Keywords
homoplasy
phylogeny
characters
monophyly
molecular data
morphological data
species flocks
How to Cite
Abstract
Background and aims – We examine the possibility of the independent evolution of the same features multiple times across the pennate diatom tree of life.
Methods and key results – Features we have studied include symmetry, raphe number and amphoroid symmetry. Phylogenetic analysis, with both morphological and molecular data suggest in each of these cases that the features evolved from 5 to 6 times independently. We also look at the possibility of certain features having evolved once and diagnosing large genera of diatoms, suggestive of an adaptive radiation in genera such as Mastogloia, Diploneis and Stauroneis.
Conclusion – Formal phylogenetic analyses and recognition of monophyletic groups allow for the recognition of homoplasious or homologous features.
References
Adl S.M., Simpson A.G.B., Farme, M.A., Andersen R.A., Anderson O.R., Barta J.R., Bowser S.S., Brugerolle G., Fensome R.A., Fredericq S., James T.Y., Karpov S., Kugrens P., Krug J., Lane C.E., Lewis L.A., Lodge J., Lynn D.H., Mann D.G., McCourt R.M., Mendoza L., Moestrup Ø., Mozley-Standridge S.E., Nerad T.A., Shearer C.A., Smirnov A.V., Spiegel F.W., Taylor M.F. Jr. (2005) The new higher-level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology 52: 399–451. https://doi.org/10.1111/j.1550-7408.2005.00053.x
Agardh C.A. (1824) Systema Algarum. Adumbravit C.A. Agardh. Lund, Literis Berlingianis.
Agardh C.A. (1830–1832) Conspectus Criticus Diatomacearum. Parts 1–4. Lundae. Litteris Berlingianis.
Anantharaman V., Lakshminarayan M. I., Aravind L. (2007) Comparative genomics of protists: new insights into the evolution of eukaryotic signal transduction and gene regulation. Annual Review of Microbiology 61: 453–475. https://doi.org/10.1146/annurev.micro.61.080706.093309
Andrews G.W. (1981) Achnanthes linkei and the origin of monoraphid diatoms. Bacillaria 4: 29–40.
Anonymous (1975) Proposals for a standardization of diatom terminology and diagnoses. Nova Hedwigia, Beiheft 53: 323–354.
Boyle J.A., Pickett-Heaps J.D., Czarnecki D.B. (1984) Valve morphogenesis in the pennate diatom Achnanthes coarctata. Journal of Phycology 20: 563–573. https://doi.org/10.1111/j.0022-3646.1984.00563.x
Brooks D.R., O’Grady R.T., Glen R.D. (1985) Phylogenetic analysis of the Digenea (Platyhelminthes: Cercomeria) with comments on their adaptive radiation. Canadian Journal of Zoology 63: 411–443. https://doi.org/10.1139/z85-062
Bruder K., Medlin L.K. (2008) Morphological and molecular investigations of naviculoid diatoms. II. Selected genera and families. Diatom Research 23: 283–329. https://doi.org/10.1080/0269249X.2008.9705759
Burliga A.L., Kociolek J.P., Salomoni S.E., Figueiredo D. (2013) A new genus and species in the diatom Family Eunotiaceae Kützing (Bacillariophyceae) from the Amazonian hydrographic region, Brazil. Phytotaxa 79: 47–57. https://doi.org/10.11646/phytotaxa.79.2.1
Cavalier-Smith T. (2009) Megaphylogeny, cell body plans, adaptive zones: Causes and timing of eukaryotic basal radiations. Journal of Eukaryotic Microbiology 56: 26–33. https://doi.org/10.1111/j.1550-7408.2008.00373.x
Cleve P.T. (1895) Synopsis of the Naviculoid Diatoms, Part II. Kongliga Svenska-Vetenskaps Akademiens Handlingar 27: 1–219.
Cox E.J. (1979) Symmetry and valve structure in naviculoid diatoms. Nova Hedwigia, Beiheft 64: 193–206.
Cox E.J. (1996) Identification of Freshwater Diatoms from Live Material. London, Chapman and Hall.
Cox E.J. (2001) What constitutes a stauros? A morphogenetic perspective. In: Jahn R., Kociolek J.P., Witkowski A., Compère P. (eds) Festschrift für H. Lange-Bertalot: 303–316. Ruggell, A.R.G. Gantner Verlag.
Cox E.J. (2006) Raphe loss and spine formation in Diadesmis gallica (Bacillariophyta) - an intriguing example of phenotypic plasticity in a diatom. Nova Hedwigia 130: 163–176.
Cox E.J. (2009) What is in a name? Diatom classification should reflect systematic relationships. Acta Botanica Croatica 68: 443–454.
Givnich T.J., Millam K.C., Mast A.R., Paterson T.B., Theim T.J., Hipp A.L., Henss J.M., Smith J.F., Wood K.R., Sytsma K.J. (2009) Adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae). Proceedings of the Royal Society B 276: 407–416. https://doi.org/10.1098/rspb.2008.1204
Grant P.R. (1981) Speciation and the adaptive radiation of Darwin’s Finches. American Scientist 69: 653–663.
Hamsher S.E., Graeff C.L., Stepanek J.G., Kociolek J.P. (2014) Variation in valve and girdle band morphology in freshwater Denticula (Bacillariophyceae) species: implications for the systematic position of the genus including the description of Tetralunata gen. nov. (Epithemiaceae, Rhopalodiales). Plant Ecology and Evolution 147: 346–365. https://doi.org/10.5091/plecevo.2014.990
Hasle G.R. (1972) Two types of valve processes in centric diatoms. Nova Hedwigia Beiheft 39: 55–78.
Hasle G.R. (1973) Thalassiosiraceae, a new diatom family. Norwegian Journal of Botany 20: 67–69.
Hasle G.R., Syvertsen E. (1996) Marine diatoms. In: Tomas C.R. (ed.) Identifying marine diatoms and dinoflagellates: 5–385. San Diego, USA, Academic Press, Inc.
Hein M.K., Winsborough B.M., Sullivan M.J. (2008) Bacillariophyta (Diatoms) of the Bahamas. Iconographia Diatomologica 19: 1–303.
Hendey N.I. (1937) The plankton diatoms of the Southern Seas. Discovery Reports 16: 151–364.
Hoban M.A., Fryxell G.A., Buck K.R. (1980) Biddulphioid diatoms: resting spores in Antarctic Eucampia and Odontella. Journal of Phycology 16: 591–602. https://doi.org/10.1111/j.1529-8817.1980.tb03078.x
Hustedt F. (1930) Bacillariophyta (Diatomeae). In: Pascher A. (ed.) Die Süsswasser-Flora Mitteleuropas. Zweite Auflage. Heft 10. Jena, Gustav Fischer.
Hustedt F. (1927–1966) Die Kieselalgen Deutschlands, Österreichs und der Schweiz unter Berücksichtigung der übrigen Länder Europas sowie der angrenzenden Meeresgebiete. In: Rabenhorst L. (ed.) Kryptogamen Flora von Deutschland, Österreich und der Schweiz. Leipzig, Akademische Verlagsgesellschaft m.b.h.
Jüttner I., Chimonides J., Cox E.J. (2011) Morphology, ecology and biogeography of diatom species related to Achnanthidium pyrenaicum (Hustedt) Kobayasi (Bacillariophyceae) in streams of the Indian and Nepalese Himalaya. Archiv für Hydrobiologie, Algological Studies 136/137: 45–76.
Karthick B., Taylor J.C., Hamilton P.B. (2017) Two new species of Achnanthidium Kützing (Bacillariophyceae) from Kolli Hills, Eastern Ghats, India. Fottea 17: 65–77. https://doi.org/10.5507/fot.2016.020
Karsten G. (1928) Abteilung Bacillariophyta (Diatomeae). In: Engler A., Prantl K. (eds) Die Natürlichen Pflanzenfamilien, Peridineae (Dinoflagellatae), Diatomeae (Bacillariophyta), Myxomycetes, Zweite Auflage: 105–303. Leipzig, Wilhelm Engelmann.
Kitchell J.A., Clark D.L., Gombos Jr. A.M. (1968) Biological selectivity of extinction: A link between background and mass extinction. Palaios 1: 504–511.
Kociolek J.P., Balasubramanian K., Blanco S., Coste M., Ector L., Liu Y., Kulikovskiy M., Lundholm N., Ludwig T., Potapova M., Rimet F., Sabbe K., Sala S., Sar E., Taylor J., Van de Vijver B., Wetzel C.E., Williams D.M., Witkowski A., Witkowski J. (2018) DiatomBase. Available from http://www.diatombase.org [accessed 27 Mar. 2019].
Kociolek J.P., Stepanek J.G., Lowe R.L., Johansen J.R., Sherwood, A.R. (2013) Molecular data show the enigmatic cave-dwelling diatom Diprora (Bacillariophyceae) to be a raphid diatom. European Journal of Phycology 48: 474–484. https://doi.org/10.1080/09670262.2013.860239
Kociolek J.P., Rhode K. (1998) Raphe vestiges in ‘‘Asterionella’’ species from Madagascar: Evidence for a polyphyletic origin of the araphid diatoms? Cryptogamie Algologie 19: 57–74.
Kociolek J.P., Stoermer E.F. (1988) A preliminary investigation of the phylogenetic relationships of the freshwater, apical pore field-bearing cymbelloid and gomphonemoid diatoms (Bacillariophyceae). Journal of Phycology 24: 377–385. https://doi.org/10.1111/j.1529-8817.1988.tb04480.x
Kociolek J.P., Stoermer E.F. (1993) Freshwater gomphonemoid diatom phylogeny: preliminary results. Hydrobiologia 269/270: 31–38. https://doi.org/10.1007/BF00028001
Kociolek J.P., Spaulding S.A., Lowe R.L. (2015a) Bacillariophyceae: The Raphid Diatoms. Chapter 16. In: Wehr J., Sheath R., Kociolek J.P. (eds) Freshwater algae of North America: 707–770. 2nd Edition. New York, Academic Press.
Kociolek J.P., You Q., Wang X., Liu Q. (2015b) Consideration of some interesting freshwater gomphonemoid diatoms from North America and China, and the description of Gomphosinica, gen. nov. Nova Hedwigia Beiheft 144: 175–198.
Kociolek J.P., Hamsher S.E., Kulikovskiy M., Bramberger A. (2017) Are there species flocks in freshwater diatoms? A review of past reports and a look to the future. Hydrobiologia 792: 17–35. https://doi.org/10.1007/s10750-016-3075-1
Kociolek J.P., Williams D.M. (1987) Unicell ontogeny and phylogeny: Examples from the diatoms. Cladistics 3: 274–284. https://doi.org/10.1111/j.1096-0031.1987.tb00511.x
Kociolek J.P., Williams D.M. (2015) How to define a diatom genus? Notes on the creation and recognition of taxa, and a call for revisionary studies of diatoms. Proceedings of the 8th Central European Diatom Meeting. Zagreb, Croatia. Acta Croatica Botanica 74(2): 195–210.
Krammer K. (2003) Cymbopleura, Delicata, Navicymbula, Gomphocymbellopsis, Afrocymbella. Diatoms of Europe 4: 1–529.
Krammer K., Lange-Bertalot H. (1986) Bacillariophyceae 1. Teil: Naviculaceae. In: Ettl H. et al. (eds) Süsswasserflora von Mitteleuropa, vol. 2, issue 1. Jena, VEB Gustav Fisher Verlag.
Kulikovskiy M., Maltsev Y., Andreeva S., Gluschenko A., Pudonay Y., Ludwig T., Tusset E., Kociolek J.P. (2019). Description of a new diatom genus Dorofeyukae gen. nov., with remarks on the phylogeny of the family Stauroneidaceae D.G.Mann. Journal of Phycology 55: 173–185. https://doi.org/10.1111/jpy.12810
Lange-Bertalot H. (1979) Simonsenia, a new genus with morphology intermediate between Nitzschia and Surirella. Bacillaria 2: 127–136.
Liu Y., Kociolek J.P., Glushenko A., Kulikovskiy M., Fan Y. (2018) A new genus of Eunotiales (Bacilleriophyta, Bacillariophyceae: Peroniaceae), Sinoperonia, from Southeast Asia, exhibiting remarkable phenotypic plasticity with regard to the raphe system. Phycologia 57: 147–158.
Lowe R.L., Kociolek J.P., You Q, Wang. Q., Stepanek J. (2017) Diversity of the diatom genus Humidophila in karst areas of Guizhou, China. Phytotaxa 305: 269–284. https://doi.org/10.11646/phytotaxa.305.4.3
Lundholm N., Daugbjerg N., Moestrup Ø. (2002a) Phylogeny of the Bacillariaceae with emphasis of the genus Pseudo-nitzschia (Bacillariophyceae) based on partial LSU rDNA. European Journal of Phycology 37: 115–134. https://doi.org/10.1017/S096702620100347X
Lundholm N., Hasle G.R., Fryxell G.A., Hargraves P.E. (2002b) Morphology, phylogeny and taxonomy of species within the Pseudo-nitzschia americana-complex (Bacillariophyceae), with description of two new species. Phycologia 41: 480–497. https://doi.org/10.2216/i0031-8884-41-5-480.1
Main S.P. (2003) Diprora haenaensis gen. et sp. nov., a filamentous, pseudoaerial, araphid diatom from Kaua’i (Hawaiian Islands). Diatom Research 18: 259–272. https://doi.org/10.1080/0269249X.2003.9705591
Mann D.G. (1986) Book review. Phycologica 25: 269–270.
Mann D.G. (1994) The systematics of amphoroid diatoms: the life history of Amphora arcus. Nova Hedwigia 58: 335–352.
Mann D.G. (1997) Shifting sands: the use of the lower taxonomic ranks in diatoms. Diatom 13: 13–17.
Mayama S., Kobayasi H. (1989) Sequential valve development in the monoraphid diatom Achnanthes minutissima var. saprophila. Diatom Research 4: 111–117. https://doi.org/10.1080/0269249X.1989.9705056
Medlin L.K. (1985) A reappraisal of the diatom genus Rhoiconeis and the description of Campylopyxis, gen. nov. British Phycological Journal 20: 313–328. https://doi.org/10.1080/00071618500650321
Medlin L.K. (1991) Evidence for parallel evolution of frustule shape in two lines of pennate diatoms from the epiphyton. Diatom Research 6: 109–124. https://doi.org/10.1080/0269249X.1991.9705150
Medlin L.K. (2010) Pursuit of a natural classification of diatoms: An incorrect comparison of published data. European Journal of Phycology 45: 155–166. https://doi.org/10.1080/09670260903511657
Medlin L.K. (2016) Opinion: Can coalescent models explain deep divergences in the diatoms and argue for the acceptance of paraphyletic taxa at all taxonomic hierarchies? Nova Hedwigia 102: 107–128. https://doi.org/10.1127/nova_hedwigia/2015/0295
Medlin L.K. (2018) Mini review: diatom species as seen through a molecular window. Brazilian Journal of Botany 41: 457–469. https://doi.org/10.1007/s40415-018-0444-1
Medlin L.K., Kaczmarska I. (2004) Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision. Phycologia 43: 245–270. https://doi.org/10.2216/i0031-8884-43-3-245.1
Majewska R., Kociolek J.P., Thomas E.W., De Stefano M., Santoro M., Bolanos F., Van de Vijver B. (2015) Chelnicola and Poulinea, two new gomphonemoid diatom (Bacillariophyta) living on marine turtles from Costa Rica. Phytotaxa 233: 236–250. https://doi.org/10.11646/phytotaxa.233.3.2
Mereschkowsky C. (1901) Étude sur l’endochrome des diatomées. Memoires of the Academy of Sciences, St. Petersburg, Series 8. 6: 1–40.
Mereschkowsky C. (1902) Les types de l’endochrome chez les Diatomées. Scripta Botanica Horti Universitatis (Imperialis) Petropolitanae St. Petersburg 21: 1–193.
Müller O. (1895) Über Achsen, Orientierungs- und Symmetrieebenen bei den Bacillariaceen. Berichte der Deutschen Botanischen Gesellschaft 13: 222–234.
Nakov T., Ruck E.C., Galachyants Y., Spaulding S.A., Theriot E.C. (2014) Molecular phylogeny of the Cymbellales (Bacillariophyceae, Heterokontophyta) with a comparison of models for accommodating rate variation across sites. Phycologia 53: 359–373.
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 Phytologist 219: 462–473. https://doi.org/10.1111/nph.15137
Paddock T.B.B., Kemp, K.D. (1990) An illustrated survey of the morphological features of the diatom genus Mastogloia. Diatom Research 5: 73–103. https://doi.org/10.1080/0269249X.1990.9705095
Patrick R.M., Reimer C.W. (1966) The diatoms of the United States. Academy of Natural of Sciences of Philadelphia, Monograph No. 13.
Patrick R.M., Reimer C.W. (1975) The diatoms of the United States. Academy of Natural of Sciences of Philadelphia, Monograph No. 13.
Pérès F., Barthès A., Ponton E., Coste M., Ten Hage L., Le Cohu R. (2012) Achnanthidium delmontii sp. nov., a new species from French rivers. Fottea 12: 189–198. https://doi.org/10.5507/fot.2012.014
Robichaux R.H., Carr D.H., Liebman M., Pearey R.W. (1990) Adaptive radiation of the Hawaiian silversword alliance (Compositae-Madiinae): ecological, morphological and physiological diversity. Annals of the Missouri Botanical Garden 77: 64–72. https://doi.org/10.2307/2399626
Ross R., Sims P.A. (1972) The fine structure of the frustule in centric diatoms: a suggested terminology. British Phycological Journal 7:139–163. https://doi.org/10.1080/00071617200650171
Ross R., Cox E.J., Karayeva N.I., Mann D.G., Paddock T.B.B., Simonsen R., Sims P.A. (1979) An amended terminology for the siliceous components of the diatom cell. Nova Hedwigia Beiheft 64: 513–533.
Round F.E., Crawford R.M., Mann D.G. (1990) Diatoms: biology and morphology of the genera. Cambridge, UK, Cambridge University Press.
Ruck E.C., Theriot E.C. (2011) Origin and evolution of the canal raphe system in diatoms. Protist 162: 723–737. https://doi.org/10.1016/j.protis.2011.02.003
Schluter D. (2000) The ecology of adaptive radiation. Oxford, Oxford University Press.
Schütt F. (1896) Bacillariales (Diatomeae). In: Engler A., Prantl K. (eds) Die natürlichen Pflanzenfamilien, vol. 1, issue 1b: 31–150. Leipzig, Verlag von Wilhelm Engelmann.
Simonsen R. (1979) The diatom system: ideas on phylogeny. Bacillaria 2: 9–71.
Sims P.A., Mann D.G., Medlin L.K. (2006) Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia 45: 361–402. https://doi.org/10.2216/05-22.1
Small J. (1950) Quantitative evolution: XVI. Increase of species-number in diatoms. Annals of Botany 14: 91–113.
Smith H.L. (1872) Conspectus of the families and genera of the Diatomaceae. The Lens 1: 1–19.
Stelbrink B., Jovanovska E., Levkov Z., Ognjanova-Rumenova O., Wilke T., Albrecht C. (2018) Diatoms do radiate: evidence for a freshwater species flock. Journal of Evolutionary Biology 31: 1969–1975. https://doi.org/10.1111/jeb.13368
Stepanek J., Kociolek J.P. (2014) Molecular phylogeny of Amphora sensu stricto (Bacillariophyta): an investigation into the monophyly and classification of the amphoroid diatoms. Protist 165: 177–195. https://doi.org/10.1016/j.protis.2014.02.002
Stephens F.C., Gibson R.A. (1980) Ultrastructural studies of some Mastogloia (Bacillariophyceae) species belonging to the groups Undulatae, Apiculatae, Lanceolatae and Paradoxae. Phycologia 19: 143–152. https://doi.org/10.2216/i0031-8884-19-2-143.1
Theriot E.C., Ashworth M.P., Nakov T., Ruck E., Jansen R.K. (2015) Dissecting signal and noise in diatom chloroplast protein encoding genes with phylogenetic information profiling. Molecular Phylogenetics and Evolution 89: 28–36. https://doi.org/10.1016/j.ympev.2015.03.012
Troughton E.L.G. (1959) The marsupial fauna: its origin and radiation. In: Keast A., Crocker R.L., Christian C.S. (eds) Biogeography and ecology in Australia: 69–88. Monographiae Biologicae. Dordrecht, Springer. https://doi.org/10.1007/978-94-017-6295-3_5
Vanormelingen P., Chepurnov V.A., Mann D.G., Cousin S., Vyverman W. (2007) Congruence of morphological, reproductive and ITS rDNA sequence data in some Australasian Eunotia bilunaris (Bacillariophyta). European Journal of Phycology 42: 61–79. https://doi.org/10.1080/09670260600942635
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. https://doi.org/10.1016/j.protis.2007.08.004
Wetzel C.E., Kociolek J.P. (2018) Burliganiella gen. nov. (Bacillariophyta, Eunotiales): another case of raphe reduction based on the type material of Fragilaria siolii Hustedt. Cryptogamie Algologie 39: 255–265. https://doi.org/10.7872/crya/v39.iss2.2018.255
Wetzel C.E., Lange-Bertalot H., Morales E.A., Bicudo D. De C., Hoffmann L., Ector L. (2012) Bicudoa amazonica gen. nov. et sp. nov. (Bacillariophyta) a new freshwater diatom from the Amazon basin with a complete raphe loss in the eunotioid lineage. Phytotaxa 75: 1–18. https://doi.org/10.11646/phytotaxa.75.1.1
Williams D.M. (1985) Morphology, taxonomy and inter-relationships of the ribbed araphid diatoms from the genera Diatoma and Meridion (Diatomaceae: Bacillariophyta). Bibliotheca Diatomologica 8: 1–228.
Williams D.M. (2007) Classification and diatom systematics: the past, the present and the future. In: Brodie J., Lewis J. (eds) Unravelling the algae: 57–91. Boca Raton, CRC Press.
Williams D.M., Kociolek J.P. (2010) Towards a comprehensive diatom classification and phylogeny (Bacillariophyta). Plant Ecology and Evolution 143: 265–270. https://doi.org/10.5091/plecevo.2010.401
Witkowski A., Gomes A., Mann D.G., Trobajo R., Li C., Barka F., Gusev E., Dąbek P., Grzonka J., Kurzydłowski K.J., Zgłobicka I., Harrison M., Boski T. (2015) Simonsenia aveniformis sp. nov. (Bacillariophyceae), molecular phylogeny and systematics of the genus and a new type of canal raphe system. Scientific Reports 5: 17115. https://doi.org/10.1038/srep17115
Yohn T.A., Gibson R.A. (1981) Marine diatoms of the Bahamas. I. Mastogloia Thw. ex Wm. Sm. species of the groups Lanceolatae and Undulatae. Botanica Marina 24: 641–665.
Yohn T.A., Gibson R.A. (1982) Marine diatoms of the Bahamas. II. Mastogloia Thw. ex Wm. Sm. species of the groups Decussatae and Ellipticae. Botanica Marina 25: 41–53. https://doi.org/10.1515/botm.1982.25.2.41
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