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Molecules and morphology reveal cryptic variation among digeneans infecting sympatric mullets in the Mediterranean

Published online by Cambridge University Press:  23 October 2009

I. BLASCO-COSTA ,
J. A. BALBUENA ,
J. A. RAGA ,
A. KOSTADINOVA  and
P. D. OLSON
I. BLASCO-COSTA*
Affiliation:
Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, PO Box 22 085, 46071 Valencia, Spain
J. A. BALBUENA
Affiliation:
Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, PO Box 22 085, 46071 Valencia, Spain
J. A. RAGA
Affiliation:
Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, PO Box 22 085, 46071 Valencia, Spain
A. KOSTADINOVA
Affiliation:
Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic Central Laboratory of General Ecology, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria
P. D. OLSON
Affiliation:
Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK
*
*Corresponding author: Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, PO Box 22 085, 46071 Valencia, Spain. Tel: +34 963543685. Fax: +34 963543733. E-mail: M.Isabel.Blasco@uv.es
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Summary

We applied a combined molecular and morphological approach to resolve the taxonomic status of Saccocoelium spp. parasitizing sympatric mullets (Mugilidae) in the Mediterranean. Eight morphotypes of Saccocoelium were distinguished by means of multivariate statistical analyses: 2 of Saccocoelium obesum ex Liza spp.; 4 of S. tensum ex Liza spp.; and 2 (S. cephali and Saccocoelium sp.) ex Mugil cephalus. Sequences of the 28S and ITS2 rRNA gene regions were obtained for a total of 21 isolates of these morphotypes. Combining sequence data analysis with a detailed morphological and multivariate morphometric study of the specimens allowed the demonstration of cryptic diversity thus rejecting the hypothesis of a single species of Saccocoelium infecting sympatric mullets in the Mediterranean. Comparative sequence analysis revealed 4 unique genotypes, thus corroborating the distinct species status of Saccocoelium obesum, S. tensum and S. cephali and a new cryptic species ex Liza aurata and L. saliens recognized by its consistent morphological differentiation and genetic divergence. However, in spite of their sharp morphological difference the 2 morphotypes from M. cephalus showed no molecular differentiation and 4 morphotypes of S. tensum were genetically identical. This wide intraspecific morphological variation within S. tensum and S. cephali suggests that delimiting species of Saccocoelium using solely morphological criteria will be misleading.

Keywords

DigeneaHaploporidaeSaccocoeliumMugilidaecryptic speciesmoleculesmorphologyrDNA

Information

Type
Research Article
Information
Parasitology , Volume 137 , Issue 2 , February 2010 , pp. 287 - 302
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Adamson, M. L. and Caira, J. N. (1994). Evolutionary factors influencing the nature of parasite specificity. Parasitology 109, S85–S95.CrossRefGoogle ScholarPubMed
Anderson, G. R. and Barker, S. C. (1993). Species differentiation in the Didymozoidae (Digenea): Restriction fragment length differences in internal transcribed spacer and 5.8S ribosomal DNA. International Journal for Parasitology 23, 133–136.CrossRefGoogle ScholarPubMed
Anderson, G. R. and Barker, S. C. (1998). Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spacer (ITS2) of ribosomal DNA. Systematic Parasitology 41, 87–94.CrossRefGoogle Scholar
Anistratenko, V. V. and Stadnichenko, A. P. (1994). Fauna Ukrainyi, Tom 29. Mollyuski, Vyipusk 1, Kniga 2: Littorinoobraznyie, Rissoiobraznyie. Naukova Dumka, Kiev.Google Scholar
Bartoli, P. and Gibson, D. I. (2007). Synopsis of the life cycles of Digenea (Platyhelminthes) from lagoons of the northern coast of the western Mediterranean. Journal of Natural History 41, 1553–1570.CrossRefGoogle Scholar
Bickford, D., Lohman, D. J., Sohdi, 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
Blair, D., Agatsuma, T., Watanobe, T., Okamoto, M. and Ito, A. (1997). Geographical genetic structure within the human lung fluke, Paragonimus westermani, detected from DNA sequences. Parasitology 115, 411–417.CrossRefGoogle ScholarPubMed
Blasco-Costa, I., Balbuena, J. A., Kostadinova, A. and Olson, P. D. (2009 a). Interrelationships of the Haploporinae (Digenea: Haploporidae): A molecular test of the taxonomic framework based on morphology. Parasitology International 58, 265–269.CrossRefGoogle ScholarPubMed
Blasco-Costa, I., Gibson, D. I., Balbuena, J. A., Raga, J. A. and Kostadinova, A. (2009 b). A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Haploporus Looss, 1902 and Lecithobotrys Looss, 1902. Systematic Parasitology 73, 107–133.CrossRefGoogle ScholarPubMed
Blasco-Costa, I., Montero, F. E., Balbuena, J. A., Raga, J. A. and Kostadinova, A. (2009 c). A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Dicrogaster Looss, 1902 and Forticulcita Overstreet, 1982. Systematic Parasitology 72, 187–206.CrossRefGoogle ScholarPubMed
Blasco-Costa, I., Montero, F. E., Gibson, D. I., Balbuena, J. A. and Kostadinova, A. (2009 d). A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Two new haploporine genera and a key to the genera of the subfamily. Systematic Parasitology 72, 207–215.CrossRefGoogle Scholar
Blasco-Costa, I., Montero, F. E., Gibson, D. I., Balbuena, J. A., Raga, J. A. and Kostadinova, A. (2009 e). A revision of the Haploporinae Nicoll, 1914 (Digenea: Haploporidae) from mullets (Mugilidae): Saccocoelium Looss, 1902. Systematic Parasitology 72, 159–186.CrossRefGoogle ScholarPubMed
Boisselier-Dubayle, M. C. and Gofas, S. (1999). Genetic relationships between marine and marginal-marine populations of Cerithium species from the Mediterranean Sea. Marine Biology 135, 671–682.CrossRefGoogle Scholar
Cardona, L., Royo, P. and Torras, X. (2001). Effects of leaping grey mullet Liza saliens (Osteichthyes, Mugilidae) in the macrophyte beds of oligohaline Mediterranean coastal lagoons. Hydrobiologia 462, 233–240.CrossRefGoogle Scholar
Chambers, C. B. and Cribb, T. H. (2006). Phylogeny, evolution and biogeography of the Quadrifoliovariinae Yamaguti, 1965 (Digenea: Lecithasteridae). Systematic Parasitology 63, 61–82.CrossRefGoogle ScholarPubMed
Combes, C. (1995). Interactions Durables. Écologie et Evolution du Parasitisme. Masson, Paris, France.Google Scholar
Combes, C. and Théron, A. (2000). Metazoan parasites and resource heterogeneity: constraints and benefits. International Journal for Parasitology 30, 299–304.CrossRefGoogle ScholarPubMed
Davis, G. M. (1994). Molecular genetics and taxonomic discrimination. The Nautilus Supplement 2, 3–23.Google Scholar
Dawes, B. (1947). The Trematoda of British Fishes. Ray Society, London, UK.CrossRefGoogle Scholar
Deblock, S. (1980). Inventaire des Trématodes larvaires parasites des Mollusques Hydrobia (Prosobranches) des côtes de France. Parassitologia 22, 1–105.Google Scholar
Donald, K. M., Kennedy, M., Poulin, R. and Spencer, H. G. (2004). Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). International Journal for Parasitology 34, 557–568.CrossRefGoogle ScholarPubMed
Edgar, R. C. (2004). MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113.CrossRefGoogle ScholarPubMed
Fares, A. and Maillard, C. (1974). Recherches sur quelques Haploporidae (Trematoda) parasites des Muges de Méditerranée Occidentale: systématique et cycles évolutifs. Zeitschrift für Parasitenkunde 45, 11–43.CrossRefGoogle Scholar
Ferretti, G. and Paggi, L. (1965). Ridescrizione di Saccocoelium obesum Looss, 1902 (sin. Saccocoelium tensum Looss,1902) trematoda parassita di Mugil cephalus. Rivista Parassitologia 26, 229–239.Google ScholarPubMed
Fischthal, J. H. and Kuntz, R. E. (1963). Trematode parasites of fishes from Egypt. Part V. Annotated record of some previously described forms. Journal of Parasitology 49, 91–98.CrossRefGoogle Scholar
Foltz, D. W. (2003). Invertebrate species with nonpelagic larvae have elevated levels of nonsynonymous substitutions and reduced nucleotide diversities. Journal of Molecular Evolution 57, 607–612.CrossRefGoogle ScholarPubMed
Hall, T. A. (1999). Bioedit: a user-friendly biological sequence editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium, Ser. 41, 95–98.Google Scholar
Holzer, A. S., Sommerville, C. and Wootten, R. (2004). Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. International Journal for Parasitology 34, 1099–1111.CrossRefGoogle Scholar
Huelsenbeck, J. P., Ronquist, F., Nielsen, R. and Bollback, J. P. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 2310–2314.CrossRefGoogle ScholarPubMed
Jousson, O. and Bartoli, P. (2001). Molecules, morphology and morphometrics of Cainocreadium labracis and Cainocreadium dentecis n. sp. (Digenea: Opecoelidae) parasitic in marine fishes. International Journal for Parasitology 31, 706–714.CrossRefGoogle Scholar
Jousson, O., Bartoli, P. and Pawlowski, J. (2000). Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). Journal of Evolutionary Biology 13, 778–785.CrossRefGoogle Scholar
Leung, T. L. F., Keeney, D. B. and Poulin, R. (2009). Cryptic species complexes in manipulative echinostomatid trematodes: when two become six. Parasitology 136, 241–252.CrossRefGoogle ScholarPubMed
Littlewood, D. T. J., Curini-Galletti, M., Herniou, E. A. (2000). The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution 16, 449–466.CrossRefGoogle ScholarPubMed
Looss, D. A. (1902). Die Distomen-Unterfamilie der Haploporinae. Archives de Parasitologie 6, 129–143.Google Scholar
Lockyer, A. E., Olson, P. D. and Littlewood, D. T. J. (2003). Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society (London) 78, 155–171.CrossRefGoogle Scholar
Maddison, D. R. and Maddison, W. P. (2005). MacClade 4: Analysis of Phylogeny and Character Evolution. Version 4.08. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Manly, B. F. J. (1997). Randomisation, Bootstrap and Monte Carlo Methods in Biology, 2nd Edn. Chapman and Hall, London, UK.Google Scholar
Mikailov, T. K. (1958). Parasite fauna of Mugil saliens Risso of the Caspian Sea. Zoologicheskyi Zhurnal 37, 373–378 (In Russian).Google Scholar
Miller, T. L. and Cribb, T. H. (2007 a). Two new cryptogonimid genera (Digenea, Cryptogonimidae) from Lutjanus bohar (Perciformes, Lutjanidae): analyses of ribosomal DNA reveals wide geographic distribution and presence of cryptic species. Acta Parasitologica 52, 104–113.CrossRefGoogle Scholar
Miller, T. L. and Cribb, T. H. (2007 b). Coevolution of Retrovarium n. gen. (Digenea: Cryptogonimidae) in Lutjanidae and Haemulidae (Perciformes) in the Indo-West Pacific. International Journal for Parasitology 37, 1023–1045.CrossRefGoogle ScholarPubMed
Miura, O., Kuris, A. M., Torchin, M. E., Hechinger, R. F., Dunham, E. J. and Chiba, S. (2005). Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). International Journal for Parasitology 35, 793–801.CrossRefGoogle ScholarPubMed
Moravec, F. and Libosvárský, J. (1975). Intestinal helminths from grey mullets, Mugil capito Cuvier and M. cephalus L., of Lake Borullus, A.R.E. Folia Parasitologica 22, 279–281.Google Scholar
Nolan, M. J. and Cribb, T. H. (2004). Two new blood flukes (Digenea: Sanguinicolidae) from Epinephelinae (Perciformes: Serranidae) of the Pacific Ocean. Parasitology International 53, 327–335.CrossRefGoogle ScholarPubMed
Nolan, M. J. and Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology 60, 101–163.CrossRefGoogle ScholarPubMed
Nolan, M. J. and Cribb, T. H. (2006). Cardicola Short, 1953 and Braya n. gen. (Digenea: Sanguinicolidae) from five families of tropical Indo-Pacific fishes. Zootaxa 1265, 1–80.CrossRefGoogle Scholar
Olson, P. D. and Tkach, V. V. (2005). Advances and trends in the molecular systematics of the parasitic platyhelminthes. Advances in Parasitology 60, 165–243.CrossRefGoogle ScholarPubMed
Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A. and Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.CrossRefGoogle ScholarPubMed
Overstreet, R. M. and Curran, S. S. (2005). Family Haploporidae Nicoll, 1914. In Keys to the Trematoda. Vol. 2 (ed. Jones, A., Bray, R. A. and Gibson, D. I.), pp. 129–165. CAB International, Wallingford, UK.Google Scholar
Pearson, J. C. (1972). A phylogeny of life-cycle patterns of the Digenea. Advances in Parasitology 58, 760–788.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Poulin, R. (2006). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.Google Scholar
Riginos, C. and Victor, B. C. (2001). Larval spatial distributions and other early life-history characteristics predict genetic differentiation in eastern Pacific blennioid fishes. Proceedings of the Royal Society London, B 268, 1931–1936.CrossRefGoogle ScholarPubMed
Russo, G. F. and Patti, F. P. (2005). Early life history of two closely related gastropods, Rissoa auriscalpium and Rissoa italiensis (Caenogastropoda: Rissoidae). Marine Biology 147, 429–437.CrossRefGoogle Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2002). PAUP – Phylogenetic Analysis Using Parsimony. Ver. 4. [Computer software and manual]. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Tatarenkov, A. and Johannesson, K. (1998). Evidence of a reproductive barrier between two forms of the marine periwinkle Littorina fabalis (Gastropoda). Biological Journal of the Linnean Society (London) 63, 349–365.Google Scholar
Tkach, V. V., Grabda-Kazubska, B., Pawlowski, J. and Swiderski, Z. (1999). Molecular and morphological evidences for close phylogenetic affinities of the genera Macrodera, Leptophallus, Metaleptophallus and Paralepoderma (Digenea, Plagiorchioidea). Acta Parasitologica 44, 170–179.Google Scholar
Wilke, T. and Davis, G. M. (2000). Infraspecific mitochondrial sequence diversity in Hydrobia ulvae and Hydrobia ventrosa (Hydrobiidae: Rissooidea: Gastropoda): Do their different life histories affect biogeographic patterns and gene flow? Biological Journal of the Linnean Society (London) 70, 89–105.CrossRefGoogle Scholar