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The incongruence of nuclear and mitochondrial DNA variation supports conspecificity of the monogenean parasites Gyrodactylus salaris and G. thymalli

  • H. HANSEN (a1), L. MARTINSEN (a1), T. A. BAKKE (a1) and L. BACHMANN (a1)

The monogenean Gyrodactylus salaris Malmberg, 1957 is an economically important parasite on Atlantic salmon whereas the morphologically very similar G. thymalli Žitňan, 1960 on grayling is considered harmless. Even molecular markers cannot unambiguously discriminate both species. The nuclear internal transcribed spacer (ITS) sequences are identical in both species, and although mitochondrial cytochrome oxidase I (COI) sequences show substantial variation, no support for monophyly of either species is found. Analysis of nucleotide sequences of the intergenic spacer (IGS) have, however, been interpreted as support for 2 species. Here, IGS and COI sequences from 81 G. salaris and G. thymalli specimens of 39 populations across the species' distribution range were determined. Mitochondrial diversity was not reflected in the nuclear marker. Since various 23 bp IGS repeat types usually differ by just one nucleotide and sequences primarily differ in the number and order of repeat types, alignments may be biased and arbitrary, impeding meaningful phylogenetic analyses. The hypothesis that parasites on rainbow trout represent hybrids of both species is rejected. The presence or absence of particular repeat types is not considered informative. We interpret the IGS data as support for G. salaris and G. thymalli being a single species.

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Bakke, T. A., Harris, P. D. and Cable, J. ( 2002). Host specificity dynamics: observations on gyrodactylid monogeneans. International Journal for Parasitology 32, 281308. DOI:10.1016/S0020-7519(01)00331-9.
Bakke, T. A., Jansen, P. A. and Hansen, L. P. ( 1990). Differences in the host resistance of Atlantic salmon, Salmo salar L., stocks to the monogenean Gyrodactylus salaris Malmberg, 1957. Journal of Fish Biology 37, 577587. DOI:10.1111/j.1095-8649.1990.tb05890.x.
Bakke, T. A., Jansen, P. A. and Harris, P. D. ( 1996). Differences in susceptibility of anadromous and resident stocks of Arctic charr to infections of Gyrodactylus salaris under experimental conditions. Journal of Fish Biology 49, 341351.
Buchmann, K., Lindenstrøm, T., Nielsen, M. E. and Bresciani, J. ( 2000). Diagnostik og forekomst af ektoparasitinfeksjoner (Gyrodactylus spp.) hos danske laksefisk. Dansk Veterinærtidskrift 83, 1519 (In Danish).
Collins, C. M. and Cunningham, C. O. ( 2000). Characterization of the Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes: Monogenea) ribosomal intergenic spacer (IGS) DNA. Parasitology 121, 555563. DOI:10.1017/S0031182099006770.
Cunningham, C. O., Collins, C. M., Malmberg, G. and Mo, T. A. ( 2003). Analysis of ribosomal RNA intergenic spacer (IGS) sequences in species and populations of Gyrodactylus (Platyhelminthes: Monogenea) from salmonid fish in northern Europe. Diseases of Aquatic Organisms 57, 237246.
Cunningham, C. O., Mo, T. A., Collins, C. M., Buchmann, K., Thiery, R., Blanc, G. and Lautraite, A. ( 2001). Redescription of Gyrodactylus teuchis Lautraite, Blanc, Thiery, Daniel & Vigneulle, 1999 (Monogenea: Gyrodactylidae); a species identified by ribosomal RNA sequence. Systematic Parasitology 48, 141150.
Dover, G. A. ( 1982). Molecular drive: a cohesive mode of species evolution. Nature, London 299, 111116.
Ergens, R. ( 1983). Gyrodactylus from Eurasian freshwater Salmonidae and Thymallidae. Folia Parasitologica 30, 1526.
Hansen, H., Bachmann, L. and Bakke, T. A. ( 2003). Mitochondrial DNA variation of Gyrodactylus spp. (Monogenea, Gyrodactylidae) populations infecting Atlantic salmon, grayling and rainbow trout in Norway and Sweden. International Journal for Parasitology 33, 14711478. DOI:10.1016/S0020-7519(03)00200-5.
Johnsen, B. O. and Jensen, A. J. ( 1991). The Gyrodactylus story in Norway. Aquaculture 98, 289302. DOI:10.1016/0044-8486(91)90393-L.
Johnsen, B. O., Møkkelgjerd, P. I. and Jensen, A. J. ( 1999). Parasitten Gyrodactylus salaris på laks i norske vassdrag, statusrapport ved inngangen til år 2000. In NINA Oppdragsmelding Vol. 617 pp. 1129 (In Norwegian).
Kimura, M. ( 1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.
Koski, P. and Malmberg, G. ( 1995). Occurrence of Gyrodactylus (Monogenea) on salmon and rainbow trout in fish farms in Northern Finland. Bulletin of the Scandinavian Society for Parasitology 5, 7688.
Koskinen, M. T., Ranta, E., Piironen, J., Veselov, A., Titov, S., Haugen, T. O., Nilsson, J., Carlstein, M. and Primmer, C. R. ( 2000). Genetic lineages and postglacial colonization of grayling (Thymallus thymallus, Salmonidae) in Europe, as revealed by mitochondrial DNA analyses. Molecular Ecology 9, 16091624. DOI:10.1046/j.1365-294x.2000.01065.x.
Kumar, S., Tamura, K. and Nei, M. ( 2004). MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150163. DOI:10.1093/bib/5.2.150.
Lindenstrøm, T., Collins, C. M., Bresciani, J., Cunningham, C. O. and Buchmann, K. ( 2003). Characterization of a Gyrodactylus salaris variant: infection biology, morphology and molecular genetics. Parasitology 127, 165177. DOI:10.1017/S003118200300341X.
Malmberg, G. ( 1957). Om förekomsten av Gyrodactylus på svenska fiskar, Skrifter utgivna av Södra Sveriges Fiskeriförening, Årsskrift (1957).
Malmberg, G. and Malmberg, M. ( 1993). Species of Gyrodactylus (Platyhelminthes, Monogenea) on salmonids in Sweden. Fisheries Research 17, 5968. DOI:10.1016/0165-7836(93)90007-T.
Matejusová, I., Gelnar, M., Mcbeath, A. J. A., Collins, C. M. and Cunningham, C. O. ( 2001). Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology 31, 738745. DOI:10.1016/S0020-7519(01)00176-X.
McHugh, E. S., Shinn, A. P. and Kay, J. W. ( 2000). Discrimination of the notifiable pathogen Gyrodactylus salaris from G. thymalli (Monogenea) using statistical classifiers applied to morphometric data. Parasitology 121, 315323. DOI:10.1017/S0031182099006381.
Meinilä, M., Kuusela, J., Ziętara, M. S. and Lumme, J. ( 2002). Primers for amplifying ~820 bp of highly polymorphic mitochondrial COI gene of Gyrodactylus salaris. Hereditas 137, 7274. DOI:10.1034/j.1601-5223.2002.1370110.x.
Meinilä, M., Kuusela, J., Ziętara, M. S. and Lumme, J. ( 2004). Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae). International Journal for Parasitology 34, 515526. DOI:10.1016/j.ijpara.2003.12.002.
Schneider, S., Roessli, D. and Excoffier, L. ( 2000). Arlequin: a Software for Population Genetics Data Analysis. Genetics and Biometry Laboratory, Department of Anthropology, University of Geneva, Geneva.
Shinn, A. P., Gibson, D. I. and Sommerville, C. ( 2001). Morphometric discrimination of Gyrodactylus salaris Malmberg (Monogenea) from species of Gyrodactylus parasitising British salmonids using novel parameters. Journal of Fish Diseases 24, 8397. DOI:10.1046/j.1365-2761.2001.00272.x.
Shinn, A. P., Hansen, H., Olstad, K., Bachmann, L. and Bakke, T. A. ( 2004). The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea). Folia Parasitologica 51, 239252.
Shinn, A. P., Kay, J. W. and Sommerville, C. ( 2000). The use of statistical classifiers for the discrimination of species of the genus Gyrodactylus (Monogenea) parasitizing salmonids. Parasitology 120, 261269. DOI:10.1017/S0031182099005454.
Soleng, A. and Bakke, T. A. ( 2001). The susceptibility of grayling, Thymallus thymallus to experimental infections with the monogenean Gyrodactylus salaris. International Journal for Parasitology 31, 793797. DOI:10.1016/S0020-7519(01)00188-6.
Sterud, E., Mo, T. A., Collins, C. M. and Cunningham, C. O. ( 2002). The use of host specificity, pathogenicity, and molecular markers to differentiate between Gyrodactylus salaris Malmberg, 1957 and G. thymalli Žitňan, 1960 (Monogenea: Gyrodactylidae). Parasitology 124, 203213. DOI:10.1017/S0031182001001044.
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 24, 48764882. DOI:doi:10.1093/nar/25.24.4876.
Weiss, S., Persat, H., Eppe, R., Schlötterer, C. and Uiblein, F. ( 2002). Complex patterns of colonization and refugia revealed for European grayling Thymallus thymallus, based on complete sequencing of the mitochondrial DNA control region. Molecular Ecology 11, 13931407. DOI:10.1046/j.-1365-294X.2002.01544.x.
Zentgraf, U., Ganal, M. and Hemleben, V. ( 1990). Length heterogeneity of the rRNA precursor in cucumber (Cucumis sativus). Plant Molecular Biology 15, 465474. DOI:10.1007/BF00019163.
Zentgraf, U. and Hemleben, V. ( 1992). Complex formation of nuclear proteins with the RNA polymerase I promoter and repeated elements in the external transcribed spacer of Cucumis sativus ribosomal DNA. Nucleic Acids Research 20, 36853691. DOI:10.1093/nar/20.14.3693.
Ziętara, M. S., Huyse, T., Lumme, J. and Volckaert, F. A. M. ( 2002). Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. Parasitology 124, 3952. DOI:10.1017/S0031182001008939.
Ziętara, M. S. and Lumme, J. ( 2002). Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea: Gyrodactylidae). Evolution 56, 24452458. DOI:10.1554/0014-3820(2002)056[2445:SBHSAA]2.0.CO;2.
Ziętara, M. S. and Lumme, J. ( 2004). Comparison of molecular phylogeny and morphological systematics in fish parasite genus Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae). Zoologica Poloniae 49, 528.
Žitňan, R. ( 1960). Gyrodactylus thymalli sp. nov. aus den Flossen der Äsche (Thymallus thymallus). Helminthologia 2, 266269 (In German, English summary).
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