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Organisms Diversity & Evolution

, Volume 15, Issue 2, pp 215–233 | Cite as

New Paramecium (Ciliophora, Oligohymenophorea) congeners shape our view on its biodiversity

  • Sascha Krenek
  • Thomas U. Berendonk
  • Sergei I. Fokin
Original Article

Abstract

Paramecium is one of the best known and most intensely studied ciliate genera. It currently comprises 18 morphospecies including the P. aurelia complex of 15 sibling species. Here, we describe the new morphospecies Paramecium buetschlii sp. nov. from a freshwater pool in Norway, featuring unusual combinations of morphological characters and a high genetic diversity relative to other congeners. Three further investigated Paramecium spp. from Germany, Hungary, and Brazil are treated as cryptic species, because they are difficult to discriminate from other members of the genus relying on morphological criteria only. However, DNA-based taxonomic markers (18S-rDNA and mitochondrial COI) clearly indicate they are separate species. Due to the lack of an appropriate systematic term within the International Code of Zoological Nomenclature for distinguishing cryptic from valid biological species, we propose the provisional status Eucandidatus as a component of the taxonomic name when describing new but cryptic eukaryotes. Based on our data, we postulate that even within Europe there is a higher biodiversity within this common ciliate group that is heavily used in the classroom. By uncovering potentially distinct species that have been classified under the same species names, our molecular analyses further suggest a higher current stock diversity in Paramecium than previously thought. We also would like to emphasize that under-sampling is another major issue in estimating protist diversity. Future large-scale studies based on extensive sampling not only in exotic and remote regions, but also in less frequently sampled areas, will therefore likely improve our understanding of species richness and diversity.

Keywords

Cryptic species Molecular analysis New morphospecies Paramecium biodiversity Paramecium buetschlii 

Notes

Acknowledgments

This work was supported by a grant from the Italian Ministry of University and Research—MIUR (Ministerio Italiano dell’ Universita e della Ricerca) to S. I. Fokin and by the German Research Foundation (DFG, grant BE-2299/3-1,2,3 and BE 2299/5-1) to T. U. Berendonk, as well as by the European Commission FP7-PEOPLE-2009-IRSES project CINAR PATHOBACTER (247658) and by the BMBS COST Action BM1102. We are grateful to D. Ammermann for sampling in Porto Alegri, to Cora Baier and M. Horn for their help with 18S-rDNA sequence of “Eucandidatus P. brazilianum”, to M. Müller, who provided a possibility of our sampling at Balaton lake region and to Dana Barth for providing cells of P. buetschlii sp. nov. and DNA samples for molecular analyses. Further gratitude is expressed to two anonymous reviewers whose valuable comments allowed an essential improvement of the manuscript.

Conflict of interest

The authors have no conflict of interest to declare.

Ethical standards

All the experiments in this study comply with the current laws of the country in which they were performed and do not infringe human and animal rights.

Supplementary material

13127_2015_207_MOESM1_ESM.htm (144 kb)
Table S1 (HTM 143 kb)
13127_2015_207_MOESM2_ESM.htm (2.5 mb)
Table S2 (HTM 2602 kb)

References

  1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic Local Alignment Search Tool. Journal of Molecular Biology, 215(3), 403–410.PubMedCrossRefGoogle Scholar
  2. Aufderheide, K. J., Daggett, P. M., & Nerad, T. A. (1983). Paramecium sonneborni n. sp., a new member of the Paramecium aurelia species-complex. Journal of Protozoology, 30, 128–131.Google Scholar
  3. Baker, A. J., Daugherty, C. H., Colbourne, R., & Mclennan, J. L. (1995). Flightless brown kiwis of New Zealand possess extremely subdivided population structure and cryptic species like small mammals. Proceedings of the National Academy of Sciences of the United States of America, 92(18), 8254–8258.PubMedCentralPubMedCrossRefGoogle Scholar
  4. Barth, D., Krenek, S., Fokin, S. I., & Berendonk, T. U. (2006). Intraspecific genetic variation in Paramecium revealed by mitochondrial cytochrome c oxidase I sequences. Journal of Eukaryotic Microbiology, 53(1), 20–25.PubMedCrossRefGoogle Scholar
  5. Beale, G. H., & Preer, J. R. J. (2008). Paramecium: genetics and epigenetics. Boca Raton: CRC.CrossRefGoogle Scholar
  6. Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., et al. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22(3), 148–155.CrossRefGoogle Scholar
  7. Boscaro, V., Fokin, S. I., Verni, F., & Petroni, G. (2012). Survey of Paramecium duboscqui using three markers and assessment of the molecular variability in the genus Paramecium. Molecular Phylogenetics and Evolution, 65(3), 1004–1013.PubMedCrossRefGoogle Scholar
  8. Bouin, P. A. (1897). Etudes sur l’évolution normale et l’involution du tube seminifère. Archives d’Anatomie Microscopique et de Morphologie Expérimentale, 1, 225–339.Google Scholar
  9. Buosi, P. R. B., Cabral, A. F., Simao, T. L. L., Utz, L. R. P., & Velho, L. F. M. (2014). Multiple lines of evidence shed light on the occurrence of Paramecium (Ciliophora, Oligohymenophorea) in bromeliad tank water. Journal of Eukaryotic Microbiology, 61(1), 2–10.PubMedCrossRefGoogle Scholar
  10. Capella-Gutiérrez, S., Silla-Martínez, J. M., & Gabaldón, T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics.Google Scholar
  11. Chatton, E., & Brachon, S. (1933). Sur une paramécie à deux races: Paramœcium dubosqui n. sp. Comptes Rendus Societe Biologie, 114, 4.Google Scholar
  12. Claparède, R.-É., & Lachmann, J. (1858). Études sur les infusoires et les rhizopodes;. Genève: Vaney, H. Georg, pp. 1–482.Google Scholar
  13. Cook, L. G., Edwards, R. D., Crisp, M. D., & Hardy, N. B. (2010). Need morphology always be required for new species descriptions? Invertebrate Systematics, 24(3), 322–326.CrossRefGoogle Scholar
  14. Corliss, J. O. (1953). Silver impregnation of ciliated protozoa by the Chatton-Lwoff technic. Stain Technology, 28(2), 97–100.PubMedGoogle Scholar
  15. Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9(8), 772.PubMedCrossRefGoogle Scholar
  16. de Leon, G. P. P., & Nadler, S. A. (2010). What we don’t recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology, 96(2), 453–464.PubMedCrossRefGoogle Scholar
  17. Diller, W. F., & Earl, P. R. (1958). Paramecium jenningsi n. sp. Journal of Protozoology, 5(2), 155–158.CrossRefGoogle Scholar
  18. Dragesco, J. (1970). Ciliés libres du Cameroun. Yaoundé: Ann. Fac. Sci. Univ. Fed. Cameroun.Google Scholar
  19. Dragesco, J. (1972). Free living ciliates from Uganda. Annal Faculty Science Cameroun, 9, 87–126.Google Scholar
  20. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797.PubMedCentralPubMedCrossRefGoogle Scholar
  21. Ehrenberg, C. G. (1838). Die Infusionsthierchen als vollkommene Organismen. Ein Blick in das tiefere organische Leben der Natur. Leipzig: L. Voss.Google Scholar
  22. Fehlauer-Ale, K. H., Mackie, J. A., Lim-Fong, G. E., Ale, E., Pie, M. R., & Waeschenbach, A. (2014). Cryptic species in the cosmopolitan Bugula neritina complex (Bryozoa, Cheilostomata). Zoologica Scripta, 43(2), 193–205.CrossRefGoogle Scholar
  23. Fenchel, T., & Finlay, B. J. (2006). The diversity of microbes: resurgence of the phenotype. Philosophical Transactions of the Royal Society, B: Biological Sciences, 361(1475), 1965–1973.PubMedCentralCrossRefGoogle Scholar
  24. Focke, G .W. (1836). Ueber einige Organisationsverhältnisse bei polygastrischen Infusorien und Räderthieren. Oken. Isis, 10, 785–787.Google Scholar
  25. Foissner, W. (1991). Basic light and scanning electron microscopic methods for taxonomic studies of ciliated protozoa. European Journal of Protistology, 27(4), 313–330.PubMedCrossRefGoogle Scholar
  26. Foissner, W., Berger, H., & Schaumburg, J. (1999). Identification and ecology of limnetic plankton ciliates. München: Bayerisches Landesamt für Wasserwirtschaft, 793 pp.Google Scholar
  27. Fokin, S. I. (2010/11). Paramecium genus: biodiversity, some morphological features and the key to the main morphospecies discrimination. Protistology, 6(4), 227–235.Google Scholar
  28. Fokin, S. I., & Chivilev, S. M. (1999). Brackish water Paramecium species and Paramecium polycaryum. Morphometrical analysis and some biological peculiarities. Acta Protozoologica, 38(2), 105–117.Google Scholar
  29. Fokin, S. I., & Chivilev, S. M. (2000). Paramecium. Morphometric analysis and taxonomy. Acta Protozoologica, 39(1), 1–14.Google Scholar
  30. Fokin, S. I., Stoeck, T., & Schmidt, H. J. (1999a). Paramecium duboscqui Chatton & Brachon, 1933. Distribution, ecology and taxonomy. European Journal of Protistology, 35(2), 161–167.CrossRefGoogle Scholar
  31. Fokin, S. I., Stoeck, T., & Schmidt, H. J. (1999b). Rediscovery of Paramecium nephridiatum Gelei, 1925 and its characteristics. Journal of Eukaryotic Microbiology, 46(4), 416–426.CrossRefGoogle Scholar
  32. Fokin, S. I., Przybos, E., & Chivilev, S. M. (2001). Nuclear reorganization variety in Paramecium (Ciliophora: Peniculida) and its possible evolution. Acta Protozoologica, 40(4), 249–261.Google Scholar
  33. Fokin, S. I., Przybos, E., Chivilev, S. M., Beier, C. L., Horn, M., Skotarczak, B., et al. (2004). Morphological and molecular investigations of Paramecium schewiakoffi sp. nov. (Ciliophora, Oligohymenophorea) and current status of distribution and taxonomy of Paramecium spp. European Journal of Protistology, 40(3), 225–243.CrossRefGoogle Scholar
  34. Funk, W. C., Caminer, M., & Ron, S. R. (2011). High levels of cryptic species diversity uncovered in Amazonian frogs. Proceedings of the Royal Society B: Biological Sciences.Google Scholar
  35. Gelei, J. (1925). Uj Paramecium szeged kornyekerol. Paramecium nephridiatum nov. sp. Allat Kozlony Zoology Mitteilungen, 22, 121–162 (In Hungarian with German summary).Google Scholar
  36. Gelei, J. (1938). Beitrage zur Ciliatenfauna der Umgebung von Szeged. VII. Paramecium nephridiatum. Archiv fuer Protistenkunde, 91, 343–356.Google Scholar
  37. Goldstein, P. Z., & DeSalle, R. (2011). Integrating DNA barcode data and taxonomic practice: determination, discovery, and description. Bioessays, 33(2), 135–147.PubMedCrossRefGoogle Scholar
  38. Görtz, H. D. (Ed.). (1988). Paramecium. Berlin: Springer.Google Scholar
  39. Greczek-Stachura, M., Potekhin, A., Przybos, E., Rautian, M., Skoblo, I., & Tarcz, S. (2012). Identification of Paramecium bursaria syngens through molecular markers—comparative analysis of three loci in the nuclear and mitochondrial DNA. Protist, 163(5), 671–685.PubMedCrossRefGoogle Scholar
  40. Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52(5), 696–704.PubMedCrossRefGoogle Scholar
  41. Gustincich, S., Manfioletti, G., Del Sal, G., Schneider, C., & Carninci, P. (1991). A fast method for high-quality genomic DNA extraction from whole human blood. BioTechniques, 11(3), 298–300. 302.PubMedGoogle Scholar
  42. Hall, M. S., & Katz, L. A. (2011). On the nature of species: insights from Paramecium and other ciliates. Genetica, 139(5), 677–684.PubMedCentralPubMedCrossRefGoogle Scholar
  43. Jörger, K. M., & Schrödl, M. (2013). How to describe a cryptic species? Practical challenges of molecular taxonomy. Frontiers in Zoology, 10.Google Scholar
  44. Kadereit, G., Piirainen, M., Lambinon, J., & Vanderpoorten, M. (2012). Cryptic taxa should have names: reflections in the glasswort genus Salicornia (Amaranthaceae). Taxon, 61(6), 1227–1239.Google Scholar
  45. Kahl, A. (1935). Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 4. Peritricha und Chonotricha. (Vol. 30, Tierwelt Dtl.). Jena: G. Fischer.Google Scholar
  46. Kosakyan, A., Heger, T. J., Leander, B. S., Todorov, M., Mitchell, E. A. D., & Lara, E. (2012). COI barcoding of nebelid testate amoebae (Amoebozoa: Arcellinida): extensive cryptic diversity and redefinition of the Hyalospheniidae Schultze. Protist, 163(3), 415–434.PubMedCrossRefGoogle Scholar
  47. Krenek, S., Petzoldt, T., & Berendonk, T. U. (2012). Coping with temperature at the warm edge—patterns of thermal adaptation in the microbial eukaryote Paramecium caudatum. PLoS ONE, 7(3), e30598.PubMedCentralPubMedCrossRefGoogle Scholar
  48. Kreutz, M., Stoeck, T., & Foissner, W. (2012). Morphological and molecular characterization of Paramecium (Viridoparamecium nov. subgen.) chlorelligerum Kahl 1935 (Ciliophora). Journal of Eukaryotic Microbiology, 59(6), 548–563.PubMedCrossRefGoogle Scholar
  49. Kruskal, J. B., & Wish, M. (1978). Multidimensional scaling (Quantitative applications in the social sciences, vol. Nr. 11). Beverly Hills and London: SAGE Publications.Google Scholar
  50. Leliaert, F., Verbruggen, H., Wysor, B., & De Clerck, O. (2009). DNA taxonomy in morphologically plastic taxa: algorithmic species delimitation in the Boodlea complex (Chlorophyta: Cladophorales). Molecular Phylogenetics and Evolution, 53(1), 122–133.PubMedCrossRefGoogle Scholar
  51. Medlin, L., Elwood, H. J., Stickel, S., & Sogin, M. L. (1988). The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene, 71(2), 491–499.PubMedCrossRefGoogle Scholar
  52. Messing, J. (1983). New M13 vectors for cloning. Methods in Enzymology, 101, 20–78.PubMedGoogle Scholar
  53. Miller, M. A., Pfeiffer, W., & Schwartz, T. (2011). The CIPRES science gateway: A community resource for phylogenetic analyses. Paper presented at the Proceedings of the 2011 TeraGrid Conference: Extreme Digital Discovery, Salt Lake City, Utah.Google Scholar
  54. Miyake, A. (1968). Induction of conjugation by chemical agents in Paramecium. Journal of Experimental Zoology, 167(3), 359.PubMedCrossRefGoogle Scholar
  55. Mohammed, A. H. H., & Nashed, N. N. (1968–1969). Paramecium wichtermani n. sp. with notes on other species of Paramecium common in fresh-water bodies in the area of Cairo and its environs. Zoological Society of Egypt Bulletin, (22), 89–104.Google Scholar
  56. Müller, O. F. (1786). Animalcula infusoria fluviatilia et marina: Hauniae.Google Scholar
  57. Murray, R. G., & Schleifer, K. H. (1994). Taxonomic notes: a proposal for recording the properties of putative taxa of procaryotes. International Journal of Systematic Bacteriology, 44(1), 174–176.PubMedCrossRefGoogle Scholar
  58. Murray, R. G., & Stackebrandt, E. (1995). Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. International Journal of Systematic Bacteriology, 45(1), 186–187.PubMedCrossRefGoogle Scholar
  59. Pawlowski, J., Audic, S., Adl, S., Bass, D., Belbahri, L., Berney, C., et al. (2012). CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biology, 10(11), e1001419.PubMedCentralPubMedCrossRefGoogle Scholar
  60. Pruesse, E., Peplies, J., & Glöckner, F. O. (2012). SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics, 28(14), 1823–1829.PubMedCentralPubMedCrossRefGoogle Scholar
  61. Przybos, E., Tarcz, S., Potekhin, A., Rautian, M., & Prajer, M. (2012). A two-locus molecular characterization of Paramecium calkinsi. Protist, 163(2), 263–273.PubMedCrossRefGoogle Scholar
  62. Przybos, E., Rautian, M., Surmacz, M., & Bieliavskaya, A. (2013). New stands of species of the Paramecium aurelia complex (Ciliophora, Protista) in Russia (Siberia, Kamchatka). Folia Biologica-Krakow, 61(1–2), 41–45.CrossRefGoogle Scholar
  63. Przybos, E., Tarcz, S., Rautian, M., & Lebedeva, N. (2014). The first European stand of Paramecium sonneborni (P. aurelia complex), a species known only from North America (Texas, USA). European Journal of Protistology, 50(3), 236–247.PubMedCrossRefGoogle Scholar
  64. Powers, J. H., & Mitchell, C. (1910). A new species of Paramecium (P. multimicronucleata) experimentally determined. Biological Bulletin, 19:324–332.Google Scholar
  65. Rambaut, A. (2012). FigTree v.1.4.0. http://tree.bio.ed.ac.uk/software/figtree/.
  66. Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12), 1572–1574.PubMedCrossRefGoogle Scholar
  67. Sánchez, R., Serra, F., Tárraga, J., Medina, I., Carbonell, J., Pulido, L., et al. (2011). Phylemon 2.0: a suite of web-tools for molecular evolution, phylogenetics, phylogenomics and hypotheses testing. Nucleic Acids Research, 39(suppl 2), W470–W474.PubMedCentralPubMedCrossRefGoogle Scholar
  68. Schrallhammer, M., Fokin, S. I., Schleifer, K. H., & Petroni, G. (2006). Molecular characterization of the obligate endosymbiont “Caedibacter macronucleorum” Fokin and Görtz, 1993 and of its host Paramecium duboscqui strain Ku4-8. Journal of Eukaryotic Microbiology, 53(6), 499–506.PubMedCrossRefGoogle Scholar
  69. Shi, X. B., Jin, M. L., & Liu, G. J. (1997). Rediscovery of Paramecium duboscqui Chatton & Brachon, 1933, and a description of its characteristics. Journal of Eukaryotic Microbiology, 44(2), 134–141.CrossRefGoogle Scholar
  70. Simon, E. M., Nanney, D. L., & Doerder, F. P. (2008). The “Tetrahymena pyriformis” complex of cryptic species. Biodiversity and Conservation, 17(2), 365–380.CrossRefGoogle Scholar
  71. Skaloud, P., & Rindi, F. (2013). Ecological differentiation of cryptic species within an asexual protist morphospecies: a case study of filamentous green alga Klebsormidium (Streptophyta). Journal of Eukaryotic Microbiology, 60(4), 350–362.PubMedCrossRefGoogle Scholar
  72. Skovorodkin, I. N. (1990). A device for immobilization of biological objects in the light microscope studies. Cytologia (St. Petersburg), 32, 515–519 (in Russian with English summary).Google Scholar
  73. Sneath, P. H. A., & Sokal, R. R. (1973). Numerical taxonomy: the principles and practice of numerical classification. San Francisco: Freeman.Google Scholar
  74. Sonneborn, T. M. (1975). The Paramecium aurelia complex of fourteen sibling species. Transactions of the American Microscopical Society, 94, 155–178.Google Scholar
  75. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22(21), 2688–2690.PubMedCrossRefGoogle Scholar
  76. Stamatakis, A., Hoover, P., & Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology, 57(5), 758–771.PubMedCrossRefGoogle Scholar
  77. Stoeck, T., Welter, H., Seitz-Bender, D., Kusch, J., & Schmidt, H. J. (2000). ARDRA and RAPD-fingerprinting reject the sibling species concept for the ciliate Paramecium caudatum (Ciliophora, Protoctista). Zoologica Scripta, 29(1), 75–82.CrossRefGoogle Scholar
  78. Strüder-Kypke, M. C., & Lynn, D. H. (2010). Comparative analysis of the mitochondrial cytochrome c oxidase subunit I (COI) gene in ciliates (Alveolata, Ciliophora) and evaluation of its suitability as a biodiversity marker. Systematics and Biodiversity, 8(1), 131–148.CrossRefGoogle Scholar
  79. Strüder-Kypke, M. C., Wright, A. D. G., Fokin, S. I., & Lynn, D. H. (2000). Phylogenetic relationships of the genus Paramecium inferred from small subunit rRNA gene sequences. Molecular Phylogenetics and Evolution, 14(1), 122–130.PubMedCrossRefGoogle Scholar
  80. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729.PubMedCentralPubMedCrossRefGoogle Scholar
  81. Tarcz, S., Potekhin, A., Rautian, M., & Przybos, E. (2012). Variation in ribosomal and mitochondrial DNA sequences demonstrates the existence of intraspecific groups in Paramecium multimicronucleatum (Ciliophora, Oligohymenophorea). Molecular Phylogenetics and Evolution, 63(2), 500–509.PubMedCrossRefGoogle Scholar
  82. Tarcz, S., Przybos, E., & Surmacz, M. (2013). An assessment of haplotype variation in ribosomal and mitochondrial DNA fragments suggests incomplete lineage sorting in some species of the Paramecium aurelia complex (Ciliophora, Protozoa). Molecular Phylogenetics and Evolution, 67(1), 255–265.PubMedCrossRefGoogle Scholar
  83. Tautz, D., Arctander, P., Minelli, A., Thomas, R. H., & Vogler, A. P. (2003). A plea for DNA taxonomy. Trends in Ecology & Evolution, 18(2), 70–74.CrossRefGoogle Scholar
  84. Thomas, R. C., Willette, D. A., Carpenter, K. E., & Santos, M. D. (2014). Hidden diversity in sardines: genetic and morphological evidence for cryptic species in the Goldstripe Sardinella, Sardinella gibbosa (Bleeker, 1849). PLoS ONE, 9(1).Google Scholar
  85. Wenrich, D. H. (1928). Paramecium woodruffi nov. spec. (Ciliata). Transactions of the American Microscopical Society, 47, 256–261.Google Scholar
  86. Wichterman, R. (1953). The biology of Paramecium. New York: Blakiston.Google Scholar
  87. Wichterman, R. (1986). The biology of Paramecium (2nd ed.). New York: Plenum.CrossRefGoogle Scholar
  88. Woodruff, L. L. (1921). The structure, life history, and intrageneric relationships of Paramecium calkinsi, sp. nov. Biological Bulletin, 41, 171–180.Google Scholar
  89. Woodruff, L. L., & Spencer, H. (1923). Paramecium polycaryum, sp. nov. Proceedings of the Society for Experimental Biology and Medicine, 20, 338–339.Google Scholar
  90. Wylezich, C., Meisterfeld, R., Meisterfeld, S., & Schlegel, M. (2002). Phylogenetic analyses of small subunit ribosomal RNA coding regions reveal a monophyletic lineage of euglyphid testate amoebae (order Euglyphida). Journal of Eukaryotic Microbiology, 49(2), 108–118.PubMedCrossRefGoogle Scholar
  91. Yi, Z., Strueder-Kypke, M., Hu, X., Lin, X., & Song, W. (2014). Sampling strategies for improving tree accuracy and phylogenetic analyses: a case study in ciliate protists, with notes on the genus Paramecium. Molecular Phylogenetics and Evolution, 71, 142–148.PubMedCrossRefGoogle Scholar
  92. Zhao, Y., Gentekaki, E., Yi, Z., & Lin, X. (2013). Genetic differentiation of the mitochondrial cytochrome oxidase c subunit I gene in genus Paramecium (Protista, Ciliophora). PLoS ONE, 8(10), e77044.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2015

Authors and Affiliations

  1. 1.Institute of HydrobiologyTechnische Universität DresdenDresdenGermany
  2. 2.Department of BiologyPisa UniversityPisaItaly
  3. 3.Department of Zoology InvertebrateSt. Petersburg State UniversitySt. PetersburgRussia

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