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

Volumn 67, Issue 1, 2013, Pages 255-265

  Tarcz, Sebastian ^a   PrzyboŚ, Ewa ^a   Surmacz, Marta ^a  

^a INSTITUTE OF SYSTEMATICS AND EVOLUTION OF ANIMALS   (Poland)

Author keywords

Hybridization; Incomplete lineage sorting; Introgression; Molecular phylogeny; Paramecium aurelia species complex

Indexed keywords

MITOCHONDRIAL DNA; PROTOZOAL DNA; RIBOSOMAL SPACER DNA;

ARTICLE; BIOLOGICAL MODEL; CLASSIFICATION; DNA SEQUENCE; GENETICS; HAPLOTYPE; MOLECULAR EVOLUTION; PARAMECIUM AURELIA; PHYLOGENY;

DNA, MITOCHONDRIAL; DNA, PROTOZOAN; DNA, RIBOSOMAL SPACER; EVOLUTION, MOLECULAR; HAPLOTYPES; MODELS, GENETIC; PARAMECIUM AURELIA; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

CILIOPHORA; EUKARYOTA; PARAMECIUM AURELIA; PROTOZOA;

EID: 84875053251     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2013.01.016     Document Type: Article

References (75)

1. Allen S.L., Farrow S.W., Golembiewski P.A. Esterase variations between 14 syngens of Paramecium aurelia under axenic growth. Genetics 1973, 73:561-573.
2. Amato A., Kooistra W.H., Ghiron J.H., Mann D.G., Pröschold T., Montresor M. Reproductive isolation among sympatric cryptic species in marine diatoms. Protist 2007, 158:193-207.
3. Aufderheide K.J., Daggett P., Nerad T.A. Paramecium sonneborni n. sp. A new member of Paramecium aurelia species-complex. J. Protozool. 1983, 30:128-131.
4. Aury J.M., Jaillon O., Duret L., Noel B., Jubin C., Porcel B.M., Seguerens B., Daubin V., Anthouard V., Aiach N., Arnaiz O., Billaut A., Beisson J., Blanc I., Bouhouche K., Camara F., Duharcourt S., Guido R., Gogendeau D., Katinka M., Keller A.M., Kissmehl R., Klotz C., Koll F., Le Mouel A., Lepere G., Malinsky S., Nowacki M., Nowak J.K., Plattner H., Poulain J., Ruiz F., Serrano V., Zagulski M., Dessen P., Betermier M., Weissenbach J., Srapelli C., Schachter V., Sperling L., Meyer E., Cohen J., Wincker P. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 2006, 444:171-178.
5. Avise J.C., Ball R.M. Principles of genealogical concordance in species concepts and biological taxonomy. Oxf. Surv. Evol. Biol. 1990, 7:45-67.
6. Barth D., Krenek S., Fokin S.I., Berendonk T.U. Intraspecific genetic variation in Paramecium revealed by mitochondrial cytochrome c oxidase I sequences. J. Eukaryot. Microbiol. 2006, 53:20-25.
7. Barth D., PrzyboŚ E., Fokin S.I., Schlegel M., Berendonk T.U. Cytochrome b sequence data suggest rapid speciation within the Paramecium aurelia species complex. Mol. Phylogenet. Evol. 2008, 49:669-673.
8. Beszteri B., ács E., Medlin L. Conventional and geometric morphometric studies of valve ultrastructural variation in two closely related Cyclotella species (Bacillariophyta). Eur. J. Phycol. 2005, 40:89-103.
9. Bickford D., Lohman D.J., Sodhi N.S., Ng P.K., Meier R., Winker K., Ingram K.K., Das I. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 2007, 22:148-155.
10. Boecklen W.J., Howard D.J. Genetic analysis of hybrid zones: numbers of markers and power of resolution. Ecology 1997, 78:2611-2616.
11. Coleman A.W. Paramecium aurelia revisited. J. Eukaryot. Microbiol. 2005, 52:68-77.
12. Catania F., Würmser F., Potekhin A.A., PrzyboŚ E., Lynch M. Genetic diversity in the Paramecium aurelia species complex. Mol. Biol. Evol. 2009, 26:421-431.
13. Currat M., Ruedi M., Petit R.J., Excoffier L. The hidden side of invasions: massive introgression by local genes. Evolution 2008, 62:1908-1920.
14. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 1981, 17:368-376.
15. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
16. Feulner P.G., Kirschbaum F., Schugardt C., Ketmaier V., Tiedemann R. Electrophysiological and molecular genetic evidence for sympatrically occuring cryptic species in African weakly electric fishes (Teleostei: Mormyridae: Campylomormyrus). Mol. Phylogenet. Evol. 2006, 39:198-208.
17. Fokin, S.I., 2010/2011. Paramecium genus: biodiversity, some morphological features and the key to the main morphospecies discrimination. Protistology 6, 227-235.
18. Fokin S.I., Chivilev S.M. Brackish water Paramecium species and Paramecium polycaryum. Morphometric analysis and some biological peculiarities. Acta Protozool. 1999, 38:105-117.
19. Fokin S.I., PrzyboŚ E., Chivilev S.M., Beier C.L., Horn M., Skotarczak B., Wodecka B., Fujishima M. Morphological and molecular investigations of Paramecium schewiakoffi nov. spec. (Ciliophora, Oligohymenophorea) and current status of Paramecium distribution, and taxonomy of Paramecium spp. Eur. J. Protistol. 2004, 40:225-243.
20. Greczek-Stachura M., Pothekin A., PrzyboŚ E., Rautian M., Skoblo I., Tarcz S. Identification of Paramecium bursaria syngens through molecular markers - comparative analysis of three loci in the nuclear and mitochondrial DNA. Protist 2012, 163:671-685.
21. Grundt H.H., Kjølner S., Borgen L., Rieseberg L.H., Brochmann C. High biological species diversity in the arctic flora. Proc. Natl. Acad. Sci. USA 2006, 103:972-975.
22. Haggard B. Interspecies crosses in Paramecium aurelia (syngen 4 by syngen 8). J. Protozool. 1974, 21:152-159.
23. Hall M.S., Katz L.A. On the nature of species: insights from Paramecium and other ciliates. Genetica 2011, 139:677-684.
24. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Sci. 1999, 41:95-98.
25. Hebert P.D., Penton E.H., Burns J.M., Janzen D.H., Hallwachs W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl. Acad. Sci. USA 2004, 101:14812-14817.
26. Heckman K.L., Mariani C.L., Rasoloarison R., Yoder A.D. Multiple nuclear loci reveal patterns of incomplete lineage sorting and complex species history within western mouse lemurs (Microcebus). Mol. Phylogenet. Evol. 2007, 43:353-367.
27. Hohenlohe P.A., Amish S.J., Catchen J.M., Allendorf F.W., Luikart G. Next-generation RAD sequencing identifies thousands of SNPs for assessing hybridization between rainbow and westslope cutthroat trout. Mol. Ecol. Resour. 2011, 11(Suppl. 1):117-122.
28. Hori M., Tomikawa I., PrzyboŚ E., Fujishima M. Comparison of the evolutionary distances among syngens and sibling species of Paramecium. Mol. Phylogenet. Evol. 2006, 38:697-704.
29. Jiggins C.D., Davies N. Genetic evidence for a sibling species of Heliconius charithonia (Lepidoptera; Nymphalidae). Biol. J. Linnean Soc. 1998, 64:57-67.
30. Kizirian D., Donnelly M.A. The criterion of reciprocal monophyly and classification of nested diversity at the species level. Mol. Phylogenet. Evol. 2004, 32:1072-1076.
31. Kreutz, M., Stoeck, T., Foissner, W., 2012. Morphological and Molecular Characterization of Paramecium (Viridoparamecium nov. subgen.) chlorelligerum Kahl (Ciliophora). J. Eukaryot. Microbiol. doi: doi:10.1111/j.1550-7408.2012.00638.x.
32. Levine M. The interactions of nucleus and cytoplasm in the isolation and evolution of species of Paramecium. Evolution 1953, 7:366-385.
33. Librado P., Rozas J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
34. Mallet J. Hybridization as an invasion of the genome. Trends Ecol. Evol. 2005, 20:229-237.
35. Mallet J. Hybrid speciation. Nature 2007, 446:279-283.
36. Messenger L.A., Llewellyn M.S., Bhattacharyya T., Franzen O., Lewis M.D., Ramirez J.D., Carrasco H.J., Andersson B., Miles M.A. Multiple mitochondrial introgression events and heteroplasmy in Trypanosoma cruzi revealed by maxicircle MLST and next generation sequencing. PLoS Negl. Trop. Dis. 2012, 6:e1584.
37. Möllenbeck M. Genetic relationship of 32 cell lines of Euplotes octocarinatus species complex revealed by random amplified polymorphic DNA (RAPD) fingerprinting. Mol. Ecol. 1999, 8:1971-1979.
38. Nanney D.L., McCoy J.W. Characterization of the species of the Tetrahymena pyriformis complex. Trans. Am. Microsc. Soc. 1976, 95:664-682.
39. Nei M. Molecular Evolutionary Genetics 1987, Columbia University Press, New York.
40. Nei M., Kumar S. Molecular Evolution and Phylogenetics 2000, Oxford University Press, New York.
41. Nekrasova I.V., PrzyboŚ E., Rautian M.S., Potekhin A.A. Electrophoretic karyotype polymorphism of sibling species of the Paramecium aurelia complex. J. Eukaryot. Microbiol. 2010, 57:494-507.
42. Nowrousian M. Next-generation sequencing techniques for eukaryotic microorganisms: sequencing-based solutions to biological problems. Eukaryot. Cell. 2010, 9(9):1300-1310.
43. Page R.D.M. TreeView: an application to display phylogenetic tress on personal computers. Bioinformatics 1996, 12:357-358.
44. Pollard D.A., Iyer V.N., Moses A.M., Eisen M.B. Widespread discordance of gene trees with species tree in Drosophila: evidence for incomplete lineage sorting. PLoS Genet. 2006, 2(10):e173.
45. PrzyboŚ E., Fokin S.I. Paramecium dodecaurelia strains from Hawaii. Folia Biol. (Kraków) 2003, 51:225-226.
46. PrzyboŚ E., Prajer M., Greczek-Stachura M., Skotarczak B., Maciejewska A., Tarcz S. Genetic analysis of the Paramecium aurelia species complex (Protozoa: Ciliophora) by classical and molecular methods. Syst. Biodiv. 2007, 5:417-434.
47. PrzyboŚ E., Surmacz M. New, world-wide data on the distribution of species of the Paramecium aurelia complex (Ciliophora, Protozoa). Folia Biol. (Kraków) 2010, 58:185-188.
48. PrzyboŚ E., Tarcz S., Pothekin A., Rautian M., Prajer M. A two-locus molecular characterisation of Paramecium calkinsi. Protist 2012, 163:263-273.
49. PrzyboŚ E., Tarcz S., Prajer M., Surmacz M., Rautian M., Sawka N. Does high intraspecific variability of two genome fragments indicate a recent speciation process of Paramecium dodecaurelia (P. aurelia species complex, Ciliophora, Protozoa)?. Syst. Biodiv. 2012, 10:289-304.
50. PrzyboŚ, E., Tarcz, S., Dusi, E. 2013. New Paramecium quadecaurelia strains (P. aurelia spp. complex, Ciliophora) identified by molecular markers (rDNA and mtDNA). Eur. J. Protist. http://dx.doi.org/10.1016/j.ejop.2012.11.001.
51. Prüfer K., Munch K., Hellmann I., Akagi K., Miller J.R., Walenz B., Koren S., Sutton G., Kodira C., Winer R., Knight J.R., Mullikin J.C., Meader S.J., Ponting C.P., Lunter G., Higashino S., Hobolth A., Dutheil J., Karakoç E., Alkan C., Sajjadian S., Catacchio C.R., Ventura M., Marques-Bonet T., Eichler E.E., André C., Atencia R., Mugisha L., Junhold J., Patterson N., Siebauer M., Good J.M., Fischer A., Ptak S.E., Lachmann M., Symer D.E., Mailund T., Schierup M.H., Andrés A.M., Kelso J., Pääbo S. The bonobo genome compared with the chimpanzee and human genomes. Nature 2012, 486(7404):527-531.
52. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
53. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
54. Schmidt S.L., Ammermann D., Schlegel M., Bernhard D. Stylonychia lemnae strains from a north American site differ in a single nucleotide within the small subunit rDNA from Eurasian strains. J. Eukaryot. Microbiol. 2006, 53:308-309.
55. Schwenk K., Brede N., Streit B. Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals. Phil. Trans. R. Soc. B. 2008, 363:2805-2811.
56. Smirnov A.V. Cryptic freshwater amoeba species in the bottom sediments of Nivå Bay (Øresund, Baltic Sea). Eur. J. Protistol. 2007, 2:87-94.
57. Sonneborn T.M. Sex, sex inheritance, and sex determination in Paramecium aurelia. Proc. Natl. Acad. Sci. 1937, 23:278-395.
58. Sonneborn T.M. A non-conformist genetic system in Paramecium aurelia. (Abstr.). Am. Zool. 1966, 6:589.
59. Sonneborn T.M. Methods in Paramecium research. Methods Cell Physiol, vol. 4 1970, 242-339. Academic Press, New York, London. D.M. Prescott (Ed.).
60. Sonneborn, T.M., 1974. Paramecium aurelia, in: King, R.C. (Ed.), Handbook of Genetics. vol. 2. Plenum Press, New York, pp. 469-594.
61. Sonneborn T.M. The Paramecium aurelia complex of fourteen sibling species. Trans. Am. Micros. Soc. 1975, 94:155-178.
62. Stoeck T., PrzyboŚ E., Schmidt H.J. Combination of genetics with inter-and intra-strain crosses and RAPD-fingerprints reveals different population structures within the Paramecium aurelia species complex. Eur. J. Protistol. 1998, 34:348-355.
63. Stoeck T., PrzyboŚ E., Kusch J., Schmidt H.J. Intra-species differentation and level of inbreeding of different sibling species of the Paramecium aurelia complex. Acta Protozool. 2000, 39:15-22.
64. Stoeck T., Welter H., Seitz-Bender D., Kusch J., Schmidt H.J. ARDRA and RAPD-fingerprinting reject the sibling species concept for the ciliate Paramecium caudatum (Ciliophora, Protoctista). Zool. Scripta 2000, 29:75-82.
65. Strüder-Kypke M.C., Wright A.-D.G., Fokin S.I., Lynn D.H. Phylogenetic relationships of the genus Paramecium inferred from small subunit rRNA sequences. Mol. Phylogenet. Evol. 2000, 14:122-130.
66. Strüder-Kypke M.C., Lynn D.L. Comparative analysis of the mitochondrial cytochrome c oxidase subunit I (COI) gene in ciliates (Alveolata, Ciliophpra) and evaluation of its suitability as a biodiversity marker. Syst. Biodiv. 2010, 8:131-148.
67. Tait A. Enzyme variation between syngens in Paramecium aurelia. Biochem. Genet. 1970, 4:461-470.
68. Tamura K., Nei M., Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Nat. Acad. Sci. USA 2004, 101:11030-11035.
69. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
70. Tarcz S., PrzyboŚ E., Prajer M., Greczek-Stachura M. Intraspecific variation of diagnostic rDNA genes in Paramecium dodecaurelia, P. tredecaurelia and P. quadecaurelia (Ciliophora: Oligohymenophorea). Acta Protozool. 2006, 45:255-263.
71. Tarcz S., Pothekin A., Rautian M., PrzyboŚ E. Variation in ribosomal and mitochondrial DNA sequences demonstrates the existence of intraspecific groups in Paramecium multimicronucleatum (Ciliophora, Oligohymenophorea). Mol. Phylogenet. Evol. 2012, 63:500-509.
72. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific penalties and weight matrix choice. Nucl. Acids Res. 1994, 22:4673-4680.
73. Twyford A.D., Ennos R.A. Next-generation hybridization and introgression. Heredity 2012, 108:179-189.
74. Vähä J.P., Primmer C.R. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol. Ecol. 2006, 15:63-72.
75. Willyard A., Cronn R., Liston A. Reticulate evolution and incomplete lineage sorting among the ponderosa pines. Mol. Phylogenet. Evol. 2009, 52:498-511.