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Type: Articles
Published: 2011-08-17
Page range: 19-36
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DNA barcoding and integrative taxonomy of Macrobiotus hufelandi C.A.S. Schultze 1834, the first tardigrade species to be described, and some related species

Department of Biology, University of Modena and Reggio Emilia, Via Campi 213/D, 41125 Modena, Italy
Department of Biology, University of Modena and Reggio Emilia, Via Campi 213/D, 41125 Modena, Italy
Department of Biology, University of Modena and Reggio Emilia, Via Campi 213/D, 41125 Modena, Italy
Department of Biology, University of Modena and Reggio Emilia, Via Campi 213/D, 41125 Modena, Italy
Tardigrada tardigrades Macrobiotus sandrae Macrobiotus vladimiri DNA cox1

Abstract

Within the framework of a DNA barcoding project on tardigrade species, a study was carried out on Macrobiotus hufelandi C.A.S. Schultze 1834, the first formally described tardigrade species. We used samples collected from the type locality and additional material from other European sites containing species of the “M. hufelandi group”. The study was performed by integrating morphological, karyological and molecular (mt-DNA cox1) information and comparing these data with morphological data from the type material. Several species from this group were found in the type locality of M. hufelandi (near Freiburg, Black Forest, Germany) and these were all barcoded. One was M. hufelandi, the other two were: Macrobiotus sandrae Bertolani & Rebecchi 1993 (originally described from the same locality), and Macrobiotus vladimiri Bertolani, Biserov, Rebecchi & Cesari in press (type locality Andalo, Italy), all with interspecific genetic distances of more than 19%. A fourth cryptic species, which had the same morphology as M. hufelandi but a genetic distance of 6.7%, was not described as a new taxon but named M. cf. hufelandi sp.1 for this study. Macrobiotus sandrae and M. vladimiri were also present (and barcoded) in Italy (Alps). Additional individuals (animals and eggs) were also found, and barcoded, in Italy (Apennines) and Switzerland that belonged to the haplogroup Macrobiotus cf. hufelandi sp. 1. These data together with other recent studies on tardigrade DNA barcoding represent a starting point for further studies on tardigrade biogeography, phylogeography and diversity.

References

  1. Barrett, R.D.H., & Hebert, P.D.N. (2005) Identifying spiders through DNA barcodes. Canadian Journal of Zoology, 83, 487–491.

    Bertolani, R. (1973) Presenza di un biotipo partenogenetico e suo effetto sul rapporto-sessi in Macrobiotus hufelandi (Tardigrada). Atti dell’Accademia Nazionale dei Lincei, Rendiconti, Serie 8a, 54, 469–473.

    Bertolani, R. (1975) Cytology and systematics in Tardigrada. Memorie dell’Istituto Italiano di Idrobiologia, 32 Suppl., 17–35.

    Bertolani, R. (1982) Cytology and reproductive mechanisms in tardigrades. In: D.R. Nelson (Ed.), Proceedings of the 3rd International Symposium on the Tardigrada, East Tennessee State University Press, Johnson City, Tennessee, pp. 93–114.

    Bertolani, R., Biserov, V.I., Rebecchi, L. & Cesari, M. (accepted) Taxonomy and biogeography of tardigrades using an integrated approach: new results on species of the Macrobiotus hufelandi group. Invertebrate Zoology, in press.

    Bertolani, R. & Rebecchi, L. (1993) A revision of the Macrobiotus hufelandi group (Tardigrada, Macrobiotidae), with some observations on the taxonomic characters of eutardigrades. Zoologica Scripta, 22, 127–152.

    Bertolani, R. & Rebecchi, L (1996) The tardigrades of Emilia (Italy). II. Monte Rondinaio. A multihabitat study on a high altitude valley of the Northern Apennines. Zoological Journal of the Linnean Society, 116, 3–12.

    Bertolani, R., Rebecchi, L. & Cesari, M. (2010) A model study for tardigrade identification. In: P.L. Nimis & R. Vignes Lebbe (Eds.), Tools for Identifying Biodiversity: Progress and Problems, EUT, Trieste, Italy, pp. 333–339.

    Biserov, V.I. (1990a). On the revision of the genus Macrobiotus. The subgenus Macrobiotus s. str.: a new systematic status of the group hufelandi (Tardigrada, Macrobiotidae). Communication 1. Zoologichesky Zhurnal, 69, 5–17 [in Russian].

    Biserov, V.I. (1990b) On the revision of the Macrobiotus genus. The subgenus Macrobiotus s. str. is a new taxonomic status of the hufelandi group (Tardigrada, Macrobiotidae). Communication 1. Zoologichesky Zhurnal, 69, 38–50 [in Russian].

    Casiraghi, M., Labra, M., Ferri, E, Galimberti, A. & De Mattia, F. (2010) DNA barcoding: theoretical aspects and practical applications. In: P.L. Nimis & R. Vignes Lebbe (Eds.), Tools for Identifying Biodiversity: Progress and Problems, EUT, Trieste, Italy, pp. 269–273.

    Cesari, M., Bertolani, R., Rebecchi, L. & Guidetti, R. (2009) DNA barcoding in Tardigrada: the first case study on Macrobiotus macrocalix Bertolani & Rebecchi 1993 (Eutardigrada, Macrobiotidae). Molecular Ecology Resources, 9, 699–706.

    Clement, M., Posada, D. & Crandall, K. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1660.

    DeSalle, R., Egan, M.G. & Siddall, M. (2005). The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society B, 360, 1905–16.

    Doyère, M. (1840) Mémoire sur les Tardigrades. Chapitre I. Annales Sciences Naturelles, Série 2°, Zoologie, 14, 269–361.

    Excoffier, L., Laval G. & Schneider S. (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.

    Faurby, S., Jönsson, K.I., Rebecchi, L. & Funch, P. (2008) Variation in anhydrobiotic survival of two eutardigrade morphospecies: a story of cryptic species and their dispersal. Journal of Zoology, London, 275, 39–145.

    Ferri, E., Barbuto, M., Bain, O., Galimberti, A., Uni, S., Guerriero, R., Ferté, H., Bandi, C., Martin, C. & Casiraghi, M. (2009) Integrated taxonomy: traditional approach and DNA barcoding for the identification of filarioid worms and related parasites (Nematoda). Frontiers of Zoology, 6, 1.

    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.

    Guidetti, R., Gandolfi, A., Rossi, V. & Bertolani, R. (2005) Phylogenetic analysis in Macrobiotidae (Eutardigrada, Parachela): a combined morphological and molecular approach. Zoologica Scripta, 34, 235–244.

    Guidetti, R., Rebecchi, L. & Bertolani, R. (2000) Cuticle structure and systematics of the Macrobiotidae (Tardigrada, Eutardigrada). Acta Zoologica, 81, 27–36.

    Guil, N. & Giribet, G. (2009) Fine scale population structure in the Echiniscus blumi-canadensis series (Heterotardigrada, Tardigrada) in an Iberian mountain range - When morphology fails to explain genetic structure. Molecular Phylogenetics and Evolution, 1, 606–613.

    Hajibabei, M., Janze, D.H., Burns, J.M., Hallwachs, W. & Hebert, P.D.N. (2006) DNA barcodes distinguish species of tropical Lepidoptera. PNAS, 103, 968–971.

    Hebert, P.D.N., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Biological Sciences Series B, 270, 313–21.

    Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S. & Francis, T.M. (2004) Identification of birds through DNA barcodes. PLoS Biology, 2, e312.

    International Code of Zoological Nomenclature. 1999. - 4.ed. - London: International trust for zoological nomenclature, - xxix, pp. 306.

    Jørgensen, A., Møbjerg, N. & Kristensen, R.M. (2007) A molecular study of the tardigrade Echiniscus testudo (Echiniscidae) reveals low DNA sequence diversity over a large geographical area. Journal of Limnology, 66 (Suppl. 1), 77–83.

    Lefébure, T., Douady, C.J., Gouy, M., & Gibert, J., (2006) Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution, 40, 435–47.

    McInnes, S.J. (1994) Zoogeographic distribution of terrestrial/freshwater tardigrades from current literature. Journal of Natural History, 28, 257–352.

    Meyer, C.P. & Paulay, G. (2005) DNA Barcoding: error rates based on comprehensive sampling. PLoS Biology, 3, e422.

    Moritz, C. & Cicero, C. (2004) DNA barcoding: promise and pitfalls. PLoS Biology, 2, e354.

    Pleijel, F., Jondelius, U., Norlinder, E., Nygren, A., Oxelman, B., Schander, C., Sundberg, P. & Thollesson, M. (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution, 48, 369–371.

    Schill, R.O., Förster, F., Dandekar, T. & Wolf, M. (2010) Using compensatory base change analysis of internal transcribed spacer 2 secondary structures to identify three new species in Paramacrobiotus (Tardigrada). Organisms Diversity & Evolution, 10, 287–296.

    Schultze, C.A.S. (1834) Macrobiotus Hufelandii animal e crustaceorum classe novum, reviviscendi post diuturnam asphyxian et ariditaten potens, etc. 8 Seiten, 1 tab. C. Curths, Berlin, 6 pp, I Table.

    Shearer, T.L. & Coffroth, M.A. (2008). Barcoding corals: limited by interspecific divergence, not intraspecific variation. Molecular Ecology Resources, 8:247–255.

    Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) Mega 4: molecular evolutionary genetics analysis (mega), software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

    Teacher, A.G.F. & Griffiths, D.J. (2011) HapStar: automated haplotypes network layout and visualization. Molecular Ecology Resources, 11, 151–153.

    Templeton, A.R., Crandall, K.A. & Sing, C.F. (1992) A cladistic analysis of phenotypic association with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–633.

    Vences, M., Thomas, M., Bonett, R.M. & Vieites, D.R. (2005) Deciphering amphibian diversity through DNA barcoding: chances and challenges. Philosophical Transactions of The Royal Society B: Biological Sciences, 360, 1859–1868.

    Ward, R.D., Holmes, B.H. & O’Hara, T. (2008) DNA barcoding discriminates echinoderm species. Molecular Ecology Resources, 8, 1202–1211

    Ward, R.D., Zemlak, T.S., Innes, B.H. & Hebert, P.D.N. (2005) DNA barcoding Australia’s fish species. Philosophical Transactions of The Royal Society B: Biological Sciences, 360, 1847–1857.

    Weigand, A.M., Jochum, A., Pfenninger, M. Steinke, D. & Klussman-Kolb A. (2011) A new approach to an old conundrum—DNA barcoding sheds new light on phenotypic plasticity and morphological stasis in microsnails (Gastropoda, Pulmonata, Carychiidae). Molecular Ecology Resources, 11, 255–265).

    Wiemers, M. & Fiedler, K. (2007) Does the DNA barcoding gap exists? – a case study in blue butterflies (Lepidoptera: Lycaenidae). Frontiers in Zoology, 4, 8.

    Will, K.W., Mishler, B.D. & Wheeler, Q.D. (2005) The perils of DNA barcoding and the need of integrative taxonomy. Systematic Biology, 54, 844–851.

    Will, K.W. & Rubinoff, D. (2004) Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics, 20, 47–55.