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PUBLIC LIBRARY of SCIENCE | plosgenetics.org | ISSN 1553-7390 | Volume 2 | Issue 12 | DECEMBER 2006 GENETICS PUBLIC LIBRARY of SCIENCE www.plosgenetics.org Volume 2 | Issue 12 | DECEMBER 2006 Interview Review Knight in Common Armor: 1949 Unraveling the Genetics 1956 An Interview with Sir John Sulston e225 of Human Obesity e188 Jane Gitschier David M. Mutch, Karine Clément Research Articles Natural Variants of AtHKT1 1964 The Complete Genome 2039 Enhance Na+ Accumulation e210 Sequence and Comparative e206 in Two Wild Populations of Genome Analysis of the High Arabidopsis Pathogenicity Yersinia Ana Rus, Ivan Baxter, enterocolitica Strain 8081 Balasubramaniam Muthukumar, Nicholas R. Thomson, Sarah Jeff Gustin, Brett Lahner, Elena Howard, Brendan W. Wren, Yakubova, David E. Salt Matthew T. G. Holden, Lisa Crossman, Gregory L. Challis, About the Cover Drosophila SPF45: A Bifunctional 1974 Carol Churcher, Karen The jigsaw image of representatives Protein with Roles in Both e178 Mungall, Karen Brooks, Tracey of various lines of eukaryote evolution Splicing and DNA Repair Chillingworth, Theresa Feltwell, refl ects the current lack of consensus as Ahmad Sami Chaouki, Helen K. Zahra Abdellah, Heidi Hauser, to how the major branches of eukaryotes Salz Kay Jagels, Mark Maddison, fi t together. The illustrations from upper Sharon Moule, Mandy Sanders, left to bottom right are as follows: a single Mammalian Small Nucleolar 1984 Sally Whitehead, Michael A. scale from the surface of Umbellosphaera; RNAs Are Mobile Genetic e205 Quail, Gordon Dougan, Julian Amoeba, the large amoeboid organism Elements Parkhill, Michael B. Prentice used as an introduction to protists for Michel J. Weber many school children; Euglena, the iconic Low Levels of Genetic 2052 fl agellate that is often used to challenge Soft Sweeps III: The Signature 1998 Divergence across e215 ideas of plants (Euglena has chloroplasts) of Positive Selection from e186 Geographically and and animals (Euglena moves); Stentor, Recurrent Mutation Linguistically Diverse one of the larger ciliates; Cacatua, the Pleuni S. Pennings, Joachim Populations from India sulphur-crested cockatoo from Australia; Hermisson Noah A. Rosenberg, Saurabh Paulinella, a shelled amoeba that Mahajan, Catalina Gonzalez- contains two cyanobacterial symbionts; Adaptive Stress Response in 2013 Quevedo, Michael G. B. Blum, Thalassionema, one of the more common Segmental Progeria Resembles e192 Laura Nino-Rosales, Vasiliki diatoms; Jakoba, a colorless free- Long-Lived Dwarfi sm and Ninis, Parimal Das, Madhuri living fl agellate; Massisteria, a marine Calorie Restriction in Mice Hegde, Laura Molinari, Gladys amoebofl agellate with fi ne radiating Marieke van de Ven, Jaan-Olle Zapata, James L. Weber, John W. pseudopodia; Deltotrichonympha, one Andressoo, Valerie B. Holcomb, Belmont, Pragna I. Patel of the large fl agellates with numerous Marieke von Lindern, Willeke fl agella that live in the guts of wood- M. C. Jong, Chris I. De Zeeuw, Evaluating Support for the 2062 eating termites; Pinus, a pine from the Yousin Suh, Paul Hasty, Jan H. J. Current Classifi cation of e220 Eastern Sierras in California; Elphidium, Hoeijmakers, Gijsbertus T. J. van Eukaryotic Diversity one of the foraminifera, the so-called der Horst, James R. Mitchell Laura Wegener Parfrey, “shelled amoebae” (see Parfrey et al., Erika Barbero, Elyse Lasser, e220). Global Mapping of Transposon 2026 Micah Dunthorn, Debashish Cover credit: layout and design by David Location e212 Bhattacharya, David J. Patterson, J. Patterson; all images by D. J. Patterson Abram Gabriel, Johannes Laura A. Katz except Deltotrichonympha, which was taken Dapprich, Mark Kunkel, David by Guy Brugerolle. Gresham, Stephen C. Pratt, doi:10.1371/journal.pgen.0020226.g001 Maitreya J. Dunham Continued on next page PLoS Genetics | www.plosgenetics.org iii December 2006 | Volume 2 | Issue 12 Evaluating Support for the Current Classification of Eukaryotic Diversity Laura Wegener Parfrey1, Erika Barbero2, Elyse Lasser2, Micah Dunthorn1, Debashish Bhattacharya3,4, David J. Patterson5, Laura A. Katz1,2* 1 Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, Massachusetts, United States of America, 2 Department of Biological Sciences, Smith College, Northampton, Massachusetts, United States of America, 3 Department of Biological Sciences, University of Iowa, Iowa City, Iowa, United States of America, 4 Roy J. Carver Center for Comparative Genomics, University of Iowa, Iowa City, Iowa, United States of America, 5 Bay Paul Center for Genomics, Marine Biological Laboratory, Woods Hole, Massachusetts, United States of America Perspectives on the classification of eukaryotic diversity have changed rapidly in recent years, as the four eukaryotic groups within the five-kingdom classification—plants, animals, fungi, and protists—have been transformed through numerous permutations into the current system of six ‘‘supergroups.’’ The intent of the supergroup classification system is to unite microbial and macroscopic eukaryotes based on phylogenetic inference. This supergroup approach is increasing in popularity in the literature and is appearing in introductory biology textbooks. We evaluate the stability and support for the current six-supergroup classification of eukaryotes based on molecular genealogies. We assess three aspects of each supergroup: (1) the stability of its taxonomy, (2) the support for monophyly (single evolutionary origin) in molecular analyses targeting a supergroup, and (3) the support for monophyly when a supergroup is included as an out-group in phylogenetic studies targeting other taxa. Our analysis demonstrates that supergroup taxonomies are unstable and that support for groups varies tremendously, indicating that the current classification scheme of eukaryotes is likely premature. We highlight several trends contributing to the instability and discuss the requirements for establishing robust clades within the eukaryotic tree of life. Citation: Parfrey LW, Barbero E, Lasser E, Dunthorn M, Bhattacharya D, et al. (2006) Evaluating support for the current classification of eukaryotic diversity. PLoS Genet 2(12): e220. doi:10.1371/journal.pgen.0020220 Introduction erally been placed in one (Protista [2–4] or Protoctista [5]) or two (Protozoa and Chromista [6]) groups (Figure 1; but see Biological research is based on the shared history of living also [7,8]). However, this historic distinction between macro- things. Taxonomy—the science of classifying organismal scopic and microscopic eukaryotes does not adequately diversity—is the scaffold on which biological knowledge is capture their complex evolutionary relationships or the vast assembled and integrated into a cohesive structure. A diversity within the microbial world. comprehensive eukaryotic taxonomy is a powerful research In the past decade, the emphasis in high-level taxonomy has tool in evolutionary genetics, medicine, and many other shifted away from the historic kingdoms and toward a new fields. As the foundation of much subsequent research, the system of six supergroups that aims to portray evolutionary framework must, however, be robust. Here we test the relationships between microbial and macrobial lineages. The existing framework by evaluating the support for and stability supergroup concept is gaining popularity as evidenced by of the classification of eukaryotic diversity into six super- several reviews [9,10] and inclusion in forthcoming editions groups. of introductory biology textbooks. In addition, the Interna- Eukaryotes (organisms containing nuclei) encompass in- tional Society of Protozoologists recently proposed a formal credible morphological diversity from picoplankton of only reclassification of eukaryotes into six supergroups, though two microns in size to the blue whale and giant sequoia that acknowledging uncertainty in some groups [7]. are eight orders of magnitude larger. Many evolutionary innovations are found only in eukaryotes, some of which are The Supergroups present in all lineages (e.g., the cytoskeleton, nucleus) and Below we introduce the six supergroups in alphabetical others that are restricted to a few lineages (e.g., multi- order (Figure 2). The supergroup ‘‘Amoebozoa’’ was proposed cellularity, photosynthetic organelles [plastids]). These and in 1996 [11]. Original evidence for the group was drawn from other eukaryotic features evolved within microbial eukar- yotes (protists) that thrived for hundreds of millions of years Editor: David M. Hillis, University of Texas, United States of America before they gave rise independently to multicellular eukar- yotes, the familiar plants, animals, and fungi [1]. Thus, Received May 11, 2006; Accepted November 9, 2006; Published December 22, 2006 elucidating the origins of novel eukaryotic traits requires a A previous version of this article appeared as an Early Online Release on November comprehensive phylogeny—an inference of organismal rela- 13, 2006 (doi:10.1371/journal.pgen.0020220.eor). tionships—that includes the diverse microbial lineages. Copyright: Ó 2006 Parfrey et al. This is an open-access article distributed under the Higher-level classifications have historically emphasized terms of the Creative Commons Attribution License, which permits unrestricted the visible diversity of large eukaryotes, as reflected by the use, distribution, and reproduction in any medium, provided the original author establishment of the plant, animal, and fungal kingdoms. In and source are credited. these schemes the diverse microbial