Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-05-26T00:28:08.526Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular data delineate cryptic Nassarius species and characterize spatial genetic structure of N. nitidus

Published online by Cambridge University Press:  13 July 2011

L. Couceiro ,
L. López ,
E.E. Sotka ,
J.M. Ruiz  and
R. Barreiro
L. Couceiro
Affiliation:
Área de Ecoloxía, Facultade de Ciencias, Universidade da Coruña, Campus da Zapateira s/n, 15071-A Coruña, Spain
L. López
Affiliation:
Área de Ecoloxía, Facultade de Ciencias, Universidade da Coruña, Campus da Zapateira s/n, 15071-A Coruña, Spain
E.E. Sotka
Affiliation:
Grice Marine Laboratory, College of Charleston, 205 Fort Johnson Road, Charleston, SC-29412, USA
J.M. Ruiz
Affiliation:
Área de Ecoloxía, Facultade de Ciencias, Universidade da Coruña, Campus da Zapateira s/n, 15071-A Coruña, Spain
R. Barreiro*
Affiliation:
Área de Ecoloxía, Facultade de Ciencias, Universidade da Coruña, Campus da Zapateira s/n, 15071-A Coruña, Spain
*
Correspondence should be addressed to: R. Barreiro, Área de Ecoloxía, Facultade de Ciencias, Universidade da Coruña, Campus da Zapateira s/n, 15071-A Coruña, Spain email: rodbar@udc.es
Get access Rights & Permissions [Opens in a new window]

Abstract

Nassarius nitidus is a marine snail species with a widespread distribution along European shorelines from the North Sea to the Mediterranean and Black Seas. Despite its widespread distribution, N. nitidus has been largely neglected due to taxonomic confusion with the congeneric Nassarius reticulatus. Discrimination between these two Nassarius is particularly challenging in areas where their ranges overlap: the European Atlantic and western Mediterranean. Here, we propose the use of the mtDNA gene cytochrome c oxidase subunit I (COI) to discriminate between these two morphologically similar congeneric species. A numerically comprehensive sampling of the areas of overlap reveals strong population-level differentiation in N. nitidus, particularly between the Mediterranean and the Atlantic. Despite this strong population structure, we found a wide (9.6 ± 1.6% mean K2P corrected sequence distance) barcoding gap with N. reticulatus that guarantees that COI barcodes may serve as a reliable diagnostic tool. A protocol using species-specific restriction patterns was developed to allow a quick and accurate discrimination between these two cryptic species.

Keywords

Nassarius reticulatusNassarius nitiduscryptic speciesDNA barcodingmtDNACOI
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 92 , Issue 5 , August 2012 , pp. 1175 - 1182
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

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

Avise, J.C. (2004) Molecular markers, natural history, and evolution. 2nd edition. Sunderland, MA: Sinauer Associates.Google Scholar
Bandelt, H.J., Forster, P. and Rohl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Barreiro, R., Couceiro, L., Quintela, M. and Ruiz, J.M. (2006) Population genetic structure of the prosobranch Nassarius reticulatus (L.) in a ria seascape (NW Iberian Peninsula) as revealed by RAPD analysis. Marine Biology 148, 1051–1060.CrossRefGoogle Scholar
Barreiro, R., González, R., Quintela, M. and Ruiz, J.M. (2001) Imposex, organotin bioaccumulation and sterililty of female Nassarius reticulatus in polluted areas of NW Spain. Marine Ecology Progress Series 218, 203–212.CrossRefGoogle Scholar
Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. and Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22, 148–155.CrossRefGoogle ScholarPubMed
Bilton, D.T., Paula, J. and Bishop, J.D.D. (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuarine, Coastal and Shelf Science 55, 937–952.CrossRefGoogle Scholar
Bird, C.E., Holland, B.S., Bowen, B.W. and Toonen, R.J. (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Molecular Ecology 16, 3173–3186.CrossRefGoogle ScholarPubMed
Borsa, P. (2002) Allozyme, mitochondrial-DNA, and morphometric variability indicate cryptic species of anchovy (Engraulis encrasicolus). Biological Journal of the Linnean Society 75, 261–269.Google Scholar
Bradbury, I.R., Laurel, B., Snelgrove, P.V.R., Bentzen, P. and Campana, S.E. (2008) Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history. Proceedings of the Royal Society, Series B—Biological Sciences 275, 1803–1809.Google ScholarPubMed
Carvajal-Rodríguez, A., Guerra-Varela, J., Fernández, B., Rolán, E. and Rolán-Álvarez, E. (2006) An example of the application of geometric morphometric tools to the morphological diagnosis of two sibling species in Nassarius (Mollusca, Prosobranchia). Iberus 24, 81–88.Google Scholar
Collyer, D.M. (1961) Differences revealed by paper partition chromatography between gastropod Nassarius reticulatus (L.) and specimens believed to be N. nitida (Jeffreys). Journal of the Marine Biological Association of the United Kingdom 41, 683–693.CrossRefGoogle Scholar
Couceiro, L., Barreiro, R., Ruiz, J.M. and Sotka, E.E. (2007) Genetic isolation by distance among populations of the netted dog whelk Nassarius reticulatus (L.) along the European Atlantic coastline. Journal of Heredity 98, 603–610.CrossRefGoogle ScholarPubMed
Cowen, R.K. and Sponaugle, S. (2009) Larval dispersal and marine population connectivity. Annual Review of Marine Science 1, 443–466.CrossRefGoogle ScholarPubMed
Craeymeersch, J. and Rietveld, M. (2005) Dog whelks in Dutch coastal waters. MarBEF Newsletter 3, 23–24.Google Scholar
Dekker, H. (2004) The netted dog whelk and its sibling, Nassarius reticulatus and N. nitidus (Gastropoda, Nassariidae), in The Netherlands. Vita Malacologica 2, 69–70.Google Scholar
Estoup, A., Largiader, C.R., Perrot, E. and Chourrout, D. (1996) Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Molecular Marine Biology and Biotechnology 5, 295–298.Google Scholar
Excoffier, L. (2006) Arlequin Version 3.1: an integrated software package for population genetics. Bern, Switzerland: Computational and Molecular Population Genetics Laboratory (CMPG), Institute of Zoology, University of Berne.Google Scholar
Excoffier, L., Smouse, P.E. and Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 21, 479–491.CrossRefGoogle 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.Google ScholarPubMed
Funk, D.J. and Omland, K.E. (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics 34, 397–423.CrossRefGoogle Scholar
Geller, J.B., Walton, E.D., Grosholz, E.D. and Ruiz, G.M. (1997) Cryptic invasions of the crab Carcinus detected by molecular phylogeography. Molecular Ecology 6, 901–906.CrossRefGoogle ScholarPubMed
Hansson, H.G. (1998) NEAT (North East Atlantic Taxa): Scandinavian marine mollusca check-list. Internet edition, [www.tmbl.gu.se].Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. and DeWaard, J.R. (2003a) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B—Biological Sciences 270, 313–321.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. and Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101, 14812–14817.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Ratnasingham, S. and deWaard, J.R. (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B—Biological Sciences 270, S96–S99.Google ScholarPubMed
Jeffreys, J.G. (1867) British conchology: or an account of the mollusca which now inhabit the British Isles and the surrounding seas, volume 4. London: J. Van Voorst.Google Scholar
Johnson, M.S. and Black, R. (1991) Genetic subdivision of the intertidal snail Bembicium vittatum (Gastropoda: Littorinidae) varies with habitat in the Houtman Abrolhos Islands, Western Australia. Heredity 67, 205–213.CrossRefGoogle Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Knowlton, N. (1993) Sibling species in the sea. Annual Review of Ecology and Systematics 24, 189–216.CrossRefGoogle Scholar
Lebour, M.V. (1931) The larval stages of Nassarius reticulatus and Nassarius incrassatus. Journal of the Marine Biological Association of the United Kingdom 17, 797–818.CrossRefGoogle Scholar
Lobel, P.B., Belkhode, S.P., Jackson, S.E. and Longerich, H.P. (1990) Recent taxonomic discoveries concerning the mussel Mytilus: implications for biomonitoring. Archives of Environmental Contamination and Toxicology 19, 508–512.CrossRefGoogle Scholar
Maggs, C.A., Castilho, R., Foltz, D., Henzler, C., Jolly, T., Kelly, J., Olsen, J., Perez, K.E., Stam, W., Vainola, R., Viard, F. and Wares, J. (2008) Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89, S108–S122.CrossRefGoogle ScholarPubMed
Meyer, C.P. and Paulay, G. (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3, 1–10.CrossRefGoogle ScholarPubMed
Moritz, C. and Cicero, C. (2004) DNA barcoding: promise and pitfalls. PLoS Biology 2, e354.CrossRefGoogle ScholarPubMed
Nei, M. (1987) Molecular evolutionary genetics. New York: Columbia University Press.CrossRefGoogle Scholar
Palmer, A.N.S., Styan, C.A. and Shearman, D.C.A. (2008) Foot mucus is a good source for non-destructive genetic sampling in Polyplacophora. Conservation Genetics 9, 229–231.CrossRefGoogle Scholar
Palumbi, S.R. (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecological Applications 13, S146–S158.CrossRefGoogle Scholar
Parsons, K.E. (1996) The genetic effects of larval dispersal depend on spatial scale and habitat characteristics. Marine Biology 126, 403–414.CrossRefGoogle Scholar
Patarnello, T., Volckaert, F.A.M.J. and Castilho, R. (2007) Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Molecular Ecology 16, 4426–4444.CrossRefGoogle ScholarPubMed
Rolán, E. and Luque, A.A. (1994) Nassarius reticulatus (Linnaeus, 1758) y Nassarius nitidus (Jeffreys, 1867) (Gastropoda, Nassariidae), dos especies válidas de los mares de Europa. Iberus 12, 59–76.Google Scholar
Rozas, J., Sanchez-DelBarrio, J.C., Messeguer, X. and Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.CrossRefGoogle ScholarPubMed
Sanjuán, A., Pérez-Losada, M. and Rolán, E. (1997) Allozyme evidence for cryptic speciation in sympatric populations of Nassarius spp (Mollusca: Gastropoda). Journal of the Marine Biological Association of the United Kingdom 77, 773–784.CrossRefGoogle Scholar
Tallmark, B. (1980) Population dynamics of Nassarius reticulatus (Gastropoda: Prosobranchia) in Gullmar Fjord, Sweden. Marine Ecology Progress Series 3, 51–62.CrossRefGoogle Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA 4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle Scholar
Watts, R.J. and Johnson, M.S. (2004) Estuaries, lagoons and enclosed embayments: habitats that enhance population subdivision of inshore fishes. Marine and Freshwater Research 55, 641–651.CrossRefGoogle Scholar