The Journal of * Published by the International Society of Eukaryotic Microbiology W? ?ocie,yProtistologists of J. Eukaryot. Microbiol., 59(5), 2012 pp. 429-493 ©2012 The Author(s) Journal o f Eukaryotic Microbiology © 2012 International Society of Protistologists DOI: 10.111 l/j.l550-7408.2012.00644.x The Revised Classification of Eukaryotes SINA M. ADL,ab ALASTAIR G. B. SIMPSON,b CHRISTOPHER E. LANE," JULIUS LUKES,d DAVID BASS," SAMUEL S. BOWSER/ MATTHEW W. BROWN/ FABIEN BURKI,h MICAH DUNTHORN/ VLADIMIR HAMPL,j AARON HEISS,b MONA HOPPENRATH,k ENRIQUE LARA,1 LINE LE GALL,111 DENIS H. LYNN,”’1 HILARY MCMANUS," EDWARD A. D. MITCHELL,1 SHARON E. MOZLEY-STANRIDGE/ LAURA W. PARFREY,“ JAN PAWLOWSKI/ SONJA RUECKERT/ LAURA SHADWICK,* CONRAD L. SCHOCH," ALEXEY SMIRNOV' and FREDERICK W. SPIEGEL* 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 o f Sciences, Institute of Parasitology, University of South Bohemia, Ceské Budêjovice, Czech Republic, and eZoology Department, Natural History Museum, London, SW 7 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 1Department of Ecology, University of Kaiserslautern, 67663, Kaiserslautern, Germany, and 3Department of Parasitology, Charles University, Prague, 128 43, Predict 2, Czech Republic, and kForschungsinstitut Senckenberg, D ZM B - Deutsches Zentrum für Marine Biodiversitätsforschung, D-26382, Wilhelmshaven, Germany, and 1Institute of Biology, University of Neuchâtel, Neuchâtel, CH-2009, Switzerland, and mMuséum National d’Histoire Naturellem, UMR 7138 Systématique, Adaptation et Evolution, Paris, 75231, Cedex Paris 05, France, and nDepartment of Integrative Biology, University of Guelph, Guelph, ON, NIG 2W1, Canada, and °Department 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 TDepartment 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 department of Biological Sciences, University of Arkansas, Fayetteville, Arkansas, 72701, USA, and uGenBank taxonomy, NIH/NLM /NCBI, Bethesda, Maryland, 20892-6510, USA, and ''Department of Invertebrate Zoology, St.Petersburg State University, St. Petersburg, 199034, Russia ABSTRACT. This revision of the classification of eukaryotes, which updates that of Adi 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 Adi et al. (2005) on behalf current revision reflects the need to have a classification of of The Society established name stability as well as a syn­ protistan eukaryotes that incorporates recent advances thesisT 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 Adi et al. (2005) are mostly retained, although some have been assembled into still higher Correponding Author: Sina M. Adi, Department of Soil Science, order groupings (Table 1, see below). One notable exception is University of Saskatchewan, 51 Campus Drive, Saskatoon, SK S7N 5A8, Canada-Telephone number: +306 966 6866; FAX number: the Chromalveolata, which was retained then as useful + 306 966 6881; e-mail:[email protected] although controversial, and with the authors noting concerns 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 429 430 J. EUKARYOT. MICROBIOL., 59, NO. 5, SEPTEMBER-OCTOBER 2012 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- Super-groups Examples based nomenclature that treats these steps as part of the same process (Adi et al., 2007; Cantino, 2004; Krön, 1997; Pleijel and Amoebozoa Tubulinea Rouse 2003). This approach provides a more stable classifica­ Mycetozoa tion that preserves names, while allowing revisions to reflect our Fungi Amorphea Opisthokonta changing understanding of evolutionary history. We have also Choanomonada Metazoa relied on ideas borrowed from phylogenetic nomenclature, dis­ Apusomonada tinguishing groups with definitions based on apomorphies, Breviata nodes, branches, or combinations of these. These kinds of defi­ Excavata Metamonada nitions are more suited to a classification based on phylogenetic Malawimonas B trees, and can be written as phylogenetic hypotheses that can be o Discoba tested. 5* Diaphoretickes Cryptophyceae The most significant changes introduced in this revision are ■a Centrohelida as follows: m Telonemia First, we recognize the grouping of Amoebozoa with Opi- Haptophyta Sar Cercozoa sthokonta. Since 2005, this has become a commonly recog­ Foraminifera nized probable clade, and at present it is usually referred to “Radiolaria” by the informal name “unikont”, sometimes rendered as the Alveolata more formal sounding “Unikonta”. However, the underlying Stramenopiles hypothesis of a monociliated (with only one ciliated basal Archaeplastida Glaucophyta body) ancestry for this cluster of organisms (Cavalier-Smith, Rhodophyceae 2002) is almost certainly incorrect (Kim et al. 2006; Roger Chloroplastida and Simpson, 2009). There is no requirement that names of Incertae sedis Eukaryota Incertae sedis, and taxa reflect the ancestral state of the clade. However, the name table 3 “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 H o m o 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