Sponge phylogeny, animal monophyly, and the origin of the nervous system: 18S rRNA evidence

Cavalier-Smith, T.; Allsopp, M. T. E. P.; Chao, E. E.; Boury-Esnault, N.; Vacelet, J.

doi:10.1139/z96-231

Cited by 180Marine Invertebrate Physiology and EcologyProtist diversity and phylogenyMarine Sponges and Natural Products

Sponge phylogeny, animal monophyly, and the origin of the nervous system: 18S rRNA evidence

Cavalier-Smith, T., Allsopp, M. T. E. P., Chao, E. E., Boury-Esnault, N., Vacelet, J.·1996·Canadian Journal of Zoology

DOI 10.1139/z96-231

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Abstract

We sequenced 18S rRNA genes of a calcareous sponge, Clathrina cerebrum, a demosponge, Axinella polypoides, and a zoanthid cnidarian, Parazoanthus axinellae. Our phylogenetic analysis supports the monophyly of kingdom Animalia and confirms that choanoflagellate protozoans are their closest relatives. Sponges as a whole are monophyletic, but possibly paraphyletic; demosponges and hexactinellids form a monophyletic group of silicious sponges. Our phylogenetic trees support a monophyletic origin of the nervous system in the immediate common ancestor of Cnidaria and Ctenophora. They weakly suggest that animals with a nervous system may be more closely related to calcareous sponges than to silicious sponges; the nervous system might have originated in an early calcareous sponge. Our trees confirm that Myxozoa and Placozoa are animals that arose by secondary loss of the nervous system, but suggest that Myxozoa may be sisters of, rather than derived from, Bilateria. Kingdom Animalia is divided into four subkingdoms: Radiata (Porifera, Cnidaria, Placozoa, Ctenophora), Myxozoa, Mesozoa, and Bilateria. The 18S rRNA genes of Myxozoa evolved over twice as fast as in Radiata. Comparison with the fossil record reveals a brief 10-fold (or greater) acceleration in the rate of rRNA evolution in early Bilateria followed by normal low rates for about 500 million years.

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SSU rRNA data weakly suggest that sponges are paraphyletically arranged at the base of Metazoa.
“This view is contradicted by SSU rRNA data, which weakly suggest that sponges are paraphyletically arranged at the base of Metazoa (21, 22) and that Cnidaria, Placozoa, and Bilateria form a well-supported clade to the exclusion of Ctenophora (22, 23).”
From Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA (2001) · cites this paper as [21]

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Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA
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Origin of the Eumetazoa: Testing ecological predictions of molecular clocks against the Proterozoic fossil record
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The phylum Cnidaria: A review of phylogenetic patterns and diversity 300 years after Linnaeus *
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Fossils, molecules and embryos: new perspectives on the Cambrian explosion
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A Post-Synaptic Scaffold at the Origin of the Animal Kingdom
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Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics
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Genesis and Expansion of Metazoan Transcription Factor Gene Classes
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A revised six‐kingdom system of life
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Cell evolution and Earth history: stasis and revolution
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Sponge paraphyly and the origin of Metazoa
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Nociceptors: a phylogenetic view
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Wnt and TGF-β Expression in the Sponge Amphimedon queenslandica and the Origin of Metazoan Embryonic Patterning
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Evaluating multiple alternative hypotheses for the origin of Bilateria: An analysis of 18S rRNA molecular evidence
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Phylogeny of Choanozoa, Apusozoa, and Other Protozoa and Early Eukaryote Megaevolution
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Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution
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Cnidarian phylogenetic relationships as revealed by mitogenomics
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The evolution of the nuclear receptor superfamily
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Classification and Phylogenetics of Myxozoa
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The Genomic and Cellular Foundations of Animal Origins
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Choanoflagellates, choanocytes, and animal multicellularity
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Poriferan paraphyly and its implications for Precambrian palaeobiology
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Early evolution of eukaryote feeding modes, cell structural diversity, and classification of the protozoan phyla Loukozoa, Sulcozoa, and Choanozoa
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A placozoan affinity for <i>Dickinsonia</i> and the evolution of late Proterozoic metazoan feeding modes
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Animal evolution: the end of the intermediate taxa?
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Biodiversity and Evolution of the Myxozoa
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An evaluation of support for order-level monophyly and interrelationships within the class Demospongiae using partial data from the large subunit rDNA and cytochrome oxidase subunit I
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Tempo and mode of early animal evolution: inferences from rocks, Hox, and molecular clocks
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The NK homeobox gene cluster predates the origin of Hox genes.
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Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa
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Deep Phylogeny and Evolution of Sponges (Phylum Porifera)
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Sponge Genes Provide New Insight into the Evolutionary Origin of the Neurogenic Circuit
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Phylogeny and Evolution of Calcareous Sponges: Monophyly of Calcinea and Calcaronea, High Level of Morphological Homoplasy, and the Primitive Nature of Axial Symmetry
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Articulated sponges from the Lower Cambrian Hetang Formation in southern Anhui, South China: their age and implications for the early evolution of sponges
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Review: How was metazoan threshold crossed? The hypothetical Urmetazoa
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Monophyly of brachiopods and phoronids: reconciliation of molecular evidence with Linnaean classification (the subphylum Phoroniformea nov.)
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Mineral skeletogenesis in sponges
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Phylum Tardigrada: an “individual” approach
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Molecular evidence that phoronids are a subtaxon of brachiopods (Brachiopoda: Phoronata) and that genetic divergence of metazoan phyla began long before the early Cambrian
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A new perspective on lower metazoan relationships from 18S rDNA sequences
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Origin of animal multicellularity: precursors, causes, consequences—the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion
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The phylogenetic position of the comb jellies (Ctenophora) and the importance of taxonomic sampling
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The earliest fossil record of the animals and its significance
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Embryogenesis and metamorphosis in a haplosclerid demosponge: Gastrulation and transdifferentiation of larval ciliated cells to choanocytes.
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Developmental Signaling in Hydra: What Does It Take to Build a “Simple” Animal?
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Molecular phylogeny of the free-living archezoanTrepomonas agilis and the nature of the first eukaryote
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Molecular biology of demosponge axial filaments and their roles in biosilicification
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The interrelationships of metazoan parasites: a review of phylum- and higher-level hypotheses from recent morphological and molecular phylogenetic analyses
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Early evolution of metazoan serine/threonine and tyrosine kinases: identification of selected kinases in marine sponges
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Phylogenetic Position of the Hexactinellida Within the Phylum Porifera Based on the Amino Acid Sequence of the Protein Kinase C from Rhabdocalyptus dawsoni
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Amoeboflagellates and mitochondrial cristae in eukaryote evolution: megasystematics of the new protozoan subkingdoms eozoa and neozoa
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Phylogenetic analysis of the Hsp70 sequences reveals the monophyly of Metazoa and specific phylogenetic relationships between animals and fungi
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Placozoa Are Not Derived Cnidarians: Evidence from Molecular Morphology
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Reconstructing early sponge relationships by using the Burgess Shale fossil <i>Eiffelia globosa</i> , Walcott
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Origin of the Metazoan Immune System: Identification of the Molecules and Their Functions in Sponges
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Origin of metazoan adhesion molecules and adhesion receptors as deduced from cDNA analyses in the marine sponge Geodia cydonium : a review
Müller, W. E. G. (1997) · Cell and Tissue Research · doi:10.1007/s004410050885 · Cited by 104 · see citing works
On the molecular phylogeny of sponges (Porifera)*
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Multigene phylogeny and cell evolution of chromist infrakingdom Rhizaria: contrasting cell organisation of sister phyla Cercozoa and Retaria
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Origin of Insulin Receptor-Like Tyrosine Kinases in Marine Sponges
Skorokhod, A. A., Gamulin, V., Gundacker, D., Kavsan, V. M., Müller, I. M., & Müller, W. E. G. (1999) · Biological Bulletin · doi:10.2307/1542615 · Cited by 96 · see citing works
Multiple origins of Heliozoa from flagellate ancestors: New cryptist subphylum Corbihelia, superclass Corbistoma, and monophyly of Haptista, Cryptista, Hacrobia and Chromista
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Defining phyla: evolutionary pathways to metazoan body plans
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Evolutionary relationships of Metazoa within the eukaryotes based on molecular data from Porifera
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Embryogenesis and larval differentiation in sponges
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The Ecdysozoa: Artifact or monophylum?
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Mitochondrial DNA of Clathrina clathrus (Calcarea, Calcinea): Six Linear Chromosomes, Fragmented rRNAs, tRNA Editing, and a Novel Genetic Code
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Non-monophyly of most supraspecific taxa of calcareous sponges (Porifera, Calcarea) revealed by increased taxon sampling and partitioned Bayesian analysis of ribosomal DNA
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Homeobox Gene Diversification in the Calcareous Sponge, Sycon raphanus
Manuel, M., & Parco, Y. L. (2000) · Molecular Phylogenetics and Evolution · doi:10.1006/mpev.2000.0822 · Cited by 79 · see citing works
Evolution
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A chemical view of the most ancient metazoa – biomarker chemotaxonomy of hexactinellid sponges
Thiel, V., Blumenberg, M., Hefter, J., Pape, T., Pomponi, S. A., Reed, J. K., Joachim Reitner, A., Wörheide, G., & Michaelis, W. (2002) · Die Naturwissenschaften · doi:10.1007/s00114-001-0284-9 · Cited by 77 · see citing works
Expansion of the SOX gene family predated the emergence of the Bilateria
Jager, M., Quéinnec, É., Houliston, E., & Manuel, M. (2006) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2005.12.005 · Cited by 73 · see citing works
Phylogenetic relationships of the family Axinellidae (Porifera: Demospongiae) using morphological and molecular data
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Where is my mind? How sponges and placozoans may have lost neural cell types
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Molecular systematics of sponges (Porifera)
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The Significance of Syncytial Tissues for the Position of the Hexactinellida in the Metazoa
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Phylogenetic analysis of freshwater sponges provide evidence for endemism and radiation in ancient lakes
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Multidomain ribosomal protein trees and the planctobacterial origin of neomura (eukaryotes, archaebacteria)
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What sponges can tell us about the evolution of developmental processes
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Agent of whirling disease meets orphan worm: phylogenomic analyses firmly place Myxozoa in Cnidaria
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What are Fungi?
Cavalier‐Smith, T. (2001) · Springer eBooks · doi:10.1007/978-3-662-10376-0_1 · Cited by 59 · see citing works
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The Origin of Bodyplans
Erwin, D. H. (1999) · American Zoologist · doi:10.1093/icb/39.3.617 · Cited by 58 · see citing works
Reproduction in a carnivorous sponge: the significance of the absence of an aquiferous system to the sponge body plan
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Sponge Development and Antiquity of Animal Pattern Formation
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Phylogeny and evolution of calcareous sponges
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THE SCUTOCOXIFERA TAX. NOV. AND THE INFORMATION CONTENT OF NUCLEAR SSU RDNA SEQUENCES FOR RECONSTRUCTION OF ISOPOD PHYLOGENY (PERACARIDA: ISOPODA)
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Support, Ribosomal Sequences and the Phylogeny Of The Eukaryotes
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Body size does not predict species richness among the metazoan phyla
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Exploring the potential of small RNA subunit and ITS sequences for resolving phylogenetic relationships within the phylum Ctenophora
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Assembling the spiralian tree of life
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Polyphyly of the genus Axinella and of the family Axinellidae (Porifera: Demospongiaep)
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MicroRNAs and metazoan phylogeny: big trees from little genes
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Phylogenetic Context and Basal Metazoan Model Systems
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Monophyletic Origins of the Metazoa: an Evolutionary Link with Fungi
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Sponge paraphyly and the origin of Metazoa
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A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals
Simion, P., Philippe, H., Baurain, D., Jager, M., Richter, D. J., Di Franco, A., Roure, B., Satoh, N., Quéinnec, É., Ereskovsky, A., et al. (2017) · Current Biology · doi:10.1016/j.cub.2017.02.031 · Cited by 518 · see citing works
Deep Phylogeny and Evolution of Sponges (Phylum Porifera)
Wörheide, G., Dohrmann, M., Erpenbeck, D., Larroux, C., Maldonado, M., Voigt, O., Borchiellini, C., & Lavrov, D. V. (2012) · Advances in Marine Biology · doi:10.1016/b978-0-12-387787-1.00007-6 · Cited by 166 · see citing works
The ctenophore lineage is older than sponges? That cannot be right! Or can it?
Halanych, K. M. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.111872 · Cited by 38 · see citing works

Authors: Cavalier-Smith, T., Allsopp, M. T. E. P., Chao, E. E., Boury-Esnault, N., & Vacelet, J.
ORCID: Vacelet, J.
Venue: Canadian Journal of Zoology
Publisher: Canadian Science Publishing
Published: 1996-11-01
Volume: 74
Issue: 11
Pages: 2031-2045
ISSN: 0008-4301 (ISSN-L)
1480-3283
DOI: 10.1139/z96-231
OpenAlex: W2077908307
Cited by: 180
References: 90
Citations by year: 2021: 1 · 2020: 1 · 2019: 1 · 2018: 4 · 2017: 2 · 2016: 4 · 2015: 7 · 2014: 1 · 2013: 5 · 2012: 5
FWCI: 14.46
Type: journal article
Language: en
Open access: closed
Licence: www.nrcresearchpress.com/page/about/CorporateTextAndDataMining (tdm)
Locations: Canadian Journal of Zoology (publishedVersion)
Funders: Canadian Institute for Advanced Research
Illinois State University
Natural Sciences and Engineering Research Council of Canada
Topics: Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
Keywords: sponge phylogeny, 18S rRNA, calcareous sponges, demosponges, Hexactinellida, choanoflagellates, Cnidaria, Ctenophora, Myxozoa, Placozoa, molecular clock, sponges

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Sponge phylogeny, animal monophyly, and the origin of the nervous system: 18S rRNA evidence

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