Hostname: page-component-7c8c6479df-24hb2 Total loading time: 0 Render date: 2024-03-28T14:30:33.279Z Has data issue: false hasContentIssue false

COI sequencing as tool for the taxonomic attribution of Patella spp. (Gastropoda): the case of morphologically undistinguishable juveniles settled on a Patella ferruginea adult

Published online by Cambridge University Press:  15 February 2010

Marco Casu*
Affiliation:
Dipartimento di Zoologia e Genetica Evoluzionistica, University of Sassari, Via Muroni 25, I-07100 Sassari, Italy
Daria Sanna
Affiliation:
Dipartimento di Zoologia e Genetica Evoluzionistica, University of Sassari, Via Muroni 25, I-07100 Sassari, Italy
Benedetto Cristo
Affiliation:
Dipartimento di Zoologia e Genetica Evoluzionistica, University of Sassari, Via Muroni 25, I-07100 Sassari, Italy
Tiziana Lai
Affiliation:
Dipartimento di Zoologia e Genetica Evoluzionistica, University of Sassari, Via Muroni 25, I-07100 Sassari, Italy
Gian Luca Dedola
Affiliation:
Dipartimento di Zoologia e Genetica Evoluzionistica, University of Sassari, Via Muroni 25, I-07100 Sassari, Italy
Marco Curini-Galletti
Affiliation:
Dipartimento di Zoologia e Genetica Evoluzionistica, University of Sassari, Via Muroni 25, I-07100 Sassari, Italy
*
Correspondence should be addressed to: M. Casu, Dipartimento di Zoologia e Genetica Evoluzionistica, University of Sassari, Via Muroni 25, I-07100 Sassari, Italy email: marcasu@uniss.it

Abstract

Patella ferruginea is an endangered marine gastropod, distributed on the western Mediterranean coasts, whose range has progressively contracted, due to intense human exploitation. A genetic analysis was performed on two unidentified young individuals belonging to the genus Patella found attached to the shell of an adult of P. ferruginea, with a twofold aim: (i) to achieve their correct taxonomic attribution by means of the DNA barcoding; and (ii) to shed some light on the hypothesized larval philopatry and/or juveniles phoresis in P. ferruginea. The survey was carried out comparing the sequences of the cytochrome c oxidase subunit I (COI) Folmer region obtained for the two juveniles with those obtained for adults of P. ferruginea, P. caerulea, P. rustica, and P. ulyssiponensis, from different sites of the western Mediterranean, by means of maximum likelihood cluster analysis and a Bayesian-based assignment test. Results obtained evidenced that: (i) COI may be used with confidence as DNA barcoding in the genus Patella; and (ii) the two juveniles studied are not conspecific: one belonged to P. ferruginea, the other to P. rustica. The latter finding raises doubts about the juvenile phoresis and about the occurrence of larval philopatry in P. ferruginea, suggesting that an extensive use of a molecular approach for a better evaluation of the recruitment features of this endangered species should be adopted.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

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

Aversano, F.R. (1986) Esperimento di insediamento artificiale di Patella ferruginea Gmelin, 1791 nelle acque del Golfo di Arzachena (Sardegna settentrionale). Bollettino Malacologico 22, 169170.Google Scholar
Bensasson, D., Zhang, D-X., Hartl, D.L. and Hewitt, G.M. (2001) Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology and Evolution 16, 314321.CrossRefGoogle ScholarPubMed
Biagi, V. and Poli, D. (1986) Considerazioni su una popolazione di Patella ferruginea Gmelin, 1791 per le acque del promontorio di Piombino. Bollettino Malacologico 22, 171174.Google Scholar
Casu, M., Casu, D., Lai, T., Cossu, P. and Curini-Galletti, M. (2006) Inter Simple Sequence Repeat markers revealed strong genetic differentiation among populations of the endangered mollusc Patella ferruginea (Gastropoda: Patellidae) from two Sardinian Marine Protected Areas. Marine Biology 149, 11631174.Google Scholar
Casu, M., Lai, T., Sanna, D., Cossu, P., Curini-Galletti, M. (2009) An integrative approach to the taxonomy of the pigmented European Pseudomonocelis Meixner, 1943 (Platyhelminthes: Proseriata). Biological Journal of the Linnean Society, 98, 907922.CrossRefGoogle Scholar
Corander, J., Waldmann, P., Marttinen, P. and Sillanpää, M.J. (2004) BAPS 2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics 20, 23632369.CrossRefGoogle ScholarPubMed
Cristo, B. and Caronni, S. (2008) Osservazioni sullo stato di conservazione di Patella ferruginea Gmelin1791 nelle vicinanze di Capo Ceraso (Golfo di Olbia, Sardegna Nord Orientale). Biologia Marina Mediterranea 15, 302303.Google Scholar
Cristo, B., Caronni, S. and Floris, A. (2007) Osservazioni su Patella ferruginea Gmelin1791 (Mollusca, Gastropoda) nel Golfo di Olbia. Biologia Marina Mediterranea 14, 344345.Google Scholar
Dunn, C.P. (2003) Keeping taxonomy based in morphology. Tree 18, 270271.Google Scholar
Duran, S., Pascual, M. and Turon, X. (2004) Low levels of genetic variation in mtDNA sequences over the western Mediterranean and Atlantic range of the sponge Crambe crambe (Poecilosclerida). Marine Biology 144, 3135.Google Scholar
Ebach, M.C. and Holdrege, C. (2005) DNA barcoding is no substitute for taxonomy. Nature 434, 434697.CrossRefGoogle ScholarPubMed
Erpenbeck, D., Hooper, J.N.A. and Worheide, G. (2006) CO1 phylogenies in diploblasts and the ‘Barcoding of life’—are we sequencing a suboptimal partition? Molecular Ecology Notes 6, 550553.Google Scholar
Espinosa, F. and Ozawa, T. (2006) Population genetics of the endangered limpet Patella ferruginea (Gastropoda: Patellidae): taxonomic, conservation and evolutionary considerations. Journal of Zoological Systematics and Evolutionary Research 44, 816.Google Scholar
Espinosa, F., Guerra García, J.M., Fa, D. and García Gomez, J.C. (2006) Aspects of reproduction and their implications for the conservation of the endangered limpet, Patella ferruginea. Invertebrate Reproduction and Development 49, 8592.Google Scholar
Espinosa, F., Rivera Ingraham, G.A. and García Gomez, J.C. (2008a) Gonochorism or protandrous hermaphroditism? Evidence of sex change in the endangered limpet Patella ferruginea. Journal of the Marine Biological Association of the United Kingdom 2—Biodiversity Records. On line publication (www.mba.ac.uk/jmba/biodiversityrecords.php).CrossRefGoogle Scholar
Espinosa, F., González, A.R., Maestre, M.J., Fa, D., Guerra-García, J.M. and García Gomez, J.C. (2008b) Responses of the endangered limpet Patella ferruginea to reintroduction under different environmental conditions: survival, growth rates and life-history. Italian Journal of Zoology 75, 371384.Google Scholar
Espinosa, F., Rivera Ingraham, G.A. and García Gomez, J.C. (2009) Effects of human pressure on population size structures of the endangered ferruginean limpet: towards future management measures. Journal of Coastal Research 25, 857863.CrossRefGoogle Scholar
Fisher-Piette, E. (1938) The concept of species and geographical isolation in the case of north Atlantic Patella. Proceedings of the Linnean Society of London 150, 268275.Google 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, 294299.Google ScholarPubMed
Frenkiel, L. (1975) Contribution à l'étude des cycles de reproduction des Patellidae en Algérie. Pubblicazione della Stazione Zoologica di Napoli 39, 153189.Google Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hebert, P.D.N., Ratnasingham, S. and deWaard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B 270, 9699.Google Scholar
Klautau, M., Russo, C.A.M., Lazoski, C., Boury-Esnault, N., Thorpe, J.P. and Solé-Cava, A.M. (1999) Does cosmopolitanism result from over conservative systematics? A case study using the marine sponge Chondrilla nucula. Evolution 53, 14141422.Google Scholar
Laborel-Deguen, F. and Laborel, J. (1991a) Une tentative de reintroduction de Patella ferruginea Gmel. (Gasteropoda) dans le Parc National de Port-Cros (Var, France). In Boudouresque, C.F., Avon, M. and Gravez, V. (eds) Les species marines a protéger en Méditerranée. Marseille, France: GIS Posidonie Publication, pp. 129132.Google Scholar
Laborel-Deguen, F. and Laborel, J. (1991b) Nouvelles observations sur la population de Patella ferruginea Gmel. de Corse. In Boudouresque, C.F., Avon, M. and Gravez, V. (eds) Les species marines a protéger en Méditerranée. Marseille, France: GIS Posidonie Publication, pp. 105117.Google Scholar
Laborel-Deguen, F. and Laborel, J. (1991c) Une tentative de reintrodution de Patella ferruginea Gmel. (Gasteropoda) dans le Parc National de Port-Cros (Var, France) In Boudouresque, C.F., Avon, M. and Gravez, V. (eds) Les species marines a protéger en Méditerranée. Marseille, France: GIS Posidonie Publication, pp. 129132.Google Scholar
Maggi, E., Bertocci, I., Vaselli, S. and Benedetti-Cecchi, L. (2009) Effects of changes in number, identity and abundance of habitat-forming species on assemblages of rocky shores. Marine Ecology Progress Series 381, 3949.CrossRefGoogle Scholar
Mariani, S. (2003) Recruitment in invertebrates with short-lived larvae: the case of the bryozoan Disporella hispida (Fleming). Helgoland Marine Research 57, 4753.Google Scholar
Markmann, M. and Tautz, D. (2005) Reverse taxonomy: an approach towards determining the diversity of meiobenthic organisms based on ribosomal RNA signature sequences. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 19171924.CrossRefGoogle ScholarPubMed
Mauro, A., Arculeo, M. and Parrinello, N. (2003) Morphological and molecular tools in identifying the Mediterranean limpets Patella caerulea, Patella aspera and Patella rustica. Journal of Experimental Marine Biology and Ecology 295, 131143.CrossRefGoogle Scholar
Meyer, C.P. and Paulay, G. (2005) DNA barcoding: error rates based on comprehensive sampling. PloS Biology 3, 22292238.CrossRefGoogle ScholarPubMed
Monaghan, M.T., Balke, M., Gregory, T.R. and Vogler, A.P. (2005) DNA-based species delineation in tropical beetles using mitochondrial and nuclear markers. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 19251933.CrossRefGoogle ScholarPubMed
Moritz, C. and Cicero, C. (2004) DNA barcoding: promise and pitfalls. PLoS Biology 2, 354.CrossRefGoogle ScholarPubMed
Nakano, T. and Ozawa, T. (2007) Worldwide phylogeography of limpets of the order patellogastropoda: molecular, morphological and palaeontological evidence. Journal of Molluscan Studies 73, 7999.Google Scholar
Padial, J.M., Castroviejo-Fisher, S., Köhler, J., Vilà, C., Chaparro, J.C. and De la Riva, I. (2009) Deciphering the products of evolution at the species level: the need for an integrative taxonomy. Zoologica Scripta 38, 431447.Google Scholar
Posada, D. and Crandall, K.A. (1998) ModelTest: testing the model of DNA substitution, version 3.7. Bioinformatics 14, 817818.Google Scholar
Ramos, M.A. (1998) Implementing the Habitats Directive for mollusc species in Spain. Journal of Conchology 2, 125132.Google Scholar
Rodríguez, F., Oliver, J.F., Marín, A. and Medina, J.R. (1990) The general stochastic model of nucleotide substitutions. Journal of Theoretical Biology 142, 485501.CrossRefGoogle Scholar
Rozas, J. and Rozas, R. (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174175.Google Scholar
Sanna, D., Lai, T., Francalacci, P., Curini-Galletti, M. and Casu, M. (2009) Development of primers for the amplification of cytochrome c oxidase subunit I (COI) partial region (mtDNA) in Monocelis lineata (Platyhelminthes: Proseriata) species complex. Genetics and Molecular Biology 32, 864867.Google Scholar
Sá-Pinto, A., Branco, M., Harris, D.J. and Alexandrino, P. (2005) Phylogeny and phylogeography of the genus Patella based on mitochondrial DNA sequence data. Journal of Experimental Marine Biology and Ecology 325, 95110.CrossRefGoogle Scholar
Schröder, H.C., Efremova, S.M., Itskovich, V.B., Belikov, S., Masuda, Y., Krasko, A., Müller, I.M. and Müller, W.E.G. (2003) Molecular phylogeny of the freshwater sponges in Lake Baikal. Journal of Zoological Systematics and Evolutionary Research 41, 8086.CrossRefGoogle Scholar
Shearer, T.L., van Oppen, J.H., Romano, S.L. and Worheide, G. (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11, 24752478.Google Scholar
Sorenson, M.D. and Quinn, T.W. (1998) Numts: a challenge for avian systematics and population biology. The Auk 115, 214221.CrossRefGoogle Scholar
Swofford, D.L. (1998) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sunderland, MA: Sinauer Associates.Google Scholar
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599.CrossRefGoogle ScholarPubMed
Tautz, D., Arctander, P., Minelli, A., Thomas, R.H. and Vogler, A.P. (2003) A plea for DNA taxonomy. Trends in Ecology and Evolution 18, 7074.Google Scholar
Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.Google Scholar
Vogler, A.P. and Monaghan, M.T. (2007) Recent advances in DNA taxonomy. Journal of Zoological Systematics and Evolutionary Research 45, 110.CrossRefGoogle Scholar