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DOI: http://dx.doi.org/10.11646/zootaxa.4007.2.1

Morphological and genetic variation in North Atlantic giant file clams, Acesta spp. (Bivalvia: Limidae), with description of a new cryptic species in the northwest Atlantic

JEAN-MARC GAGNON, ELLEN KENCHINGTON, ANTONY PORT, LYNNE J. ANSTEY, FRANCISCO JAVIER MURILLO

Abstract


We analyze the morphological and genetic variability within and between seven species of Acesta and specimens recently collected in the northwest Atlantic using traditional morphological measurements, landmark-based geometric morphometrics, and the cytochrome oxidase subunit I (COI) gene sequences, with particular emphasis on North Atlantic species. Shell morphology and external shell appearance do not allow reliable distinction between the widely recognized northeastern Atlantic A. excavata and other northwest Atlantic species or populations of Acesta, with the exception of A. oophaga. Similarly, shape analysis reveals a wide variability within northeastern Atlantic A. excavata, and significant morphological overlap with A. bullisi from the Gulf of Mexico and A. rathbuni from the southwestern Pacific and South China Sea. Specimens from the northwestern and Mid-Atlantic display shell shapes marginally similar to that of A. excavata. These differences are at least partly related to anterior or posterior shifting of the shell body and to the opposite shifting of the hinge line/dorsal region and upper lunule. These morphological variations, along with the midline-width-ratio, explain much of the variability extracted by principal component analysis. Results from a mitochondrial DNA barcode approach (COI), however, suggest that the northwest Atlantic specimens belong to a new species for which we propose the name Acesta cryptadelphe sp. nov. Differences in larval shell sizes between northeastern and northwestern Atlantic specimens are consistent with this result.

 


Keywords


Mollusca, Newfoundland, Nova Scotia, deep-water canyons, geometric morphometrics, shape analysis, COI

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References


Adam, W. & Knudsen, J. (1955) Note sur quelques espèces de mollusques marins nouveaux ou peu connus de l’Afrique Occidentale. Mededelingen Koninklijk Belgisch Instituut voor Natuurwetenschappen, 31 (61), 1–25.

Bartsch, P. (1913) The giant species of the molluscan genus Lima obtained in the Philippine and adjacent waters. Proceedings of the U.S. National Museum, 45, 235–240.

Bookstein, F. (1997) Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Medical Image Analysis, 1, 225–243.
http://dx.doi.org/10.1016/S1361-8415(97)85012-8

Boss, K. (1965) Note on Lima (Acesta) angolensis. Nautilus, 79, 54–58.

Bruguière, J.G. (1797) Tableau encyclopédique et méthodique des trois règnes de la nature. Contenant l'helminthologie, ou les vers infusoires, les vers intestins, les vers mollusques, etc. Troisième livraison, Panckoucke, Paris, 97 pls. [pls. 190–286]

Brusoni, F. & Basso, D. (2007) Canonical morphometry versus statistical treatment of outlines through Fourier shape analysis: an empirical comparison. Bollettino Malacologico, 43, 131–138. Available from: http://www.societaitalianadimalacologia
.it/Bollettino/Volume-43/Abstract43(9-12)%20131-138.pdf (Accesses 25 Aug. 2015)

Clague, G.E., Jones, W.J., Paduan, J.B., Clague, D.A. & Vrijenhoek, R.C. (2012) Phylogeography of Acesta clams from submarine seamounts and escarpments along the western margin of North America. Marine Ecology, 33, 75–87.
http://dx.doi.org/10.1111/j.1439-0485.2011.00458.x

Copley, J.T.P., Tyler, P.A., Sheader, M., Murton, B.J. & German, C.R. (1996) Megafauna from sublittoral to abyssal depths along the Mid-Atlantic Ridge south of Iceland. Oceanologica Acta, 19, 549–559.
http://archimer.ifremer.fr/doc/00096/20725/ (accessed 10 August 2015)

Dautzenberg, P. (1927) Mollusques provenant des campagnes scientifiques du Prince Albert 1er de Monaco dans l’Océan Atlantique et dans le Golfe de Gascogne. Résultats des Campagnes Scientifiques du Prince Albert 1er de Monaco, 52, 1–400.

Durán Muñoz, P., Sacau, M., Del Rio, J.L., López-Abellán, L.J. & Sarralde, R. (2014) Seabed mapping and vulnerable marine ecosystems protection on the high-seas fisheries: Four case studies on progress in the Atlantic Ocean. ICES CM 2014/3527 B:22. Available from: http://www.ices.dk/sites/pub/CM%20Doccuments/CM-2014/Theme%20Session%20B%20contribu
tions/B2214.pdf (accessed 18 July 2015)

Fabricius, J.C. (1779) Reise nach Norwegen mit Bemerkungen aus des Naturhistorie und Oekonomie. Verlag Carl Ernst Bohn, Hamburg, 398 pp.

Folmer, O., Black, M., Hoeh, W., Lutz, R. & 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. Available from: http://www.mbari.org/staff/vrijen/PDFS/Folmer_94MMBB.pdf (accessed 10 August 2015)

Gagnon, J.-M. & Haedrich, R.L. (2003) First record of the European giant file clam, Acesta excavata (Bivalvia: Pectinoidea: Limidae), in the northwest Atlantic. The Canadian Field-Naturalist, 117, 440–447. Available from: http://canadianfieldnaturalist.ca/index.php/cfn/article/viewFile/748/748 (accessed 10 August 2015)

Gmelin, J.F. (1791) Caroli a Linné, systema naturae. Tom. I. Pars VI. Beer, Lipsiae, 890 [pp. 3021–3910]

Goldstein, P.Z. & DeSalle, R. (2011) Integrating DNA barcode data and taxonomic practice: Determination, discovery and description. BioEssays, 33, 135–147.
http://dx.doi.org/10.1002/bies.201000036

Haedrich, R.L. & Gagnon, J.-M. (1991) Rock wall fauna of Newfoundland Fjords. Continental Shelf Research, 11, 1199–1208.
http://dx.doi.org/10.1016/0278-4343(91)90097-P

Hammer, Ø. (2014) PAST–Paleontological Statistics. Version 3.05. Reference Manual. Natural History Museum, University of Oslo, 222 pp. Available from: http://folk.uio.no/ohammer/past/ (accessed 23 June 2015)

Hebert, P.D.N. & Gregory, T.R. (2005) The promise of DNA barcoding for taxonomy. Systematic Biology, 54, 852–859.
http://dx.doi.org/10.1080/10635150500354886

Hebert, P.D.N., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society Series B–Biological Sciences, 270, 313–321.

http://dx.doi.org/10.1098/rspb.2002.2218

Hertlein, L.G. (1952) Description of a new pelecypod of the genus Lima from deep water off central California. Proceedings of the California Academy of Sciences, 27, 377–381.

Hertlein, L.G. (1963) A new species of giant Lima from off southern California (Mollusca: Pelecypoda). Occasional Papers California Academy of Sciences, 40, 1–6.

Jablonski, D. & Lutz, R.A. (1983) Larval ecology of marine benthic invertebrates: paleobiological implications. Biological Review, 58, 21–89.

Järnegren, J. & Altin, D. (2006) Filtration and respiration of the deep living bivalve Acesta excavata (J.C. Fabricius, 1779) (Mollusca: Bivalvia). Journal of Experimental Biology and Ecology, 334, 122–129.

http://dx.doi.org/10.1016/j.jembe.2006.01.014

Järnegren, J., Schander, C., Sneli, J.-A., Rønningen, V. & Young, C.M. (2007) Four genes, morphology and ecology: distinguishing a new species of Acesta (Mollusca; Bivalvia) from the Gulf of Mexico. Marine Biology, 152 (1), 43–55.
http://dx.doi.org/10.1007/s00227-007-0651-y

Johnson, M.P., White, M., Wilson, A., Würzberg, L., Schwabe, E., Folch, H. & Allcock, A.L. (2013) A vertical wall dominated by Acesta excavata and Neopycnodonte zibrowii, part of an undersampled group of deep-sea habitats. PLoS ONE, 8 (11), e79917.
http://dx.doi.org/10.1371/journal.pone.0079917

Kenchington, E., Cogswell, A., MacIsaac, K., Beazley, L., Law, B. & Kenchington, T. (2014) Limited depth zonation among bathyal epibenthic megafauna of the Gully submarine canyon, northwest Atlantic. Deep-Sea Research II, 104, 67–82.
http://dx.doi.org/10.1016/j.dsr2.2013.08.016

Kenchington, E. & Full, W.E. (1994) Fourier analysis of scallop shells (Placopecten magellanicus) in determining population structure. Canadian Journal of Fisheries and Aquatic Sciences, 51, 348–356.

http://dx.doi.org/10.1139/f94-035

Kendall, D.G. (1984) Shape manifolds, Procrustean metrics, and complex projective spaces. Bulletin of the London Mathematical Society, 16, 81–121.
http://dx.doi.org/10.1112/blms/16.2.81

Leyva-Valencia, I., Álvarez-Castañeda, S.T., Lluch-Cota, D.B., González-Peláez, S., Pérez-Valencia, S., Vadopalas, B., Ramírez-Pérez, S. & Cruz-Hernández, P. (2012) Shell shape differences between two Panopea species and phenotypic variation among P. globosa at different sites using two geometric morphometrics approaches. Malacologia, 55, 1–13.
http://dx.doi.org/10.4002/040.055.0101

Lima, G.M. & Lutz, R.A. (1990) The relationship of larval shell morphology to mode of development in marine prosobranch gastropods. Journal of the Marine Biological Association of the United Kingdom, 70, 611–637.
http://dx.doi.org/10.1017/S0025315400036626

Link, D.H.F. (1807) Beschreibung der Naturalien-Sammlung der Universität zu Rostock. 3 Abt. [Part 3], p. 157. Rostock, Adlers Erben.

Linnaeus, C. (1758) Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata, Laurentii Salvii, Holmiæ [Lipsiae, Stockholm], pp. [1–4], 1–824.

López Correa, M., Freiwald, A., Hall-Spencer, J. & Taviani, M. (2005) Distribution and habitats of Acesta excavata (Bivalvia: Limidae) with new data on its shell ultrastructure. In: Freiwald, A. & Roberts, J.M. (Eds.), Cold-water corals and ecosystems. Springer, Berlin, Heidelberg, pp. 173–205.

Malchus, N. & Sartori, A.F. (2013) Part N, Revised, Volume 1, Chapter 4 : The early shell: Ontology, features and evolution. Treatise Online, 61, 1–144.

Marshall, B.A. (2001) The genus Acesta H. & A. Adams, 1858 in the south-west Pacific (Bivalvia: Limidae). In: Bouchet, P. & Marshall, B.A. (Eds.), Tropical deep-sea benthos. Publications Scientifiques du Muséum, 22, pp. 97–109. [Paris]

McWilliam, H., Li, W., Uludag, M., Squizzato, S., Park, Y.M., Buso, N., Cowley, A.P. & Lopez, R. (2013) Analysis tool web services from the EMBL-EBI. Nucleic Acids Research, 41, W597–W600.

http://dx.doi.org/10.1093/nar/gkt376

Ménard de la Groye, F.J.B. (1807) Mémoire sur un nouveau genre de la famille des Solénoides. Annales du Muséum d’Histoire naturelle de Paris, 9, 131–139.

Meyer, C.P. (2003) Molecular systematics of cowries (Gastropoda: Cypraeidae) and diversification patterns in the tropics. Biological Journal of the Linnean Society, 79, 401–459.
http://dx.doi.org/10.1046/j.1095-8312.2003.00197.x

Montagu, G. (1803) Testacea Britannica or Natural History of British Shells, Marine, Land, and Fresh-water, Including the Most Minute: Systematically Arranged and Embellished with Figures. Vol. 1. & 2. J. White, London, 606 pp. [xxxvii + 291 pp. & 293–606 pp.]

Murillo, F.J., Duran Munoz, P., Altuna, A. & Serrano, A. (2011) Distribution of deep-water corals of the Flemish Cap, Flemish Pass and the Grand Banks of Newfoundland (northwest Atlantic Ocean): interaction with fishing activities. ICES Journal of Marine Science, 68, 319–332.

http://dx.doi.org/10.1093/icesjms/fsq071

Nei, M. & Kumar, S. (2000) Molecular Evolution and Phylogenetics. Oxford University Press, New York, 333 pp.

Ockelmann, K.W. (1965) Developmental types in marine bivalves and their distribution along the Atlantic coast of Europe. In: Cox, L.R. & Peake, J.F. (Eds.), Proceedings of the First European Malacological Congress, London, 1962. Conchological Society of Great Britain and Ireland and the Malacological Society of London, London, pp. 25–35.

Parr, W.C., Ruto, A., Soligo, C. & Chatterjee, H.J. (2011) Allometric shape vector projection: a new method for the identification of allometric shape characters and trajectories applied to the human astragalus (talus). Journal of Theoretical Biology, 272, 64–71.
http://dx.doi.org/10.1016/j.jtbi.2010.11.030

Perez, I., Bernal, V. & Gonzalez, P. (2006) Differences between sliding semilandmark methods in geometric morphometrics, with an application to human craniofacial and dental variation, Journal of Anatomy, 208, 769–784.
http://dx.doi.org/10.1111/j.1469-7580.2006.00576.x

Redfearn, P., Chanley, P. & Chanley, M. (1986) Larval shell development of four species of New Zealand mussels: (Bivalvia, Mytilacea). New Zealand Journal of Marine and Freshwater Research, 20, 157–172.

http://dx.doi.org/10.1080/00288330.1986.9516140

Rohlf, F.J. (1999) Shape statistics: Procrustes superimpositions and tangent spaces. Journal of Classification, 16, 197–223.
http://dx.doi.org/10.1007/s003579900054

Ryan, W.B.F., Carbotte, S.M., Coplan, J.O., O'Hara, S., Melkonian, A., Arko, R., Weissel, R.A., Ferrini, V., Goodwillie, A., Nitsche, F., Bonczkowski, J. & Zemsky, R. (2009) Global Multi-Resolution Topography synthesis. Geochemistry, Geophysics, Geosystems, 10, Q03014.
http://dx.doi.org/10.1029/2008GC002332

Sheets, H.D. (2001) IMP: PCAGen6- Principal Components Generation Utility. Department of Physics, Canisius College, Buffalo, NY. Available from: http://www3.canisius.edu/~sheets/morphsoft.html (accessed 23 June 2015)

Sheets, H.D. (2002) Imp: SemiLand6. Department of Physics, Canisius College, Buffalo, NY. Available from: http://www3.canisius.edu/~sheets/morphsoft.html (accessed 23 June 2015)

Sheets, H.D. (2003) IMP: CoordGen6–Coordinate Generation Utility: User’s Manual. Department of Physics, Canisius College, Buffalo, NY. Available from: http://www3.canisius.edu/~sheets/morphsoft.html (accessed 23 June 2015)

Sheets, H.D. (2004) IMP - Integrated Morphometrics Package. Department of Physics, Canisius College, Buffalo, NY. Available from: http://www3.canisius.edu/~sheets/morphsoft.html (accessed 23 June 2015)

Sheets, H.D. (2006) CVAGen version 6. Department of Physics, Canisius College, Buffalo, NY. Available from: http://www3.canisius.edu/~sheets/moremorph.html (accessed 23 June 2015)

Sheets, H.D., Covino, K.M., Panasiewicz, J.M. & Morris, S.R. (2006) Comparison of geometric morphometric outline methods in the discrimination of age related differences in feather shape. Frontiers in Zoology, 3, 15.
http://dx.doi.org/10.1186/1742-9994-3-15

Sneli, J.-A., Knudsen, J. & Vedelsby, A. (2009) Johan Christian Fabricius and his molluscan species, Acesta excavata (J. C. Fabricius, 1779). Steenstrupia, 30, 153–162. Available from: http://zoologi.snm.ku.dk/english/about_the_zoological_muse
um/publications/steenstrupia/early_volumes/Sneli_et_al 2009.pdf (accessed 10 August 2015)

Sowerby, G.B.I. (1823) The genera of Recent and fossil shells, for the use of students in conchology and geology. Vol. 1. London, pl. 113, fig. 4.

Sowerby, G.B. III. (1883) Descriptions of five new species of shells. Proceedings of the Zoological Society of London, 1883, 30–32.

Sowerby, G.B. III. (1888) Descriptions of sixteen new species of shells. Proceedings of the Zoological Society of London, 1888, 207–213.

Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526. Available from: http://mbe.oxfordjournals.org/content/10/3/512 (accessed 10 August 2015)

Tamura, K., Nei, M. & Kumar, S. (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences, 101, 11030–11035.
http://dx.doi.org/10.1073/pnas.0404206101

Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

http://dx.doi.org/10.1093/molbev/mst197

Tautz, D., Arctander, P., Minelli, A., Thomas, R.H. & Vogler, A.P. (2003) A plea for DNA taxonomy. Trends in Ecology and Evolution, 18, 70–74.
http://dx.doi.org/10.1016/S0169-5347(02)00041-1

Vokes, H.E. (1963) Studies on Tertiary and Recent giant Limidae. Tulane Studies in Geology, 1, 73–92.

Webster, M. & Sheets, H.D. (2010) A Practical introduction to landmark-based geometric morphometrics. In: Alroy, J. & Hunt, G. (Eds), Quantitative methods in Paleobiology. Paleontological Society Papers, 16, 163–188, plus Supplementary Online Material, 43 pp. Available from: http://www.paleosoc.org/shortcourse2010/webster_and_Sheets2010SOM.pdf (accessed 23 June 2015)

Zelditch, M.L., Swiderski, D.L. & Sheets, H.D. (2012) Geometric morphometrics for biologists: a primer. 2nd Edition. Elsevier Academic Press, London, 478 pp.


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