Multicellularity arose several times in the evolution of eukaryotes (Response to DOI 10.1002/bies.201100187)

The cellular slime mold Dictyostelium has cell‐cell connections similar in structure, function, and underlying molecular mechanisms to animal epithelial cells. These similarities form the basis for the proposal that multicellularity is ancestral to the clade containing animals, fungi, and Amoebozoa (including Dictyostelium): Amorphea (formerly “unikonts”). This hypothesis is intriguing and if true could precipitate a paradigm shift. However, phylogenetic analyses of two key genes reveal patterns inconsistent with a single origin of multicellularity. A single origin in Amorphea would also require loss of multicellularity in each of the many unicellular lineages within this clade. Further, there are numerous other origins of multicellularity within eukaryotes, including three within Amorphea, that are not characterized by these structural and mechanistic similarities. Instead, convergent evolution resulting from similar selective pressures for forming multicellular structures with motile and differentiated cells is the most likely explanation for the observed similarities between animal and dictyostelid cell‐cell connections.

[1]  W. Weis,et al.  An epithelial tissue in Dictyostelium challenges the traditional origin of metazoan multicellularity , 2012, Bioessays.

[2]  P. Winn,et al.  ARABIDILLO gene homologues in basal land plants: species-specific gene duplication and likely functional redundancy , 2012, Planta.

[3]  Matthew W. Brown,et al.  The Revised Classification of Eukaryotes , 2012, The Journal of eukaryotic microbiology.

[4]  D. Richter,et al.  Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/β-catenin complex , 2012, Proceedings of the National Academy of Sciences.

[5]  J. G. Burleigh,et al.  Turning the crown upside down: gene tree parsimony roots the eukaryotic tree of life. , 2012, Systematic biology.

[6]  Matthew W. Brown,et al.  Aggregative Multicellularity Evolved Independently in the Eukaryotic Supergroup Rhizaria , 2012, Current Biology.

[7]  P. Keeling,et al.  The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins , 2012, Proceedings of the Royal Society B: Biological Sciences.

[8]  E. Yang,et al.  Ancient gene paralogy may mislead inference of plastid phylogeny. , 2012, Molecular biology and evolution.

[9]  S. Baldauf,et al.  Evolution and diversity of dictyostelid social amoebae. , 2012, Protist.

[10]  G. Manning,et al.  Genomic Survey of Premetazoans Shows Deep Conservation of Cytoplasmic Tyrosine Kinases and Multiple Radiations of Receptor Tyrosine Kinases , 2012, Science Signaling.

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

[12]  Riet De Smet,et al.  Redundancy and rewiring of genetic networks following genome-wide duplication events. , 2012, Current opinion in plant biology.

[13]  B. Lang,et al.  Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single-copy protein domains. , 2012, Molecular biology and evolution.

[14]  M. Travisano,et al.  Experimental evolution of multicellularity , 2012, Proceedings of the National Academy of Sciences.

[15]  L. Katz,et al.  Subulatomonas tetraspora nov. gen. nov. sp. is a member of a previously unrecognized major clade of eukaryotes. , 2011, Protist.

[16]  Matthias Platzer,et al.  Phylogeny-wide analysis of social amoeba genomes highlights ancient origins for complex intercellular communication. , 2011, Genome research.

[17]  T. Cavalier-smith,et al.  A revised classification of naked lobose amoebae (Amoebozoa: lobosa). , 2011, Protist.

[18]  Daniel J. G. Lahr,et al.  Estimating the timing of early eukaryotic diversification with multigene molecular clocks , 2011, Proceedings of the National Academy of Sciences.

[19]  Daniel J. G. Lahr,et al.  Comprehensive Phylogenetic Reconstruction of Amoebozoa Based on Concatenated Analyses of SSU-rDNA and Actin Genes , 2011, PloS one.

[20]  E. Gaucher,et al.  The evolutionary history of the catenin gene family during metazoan evolution , 2011, BMC Evolutionary Biology.

[21]  M. Perez-Moreno,et al.  Faculty Opinions recommendation of A polarized epithelium organized by beta- and alpha-catenin predates cadherin and metazoan origins. , 2011 .

[22]  A. Knoll The Multiple Origins of Complex Multicellularity , 2011 .

[23]  Matthew W. Brown,et al.  "Slime molds" among the Tubulinea (Amoebozoa): molecular systematics and taxonomy of Copromyxa. , 2011, Protist.

[24]  W. Weis,et al.  A Polarized Epithelium Organized by β- and α-Catenin Predates Cadherin and Metazoan Origins , 2011, Science.

[25]  B Franz Lang,et al.  Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. , 2011, Molecular biology and evolution.

[26]  Mark A. Miller,et al.  Creating the CIPRES Science Gateway for inference of large phylogenetic trees , 2010, 2010 Gateway Computing Environments Workshop (GCE).

[27]  N. King,et al.  Diverse evolutionary paths to cell adhesion. , 2010, Trends in cell biology.

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

[29]  A. Sebé-Pedrós,et al.  Integrin-mediated adhesion complex , 2010, Communicative & integrative biology.

[30]  Philip C. J. Donoghue,et al.  Early life: Origins of multicellularity , 2010, Nature.

[31]  Tal Pupko,et al.  GUIDANCE: a web server for assessing alignment confidence scores , 2010, Nucleic Acids Res..

[32]  A. Roger,et al.  Ancient origin of the integrin-mediated adhesion and signaling machinery , 2010, Proceedings of the National Academy of Sciences.

[33]  Yang Liu,et al.  Convergent sequence evolution between echolocating bats and dolphins , 2010, Current Biology.

[34]  Matthew W. Brown,et al.  Phylogeny of the "forgotten" cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. , 2009, Molecular biology and evolution.

[35]  S. Leys,et al.  Epithelia and integration in sponges. , 2009, Integrative and comparative biology.

[36]  Peter V. Troshin,et al.  The origin of Metazoa: a transition from temporal to spatial cell differentiation , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[37]  A. Simpson,et al.  Evolution: Revisiting the Root of the Eukaryote Tree , 2009, Current Biology.

[38]  J. Rougemont,et al.  A rapid bootstrap algorithm for the RAxML Web servers. , 2008, Systematic biology.

[39]  Kazutaka Katoh,et al.  Recent developments in the MAFFT multiple sequence alignment program , 2008, Briefings Bioinform..

[40]  M. Martindale,et al.  Cell-Cell Adhesion in the Cnidaria: Insights Into the Evolution of Tissue Morphogenesis , 2008, The Biological Bulletin.

[41]  H. Urushihara Developmental biology of the social amoeba: History, current knowledge and prospects , 2008, Development, growth & differentiation.

[42]  R. Grosberg,et al.  The Evolution of Multicellularity: A Minor Major Transition? , 2007 .

[43]  Carien M Niessen,et al.  Tight junctions/adherens junctions: basic structure and function. , 2007, The Journal of investigative dermatology.

[44]  Michael Weiss,et al.  A higher-level phylogenetic classification of the Fungi. , 2007, Mycological research.

[45]  Ralph Gräf,et al.  Towards a molecular understanding of human diseases using Dictyostelium discoideum. , 2006, Trends in molecular medicine.

[46]  L. Laplaze,et al.  Armadillo-related proteins promote lateral root development in Arabidopsis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[48]  David L. Steffen,et al.  The genome of the social amoeba Dictyostelium discoideum , 2005, Nature.

[49]  David Posada,et al.  ProtTest: selection of best-fit models of protein evolution , 2005, Bioinform..

[50]  E. Fuchs,et al.  α-catenin: at the junction of intercellular adhesion and actin dynamics , 2004, Nature Reviews Molecular Cell Biology.

[51]  M. Martindale,et al.  An ancient role for nuclear β-catenin in the evolution of axial polarity and germ layer segregation , 2003, Nature.

[52]  T. Cavalier-smith,et al.  The root of the eukaryote tree pinpointed , 2003, Current Biology.

[53]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[54]  J. W. Valentine,et al.  Phylogeny of Opisthokonta and the evolution of multicellularity and complexity in Fungi and Metazoa , 2003, International Journal of Astrobiology.

[55]  Jianzhi Zhang Evolution by gene duplication: an update , 2003 .

[56]  J. Finnerty,et al.  Protein evolution: structure-function relationships of the oncogene beta-catenin in the evolution of multicellular animals. , 2003, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[57]  A. Harwood,et al.  Loss of the β-catenin homologue aardvark causes ectopic stalk formation in Dictyostelium , 2002, Mechanisms of Development.

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

[59]  Hidetoshi Shimodaira An approximately unbiased test of phylogenetic tree selection. , 2002, Systematic biology.

[60]  J. Coates,et al.  Cell-cell adhesion and signal transduction during Dictyostelium development. , 2001, Journal of cell science.

[61]  Masami Hasegawa,et al.  CONSEL: for assessing the confidence of phylogenetic tree selection , 2001, Bioinform..

[62]  R. Kessin Dictyostelium: Membranes and Organelles of Dictyostelium , 2001 .

[63]  J. Coates,et al.  Adherens junctions and β-catenin-mediated cell signalling in a non-metazoan organism , 2000, Nature.

[64]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

[65]  M. Nei,et al.  Purifying selection and birth-and-death evolution in the ubiquitin gene family. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[68]  A. Wilson,et al.  Molecular adaptation of a leaf-eating bird: stomach lysozyme of the hoatzin. , 1994, Molecular biology and evolution.

[69]  R. Blanton,et al.  Aerial Sorocarp Development By the Aggregative Ciliate, Sorogena Stoianovitchae*: Sorogena stoianovitchae: SOROCARP DEVELOPMENT , 1980 .

[70]  M. Dykstra,et al.  Sorodiplophrys: An Unusual Sorocarp-Producing Protist , 1975 .

[71]  Dr. Susumu Ohno Evolution by Gene Duplication , 1970, Springer Berlin Heidelberg.

[72]  Arnau Sebé Pedrós,et al.  The integrin-mediated adhesion complex: cooption of signaling systems at the dawn of Metazoa , 2010 .

[73]  M. Kojima,et al.  Dynamic Enumeration of All Mixed Cells Dynamic Enumeration of All Mixed Cells , 2006 .

[74]  T. Cavalier-smith Protist phylogeny and the high-level classification of Protozoa , 2003 .

[75]  J. B. Walsh,et al.  How often do duplicated genes evolve new functions? , 1995, Genetics.