivalves. Ph.D dissertation, University of North Carolina, Chapel Hill. 207 pp.Google Scholar
Galtier, N., Gouy, M. and Gautiel, C. (1996) SEAVIEW and PHYLOWIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in Biosciences 12, 543548.Google ScholarPubMed
Gofas, S. (2015) Basterotiidae. In MolluscaBase. Accessed through World Register of Marine Species. Available at http://www.marinespecies.org/aphia.php?p=taxdetails&id=489090.Google Scholar
Goto, R. (2016) A comprehensive molecular phylogeny of spoon worms (Echiura, Annelida): Implications for morphological evolution, the origin of dwarf males, and habitat shifts. Molecular Phylogenetics and Evolution 99, 247260.CrossRefGoogle ScholarPubMed
Goto, R., Hamamura, Y. and Kato, M. (2011) Morphological and ecological adaptation of Basterotia bivalves (Galeommatoidea: Sportellidae) to symbiotic association with burrowing echiuran worms. Zoological Science 28, 225234.CrossRefGoogle ScholarPubMed
Goto, R., Ishikawa, H., Hamamura, Y., Sato, S. and Kato, M. (2014) Evolution of symbiosis with Lingula (Brachiopoda) in the bivalve superfamily Galeommatoidea (Heterodonta), with description of a new species of Koreamya . Journal of Molluscan Studies 80, 148160.CrossRefGoogle Scholar
Goto, R. and Kato, M. (2012) Geographic mosaic of mutually exclusive dominance of obligate commensals in symbiotic communities associated with a burrowing echiuran worm. Marine Biology 159, 319330.CrossRefGoogle Scholar
Goto, R., Kawakita, A., Ishikawa, H., Hamamura, Y. and Kato, M. (2012) Molecular phylogeny of the bivalve superfamily Galeommatoidea (Heterodonta, Veneroida) reveals dynamic evolution of symbiotic life style and interphylum host switching. BMC Evolutionary Biology 12, 172.CrossRefGoogle Scholar
Goto, R., Okamoto, T., Ishikawa, H., Hamamura, Y. and Kato, M. (2013) Molecular phylogeny of echiuran worms (Phylum: Annelida) reveals evolutionary pattern of feeding mode and sexual dimorphism. PLoS ONE 8, e56809.CrossRefGoogle ScholarPubMed
Gouy, M., Guindon, S. and Gascuel, O. (2010) Seaview version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221224.CrossRefGoogle ScholarPubMed
Habe, T. (1977) Systematics of Mollusca in Japan. Bivalvia and Scaphopoda. Tokyo: Hokuryukan (In Japanese).Google Scholar
Henry, C.A. (1976) The commensal clam, Paramya subovata (Bivalvia: Myidae) and Thalassema hartmani (Echiuroidea) off Galveston. Texas. The Nautilus 90, 7374.Google Scholar
Hillis, D.M. and Dixon, M.T. (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66, 411453.CrossRefGoogle ScholarPubMed
Hörnes, M. (1859) Charaktere eines neuen Bivalven-Geschlechtes. Verhandlungen der Kaiserlich-Königlichen Zoologisch–Botanischen Gesellschaft in Wien 9, 7273.Google Scholar
Hoso, M., Kameda, Y., Wu, S.P., Asami, T., Kato, M. and Hori, M. (2010) A speciation gene for left-right reversal in snails results in anti-predator adaptation. Nature Communications 1, 133.CrossRefGoogle ScholarPubMed
Huber, M. (2010) Compendium of bivalves. Hackenheim: Conch Books.Google Scholar
Itani, G. and Kato, M. (2002) Cryptomya (Venatomya) truncata (Bivalvia: Myidae): association with thlassinidean shrimp burrows and morphometric variation in Japanese waters. Venus 61, 193202.Google Scholar
Jenner, C.E. and McCary, A.B. (1969) Paramya subovata, a commensal with the echiuroid Thalassema hartmani . American Malacological Union Annual Report 1969, 4243.Google Scholar
Jobb, G. (2007) TREEFINDER. Available at http://www.treefinder.de.Google Scholar
Jobb, G., Haeseler, A. and Strimmer, K. (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evolutionary Biology 4, 18.CrossRefGoogle ScholarPubMed
Lawly, E.V. (1978) Cryptomya californica (Conrad, 1837): observations on its habitat, behavior, anatomy, and physiology. The Veliger 30, 4654.Google Scholar
Li, J., Ó Foighil, D. and Middelfart, P. (2012) The evolutionary ecology of biotic association in a megadiverse bivalve superfamily: sponsorship required for permanent residency in sediment. PLoS ONE 7, e42121.Google Scholar
MacGinitie, G.E. (1934) The natural history of Callianassa californiensis Dana. American Midland Naturalist 15, 166177.CrossRefGoogle Scholar
Nara, M., Akiyama, H. and Itani, G. (2008) Macrosymbiotic association of the myid bivalve Cryptomya with thalassinidean shrimps: Examples from modern and Pleistocene tidal flats of Japan. PALeO 261, 100104.Google Scholar
Nickell, L.A., Atkinson, R.J.A., Hughes, D.J., Ansell, A.D. and Smith, C.J. (1995) Burrow morphology of the echiuran worm Maxmuelleria lankesteri (Echiura: Bonelliidae), and a brief review of burrow structure and related ecology of the Echiura. Journal of Natural History 29, 871885.CrossRefGoogle Scholar
Oliver, P.G. (2013) Description of Atopomya dolobrata gen. et sp. nov.; first record of bacterial symbiosis in the Saxicavellinae (Bivalvia). Journal of Conchology 41, 359367.Google Scholar
Oliver, P.G., Holmes, A.M., Kileen, I.J., Light, J.M. and Wood, H. (2004) Annotated checklist of the marine Bivalvia of Rodrigues. Journal of Natural History 38, 32293272.CrossRefGoogle Scholar
Prashad, B. (1932) The Lamellibranchia of the Siboga expedition: Systematic part. II. Pelecypoda (exclusive of the Pectinidae), Volume 53. Leiden: Brill.Google Scholar
Ronquist, F. and Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.CrossRefGoogle ScholarPubMed
Saunders, G.W. and Kraft, G.T. (1994) Small-subunit rRNA gene sequences from representatives of selected families of the Gigartinales and Rhodymeniales (Rhodophyta). 1. Evidence for the Plocamiales ord. nov. Canadian Journal of Botany 72, 12501263.CrossRefGoogle Scholar
Scott, P.H. (1994) A new species of Saxicavella (Bivalvia: Hiatellidae) from California with unique brood protection. The Veliger 37, 6268.Google Scholar
Tanabe, A.S. (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Molecular Ecology Resources 11, 914921.CrossRefGoogle ScholarPubMed
Tanaka, M., Kon, T. and Nishikawa, T. (2014) Unraveling a 70-year-old taxonomic puzzle: redefining the genus Ikedosoma (Annelida: Echiura) on the basis of morphological and molecular analyses. Zoological Science 31, 849861.CrossRefGoogle ScholarPubMed
Tanaka, M. and Nishikawa, T. (2013) A new species of the genus Arhynchite (Annelida, Echiura) from sandy flats of Japan, previously referred as Thalassema owstoni Ikeda, 1904. ZooKeys 312, 1321.CrossRefGoogle Scholar
Tsubaki, R., Kameda, Y. and Kato, M. (2010) Pattern and process of diversification in an ecologically diverse epifaunal bivalve group Pterioidea (Pteriomorphia, Bivalvia). Molecular Phylogenetics and Evolution 58, 97104.CrossRefGoogle Scholar
Vonnemann, V., Schrödl, M., Klussmann-Kolb, A. and Wägele, H. (2005) Reconstruction of the phylogeny of the Opisthobranchia (Mollusca: Gastropoda) by means of 18S and 28S rRNA gene sequences. Journal of Molluscan Studies 71, 113125.CrossRefGoogle Scholar
Wollscheid, E. and Wägele, H. (1999) Initial results on the molecular phylogeny of the Nudibranchia (Gastropoda, Opisthobranchia) based on 18S rDNA data. Molecular Phylogenetics and Evolution 13, 215226.CrossRefGoogle ScholarPubMed
Zhang, J.-L., Xu, F.-S., Liu, R.-Y. (Liu, J.Y.) (2012) The Myidae (Mollusca, Bivalvia) from Chinese waters with description of a new species. Zootaxa 3383, 3960.CrossRefGoogle Scholar