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The Diploblast-Bilateria sister hypothesis

The Diploblast-Bilateria sister hypothesis [Communicative & Integrative Biology 2:5, 403-405; September/October 2009]; ©2009 Landes Bioscience Article Addendum Parallel evolution of a nervous systems may have been a simple step 1,2, 2 1 2, Bernd Schierwater, * Sergios-Orestis Kolokotronis, Michael Eitel and Rob DeSalle * 1 2 ITZ; Ecology and Evolution; Tierärztliche Hochschule Hannover; Hannover, Germany; Sackler Institute for Comparative Genomics, American Museum of Natural History; New York, NY USA Key words: placozoa, trichoplax, urmetazoon hypothesis, basal metazoan evolution, trichoplax.com, pre-nervous system, placula hypothesis For many familiar with metazoan relationships and body plans, We could not overturn the sister group relationship of these two the hypothesis of a sister group relationship between Diploblasta groups regardless of the larger taxonomic sampling or the statistical and Bilateria comes as a surprise. One of the consequences of tests we used in the present analysis (Fig. 1A). It is clear to us from this hypothesis—the independent evolution of a nervous system analyses with broader taxonomic representation that the sister rela- in Coelenterata and Bilateria—seems highly unlikely to many. tionship of Bilateria and Diploblasta is a valid hypothesis. However, to a small number of scientists working on Metazoa, With respect to the controversial aspect of parallel nervous the parallel evolution of the nervous system is not surprising system evolution, we point out that a definition of a nervous at all and rather a confirmation of old morphological and new system that satisfies most is that nervous systems are spatially 2-4 genetic knowledge. The controversial hypothesis that the organized systems of aggregated nerve cells. The simple question, Diploblasta and Bilateria are sister taxa is, therefore, tantamount “what is a nerve cell?” then becomes the crux of the argument. But, to reconciling the parallel evolution of the nervous system in this question elicits a spectrum of answers from different experts. Coelenterata and Bilateria. In this addendum to Schierwater Accurate homology statements concerning nerve cells are crucial et al. we discuss two aspects critical to the controversy. First to the story and these have to wait for a general definition of what we discuss the strength of the inference of the proposed sister a nerve cell is. The key to these definitions lies in examining the 2,6 relationship of Diploblasta and Bilateria and second we discuss non-bilaterian animals. In most modern views “early nervous the implications for the evolution of nerve cells and nervous system evolution” is the equivalent of “early co-evolution of elec- systems. trical excitability and functional synapses organizing intracellular and extracellular signaling processes spatio-temporally”. Most The analysis in Schierwater et al. involved 24 ingroup taxa zoologists agree that neither Placozoa nor Porifera have nerve cells and several carefully chosen outgroups. Here we present a larger or a nervous system, but it is important to recognize that both analysis of 72 taxa to reinforce the inference we obtained with sponges and placozoans show behavior. They respond in a coordi- the smaller taxonomic sample. Figure 1A presents the results of nated way to external stimuli that must be perceived and mediated this analysis and shows clearly that the Bilateria and Diploblasta by some kind of perception and transduction cells. Both sponges are monophyletic and sister to each other with robust bootstrap and placozoans harbor a pre-nervous integration system with many support for both parsimony and maximum likelihood analyses. so-called “nerve cell typical” features, molecules and related genes, but these characteristics cannot be co-localized with any specific 7-10 *Correspondence to: Bernd Schierwater; ITZ; Ecology and Evolution; Tierärztliche cell type. While in sponges several cell types are likely involved Hochschule Hannover; Hannover D-30559 Germany; Email: bernado@trichoplax. in signal perception and transduction, in placozoans it seems to be com/Rob DeSalle; Sackler Institute for Comparative Genomics, American Museum a single cell type only, the fiber cells, which form a loose connec- of Natural History, Central Park West at 79th Street, New York, NY 10024, USA; tion network in the center of the placozoan body. Email: [email protected] Although we are far away from a general definition of a nerve Submitted: 04/16/09; Accepted: 04/17/09 cell (and therefore a definition for nervous system), we can still Previously published online as a Communicative & Integrative Biology summarize our current knowledge on early nerve cell evolu- E-publication: tion (Fig. 1B) as follows: The last common metazoan ancestor http://www.landesbioscience.com/journals/cib/article/8763 (LCMA) likely possessed a pre-nervous system with some kind of Addendum to: Schierwater B, Eitel M, Jakob W, Osigus HJ, Hadrys H, Dellaporta SL, et al. unspecialized proto-nerve cells. Placozoa and Porifera cum grano Concatenated analysis sheds light on early metazoan evolution and fuels a mod- salis conserved this stage, while both Coelenterata and Bilateria ern “urmetazoon” hypothesis. PLoS Biol 2009; 7:1000020; PMID: 19175291 developed specialized nerve cells from this stage (top; scenario in DOI:10.1371/journal.pbio.1000020. www.landesbioscience.com Communicative & Integrative Biology 403 AUTHOR: please complete mailing address The Diploblast-Bilateria Sister hypothesis Figure 1. (A) Phylogenetic tree with relationships within Bilateria, Coelenterata and Porifera collapsed. The 72 taxa are comprised of the 64 taxa from (5) plus eight taxa added from (1). Numbers in parentheses refer to number of species in each of these groups. Phylogenetic matrices and tree topologies within the collapsed groups are available from the authors. We inferred the phylogeny using a maximum likelihood (ML) and maximum parsimony (MP) optimality criterion. Node support values (ML/MP) for nodes marked by circles with inset letters are: (B) Bilateria 100/100, (C) Coelenterata 100/82, (S) Porifera 100/100, (D) Diploblasta 100/99, (M) Metazoa 100/63; (P) Placozoa is a single taxon. Within the Bilateria: Deuterostomia 100/100, Protostomia 100/100. (B) Phylogenetic scenarios for the evolution of nerve cells mapped onto the Diploblast-Bilateria Sister hypothesis. Five potential characters (represented by colored boxes in the figure) important in the evolution of nerve cells are mapped onto the Diploblast-Bilateria Sister. Most qualities of a nerve cell seem to have been present already in the last common metazoan ancestor (LCMA in light blue). In the top figure we present the most parsimonious explanation for the evolution of these five characters (6 parsimony steps). Only the specialization of multifunctional proto-nerve cells into unifunctional nerve cells would have occurred in parallel in Bilateria and Coelenterata in the above scenario. The middle scenario is similar to the top only instead of hypothesizing independent gain of specialized nerve cells it hypothesizes independent loss of specialized nerve cells (7 steps). The bottom tree shows a highly unlikely scenario where the number of steps is nearly twice that of the top scenario. Fig. 1B). In this light the parallel invention of nerve cells, and invention in metazoans, if the LCMA already possessed proto- consequently a nervous system, in Bilateria and Coelenterata is nerve cells, which obviously seems to be the case. hardly problematic and not much more than a morphological References and physiological specialization of already existing proto-nerve 1. Schierwater B, Eitel M, Jakob W, Osigus HJ, Hadrys H, Dellaporta SL, et al. Concatenated analysis sheds light on early metazoan evolution and fuels a modern cells. Since specialization of totipotent cells into unipotent cells is “urmetazoon” hypothesis. PLoS Biol 2009; 7:1000020. a routine step in all metazoan lineages it seems possible to evolve 2. Blackstone NW. A new look at some old animals. PLoS Biol 2009; 7:7. 3. Hanström B. Vergleichende Anatomie des Nervensystems der Wirbellosen Tiere. specialized nerve cells directly from proto-nerve cells. In other Springer, Berlin 1928. words, the invention of so-called nerve cells is anything but a major 404 Communicative & Integrative Biology 2009; Vol. 2 Issue 5 AUTHOR: please complete mailing address The Diploblast-Bilateria Sister hypothesis 4. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, et al. The Trichoplax genome and the nature of placozoans. Nature 2008; 454:955-60. 5. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, et al. Broad phylog- enomic sampling improves resolution of the animal tree of life. Nature 2008; 452:745-9. 6. Nickel M. The Pre-Nervous System and Beyond. in: DeSalle R & Schierwater B eds. Key Transitions in Animal Evolution. Oxford University Press 2009; Oxford (in prep.). 7. Nickel M. Movements without muscles, information processing without nerves. JMBA GME 2007; 6:8-9. 8. Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, et al. A post- synaptic scaffold at the origin of the animal kingdom. PLoS ONE 2007; 2:506. 9. Ellwanger K, Nickel M. Neuroactive substances specifically modulate rhythmic body contractions in the nerveless metazoon Tethya wilhelma (Demospongiae, Porifera). Front Zool 2006; 27:3-7. 10. Schierwater B, de Jong D, DeSalle R. Placozoa, and the evolution of Metazoa and intra- somatic cell differentiation. Int J Biochem Cell Biol 2009; 41:370-9. 11. Hadrys T, DeSalle R, Sagasser S, Fischer N, Schierwater B. The trichoplax PaxB gene: a putative proto-PaxA/B/C gene predating the origin of nerve and sensory cells. Mol Biol Evol 2005; 22:1569-78. www.landesbioscience.com Communicative & Integrative Biology 405 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Communications & Integrative Biology Taylor & Francis

The Diploblast-Bilateria sister hypothesis

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Publisher
Taylor & Francis
Copyright
Copyright © 2009 Landes Bioscience
ISSN
1942-0889
DOI
10.4161/cib.2.5.8763
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Abstract

[Communicative & Integrative Biology 2:5, 403-405; September/October 2009]; ©2009 Landes Bioscience Article Addendum Parallel evolution of a nervous systems may have been a simple step 1,2, 2 1 2, Bernd Schierwater, * Sergios-Orestis Kolokotronis, Michael Eitel and Rob DeSalle * 1 2 ITZ; Ecology and Evolution; Tierärztliche Hochschule Hannover; Hannover, Germany; Sackler Institute for Comparative Genomics, American Museum of Natural History; New York, NY USA Key words: placozoa, trichoplax, urmetazoon hypothesis, basal metazoan evolution, trichoplax.com, pre-nervous system, placula hypothesis For many familiar with metazoan relationships and body plans, We could not overturn the sister group relationship of these two the hypothesis of a sister group relationship between Diploblasta groups regardless of the larger taxonomic sampling or the statistical and Bilateria comes as a surprise. One of the consequences of tests we used in the present analysis (Fig. 1A). It is clear to us from this hypothesis—the independent evolution of a nervous system analyses with broader taxonomic representation that the sister rela- in Coelenterata and Bilateria—seems highly unlikely to many. tionship of Bilateria and Diploblasta is a valid hypothesis. However, to a small number of scientists working on Metazoa, With respect to the controversial aspect of parallel nervous the parallel evolution of the nervous system is not surprising system evolution, we point out that a definition of a nervous at all and rather a confirmation of old morphological and new system that satisfies most is that nervous systems are spatially 2-4 genetic knowledge. The controversial hypothesis that the organized systems of aggregated nerve cells. The simple question, Diploblasta and Bilateria are sister taxa is, therefore, tantamount “what is a nerve cell?” then becomes the crux of the argument. But, to reconciling the parallel evolution of the nervous system in this question elicits a spectrum of answers from different experts. Coelenterata and Bilateria. In this addendum to Schierwater Accurate homology statements concerning nerve cells are crucial et al. we discuss two aspects critical to the controversy. First to the story and these have to wait for a general definition of what we discuss the strength of the inference of the proposed sister a nerve cell is. The key to these definitions lies in examining the 2,6 relationship of Diploblasta and Bilateria and second we discuss non-bilaterian animals. In most modern views “early nervous the implications for the evolution of nerve cells and nervous system evolution” is the equivalent of “early co-evolution of elec- systems. trical excitability and functional synapses organizing intracellular and extracellular signaling processes spatio-temporally”. Most The analysis in Schierwater et al. involved 24 ingroup taxa zoologists agree that neither Placozoa nor Porifera have nerve cells and several carefully chosen outgroups. Here we present a larger or a nervous system, but it is important to recognize that both analysis of 72 taxa to reinforce the inference we obtained with sponges and placozoans show behavior. They respond in a coordi- the smaller taxonomic sample. Figure 1A presents the results of nated way to external stimuli that must be perceived and mediated this analysis and shows clearly that the Bilateria and Diploblasta by some kind of perception and transduction cells. Both sponges are monophyletic and sister to each other with robust bootstrap and placozoans harbor a pre-nervous integration system with many support for both parsimony and maximum likelihood analyses. so-called “nerve cell typical” features, molecules and related genes, but these characteristics cannot be co-localized with any specific 7-10 *Correspondence to: Bernd Schierwater; ITZ; Ecology and Evolution; Tierärztliche cell type. While in sponges several cell types are likely involved Hochschule Hannover; Hannover D-30559 Germany; Email: bernado@trichoplax. in signal perception and transduction, in placozoans it seems to be com/Rob DeSalle; Sackler Institute for Comparative Genomics, American Museum a single cell type only, the fiber cells, which form a loose connec- of Natural History, Central Park West at 79th Street, New York, NY 10024, USA; tion network in the center of the placozoan body. Email: [email protected] Although we are far away from a general definition of a nerve Submitted: 04/16/09; Accepted: 04/17/09 cell (and therefore a definition for nervous system), we can still Previously published online as a Communicative & Integrative Biology summarize our current knowledge on early nerve cell evolu- E-publication: tion (Fig. 1B) as follows: The last common metazoan ancestor http://www.landesbioscience.com/journals/cib/article/8763 (LCMA) likely possessed a pre-nervous system with some kind of Addendum to: Schierwater B, Eitel M, Jakob W, Osigus HJ, Hadrys H, Dellaporta SL, et al. unspecialized proto-nerve cells. Placozoa and Porifera cum grano Concatenated analysis sheds light on early metazoan evolution and fuels a mod- salis conserved this stage, while both Coelenterata and Bilateria ern “urmetazoon” hypothesis. PLoS Biol 2009; 7:1000020; PMID: 19175291 developed specialized nerve cells from this stage (top; scenario in DOI:10.1371/journal.pbio.1000020. www.landesbioscience.com Communicative & Integrative Biology 403 AUTHOR: please complete mailing address The Diploblast-Bilateria Sister hypothesis Figure 1. (A) Phylogenetic tree with relationships within Bilateria, Coelenterata and Porifera collapsed. The 72 taxa are comprised of the 64 taxa from (5) plus eight taxa added from (1). Numbers in parentheses refer to number of species in each of these groups. Phylogenetic matrices and tree topologies within the collapsed groups are available from the authors. We inferred the phylogeny using a maximum likelihood (ML) and maximum parsimony (MP) optimality criterion. Node support values (ML/MP) for nodes marked by circles with inset letters are: (B) Bilateria 100/100, (C) Coelenterata 100/82, (S) Porifera 100/100, (D) Diploblasta 100/99, (M) Metazoa 100/63; (P) Placozoa is a single taxon. Within the Bilateria: Deuterostomia 100/100, Protostomia 100/100. (B) Phylogenetic scenarios for the evolution of nerve cells mapped onto the Diploblast-Bilateria Sister hypothesis. Five potential characters (represented by colored boxes in the figure) important in the evolution of nerve cells are mapped onto the Diploblast-Bilateria Sister. Most qualities of a nerve cell seem to have been present already in the last common metazoan ancestor (LCMA in light blue). In the top figure we present the most parsimonious explanation for the evolution of these five characters (6 parsimony steps). Only the specialization of multifunctional proto-nerve cells into unifunctional nerve cells would have occurred in parallel in Bilateria and Coelenterata in the above scenario. The middle scenario is similar to the top only instead of hypothesizing independent gain of specialized nerve cells it hypothesizes independent loss of specialized nerve cells (7 steps). The bottom tree shows a highly unlikely scenario where the number of steps is nearly twice that of the top scenario. Fig. 1B). In this light the parallel invention of nerve cells, and invention in metazoans, if the LCMA already possessed proto- consequently a nervous system, in Bilateria and Coelenterata is nerve cells, which obviously seems to be the case. hardly problematic and not much more than a morphological References and physiological specialization of already existing proto-nerve 1. Schierwater B, Eitel M, Jakob W, Osigus HJ, Hadrys H, Dellaporta SL, et al. Concatenated analysis sheds light on early metazoan evolution and fuels a modern cells. Since specialization of totipotent cells into unipotent cells is “urmetazoon” hypothesis. PLoS Biol 2009; 7:1000020. a routine step in all metazoan lineages it seems possible to evolve 2. Blackstone NW. A new look at some old animals. PLoS Biol 2009; 7:7. 3. Hanström B. Vergleichende Anatomie des Nervensystems der Wirbellosen Tiere. specialized nerve cells directly from proto-nerve cells. In other Springer, Berlin 1928. words, the invention of so-called nerve cells is anything but a major 404 Communicative & Integrative Biology 2009; Vol. 2 Issue 5 AUTHOR: please complete mailing address The Diploblast-Bilateria Sister hypothesis 4. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, et al. The Trichoplax genome and the nature of placozoans. Nature 2008; 454:955-60. 5. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, et al. Broad phylog- enomic sampling improves resolution of the animal tree of life. Nature 2008; 452:745-9. 6. Nickel M. The Pre-Nervous System and Beyond. in: DeSalle R & Schierwater B eds. Key Transitions in Animal Evolution. Oxford University Press 2009; Oxford (in prep.). 7. Nickel M. Movements without muscles, information processing without nerves. JMBA GME 2007; 6:8-9. 8. Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, et al. A post- synaptic scaffold at the origin of the animal kingdom. PLoS ONE 2007; 2:506. 9. Ellwanger K, Nickel M. Neuroactive substances specifically modulate rhythmic body contractions in the nerveless metazoon Tethya wilhelma (Demospongiae, Porifera). Front Zool 2006; 27:3-7. 10. Schierwater B, de Jong D, DeSalle R. Placozoa, and the evolution of Metazoa and intra- somatic cell differentiation. Int J Biochem Cell Biol 2009; 41:370-9. 11. Hadrys T, DeSalle R, Sagasser S, Fischer N, Schierwater B. The trichoplax PaxB gene: a putative proto-PaxA/B/C gene predating the origin of nerve and sensory cells. Mol Biol Evol 2005; 22:1569-78. www.landesbioscience.com Communicative & Integrative Biology 405

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Published: Sep 1, 2009

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