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Molecular Phylogeny and Evolution of Morphology in the Social Amoebas

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Molecular Phylogeny and Evolution of Morphology in the Social Amoebas REPORTS 26. R. Vassar, J. Ngai, R. Axel, Cell 74, 309 (1993). fellowship of JSPS. We thank A. Miyawaki, R. Sprengel, Figs. S1 to S6 27. K. Miyamichi, S. Serizawa, H. M. Kimura, H. Sakano, S. McKnight, and M. Mishina for cDNA clones and Table S1 J. Neurosci. 25, 3586 (2005). T. Yamamori, H. Matsunami, and members of our laboratory References 28. This work was supported by the CREST Program of the for valuable comments. Japan Science and Technology Agency and by grants from 27 June 2006; accepted 8 September 2006 Mitsubishi Foundation, Japan Society for the Promotion of Supporting Online Material Published online 21 September 2006; Science (JSPS), and the Ministry of Education, Culture and www.sciencemag.org/cgi/content/full/1131794/DC1 10.1126/science.1131794 Science of Japan. T.I. was supported by a predoctoral Materials and Methods Include this information when citing this paper. Nearly complete small subunit rRNA (SSU Molecular Phylogeny and Evolution of rDNA) gene sequences were determined from more than 100 isolates of Dictyostelia, including Morphology in the Social Amoebas nearly every described species currently in culture worldwide (7). Phylogenetic analyses of these data identified four major subdivisions Pauline Schaap,1 Thomas Winckler,2 Michaela Nelson,3 Elisa Alvarez-Curto,1 Barrie Elgie,3 of the group, which we numbered 1 to 4 (Fig. Hiromitsu Hagiwara,4 James Cavender,5 Alicia Milano-Curto,1 Daniel E. Rozen,1* 1 and fig. S1). Group 1 consists of a morpho- Theodor Dingermann,6,7 Rupert Mutzel,8 Sandra L. Baldauf3† logically diverse set of Dictyostelium species. Group 2 is a mixture of species with representa- The social amoebas (Dictyostelia) display conditional multicellularity in a wide variety of forms. tives of all three traditional genera, including Despite widespread interest in Dictyostelium discoideum as a model system, almost no molecular all pale-colored species of Polysphondylium, data exist from the rest of the group. We constructed the first molecular phylogeny of the at least two species of Dictyostelium, and all Dictyostelia with parallel small subunit ribosomal RNA and a-tubulin data sets, and we found that species of Acytostelium. Group 3 is again a di- dictyostelid taxonomy requires complete revision. A mapping of characters onto the phylogeny verse set of purely Dictyostelium species, also shows that the dominant trend in dictyostelid evolution is increased size and cell type including the single cannibalistic species, D. specialization of fruiting structures, with some complex morphologies evolving several times caveatum. The largest group is group 4, which independently. Thus, the latter may be controlled by only a few genes, making their underlying consists almost entirely of Dictyostelium spe- mechanisms relatively easy to unravel. cies but may also include a clade of two violet- colored species from two separate traditional ulticellular animals and plants display region of the slug senses environmental stimuli genera, P. violaceum and D. laterosorum. With an enormous variety of forms, but their such as temperature and light and directs the slug the exception of the violet-colored species, Munderlying genetic diversity is small toward the soil’s outer surface, where spores will group 4 is a fairly homogeneous set of large compared with the genetic diversity of microbes. be readily dispersed. The slug then stands up to robust species, including the model organism Eukaryotic microbes include a broad range of form the fruiting body, or sorocarp. The cells in D. discoideum and the cosmopolitan species, unicellular life forms, with multiple independent the head region move into a prefabricated cel- D. mucoroides, which appears to be polyphy- inventions of multicellularity. One of the most lulose tube and differentiate into stalk cells that letic (8). intriguing challenges in biology is to understand ultimately die. The remaining “body” cells then The four SSU rDNA groupings are con- the reason behind the repeated occurrence of this crawl up the stalk and encapsulate to form spores. firmed by a-tubulin phylogeny (fig. S2) with particular evolutionary stratagem. Thus, the Dictyostelia display distinct character- two exceptions: (i) A. ellipticum is only weakly The social amoebas, or Dictyostelia, are a istics of true multicellularity, such as cell-cell placed with group 2 in the a-tubulin tree (fig. group of organisms that hover on the borderline signaling, cellular specialization, coherent cell S2), and (ii) the D. laterosorum and P.violaceum between uni- and multicellularity. Each orga- movement, programmed cell death, and altruism clade is grouped together with D. polycephalum nism starts its life as a unicellular amoeba, but (1, 2). as the sister group to a weakly supported group 3 they aggregate to form a multicellular fruiting Traditionally, social amoebas have been plus group 4 clade (0.64 Bayesian inference body when starved. This process has been best classified according to their most notable trait, posterior probability, 51% maximum likelihood described for the model organism Dictyostelium fruiting body morphology. Based on this, three bootstrap, fig. S2). This is in contrast to its discoideum. The aggregate of up to 100,000 genera have been proposed: Dictyostelium,with position as the exclusive sister lineage to group 4 D. discoideum cells first transforms into a unbranched or laterally branched fruiting in the SSU rDNA tree (Fig. 1). The SSU rDNA finger-shaped structure, the “slug.” The head bodies; Polysphondylium, whose fruiting bodies phylogeny also strongly supports group 1 as the consist of repetitive whorls of regularly spaced deepest major divergence in Dictyostelia (Fig. 1School of Life Sciences, University of Dundee, DD15EH Dun- side branches; and Acytostelium,which,unlike 1 and fig. S1), as do analyses of combined SSU dee, UK. 2Lehrstuhl für Pharmazeutische Biologie, Universität a 3 the other genera, forms acellular fruiting body rDNA plus -tubulin nucleotide sequences (fig. Jena, Semmelweisstrasse 10, 07743 Jena, Germany. Depart- 1 ment of Biology, University of York, Box 373, York YO10 5YW, stalks ( ). S3). However, an alternative root is weakly re- UK. 4Department of Botany, Tokyo National Science Mu- Despite the widespread use of D. discoideum covered in the a-tubulin amino acid phylogeny seum, Tsukuba Botanical Garden, 4-1-1, Amakubo, Tsukuba-shi, as a model organism (2, 3), the Dictyostelia as a (fig. S2). Thus, the position of the dictyostelid Ibaraki 305-0005, Japan. 5Department of Environmental and whole are poorly characterized in molecular root still requires confirmation, which will Plant Biology, Ohio University, 307 Porter Hall, Athens, OH terms; nearly all currently available data are from probably require multiple additional genes. 45701, USA. 6Institut für Pharmazeutische Biologie, Universität Frankfurt, Marie-Curie-Strasse 9, 60439 Frankfurt, Germany. a single species. Nonetheless, the social amoebas A notable feature of both phylogenies is 7Zentrum für Arzneimittelforschung, Entwicklung und Sicher- provide a unique opportunity to understand the the split of the genus Polysphondylium. The heit (ZAFES), Frankfurt, Germany. 8Institut für Biologie, evolution of multicellularity (4–6). A primary and violet-colored P. violaceum is unequivocally Fachbereich Biologie, Chemie, Pharmazie, Freie Universität essential prerequisite for this is an understanding grouped together with D. laterosorum, and Berlin, Königin-Luise Strasse 12-16, 14195 Berlin, Germany. of the true phylogeny of the group. Here, we these two lie together at the base of group 4 *Present address: Faculty of Life Sciences, University of Manchester, Oxford Road, Manchester M13 9PT, UK. describe the phylogeny of social amoeba species (Fig. 1) or in groups 3 and 4 (fig. S2). Mean- †To whom correspondence should be addressed. E-mail: and trace the acquisition of morphological and while, the pale-colored polysphondylids are [email protected] functional complexity during their evolution. all found nested within group 2 (Fig. 1 and www.sciencemag.org SCIENCE VOL 314 27 OCTOBER 2006 661 REPORTS D. brefeldianum TNS-C-115 D. mucoroides S28b D. capitatum 91HO-50 Bayesian Inference D. pseudobrefeldianum 91HO-8 posterior probabilities Group 4 D. aureocephalum TNS-C-180 D. aureum SL1 0.97-1.0 D. septentrionalis IY49 0.90-0.96 D. septentrionalis AK2 0.75-0.89 D. implicatum 93HO-1 0.50-0.74 D. medium TNS-C-205 D. laterosorum AE4 D. mucoroides var. stoloniferum FOII-1 <0.50 P. violaceum P6 D. crassicaule 93HO-33 D. australe NZ80B D. mucoroides TNS-C-114 D. monochasioides HAG653 D. sphaerocephalum GR11 D. tenue Pan52 D. rosarium M45 D. potamoides FP1A D. clavatum TNS-C-220 D. minutum 71-2 D. clavatum TNS-C-189 D. tenue PJ6 D. longosporum TNS-C-109 D. tenue PR4 Group 3 D. purpureum C143 D. gracile TNS-C-183 D. purpureum WS321 D. lavandulum B15 D. macrocephalum B33 D. vinaceo-fuscum CC4 D. discoideum 91HO-9 D. rhizopodium AusKY-4 D. discoideum AX4 D. coeruleo-stipes CRLC53B D. discoideum AX2 D. lacteum D. menorum M1 D. discoideum X00134 D. caveatum WS695 ] D. discoideum NC4 D. discoideum AC4 D. polycephalum MY1-1 D. citrinum OH494 D. polycarpum VE1b D. discoideum V34 D. polycarpum OhioWILDS D. dimigraformum AR5b P. filamentosum SU-1 D. intermedium PJ11 P. luridum LR-2 D. firmibasis TNS-C-14 P. pallidum TNS-C-98 D. brunneum WS700 0.01 P. equisetoides B75B D. giganteum WS589 P. nandutensis YA1 D. robustum TNS-C-219 1.00 P. colligatum OH538 D. laterosorum AE4 P. tikaliensis OH595 P. violaceum P6 P. anisocaule NZ47B P. pseudocandidum TNS-C-91 P. tenuissimum TNS-C-97 D. gloeosporum TCK52 Group 2 P. pallidum PN500 P. asymmetricum OH567 D. oculare DB4B A. ellipticum AE2 A. anastomosans PP1 A. longisorophorum DB10A A. leptosomum FG12 A. digitatum OH517 A. serpentarium SAB3A ] A. subglobosum Lb1 D. antarcticum NZ43B D. fasciculatum SmokOW9A D. delicatum TNS-C-226 D. fasciculatum SH3 D. aureo-stipes var. helveticum GE1 D. aureo-stipes YA6 D. aureo-stipes JKS150 D. granulophorum CHII-4 Group 1 D.
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