Fottea 2021, 21(1):62-72 | DOI: 10.5507/fot.2020.017

A time-calibrated multi-gene phylogeny provides insights into the evolution, taxonomy and DNA barcoding of the Pinnularia gibba group (Bacillariophyta)

Jan Kollár1, *, Eveline Pinseel2, 3, Wim Vyverman2, Aloisie Poulíčková1
1 Department of Botany, Faculty of Science, Palacký University Olomouc, Šlechtitelů 27, CZ-78371 Olomouc, CZ; *Corresponding author e-mail: jan.kollar@upol.cz
2 Laboratory of Protistology and Aquatic Ecology, Department of Biology, Faculty of Science, Ghent University, Krijgslaan 281 - S8, 9000 Gent, BE
3 Research Department, Meise Botanic Garden, Nieuwelaan 38, 1860 Meise, BE
+ Current working address: Department of Biological Sciences, University of Arkansas, 850 W. Dickson St., Fayetteville AR 72701-1201, USA

Many diatom groups are known for widespread (pseudo)cryptic species diversity and Pinnularia gibba group is one of them. Recently, Kollár et al. (2019) delimited species within the group by means of a polyphasic approach, providing an evidence for the existence of fifteen species. In order to further guide the systematic revision of the group, the present study focuses on the evolution and morphology of the P. gibba group. Using representatives of the fifteen species we used fossils to constrain and calibrate a multi-gene species-level phylogeny. Although many species are morphologically highly similar, significant differences in cell size were detected in different sections of the tree, suggestive of ongoing morphological differentiation. We further used the phylogenetic analysis to assess marker resolution for DNA barcoding, showing that the proposed diatom barcode markers rbcL and V4 SSU rDNA can distinguish closely related (pseudo)cryptic species of the group.

Keywords: cryptic species, diatoms, subgibba group, molecular phylogenetics, molecular clocks, species complex

Received: April 15, 2020; Accepted: November 5, 2020; Prepublished online: March 2, 2021; Published: April 1, 2021  Show citation

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Kollár, J., Pinseel, E., Vyverman, W., & Poulíčková, A. (2021). A time-calibrated multi-gene phylogeny provides insights into the evolution, taxonomy and DNA barcoding of the Pinnularia gibba group (Bacillariophyta). Fottea, 21(1), 62-72. doi: 10.5507/fot.2020.017
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    References

    1. Abarca, N.; Jahn, R.; Zimmermann, J. & Enke, N. (2014): Does the cosmopolitan diatom Gomphonema parvulum (Kützing) Kützing have a biogeography? - PLoS ONE 9:1-18. Go to original source...
    2. Adl, S.M.; Leander, B.S.; Simpson, A.G.B.; Archibald, J.M.; Anderson, O.R.; Bass, D.; Bowser, S.S.; Brugerolle, G.; Farmer, M.A.; Karpov, S.; Kolisko, M.; Lane, C.E.; Lodge, D.J.; Mann, D.G.; Meisterfeld, R.; Mendoza, L.; Moestrup, Ø.; Mozley-Standridge, S.E.; Smirnov, A.V. & Spiegel, F. (2007): Diversity, nomenclature, and taxonomy of protists. - Syst. Biol. 56:684-689. Go to original source...
    3. Amato, A.; Kooistra, W.H.C.F. & Montresor, M. (2019): Cryptic Diversity: a Long-lasting Issue for Diatomologists. - Protist 170:1-7. Go to original source...
    4. Andersen, R.A. (1992): Diversity of eukaryotic algae. - Biodivers. Conserv. 1:267-292. Go to original source...
    5. Atkinson, K.M. (1972): Birds as transporters of algae. - Br. Phycol. J. 7:319-321. Go to original source...
    6. Atkinson, K.M. (1980): Experiments in dispersal of phytoplankton by ducks. - Br. Phycol. J. 15:49-58. Go to original source...
    7. Bock, C.; Chatzinotas, A. & Boenigk, J. (2017): Genetic diversity in chrysophytes: Comparison of different gene markers. - Fottea 17:209-221. Go to original source...
    8. Bofkin, L. & Goldman, N. (2007): Variation in evolutionary processes at different codon positions. - Mol. Biol. Evol. 24:513-521. Go to original source...
    9. Bouckaert, R.; Vaughan, T.G.; Barido-Sottani, J.; Duchêne, S.; Fourment, M.; Gavryushkina, A.; Heled, J.; Jones, G.; Kühnert, D.; De Maio, N.; Matschiner, M.; Mendes, F.K.; Müller, N.F.; Ogilvie, H.A.; du Plessis, L.; Popinga, A.; Rambaut, A.; Rasmussen, D.; Siveroni, I.; Suchard, M.A.; Wu, C.H.; Xie, D.; Zhang, C.; Stadler, T. & Drummond, A.J. (2019): BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. - PLoS Comput. Biol. 15:1-28. Go to original source...
    10. Callahan, B.J.; McMurdie, P.J.; Rosen, M.J.; Han, A.W.; Johnson, A.J.A. & Holmes, S.P. (2016): DADA2: High-resolution sample inference from Illumina amplicon data. - Nat. Methods. 13:581-583. Go to original source...
    11. Castresana, J. (2000): Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis. - Mol. Biol. Evol. 17:240-552. Go to original source...
    12. Christenhusz, M.J.M. & Byng, J.W. (2016): The number of known plants species in the world and its annual increase. - Phytotaxa 261:201-217. Go to original source...
    13. Connolly, J.A.; Oliver, M.J.; Beaulieu, J.M.; Knight, C.A.; Tomanek, L. & Moline, M.A. (2008): Correlated evolution of genome size and cell volume in diatoms (Bacillariophyceae). - J. Phycol. 44:124-131. Go to original source...
    14. Cox, E.J. (2009): What's in a name? - Diatom classification should reflect systematic relationships. - Acta Bot.Croat. 68:443-454.
    15. Croll, D.A. & Holmes, R.W. (1982): A Note on the Occurrence of Diatoms on the Feathers of Diving Seabirds. - Auk. 99:765-766. Go to original source...
    16. Drum, R.W. & Gordon, R. (2003): Star Trek replicators and diatom nanotechnology. - Trends Biotechnol. 21:325-328. Go to original source...
    17. Edgar, R.C. (2004): MUSCLE: multiple sequence alignment with improved accuracy and speed. - Proceedings. 2004 IEEE Comput. Syst. Bioinforma. Conf. 2004. CSB 2004. 689-690.
    18. Edgar, R.C. (2016): UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. - bioRxiv. 81257. DOI: https://doi.org/10.1101/081257. Go to original source...
    19. Ehrenberg, C.G. (1843a): Mittheilungen über 2 neue asiatische Lager fossiler Infusorien-Erden aus dem russischen Trans-Kaukasien (Grusien) und Sibirien. - Bericht über die zur Bekanntmachung geeigneten Verhandlungen der Königlich-Preussischen Akad. der Wissenschaften zu Berlin: 43-49.
    20. Ehrenberg, C.G. (1843b): Verbreitung und Einfluss des mikroskopischen Lebens in Süd- und Nord-Amerika. - Abhandlungen der Königlichen Akademie der Wissenschaften zu Berlin 1841: 466 pp.
    21. Elwood, H.J.; Olsen, G.J. & Sogin, M.L. (1985): The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. - Mol. Biol. Evol. 2: 399-410.
    22. Fijn, R.C.; Hiemstra, D.; Phillips, R.A. & van der Winden, J. (2013): Arctic Terns Sterna paradisaea from the Netherlands Migrate Record Distances Across Three Oceans to Wilkes Land, East Antarctica. - Ardea 101: 3-12. Go to original source...
    23. Finkel, Z.V.; Katz, M.E.; Wright, J.D.; Schofield, O.M.E. & Falkowski, P.G. (2005): Climatically driven macroevolutionary patterns in the size of marine diatoms over the Cenozoic. - Proc. Natl. Acad. Sci. U. S. A. 102: 8927-8932. Go to original source...
    24. Guillou, L.; Medlin, L.K.; Oce, O. & Vaulot, D. (1999): Bolidomonas: A new genus with two species belonging to a new algal class, the Bolidophyceae (Heterokonta). - J. Phycol. 35: 368-381. Go to original source...
    25. Gunderson, J.H.; McCutchan, T.F. & Sogin, M.L. (1986): Sequence of the Small Subunit Ribosomal RNA Gene Expressed in the Bloodstream Stages of Plasmodium berghei: Evolutionary Implications. - J. Protozool. 33: 525-529. Go to original source...
    26. Hall, K.; Meiklejohn, I. & Bumby, A. (2011): Marion Island volcanism and glaciation. - Antarct. Sci. 23: 155-163. Go to original source...
    27. Hamsher, S.E.; Evans, K.M.; Mann, D.G.; Poulíčková, A. & Saunders, G.W. (2011): Barcoding diatoms: Exploring alternatives to COI-5P. - Protist 162: 405-422. Go to original source...
    28. Hartmann, D.L. (2015): Global physical climatology (2nd ed.). - 498 pp., Newnes, Boston.
    29. Hasegawa, M.; Kishino, H. & Yano, T. (1985): Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. - J. Mol. Evol. 22: 160-174. Go to original source...
    30. Hebert, P.D.N.; Cywinska, A.; Ball, S.L. & deWaard, J.R. (2003): Biological identifications through DNA barcodes. - Proc. R. Soc. B Biol. Sci. 270: 313-321. Go to original source...
    31. Hu, Q.; Sommerfeld, M.; Jarvis, E.; Ghirardi, M.; Posewitz, M.; Seibert, M. & Darzins, A. (2008): Microalgal triacylglycerols as feedstocks for biofuel production: Perspectives and advances. - The Plant J. 54: 621-639. Go to original source...
    32. Kelly, M.; Boonham, N.; Juggins, S.; Kille, P.; Mann, D.G.; Pass, D.; Sapp, M.; Shinya, S. & Glover, R. (2018): A DNA based diatom metabarcoding approach for Water Framework Directive classification of rivers. - Science Report SC140024/R, Environment Agency, Bristol.
    33. Kimura, M. (1981): Estimation of evolutionary distances between homologous nucleotide sequences b. - Proc. Natl. Acad. Sci. U. S. A. 78: 454-458. Go to original source...
    34. Koester, J.A.; Swalwell, J.E.; Von Dassow, P. & Armbrust, E.V. (2010): Genome size differentiates co-occurring populations of the planktonic diatom Ditylum brightwellii (Bacillariophyta). - BMC Evol. Biol. 10: 1-11. Go to original source...
    35. Kollár, J. (2020): Polyphasic approach to the study of diatom diversity (Doctoral Thesis). - 31 pp., Palacký University Olomouc, Olomouc.
    36. Kollár, J.; Pinseel, E.; Vanormelingen, P.; Poulíčková, A.; Souffreau, C.; Dvořák, P. & Vyverman, W. (2019): A Polyphasic approach to the delimitation of diatom species: a case study for the genus Pinnularia (Bacillariophyta). - J. Phycol. 55: 365-379. Go to original source...
    37. Krammer, K. (1992): Pinnularia eine Monographie de europäischen Taxa. - Bibl. Diatomol. 26: 1-353.
    38. Krammer, K. (2000): The genus Pinnularia. - 703 pp., A.R.G. Ganter Verlag K.G., Ruggell.
    39. Kumar, S.; Stecher, G.; Li, M.; Knyaz, C. & Tamura, K. (2018): MEGA X: Molecular evolutionary genetics analysis across computing platforms. - Mol. Biol. Evol. 35: 1547-1549. Go to original source...
    40. Leliaert, F.; Verbruggen, H.; Vanormelingen, P.; Steen, F.; López-Bautista, J.M.; Zuccarello, G.C. & De Clerck, O. (2014): DNA-based species delimitation in algae. - Eur. J. Phycol. 49: 179-196. Go to original source...
    41. Lemey, P.; Salemi, M. & Vandamme, A.M. (eds; 2009): The Phylogenetic Handbook (2nd ed.). - 723 pp., Cambridge University Press, New York. Go to original source...
    42. Lewis, A.R.; Marchant, D.R.; Ashworth, A.C.; Hedenäs, L.; Hemming, S.R.; Johnson, J. V.; Leng, M.J.; Machlus, M.L.; Newton, A.E.; Raine, J.I.; Wilenbring, J.K.; Williams, M. & Wolfe, A.P. (2008): Mid-Miocene cooling and the extinction of tundra in continental Antarctica. - Proc. Natl. Acad. Sci. 105: 10676-10680. Go to original source...
    43. Mann, D.G.; McDonald, S.M.; Bayer, M.M.; Droop, S.J.M.; Chepurnov, V.A.; Loke, R.E.; Ciobanu, A. & du Buf, J.M.H. (2004): The Sellaphora pupula species complex (Bacillariophyceae): Morphometric analysis, ultrastructure and mating data provide evidence for five new species. - Phycologia 43: 459-482. Go to original source...
    44. Mann, D.G. & Evans, K.M. (2008): The species concept and cryptic diversity. - In: Moestrup, Ø.; Doucette, G.; Enevoldsen, H.; Godhe, A.; Hallegraeff, G.; Luckas, B.; Lundholm, N.; Lewis, J.; Rengefors, K.; Sellner, K.; Steidinger, K.; Tester, P. & Zingone, A. (eds): Proceedings of the 12th International Conference on Harmful Algae. - pp. 262-268, International Society for the Study of Harmful Algae and Intergovernmental Oceanographic Commission of UNESCO, Copenhagen.
    45. Mann, D.G. & Poulíčková, A. (2010): Mating system, auxosporulation, species taxonomy and evidence for homoploid evolution in Amphora (Bacillariophyta). - Phycologia 49: 183-201. Go to original source...
    46. Mann, D.G.; Sato, S.; Trobajo, R.; Vanormelingen, P. & Souffreau, C. (2010): DNA barcoding for species identification and discovery in diatoms. - Cryptogam. Algol. 31: 557-577.
    47. Mann, D.G. & Vanormelingen, P. (2013): An inordinate fondness? The number, distributions, and origins of diatom species. - J. Eukaryot. Microbiol. 60: 414-420. Go to original source...
    48. Marshall, W.F.; Young, K.D.; Swaffer, M.; Wood, E.; Nurse, P. & Kimura, A. (2012): What determines cell size? - BMC Biol. 10: 1-22. Go to original source...
    49. Minh, B.Q.; Nguyen, M.A.T. & Von Haeseler, A. (2013): Ultrafast approximation for phylogenetic bootstrap. - Mol. Biol. Evol. 30: 1188-1195. Go to original source...
    50. Mora, D.; Abarca, N.; Proft, S.; Grau, J.H.; Enke, N. & Carmona, J. (2019): Morphology and metabarcoding: a test with stream diatoms from Mexico highlights the complementarity of identification methods. - Freshw. Sci. 38: 448-464. Go to original source...
    51. Mueller, R.L. (2015): Genome biology and the evolution of cell-size diversity. - Cold Spring Harb. Perspect. Biol. 7: 1-9. Go to original source...
    52. Nakov, T.; Theriot, E.C. & Alverson, A.J. (2014): Using phylogeny to model cell size evolution in marine and freshwater diatoms Using phylogeny to model cell size evolution in marine and freshwater diatoms. - Limnol. Oceanogr. 59: 79-86. Go to original source...
    53. Nakov, T.; Beaulieu, J.M. & Alverson, A.J. (2018): Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta). - New Phytol. 219: 462-473. Go to original source...
    54. NASA (1976): U.S. Standard Atmosphere. - 241 pp., National Aeronautics and Space Administration, Washington D.C.
    55. Parks, M.B.; Nakov, T.; Ruck, E.C.; Wickett, N.J. & Alverson, A.J. (2018): Phylogenomics reveals an extensive history of genome duplication in diatoms (Bacillariophyta). - Am. J. Bot. 105: 330-347. Go to original source...
    56. Pinseel, E.; Vanormelingen, P.; Hamilton, P.B.; Vyverman, W.; Van de Vijver, B. & Kopalova, K. (2017): Molecular and morphological characterization of the Achnanthidium minutissimum complex (Bacillariophyta) in Petuniabukta (Spitsbergen, High Arctic) including the description of A. digitatum sp. nov. - Eur. J. Phycol. 52: 264-280. Go to original source...
    57. Pinseel, E.; Kulichová, J.; Scharfen, V.; Urbánková, P.; Van de Vijver, B. & Vyverman, W. (2019): Extensive Cryptic Diversity in the Terrestrial Diatom Pinnularia borealis (Bacillariophyceae). - Protist 170: 121-140. Go to original source...
    58. Pinseel, E.; Janssens, S.B.; Verleyen, E.; Vanormelingen, P.; Kohler, T.J.; Biersma, E.M.; Sabbe, K.; Van de Vijver, B. & Vyverman, W. (2020): Global Radiation in a Rare Biosphere Soil Diatom. - Nat. Commun. 11: 1-12. Go to original source...
    59. Posada, D. (2003): Using Modeltest and PAUP* to Select a Model of Nucleotide Substitution. In: Current Protocols in Bioinformatics. - pp. 6.5.1-6.5.14, John Wiley & Sons, Inc., New York. Go to original source...
    60. Poulíčková, A.; Mayama, S.; Chepurnov, V.A. & Mann, D.G. (2007): Heterothallic auxosporulation, incunabula and perizonium in Pinnularia (Bacillariophyceae). - Eur. J. Phycol. 42: 367-390. Go to original source...
    61. Poulíčková, A.; Veselá, J.; Neustupa, J. & Škaloud, P. (2010): Pseudocryptic Diversity versus cosmopolitanism in diatoms: A case study on Navicula cryptocephala Kütz. (Bacillariophyceae) and morphologically similar taxa. - Protist 161: 353-369. Go to original source...
    62. Poulíčková, A.; Kollár, J.; Hašler, P.; Dvořák, P. & Mann, D.G. (2018): A new species Pinnularia lacustrigibba sp. nov. within the Pinnularia subgibba group (Bacillariophyceae). - Diatom Res. 33: 273-282. Go to original source...
    63. R Core Team (2016): R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna, Austria (https://www.R-project.org/).
    64. Rambaut, A.; Drummond, A.J.; Xie, D.; Baele, G. & Suchard, M.A. (2018): Posterior summarization in Bayesian phylogenetics using Tracer 1.7. - Syst. Biol. 67: 901-904. Go to original source...
    65. Ronquist, F.; Teslenko, M.; Van Der Mark, P.; Ayres, D.L.; Darling, A.; Höhna, S.; Larget, B.; Liu, L.; Suchard, M.A. & Huesenbeck, J.P. (2012): Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. - Syst. Biol. 61: 539-542. Go to original source...
    66. Saint Martin, S. & Saint Martin, J.P. (2005): The diatom assemblages as environmental evolution recording of the Paratethys area during Sarmatian times. - Comptes Rendus Palevol 4: 191-201. Go to original source...
    67. Smol, J.P. & Stoermer, E.F. (2010): The Diatoms: Applications for the Environmental and Earth Sciences (2nd ed.). - 667 pp., Cambridge University Press, Cambridge. Go to original source...
    68. Souffreau, C. (2011): Biogeography, species diversity and stress tolerance of aquatic and terrestrial diatoms (Doctoral Thesis). - 285 pp., Ghent University, Ghent.
    69. Souffreau, C.; Vanormelingen, P.; Verleyen, E.; Sabbe, K. & Vyverman, W. (2010): Tolerance of benthic diatoms from temperate aquatic and terrestrial habitats to experimental dessication and temperature stress. - Phycologia 49: 309-324. Go to original source...
    70. Souffreau, C.; Verbruggen, H.; Wolfe, A.P.; Vanormelingen, P.; Siver, P.A.; Cox, E.J.; Mann, D.G.; Van de Vijver, B.; Sabbe, K. & Vyverman, W. (2011): A time-calibrated multi-gene phylogeny of the diatom genus Pinnularia. - Mol. Phylogenet. Evol. 61: 866-879. Go to original source...
    71. Souffreau, C.; Vanormelingen, P.; Sabbe, K. & Vyverman, W. (2013a): Tolerance of resting cells of freshwater and terrestrial benthic diatoms to experimental desiccation and freezing is habitat-dependent. - Phycologia 52: 246-255. Go to original source...
    72. Souffreau, C.; Vanormelingen, P.; Van de Vijver, B.; Isheva, T.; Verleyen, E.; Sabbe, K. & Vyverman, W. (2013b): Molecular Evidence for Distinct Antarctic Lineages in the Cosmopolitan Terrestrial Diatoms Pinnularia borealis and Hantzschia amphioxys. - Protist 164: 101-115. Go to original source...
    73. Stock, W.; Pinseel, E.; De Decker, S.; Sefbom, J.; Blommaert, L.; Chepurnova, O.; Sabbe, K. & Vyverman, W. (2018): Expanding the toolbox for cryopreservation of marine and freshwater diatoms. - Sci. Rep. 8: 1-9. Go to original source...
    74. Stoyneva, M.P. (2016): Allochthonous planktonic algae recorded during the last 25 years in Bulgaria and their possible dispersal agents. - Hydrobiologia 764: 53-64. Go to original source...
    75. Tavaré, S. (1986): Some Probabilistic and Statistical Problems in the Analysis of DNA Sequences. - Lect. Math. Life Sci. 17: 57-86.
    76. Trifinopoulos, J.; Nguyen, L.T.; von Haeseler, A. & Minh, B.Q. (2016): W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. - Nucleic Acids Res. 44: 232-235. Go to original source...
    77. Trobajo, R.; Clavero, E.; Chepurnov, V.A.; Sabbe, K.; Mann, D.G.; Ishihara, S. & Cox, E.J. (2009): Morphological, genetic and mating diversity within the widespread bioindicator Nitzschia palea (Bacillariophyceae). - Phycologia 48: 443-459. Go to original source...
    78. Van de Vijver, B.; Chattová, B.; Metzeltin, D. & Lebouvier, M. (2012): The genus Pinnularia (Bacillariophyta) on Ile Amsterdam (TAAF, Southern Indian Ocean). - Nova Hedwigia 141: 201-236.
    79. Van de Vijver, B.; Frenot, Y. & Beyens, L. (2002): Freshwater diatoms from Île de la Possession (Crozet Archipelago, sub-Antarctica). - Bibl. Diatomol. 46: 1-412.
    80. Van De Vijver, B.; Gremmen, N.J.M. & Beyens, L. (2005): The genus Stauroneis (Bacillariophyceae) in the Antarctic region. - J. Biogeogr. 32: 1791-1798. Go to original source...
    81. Van Hannen, E.J.; Mooij, W.; Van Agterveld, M.P.; Gons, H.J. & Laanbroek, H.J. (1999): Detritus-dependent development of the microbial community in an experimental system: Qualitative analysis by denaturing gradient gel electrophoresis. - Appl. Environ. Microbiol. 65: 2478-2484. Go to original source...
    82. Vanormelingen, P.; Chepurnov, V.A.; Mann, D.G.; Sabbe, K. & Vyverman, W. (2008): Genetic Divergence and Reproductive Barriers among Morphologically Heterogeneous Sympatric Clones of Eunotia bilunaris Sensu Lato (Bacillariophyta). - Protist 159: 73-90. Go to original source...
    83. Vasselon, V.; Rimet, F.; Tapolczai, K. & Bouchez, A. (2017): Assessing ecological status with diatoms DNA metabarcoding: Scaling-up on a WFD monitoring network (Mayotte island, France). - Ecol. Indic. 82: 1-12. Go to original source...
    84. Verbruggen, H. & Theriot, E.C. (2008): Building trees of algae: Some advances in phylogenetic and evolutionary analysis. - Eur. J. Phycol. 43: 229-252. Go to original source...
    85. Vyverman, W.; Verleyen, E.; Wilmotte, A.; Hodgson, D.A.; Willems, A.; Peeters, K.; Van de Vijver, B.; de Wever, A.; Leliaert, F. & Sabbe, K. (2010): Evidence for widespread endemism among Antarctic micro-organisms. - Polar Sci. 4: 103-113. Go to original source...
    86. Xia, X. (2013): DAMBE5: A comprehensive software package for data analysis in molecular biology and evolution. - Mol. Biol. Evol. 30: 1720-1728. Go to original source...
    87. Xia, X.; Xie, Z.; Salemi, M.; Chen, L. & Wang, Y. (2003): An index of substitution saturation and its application. - Mol. Phylogenet. Evol. 26: 1-7. Go to original source...
    88. Zimmermann, J.; Jahn, R. & Gemeinholzer, B. (2011): Barcoding diatoms: Evaluation of the V4 subregion on the 18S rRNA gene, including new primers and protocols. - Org. Divers. Evol. 11: 173-192. Go to original source...

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