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The Revised Classification of Eukaryotes

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The Revised Classification of Eukaryotes Published in Journal of Eukaryotic Microbiology 59, issue 5, 429-514, 2012 which should be used for any reference to this work 1 The Revised Classification of Eukaryotes SINA M. ADL,a,b ALASTAIR G. B. SIMPSON,b CHRISTOPHER E. LANE,c JULIUS LUKESˇ,d DAVID BASS,e SAMUEL S. BOWSER,f MATTHEW W. BROWN,g FABIEN BURKI,h MICAH DUNTHORN,i VLADIMIR HAMPL,j AARON HEISS,b MONA HOPPENRATH,k ENRIQUE LARA,l LINE LE GALL,m DENIS H. LYNN,n,1 HILARY MCMANUS,o EDWARD A. D. MITCHELL,l SHARON E. MOZLEY-STANRIDGE,p LAURA W. PARFREY,q JAN PAWLOWSKI,r SONJA RUECKERT,s LAURA SHADWICK,t CONRAD L. SCHOCH,u ALEXEY SMIRNOVv and FREDERICK W. SPIEGELt aDepartment of Soil Science, University of Saskatchewan, Saskatoon, SK, S7N 5A8, Canada, and bDepartment of Biology, Dalhousie University, Halifax, NS, B3H 4R2, Canada, and cDepartment of Biological Sciences, University of Rhode Island, Kingston, Rhode Island, 02881, USA, and dBiology Center and Faculty of Sciences, Institute of Parasitology, University of South Bohemia, Cˇeske´ Budeˇjovice, Czech Republic, and eZoology Department, Natural History Museum, London, SW7 5BD, United Kingdom, and fWadsworth Center, New York State Department of Health, Albany, New York, 12201, USA, and gDepartment of Biochemistry, Dalhousie University, Halifax, NS, B3H 4R2, Canada, and hDepartment of Botany, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada, and iDepartment of Ecology, University of Kaiserslautern, 67663, Kaiserslautern, Germany, and jDepartment of Parasitology, Charles University, Prague, 128 43, Praha 2, Czech Republic, and kForschungsinstitut Senckenberg, DZMB – Deutsches Zentrum fu¨r Marine Biodiversita¨tsforschung, D-26382, Wilhelmshaven, Germany, and lInstitute of Biology, University of Neuchaˆtel, Neuchaˆtel, CH-2009, Switzerland, and mMuse´um National d’Histoire Naturellem, UMR 7138 Syste´matique, Adaptation et Evolution, Paris, 75231, Cedex Paris 05, France, and nDepartment of Integrative Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada, and oDepartment of Biological Sciences, LeMoyne College, Syracuse, New York, 13214, USA, and pDepartment of Biology, Middle Georgia College, Cochran, Georgia, 31014, USA, and qDepartment of Chemistry and Biochemistry, University of Colorado, Boulder, Colorado, 80309, USA, and rDepartment of Genetics and Evolution, University of Geneva, 1211, Geneva 4, Switzerland, and sSchool of Life, Sport and Social Sciences, Edinburgh Napier University, Edinburgh, EH11 4BN, United Kingdom, and tDepartment of Biological Sciences, University of Arkansas, Fayetteville, Arkansas, 72701, USA, and uGenBank taxonomy, NIH/NLM/NCBI, Bethesda, Maryland, 20892-6510, USA, and vDepartment of Invertebrate Zoology, St.Petersburg State University, St. Petersburg, 199034, Russia ABSTRACT. This revision of the classification of eukaryotes, which updates that of Adl et al. [J. Eukaryot. Microbiol. 52 (2005) 399], retains an emphasis on the protists and incorporates changes since 2005 that have resolved nodes and branches in phyloge- netic trees. Whereas the previous revision was successful in re-introducing name stability to the classification, this revision provides a classification for lineages that were then still unresolved. The supergroups have withstood phylogenetic hypothesis testing with some modifications, but despite some progress, problematic nodes at the base of the eukaryotic tree still remain to be statistically resolved. Looking forward, subsequent transformations to our understanding of the diversity of life will be from the discovery of novel lineages in previously under-sampled areas and from environmental genomic information. Key Words. Algae, amoebae, biodiversity, ciliates, flagellates, fungi, parasites, protozoa, systematics, taxonomy. HE classification proposed by Adl et al. (2005) on behalf current revision reflects the need to have a classification of T of The Society established name stability as well as a syn- protistan eukaryotes that incorporates recent advances thesis of the overall structure of the classification of eukary- wrought both by the widespread use of phylogenomic-scale otes, based on the information available at that time, and phylogenetic analyses and by massively increased taxon sam- after the upheaval introduced by molecular phylogenetic stud- pling in rRNA-based phylogenies, partly due to a renaissance ies over the preceding two decades. Overall, the system pro- in novel organism discovery. With the current revision, we posed was conservative enough to largely avoid erroneous or have again tried to strike a conservative balance between premature groupings, whilst eliminating wherever possible updating the classification where needed and avoiding formal known polyphyletic groups or groups of convenience, encour- recognition of uncertain groupings where further investigation aging correction of many of the errors in text books. The would be warranted. One notable advance since 2005 is the consolidation of a classification founded on robust phylogenetic relatedness. The super-groups formalized by Adl et al. (2005) are mostly retained, although some have been assembled into still higher Correponding Author: Sina M. Adl, Department of Soil Science, order groupings (Table 1, see below). One notable exception is University of Saskatchewan, 51 Campus Drive, Saskatoon, SK S7N – the Chromalveolata, which was retained then as useful 5A8, Canada Telephone number: +306 966 6866; FAX number: although controversial, and with the authors noting concerns +306 966 6881; e-mail: [email protected] 1 Present Address: Department of Zoology, University of British with this grouping of Cryptophyceae, Haptophyta, Strameno- Columbia, Vancouver, BC, V6T 1Z4, Canada. piles, and Alveolata. Since then, evidence has mounted that 2 Table 1. The classification of eukaryotes at the highest ranks. system despite changes; and (iv) separating naming clades from assembling nested hierarchies – in contrast to rank- based nomenclature that treats these steps as part of the same process (Adl et al., 2007; Cantino, 2004; Kron, 1997; Pleijel and Rouse 2003). This approach provides a more stable classifica- tion that preserves names, while allowing revisions to reflect our changing understanding of evolutionary history. We have also relied on ideas borrowed from phylogenetic nomenclature, dis- tinguishing groups with definitions based on apomorphies, nodes, branches, or combinations of these. These kinds of defi- nitions are more suited to a classification based on phylogenetic trees, and can be written as phylogenetic hypotheses that can be tested. The most significant changes introduced in this revision are as follows: First, we recognize the grouping of Amoebozoa with Opi- sthokonta. Since 2005, this has become a commonly recog- nized probable clade, and at present it is usually referred to by the informal name “unikont”, sometimes rendered as the more formal sounding “Unikonta”. However, the underlying hypothesis of a monociliated (with only one ciliated basal body) ancestry for this cluster of organisms (Cavalier-Smith, 2002) is almost certainly incorrect (Kim et al. 2006; Roger and Simpson, 2009). There is no requirement that names of taxa reflect the ancestral state of the clade. However, the name “unikonts” causes confusion because of the apomorphy hypothesized for the ancestral character. To address, this we introduce a new formal name for the probable clade. We have formalized this clade as a new taxon, Amorphea, with a node- Chromalveolates are probably polyphyletic (Baurain et al. based phylogenetic definition: 2010; Parfrey et al. 2010; Stiller et al. 2009). Instead, multi- gene phylogenetics and phylogenomic studies generally sup- port Stramenopiles and Alveolata as specifically related to Amorphea: the least inclusive clade containing Homo sapi- Rhizaria (Burki et al. 2009, 2010, 2012; Hampl et al. 2009; ens Linnaeus 1758, Neurospora crassa Shear & Dodge 1927 Parfrey et al. 2010). The two remaining major lineages that (both Opisthokonta), and Dictyostelium discoideum Raper were formerly assigned to the chromalveolates – Haptophyta 1935 (Amoebozoa). This is a node-based definition in and Cryptophyceae/cryptomonads – have been more challeng- which all of the specifiers are extant; it is intended to apply ing to place phylogenetically (Burki et al. 2010, 2012), and are to a crown clade; qualifying clause – the name does not two examples of several where stable, deep relationships still apply if any of the following fall within the specified clade remain to be established. Analyses with abundant data for – Arabidopsis thaliana (Linnaeus) Heynhold 1842 (Archaep- each taxon are subject to systematic biases that can lead to lastida), Tetrahymena thermophila Nanney & McCoy 1976 high support for incorrect clades (Hedtke et al. 2006; Zwickl (Alveolata), Thalassiosira pseudonana Hasle & Hiemdal and Hillis 2002). Broader taxonomic sampling is likely the 1970 (Stramenopiles), Bigelowiella natans Moestrup & most important factor in alleviating these kinds of systematic Sengco 2001 (Rhizaria), Euglena gracilis Klebs 1883 (Ex- biases (Heath et al. 2008; Hedtke et al. 2006; Zwickl and Hil- cavata), and Emiliania huxleyi (Lohmann) Hay & Mohler lis 2002), although adding more taxa may also introduce addi- 1967 (Haptophyta). tional missing sequence data (Wiens 2006). Thus, emerging Note that the term Amorphea (a, Gr. – without; morphe, relationships should be confirmed by multiple studies before Gr. – form, shape) relates to the cells of most taxa in this proposing revisions to the classification. It is
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