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Article
Published: 2016-11-23

New molecular phylogeny of Lucinidae: increased taxon base with focus on tropical Western Atlantic species (Mollusca: Bivalvia)

Department of Life Sciences, The Natural History Museum, London SW7 5BD, United Kingdom.
Department of Life Sciences, The Natural History Museum, London SW7 5BD, United Kingdom.
Department of Life Sciences, The Natural History Museum, London SW7 5BD, United Kingdom.
Department of Life Sciences, The Natural History Museum, London SW7 5BD, United Kingdom.
Department of Life Sciences, The Natural History Museum, London SW7 5BD, United Kingdom.
Mollusca Caribbean classification cryptic species chemosymbiosis

Abstract

A new molecular phylogeny of the Lucinidae using 18S and 28S rRNA and cytochrome b genes includes many species from the tropical Western Atlantic as well as additional taxa from the Indo-West Pacific. This study provides a phylogenetic framework for a new taxonomy of tropical Western Atlantic lucinids. The analysis confirmed five major clades—Pegophyseminae, Leucosphaerinae, Myrteinae, Codakiinae and Lucininae, with Monitilorinae and Fimbriinae represented by single species. The Leucosphaerinae are expanded and include Callucina winckworthi and the W. Atlantic Myrtina pristiphora that groups with several Indo-West Pacific Myrtina species. Within the Codakiinae two abundant species of Ctena from the Western Atlantic with similar shells are discriminated as C. orbiculata and C. imbricatula, while in the Indo-West Pacific Ctena bella is a probable species complex. The Lucininae is the most species rich and disparate subfamily with several subclades apparent. Three species of Lucina are recognized in the W. Atlantic L. aurantia, L. pensylvanica and L. roquesana. Pleurolucina groups near to Cavilinga and Lucina, while Lucinisca muricata is more closely related to the E. Pacific L. fenestrata than to the Atlantic L. nassula. A new species of Parvilucina is identified from molecular analyses having been confounded with Parvilucina pectinata but differs in ligament structure. Also, the former Parvilucina clenchi is more distant and assigned to Guyanella.

 

References

  1. Abbott, R.T. (1974) American Seashells. 2nd Ed. Van Nostrand-Reinhold, New York, 663 pp.

    Adams, C.B. (1845) Specierum novarum conchyliorum, in Jamaica reportorum, synopsis. Proceedings of the Boston Society of Natural History, 2, 1–17.

    Altena, C.O. van (1968) The Holocene and Recent marine bivalve Mollusca of Surinam. Studies on the Fauna of Suriname and other Guyanas, 42 (10), 153–179.

    Bieler, R., Mikkelsen, P.M., Collins, T.M., Glover, E.A., González, V.L., Graf, D.L., Harper, E.M., Healy, J., Kawauchi, G.Y., Sharma, P.P., Staubach, S., Strong, E.E., Taylor, J.D., Temkin, T., Zardus, J.D., Clark, S., Guzmán, A., McIntyre, E., Sharp, P. & Giribet, G. (2014) Investigating the Bivalve Tree of Life—an exemplar-based approach combining molecular and novel morphological characters. Invertebrate Systematics, 28, 32–115.

    http://dx.doi.org/10.1071/is13010

    Bretsky, S.S. (1976) Evolution and classification of the Lucinidae (Mollusca; Bivalvia). Palaeontographica Americana, 8 (50), 219–337.

    Britton, J.C. (1972) Two new species and a new subgenus of Lucinidae (Mollusca: Bivalvia), with notes on certain aspects of lucinid phylogeny. Smithsonian Contributions to Zoology, 129, 1–19.

    http://dx.doi.org/10.5479/si.00810282.129

    Castresana J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17, 540–552.
    http://dx.doi.org/10.1093/oxfordjournals.molbev.a026334

    Chavan, A. (1937) Essai critique de classification des lucines. Journal de Conchyliologie, 81 (2), 133–153; 81 (3), 193–216; 81 (4), 237–282.

    Chavan, A. (1938) Essai critique de classification des lucines. Journal de Conchyliologie, 82 (1), 59–97; 82 (2),105–130; 82 (3), 215–241.

    Chavan, A. (1969) Superfamily Lucinacea Fleming, 1828. In: Moore, R.C. (Ed.), Treatise on Invertebrate Paleontology, Part N, Mollusca 6, Bivalvia, volume 2. Geological Society of America and University of Kansas Press, pp. N491–N518.

    Combosch, D.J. & Giribet, G. (2016) Clarifying phylogenetic relationships and the evolutionary history of the bivalve order Arcida (Mollusca: Bivalvia: Pteriomorphia) Molecular Phylogenetics and Evolution, 94, 298–312.

    http://dx.doi.org/10.1016/j.ympev.2015.09.016

    Cosel, R. von & Bouchet, P. (2008) Tropical deep-water lucinids (Mollusca: Bivalvia) from the Indo-Pacific: essentially unknown, but diverse and occasionally gigantic. In: Héros, V.,Cowie, R.H. & Bouchet, P. (Eds.), Tropical Deep Sea Benthos 25. Mémoires du Muséum national d’Histoire naturelle, 196, 115–213.

    Distel, D.L. & Felbeck, H. (1987) Endosymbiosis in the lucinid clams Lucinoma aequizonata, Lucinoma annulata and Lucina floridana: a reexamination of the functional morphology of the gills as bacteria-bearing organs. Marine Biology, 96, 79–86.
    http://dx.doi.org/10.1007/BF00394840

    Dockery, D.T. (1982) Lower Oligocene Bivalvia of the Vicksburg Group in Mississippi. Mississippi Department of Natural Resources Bureau of Geology, Bulletin, 123, 1–261.

    Elisabeth, N.H., Gustave, S.D.D. & Gros, O. (2012) Cell proliferation and apoptosis in gill filaments of the lucinid Codakia orbiculata (Montagu, 1808) (Mollusca: Bivalvia) during bacterial decolonization and recolonization. Microscopy Research and Technique, 75, 1136–1146.

    http://dx.doi.org/10.1002/jemt.22041

    Elisabeth, N.H., Caro, A., Césaire, T., Mansot, J.-L., Escalas, A., Sylvestre, M.-N., Jean-Louis, P. & Gros, O. (2014) Comparative modifications in bacterial gill-endosymbiotic populations of the two bivalves Codakia orbiculata and Lucina pensylvanica during bacterial loss and reacquisition. FEMS Microbiology Ecology, 89, 646–658.

    http://dx.doi.org/10.1111/1574-6941.12366

    Fisher, M.R. & Hand, S.C. (1984) Chemautotrophic symbionts in the bivalve Lucina floridana from seagrass beds. Biological Bulletin, Woods Hole, 167, 445–459.

    http://dx.doi.org/10.2307/1541289

    Frenkiel, L. & Mouëza, M. (1995) Gill ultrastructure and symbiotic bacteria in Codakia orbicularis (Bivalvia, Lucinidae). Zoomorphology, 115, 51–61.

    http://dx.doi.org/10.1007/bf00397934

    Frenkiel, L., Gros, O. & Mouëza, M. (1996) Gill structure in Lucina pectinata (Bivalvia: Lucinidae) with reference to hemoglobin in bivalves with symbiotic sulphur-oxidising bacteria. Marine Biology, 125, 511–524.

    Galindo, L.A., Puillandre, N., Strong, E.E. & Bouchet, P. (2014) Using microwaves to prepare gastropods for DNA barcoding. Molecular Ecology Resources, 14 (4), 700–705.

    http://dx.doi.org/10.1111/1755-0998.12231

    Geest, van der M., Sall, A.A., Ely, S.O., Nauta, R.W., Gils, van J.A. & Piersma, T. (2014) Nutritional and reproductive strategies in a chemosymbiotic bivalve living in a tropical intertidal seagrass bed. Marine Ecology Progress Series, 501, 113–126.
    http://dx.doi.org/10.3354/meps10702

    Gibson-Smith, J. & Gibson-Smith, W. (1982) Lucina s.s. (Mollusca: Bivalvia) in the western Atlantic: a reappraisal. Veliger, 25, 139–14.

    Giribet, G. & Distel, D.L. (2003) Bivalve phylogeny and molecular data. In: Lydeard, C. & Lindberg, D.R. (Eds.), Molecular Systematics and Phylogeography of Mollusks. Smithsonian Books, Washington, pp. 45–90.

    Glover, E.A. & Taylor, J.D. (2007) Diversity of chemosymbiotic bivalves on coral reefs: Lucinidae of New Caledonia and Lifou (Mollusca, Bivalvia). Zoosystema, 29, 109–181.

    Glover, E.A. & Taylor, J.D. (2016a) Lucinidae of the Philippines: highest known diversity and ubiquity of chemosymbiotic bivalves from intertidal to bathyal depths (Mollusca: Bivalvia). In: Héros, V., Strong, E. & Bouchet, P. (Eds). Tropical Deep-Sea Benthos 29. Mémoires du Muséum national d’Histoire naturelle, 208, 65–234. ISBN: 978-2-85653-774-9

    Glover, E.A. & Taylor, J.D. (2016b) Pleurolucina from the western Atlantic and eastern Pacific: a new intertidal species from Curaçao with unusual shell microstructure (Mollusca, Bivalvia, Lucinidae). ZooKeys, 620, 1–19.

    http://dx.doi.org/10.3897/zookeys.620.9569

    Glover, E.A., Williams, S.T. & Taylor, J.D. (2016) Lucinid bivalves of Singapore and their relationships (Bivalvia: Lucinidae). Raffles Bulletin of Zoology Supplement, 34, 165–191.

    González, V.L. & Giribet, G. (2014) A multilocus phylogeny of archiheterodont bivalves (Mollusca, Bivalvia, Archiheterodonta). Zoologica Scripta, 44, 41–58.

    http://dx.doi.org/10.1111/zsc.12086

    González, V.L., Andrade, S.C.S., Bieler, R., Collins, T.M., Dunn, C.W., Mikkelsen, P.M., Taylor, J.D. & Giribet, G. (2015) A phylogenetic backbone for Bivalvia: an RNA-seq approach. Proceedings of the Royal Society B Biological Sciences, 282, 2014.2332

    http://dx.doi.org/10.1098/rspb.2014.2332

    Gros, O., Frenkiel, L. & Mouëza, M. (1996) Gill ultrastructure and symbiotic bacteria in the tropical lucinid, Linga pensylvanica (Linné). Symbiosis, 20, 259–280.

    Gros, O., Liberge, M. & Felbeck, H. (2003) Interspecific infection of aposymbiotic juveniles of Codakia orbicularis by various tropical lucinid gill-endosymbionts. Marine Biology, 142, 57–66.

    Gros, O., Elisabeth, N.H., Gustave, S.D.D., Caro, A. & Dubilier, N. (2012) Plasticity of symbiont acquisition throughout the life cycle of the shallow-water tropical lucinid Codakia orbiculata (Mollusca: Bivalvia). Environmental Microbiology, 14, 1584–1595.

    http://dx.doi.org/10.1111/j.1462-2920.2012.02748.x

    Harris, G.D. (1896) The Midway Stage. Bulletins of American Paleontology, 1 (4), 115–271.

    Herrera N.D., ter Poorten, J.J., Bieler, R., Mikkelsen, P.M., Strong, E.E., Jablonski, D. & Steppan, S.J. (2015)Molecular phylogenetics and historical biogeography amid shifting continents in the cockles and giant clams (Bivalvia: Cardiidae). Molecular Phylogenetics and Evolution, 93, 94–106.
    http://dx.doi.org/10.1016/j.ympev.2015.07.013

    Huber, M. (2010) Compendium of bivalves. ConchBooks, Hackenheim, Germany. 900 pp.

    Huber, M. (2015) Compendium of bivalves 2. ConchBooks, Hackenheim, Germany. 907 pp.

    Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755. http://dx.doi.org/10.1093/bioinformatics/17.8.75

    Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.

    http://dx.doi.org/10.1093/nar/gkf436

    Katoh, K., Kuma, K., Toh, H. & Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511–518.

    http://dx.doi.org/10.1093/nar/gki198

    Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649.

    http://dx.doi.org/10.1093/bioinformatics/bts199

    Lemer, S., González, V.L., Bieler, R. & Giribet, G. (2016) Cementing mussels to oysters in the pteriomorphian tree: a phylogenomic approach. Proceedings of the Royal Society B: Biological Sciences, 283, 20160857.
    http://dx.doi.org/10.1098/rspb.2016.0857

    Kuhara, T., Kano, Y., Yoshikoshi, K. & Hashimoto, J. (2014) Shell morphology, anatomy and gill histology of the deep-sea bivalve Elliptiolucina ingens and molecular phylogenetic reconstruction of the chemosynthetic family Lucinidae. Venus, 72, 13–27.

    Mikkelsen, P.M., Bieler, R., Kappner, I. & Rawlings, T.A. (2006) Phylogeny of Veneroidea (Mollusca: Bivalvia) based on morphology and molecules. Zoological Journal of the Linnean Society, 148, 439–521.

    http://dx.doi.org/10.1111/j.1096-3642.2006.00262.x

    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 November 2010, New Orleans, LA pp. 1–8.
    http://dx.doi.org/10.1109/GCE.2010.5676129

    Nylander, J.A.A. (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.

    Sharma, P.P., González, V.L., Kawauchi, G.Y., Andrade, S.C.S., Guzmán, A., Collins, T.M., Glover, E.A., Harper, E.M., Healy, J.M., Mikkelsen, P.M., Taylor, J.D., Bieler, R. & Giribet, G. (2012) Phylogenetic analysis of four nuclear protein-encoding genes largely corroborates the traditional classification of Bivalvia (Mollusca). Molecular Phylogenetics and Evolution, 65, 64–74.

    http://dx.doi.org/10.1016/j.ympev.2012.05.025

    Sharma, P.P., Zardus, J.D., Boyle, E.E., González, V.L., Jennings, R.M., McIntyre, E., Wheeler, W.C., Etter, R.J. & Giribet, G. (2013) Into the deep: a phylogenetic approach to the bivalve subclass Protobranchia. Molecular Phylogenetics and Evolution, 69, 188–204.

    http://dx.doi.org/10.1016/j.ympev.2013.05.018

    Taylor, J.D. & Glover, E.A. (2013) New lucinid bivalves from shallow and deeper water of the Indian and West Pacific Oceans (Mollusca: Bivalvia: Lucinidae). ZooKeys, 326, 69–90.

    http://dx.doi.org/10.3897/zookeys.326.5786

    Taylor, J.D. & Glover, E.A. (2016) Lucinid bivalves of Guadeloupe: diversity and systematics in the context of the tropical western Atlantic (Mollusca: Bivalvia: Lucinidae). Zootaxa, 4196 (3), 301–380.
    http://doi.org/10.11646/zootaxa.4196.3.1

    Taylor, J.D., Glover, E.A., Smith, L., Dyal, P. & Williams, S.T. (2011) Molecular phylogeny and classification of the chemosymbiotic bivalve family Lucinidae (Mollusca: Bivalvia). Zoological Journal of the Linnean Society, 163, 15–49.

    http://dx.doi.org/10.1111/j.1096-3642.2011.00700.x

    Taylor, J.D., Glover, E.A. & Williams, S.T. (2009) Phylogenetic position of the bivalve family Cyrenoididae—removal from (and further dismantling of) the superfamily Lucinoidea. The Nautilus, 123, 1–5.

    Taylor, J.D., Glover, E.A. & Williams, S.T. (2013) Taxonomy and phylogeny of western Atlantic Lucinidae: new genus for Lucina costata d’Orbigny, 1846, a new species of Ferrocina and neotype designation for Venus orbiculata (Montagu, 1808). The Nautilus, 127, 131–146.

    Taylor, J.D., Glover, E.A. & Williams, S.T. (2014) Diversification of chemosymbiotic bivalves: origins and relationships of deeper water Lucinidae. Biological Journal of the Linnean Society, 111, 401–420.

    http://dx.doi.org/10.1111/bij.12208

    Taylor, J.D., Williams, S.T., Glover, E.A. & Dyal, P. (2007) A molecular phylogeny of heterodont bivalves (Mollusca: Bivalvia: Heterodonta): new analyses of 18S rRNA and 28S rRNA genes. Zoologica Scripta, 36, 587–606.

    http://dx.doi.org/10.1111/j.1463-6409.2007.00299.x

    Williams S.T. & Ozawa, T. (2006) Molecular phylogeny suggests polyphyly of both the turban shells (family Turbinidae) and the superfamily Trochoidea (Mollusca: Vetigastropoda). Molecular Phylogenetics and Evolution, 39, 33–51.

    http://dx.doi.org/10.1016/j.ympev.2005.12.017

    Williams, S.T., Taylor, J.D. & Glover, E.A. (2004) Molecular phylogeny of the Lucinoidea (Bivalvia): non-monophyly and separate acquisition of bacterial chemosymbiosis. Journal of Molluscan Studies, 70, 187–202.

    http://dx.doi.org/10.1093/mollus/70.2.187

    Woodring, W.P. (1925) Contributions to the geology and palaeontology of the West Indies. Miocene molluscs from Bowden, Jamaica. Pelecypods and scaphopods. Carnegie Institute Washington Publication, 366, 222 pp.

How to Cite

TAYLOR, J. D., GLOVER, E. A., SMITH, L., IKEBE, C., & WILLIAMS, S. T. (2016). New molecular phylogeny of Lucinidae: increased taxon base with focus on tropical Western Atlantic species (Mollusca: Bivalvia). Zootaxa, 4196(3), 381–398. https://doi.org/10.11646/zootaxa.4196.3.2