Turning the crown upside down: gene tree parsimony roots the eukaryotic tree of life.

The first analyses of gene sequence data indicated that the eukaryotic tree of life consisted of a long stem of microbial groups "topped" by a crown-containing plants, animals, and fungi and their microbial relatives. Although more recent multigene concatenated analyses have refined the relationships among the many branches of eukaryotes, the root of the eukaryotic tree of life has remained elusive. Inferring the root of extant eukaryotes is challenging because of the age of the group (∼1.7-2.1 billion years old), tremendous heterogeneity in rates of evolution among lineages, and lack of obvious outgroups for many genes. Here, we reconstruct a rooted phylogeny of extant eukaryotes based on minimizing the number of duplications and losses among a collection of gene trees. This approach does not require outgroup sequences or assumptions of orthology among sequences. We also explore the impact of taxon and gene sampling and assess support for alternative hypotheses for the root. Using 20 gene trees from 84 diverse eukaryotic lineages, this approach recovers robust eukaryotic clades and reveals evidence for a eukaryotic root that lies between the Opisthokonta (animals, fungi and their microbial relatives) and all remaining eukaryotes.

[1]  B. Lang,et al.  Rooting the eukaryotic tree with mitochondrial and bacterial proteins. , 2012, Molecular biology and evolution.

[2]  Oliver Eulenstein,et al.  Genome-scale phylogenetics: inferring the plant tree of life from 18,896 gene trees. , 2011, Systematic biology.

[3]  David Fernández-Baca,et al.  iGTP: A software package for large-scale gene tree parsimony analysis , 2010, BMC Bioinformatics.

[4]  L. Katz,et al.  Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life. , 2010, Systematic biology.

[5]  T. Cavalier-smith.  Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree , 2010, Biology Letters.

[6]  Oliver Eulenstein,et al.  Efficient genome-scale phylogenetic analysis under the duplication-loss and deep coalescence cost models , 2010, BMC Bioinformatics.

[7]  Y. Inagaki,et al.  Large-Scale Phylogenomic Analyses Reveal That Two Enigmatic Protist Lineages, Telonemia and Centroheliozoa, Are Related to Photosynthetic Chromalveolates , 2009, Genome biology and evolution.

[8]  L. Katz,et al.  Molecular Data are Transforming Hypotheses on the Origin and Diversification of Eukaryotes , 2009, Bioscience.

[9]  L. Hug,et al.  Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups” , 2009, Proceedings of the National Academy of Sciences.

[10]  Anne Bruneau,et al.  Measuring branch support in species trees obtained by gene tree parsimony. , 2009, Systematic biology.

[11]  Oliver Eulenstein,et al.  DupTree: a program for large-scale phylogenetic analyses using gene tree parsimony , 2008, Bioinform..

[12]  L. Katz,et al.  BMC Evolutionary Biology BioMed Central Research article Broadly sampled multigene trees of eukaryotes , 2008 .

[13]  M. Sanderson,et al.  Inferring angiosperm phylogeny from EST data with widespread gene duplication , 2007, BMC Evolutionary Biology.

[14]  Jerzy Tiuryn,et al.  URec: a system for unrooted reconciliation , 2007, Bioinform..

[15]  Laura Wegener Parfrey,et al.  Evaluating Support for the Current Classification of Eukaryotic Diversity , 2006, PLoS genetics.

[16]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[17]  L. Hug,et al.  The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[18]  J. G. Burleigh,et al.  Supertree bootstrapping methods for assessing phylogenetic variation among genes in genome-scale data sets. , 2006, Systematic biology.

[19]  S. Adl,et al.  The New Higher Level Classification of Eukaryotes with Emphasis on the Taxonomy of Protists , 2005, The Journal of eukaryotic microbiology.

[20]  T. Kuroiwa,et al.  PHYLOGENETIC IMPLICATIONS OF THE CAD COMPLEX FROM THE PRIMITIVE RED ALGA CYANIDIOSCHYZON MEROLAE (CYANIDIALES, RHODOPHYTA) 1 , 2005 .

[21]  Masami Hasegawa,et al.  Root of the Eukaryota tree as inferred from combined maximum likelihood analyses of multiple molecular sequence data. , 2005, Molecular biology and evolution.

[22]  P. Jallepalli,et al.  Ufd2, a Novel Autoantigen in Scleroderma, Regulates Sister Chromatid Separation , 2004, Cell cycle.

[23]  E. Koonin,et al.  Comparative Genomics, Evolution and Origins of the Nuclear Envelope and Nuclear Pore Complex , 2004, Cell cycle.

[24]  O. Bininda-Emonds.  Phylogenetic Supertrees: Combining Information To Reveal The Tree Of Life , 2004 .

[25]  T. Cavalier-smith,et al.  Phylogenetic Analysis of Eukaryotes Using Heat-Shock Protein Hsp90 , 2003, Journal of Molecular Evolution.

[26]  W. Martin,et al.  Early Cell Evolution, Eukaryotes, Anoxia, Sulfide, Oxygen, Fungi First (?), and a Tree of Genomes Revisited , 2003, IUBMB life.

[27]  Roderic D. M. Page,et al.  Going nuclear: gene family evolution and vertebrate phylogeny reconciled , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  T. Cavalier-smith,et al.  Rooting the Eukaryote Tree by Using a Derived Gene Fusion , 2002, Science.

[29]  W. Doolittle,et al.  A kingdom-level phylogeny of eukaryotes based on combined protein data. , 2000, Science.

[30]  Bin Ma,et al.  From Gene Trees to Species Trees , 2000, SIAM J. Comput..

[31]  James R. Brown,et al.  Gene Descent, Duplication, and Horizontal Transfer in the Evolution of Glutamyl- and Glutaminyl-tRNA Synthetases , 1999, Journal of Molecular Evolution.

[32]  D. Patterson,et al.  The Diversity of Eukaryotes , 1999, The American Naturalist.

[33]  M. Sogin,et al.  Primary Structure and Phylogenetic Relationships of a Malate Dehydrogenase Gene from Giardia lamblia , 1999, Journal of Molecular Evolution.

[34]  E. Canning,et al.  A mitochondrial Hsp70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria , 1997, Current Biology.

[35]  Yves Van de Peer,et al.  Evolutionary Relationships Among the Eukaryotic Crown Taxa Taking into Account Site-to-Site Rate Variation in 18S rRNA , 1997, Journal of Molecular Evolution.

[36]  Temple F. Smith,et al.  Reconstruction of ancient molecular phylogeny. , 1996, Molecular phylogenetics and evolution.

[37]  T. Cavalier-smith,et al.  Kingdom protozoa and its 18 phyla. , 1993, Microbiological reviews.

[38]  William R. Taylor,et al.  The rapid generation of mutation data matrices from protein sequences , 1992, Comput. Appl. Biosci..

[39]  S. Osawa,et al.  Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Masasuke Yoshida,et al.  Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[41]  M. Sogin,et al.  Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. , 1989, Science.

[42]  J. Felsenstein.  CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[43]  A. R. Templeton,et al.  PHYLOGENETIC INFERENCE FROM RESTRICTION ENDONUCLEASE CLEAVAGE SITE MAPS WITH PARTICULAR REFERENCE TO THE EVOLUTION OF HUMANS AND THE APES , 1983, Evolution; international journal of organic evolution.

[44]  G. Moore,et al.  Fitting the gene lineage into its species lineage , 1979 .

[45]  J. Felsenstein.  Cases in which Parsimony or Compatibility Methods will be Positively Misleading , 1978 .

[46]  F. Wilcoxon.  Individual Comparisons by Ranking Methods , 1945 .

[47]  H. Philippe,et al.  The diversity of eukaryotes and the root of the eukaryotic tree. , 2007, Advances in experimental medicine and biology.

[48]  Roderic D. M. Page,et al.  Taxonomy, Supertrees, and the Tree of Life , 2004 .