Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences

Peterson, Kevin J.; Eernisse, Douglas J.

doi:10.1046/j.1525-142x.2001.003003170.x

Cited by 531Marine Invertebrate Physiology and EcologyInvertebrate Taxonomy and EcologyProtist diversity and phylogeny

Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences

Peterson, Kevin J., Eernisse, Douglas J.·2001·Evolution & Development

DOI 10.1046/j.1525-142x.2001.003003170.x

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Abstract

SUMMARY Insight into the origin and early evolution of the animal phyla requires an understanding of how animal groups are related to one another. Thus, we set out to explore animal phylogeny by analyzing with maximum parsimony 138 morphological characters from 40 metazoan groups, and 304 18S rDNA sequences, both separately and together. Both types of data agree that arthropods are not closely related to annelids: the former group with nematodes and other molting animals (Ecdysozoa), and the latter group with molluscs and other taxa with spiral cleavage. Furthermore, neither brachiopods nor chaetognaths group with deuterostomes; brachiopods are allied with the molluscs and annelids (Lophotrochozoa), whereas chaetognaths are allied with the ecdysozoans. The major discordance between the two types of data concerns the rooting of the bilaterians, and the bilaterian sister‐taxon. Morphology suggests that the root is between deuterostomes and protostomes, with ctenophores the bilaterian sister‐group, whereas 18S rDNA suggests that the root is within the Lophotrochozoa with acoel flatworms and gnathostomulids as basal bilaterians, and with cnidarians the bilaterian sister‐group. We suggest that this basal position of acoels and gnathostomulids is artifactal because for 1000 replicate phylogenetic analyses with one random sequence as outgroup, the majority root with an acoel flatworm or gnathostomulid as the basal ingroup lineage. When these problematic taxa are eliminated from the matrix, the combined analysis suggests that the root lies between the deuterostomes and protostomes, and Ctenophora is the bilaterian sister‐group. We suggest that because chaetognaths and lophophorates, taxa traditionally allied with deuterostomes, occupy basal positions within their respective protostomian clades, deuterostomy most likely represents a suite of characters plesiomorphic for bilaterians.

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The new matrix builds on previously available datasets through the incorporation of new morphological information and an expanded taxon sample.
“The new matrix builds on previously available datasets [2, 11, 13, 53”
From Cambrian Sessile, Suspension Feeding Stem-Group Ctenophores and Evolution of the Comb Jelly Body Plan (2019) · cites this paper as [11]
Bilateria derive from a common ancestor.
“The Bilateria thus derive from a common ancestor, a point repeatedly substantiated in current molecular phylogenies (reviewed in Adoutte et al., 2000;Peterson and Eernisse, 2001).”
From Precambrian Animal Life: Probable Developmental and Adult Cnidarian Forms from Southwest China (2002) · cites this paper as Peterson and Eernisse, 2001
The bilaterian-cnidarian ancestor likely lived well before the Cambrian.
“Molecular and morphological phylogenies agree that the bilaterian stem group emerged from a common ancestor of bilaterians and cnidarians, which probably existed much deeper in time (Peterson and Eernisse, 2001;Medina et al., 2001;Peterson and Davidson, 2000).”
From Precambrian Animal Life: Probable Developmental and Adult Cnidarian Forms from Southwest China (2002) · cites this paper as Peterson and Eernisse, 2001
Both molecular and morphological phylogenies indicate that the bilaterian stem lineage arose from an ancestor shared with cnidarians.
“Molecular and morphological phylogenies agree that the bilaterian stem group emerged from a common ancestor of bilaterians and cnidarians, which probably existed much deeper in time (Peterson and Eernisse, 2001;Medina et al., 2001;Peterson and Davidson, 2000).”
From Precambrian Animal Life: Probable Developmental and Adult Cnidarian Forms from Southwest China (2002) · cites this paper as Peterson and Eernisse, 2001

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A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes
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Analysis of evolution of exon-intron structure of eukaryotic genes
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The Evolution of Organ Systems
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Deep metazoan phylogeny: When different genes tell different stories
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Testing the New Animal Phylogeny: First Use of Combined Large-Subunit and Small-Subunit rRNA Gene Sequences to Classify the Protostomes
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Coelomata and Not Ecdysozoa: Evidence From Genome-Wide Phylogenetic AnalysisPreprint
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A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus
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A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians
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The ascidian tadpole larva: comparative molecular development and genomics
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MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda
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Cnidarians: An evolutionarily conserved model system for regeneration?
Holstein, T. W., Hobmayer, E., & Technau, U. (2003) · Developmental Dynamics · doi:10.1002/dvdy.10227 · Cited by 225 · see citing works
The evolutionary position of nematodes
Blair, J. E., Ikeo, K., Gojobori, T., & Hedges, S. B. (2002) · BMC Evolutionary Biology · doi:10.1186/1471-2148-2-7 · Cited by 218 · see citing works
Phylogenomics of Lophotrochozoa with Consideration of Systematic Error
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The evolution of metazoan axial properties
Martindale, M. Q. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1725 · Cited by 204 · see citing works
Origin and early evolution of vertebrate skeletonization
Donoghue, P. C. J., & Sansom, I. J. (2002) · Microscopy Research and Technique · doi:10.1002/jemt.10217 · Cited by 232 · see citing works
Poriferan paraphyly and its implications for Precambrian palaeobiology
Sperling, E. A., Pisani, D., & Peterson, K. J. (2007) · Geological Society, London, Special Publications · doi:10.1144/sp286.25 · Cited by 206 · see citing works
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Dating the Time of Origin of Major Clades: Molecular Clocks and the Fossil Record
Smith, A. B., & Peterson, K. J. (2002) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.30.091201.140057 · Cited by 193 · see citing works
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The evolution of the Ecdysozoa
Telford, M. J., Bourlat, S., Economou, A. D., Papillon, D., & Rota-Stabelli, O. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2243 · Cited by 191 · see citing works
A placozoan affinity for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes
Sperling, E. A., & Vinther, J. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00404.x · Cited by 194 · see citing works
The new head hypothesis revisited
Northcutt, R. G. (2005) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21063 · Cited by 192 · see citing works
The Articulata hypothesis ? or what is a segment?
Scholtz, G. (2002) · Organisms Diversity & Evolution · doi:10.1078/1439-6092-00046 · Cited by 190 · see citing works
Fossil sister group of craniates: Predicted and found
Mallatt, J. M., & Chen, J. (2003) · Journal of Morphology · doi:10.1002/jmor.10081 · Cited by 186 · see citing works
Biodiversity and Evolution of the Myxozoa
Canning, E., & Okamura, B. (2003) · Advances in Parasitology/Advances in parasitology · doi:10.1016/s0065-308x(03)56002-x · Cited by 184 · see citing works
Accepting Partnership by Submission? Morphological Phylogenetics in a Molecular Millennium
Jenner, R. A. (2004) · Systematic Biology · doi:10.1080/10635150490423962 · Cited by 182 · see citing works
Improvement of molecular phylogenetic inference and the phylogeny of Bilateria
Lartillot, N., & Philippe, H. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2236 · Cited by 178 · see citing works
Large-scale sequencing and the new animal phylogeny
Philippe, H., & Telford, M. J. (2006) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2006.08.004 · Cited by 177 · see citing works
Neurophylogeny: Architecture of the nervous system and a fresh view on arthropod phyologeny
Harzsch, S. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icj011 · Cited by 176 · see citing works
Ecdysozoan Mitogenomics: Evidence for a Common Origin of the Legged Invertebrates, the Panarthropoda
Rota-Stabelli, O., Kayal, E., Gleeson, D., Daub, J., Boore, J., Telford, M. J., Pisani, D., Blaxter, M., & Lavrov, D. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq030 · Cited by 162 · see citing works
Tempo and mode of early animal evolution: inferences from rocks, Hox, and molecular clocks
Peterson, K. J., McPeek, M. A., & Evans, D. A. D. (2005) · Paleobiology · doi:10.1666/0094-8373(2005)031[0036:tamoea]2.0.co;2 · Cited by 173 · see citing works
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The Opisthokonta and the Ecdysozoa May Not Be Clades: Stronger Support for the Grouping of Plant and Animal than for Animal and Fungi and Stronger Support for the Coelomata than Ecdysozoa
Philip, G. K., Creevey, C. J., & McInerney, J. O. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi102 · Cited by 170 · see citing works
Arthropod phylogeny: onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage
Strausfeld, N. J., Strausfeld, C. M., Loesel, R., Rowell, D. M., & Stowe, S. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3536 · Cited by 169 · see citing works
Lophotrochozoan phylogeny assessed with LSU and SSU data: Evidence of lophophorate polyphyly
Passamaneck, Y. J., & Halanych, K. M. (2006) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2006.02.001 · Cited by 169 · see citing works
Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa
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Phylogeny and Systematics of Demospongiae in Light of New Small-Subunit Ribosomal DNA (18S) Sequences
Redmond, N. E., Morrow, C. C., THACKER, R. W., Díaz, M. C., Boury‐Esnault, N., Cárdenas, P., Hajdu, E., Lôbo‐Hajdu, G., PICTON, B. E., Pomponi, S. A., et al. (2013) · Integrative and Comparative Biology · doi:10.1093/icb/ict078 · Cited by 167 · see citing works
Current advances in the phylogenetic reconstruction of metazoan evolution. A new paradigm for the Cambrian explosion?
Giribet, G. (2002) · Molecular Phylogenetics and Evolution · doi:10.1016/s1055-7903(02)00206-3 · Cited by 167 · see citing works
Deep Phylogeny and Evolution of Sponges (Phylum Porifera)
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Precambrian Animal Life: Probable Developmental and Adult Cnidarian Forms from Southwest China
Chen, J.-Y., Oliveri, P., Gao, F., Dornbos, S. Q., Li, C.-W., Bottjer, D. J., & Davidson, E. H. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0714 · Cited by 165 · see citing works
Investigation of molluscan phylogeny using large-subunit and small-subunit nuclear rRNA sequences
Passamaneck, Y. J., Schänder, C., & Halanych, K. M. (2004) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2003.12.016 · Cited by 164 · see citing works
Distinguishing heat from light in debate over controversial fossils
Donoghue, P. C. J., & Purnell, M. A. (2009) · BioEssays · doi:10.1002/bies.200800128 · Cited by 160 · see citing works
Phylogeny and Evolution of Calcareous Sponges: Monophyly of Calcinea and Calcaronea, High Level of Morphological Homoplasy, and the Primitive Nature of Axial Symmetry
Manuel, M., Borchiellini, C., Alivon, E., Parco, Y. L., Vacelet, J., & Boury‐Esnault, N. (2003) · Systematic Biology · doi:10.1080/10635150309322 · Cited by 158 · see citing works
Larval development in the Homoscleromorpha (Porifera, Demospongiae)
Boury‐Esnault, N., Ereskovsky, A. V., Bézac, C., & Tokina, D. B. (2003) · Invertebrate Biology · doi:10.1111/j.1744-7410.2003.tb00084.x · Cited by 156 · see citing works
Molecular phylogeny of the protochordates: chordate evolution
Zeng, L., & Swalla, B. J. (2005) · Canadian Journal of Zoology · doi:10.1139/z05-010 · Cited by 154 · see citing works
Phylogeny of Eunicida (Annelida) and Exploring Data Congruence Using a Partition Addition Bootstrap Alteration (PABA) Approach
Struck, T. H., Purschke, G., & Halanych, K. M. (2006) · Systematic Biology · doi:10.1080/10635150500354910 · Cited by 153 · see citing works
Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca
Nielsen, C. (2004) · Journal of Experimental Zoology Part B: Molecular and Developmental Evolution · doi:10.1002/jez.b.20001 · Cited by 150 · see citing works
Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms
Telford, M. J., Lockyer, A. E., Cartwright–Finch, C., & Littlewood, D. T. J. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2003.2342 · Cited by 151 · see citing works
Putative cross-kingdom horizontal gene transfer in sponge (Porifera) mitochondria
Rot, C., Goldfarb, I., Ilan, M., & Huchon, D. (2006) · BMC Evolutionary Biology · doi:10.1186/1471-2148-6-71 · Cited by 149 · see citing works
The tardigrade Hypsibius dujardini, a new model for studying the evolution of development
Gabriel, W. N., McNuff, R., Patel, S. K., Gregory, T. R., Jeck, W. R., Jones, C. D., & Goldstein, B. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.09.055 · Cited by 147 · see citing works
Acoel Flatworms Are Not Platyhelminthes: Evidence from Phylogenomics
Philippe, H., Brinkmann, H., Martı́nez, P., Riutort, M., & Baguñà, J. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000717 · Cited by 148 · see citing works
Hox Gene Loss during Dynamic Evolution of the Nematode Cluster
Aboobaker, A. A., & Blaxter, M. (2003) · Current Biology · doi:10.1016/s0960-9822(02)01399-4 · Cited by 148 · see citing works
The sperm outer dense fiber protein is the 10th member of the superfamily of mammalian small stress proteins
Fontaine, J., Rest, J. S., Welsh, M. J., & Benndorf, R. (2003) · Cell Stress and Chaperones · doi:10.1379/1466-1268(2003)8 · Cited by 145 · see citing works
Molecular evidence that phoronids are a subtaxon of brachiopods (Brachiopoda: Phoronata) and that genetic divergence of metazoan phyla began long before the early Cambrian
COHEN, B., & Weydmann‐Zwolicka, A. (2005) · Organisms Diversity & Evolution · doi:10.1016/j.ode.2004.12.002 · Cited by 142 · see citing works
Biology of the Phylum Nematomorpha
Hanelt, B., Frédéric Thomas, A., & Schmidt‐Rhaesa, A. (2005) · Advances in Parasitology/Advances in parasitology · doi:10.1016/s0065-308x(05)59004-3 · Cited by 143 · see citing works
The Evolution of Brachiopoda
Carlson, S. J. (2016) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev-earth-060115-012348 · Cited by 142 · see citing works
The phylogenetic position of the comb jellies (Ctenophora) and the importance of taxonomic sampling
Wållberg, A., Thollesson, M., Farris, J. S., & Jondelius, U. (2004) · Cladistics · doi:10.1111/j.1096-0031.2004.00041.x · Cited by 141 · see citing works
The pre‐radial history of echinoderms
Smith, A. B. (2005) · Geological Journal · doi:10.1002/gj.1018 · Cited by 139 · see citing works
Lophotrochozoa internal phylogeny: new insights from an up-to-date analysis of nuclear ribosomal genes
Paps, J., Baguñà, J., & Riutort, M. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2008.1574 · Cited by 138 · see citing works
The mitochondrial genome of Paraspadella gotoi is highly reduced and reveals that chaetognaths are a sister group to protostomes
Helfenbein, K. G., Fourcade, H. M., Vanjani, R. G., & Boore, J. L. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400941101 · Cited by 137 · see citing works
Assembling the lophotrochozoan (=spiralian) tree of life
Giribet, G. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2241 · Cited by 138 · see citing works
The Early Cambrian Halkieria is a mollusc
Vinther, J., & Nielsen, C. (2005) · Zoologica Scripta · doi:10.1111/j.1463-6409.2005.00177.x · Cited by 135 · see citing works
Identification of Chaetognaths as Protostomes Is Supported by the Analysis of Their Mitochondrial Genome
Papillon, D., Perez, Y., Caubit, X., & Parco, Y. L. (2004) · Molecular Biology and Evolution · doi:10.1093/molbev/msh229 · Cited by 134 · see citing works
Key characters uniting hemichordates and chordates: homologies or homoplasies?
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Authors: Peterson, K. J., & Eernisse, D. J.
Affiliations: Dartmouth College (US)
California State University, Fullerton (US)
ORCID: Peterson, Kevin J.
Eernisse, Douglas J.
Venue: Evolution & Development
Publisher: Wiley
Published: 2001-05
Volume: 3
Issue: 3
Pages: 170-205
ISSN: 1520-541X (ISSN-L)
1525-142X
DOI: 10.1046/j.1525-142x.2001.003003170.x
OpenAlex: W2128919173
Semantic Scholar: b53cb97dcc586e3a139989e3611350c2c6a26feb
Cited by: 529
References: 270
Citations by year: 2026: 4 · 2025: 10 · 2024: 12 · 2023: 4 · 2022: 6 · 2021: 8 · 2020: 5 · 2019: 5 · 2018: 5 · 2017: 4 · 2016: 10 · 2015: 12 · 2014: 11 · 2013: 15 · 2012: 11
FWCI: 41.38
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 233 d)
Locations: Evolution & Development (publishedVersion)
PubMed (publishedVersion)
Topics: Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Invertebrate Taxonomy and Ecology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
Keywords: animal phylogeny, bilaterian origin, 18S rDNA, morphological characters, Ecdysozoa, Lophotrochozoa, deuterostomes, protostomes, ctenophores, acoel flatworms, chaetognaths, lophophorates, root placement
MeSH terms: Animals, Annelida, Arthropods, Classification, DNA, Ribosomal, Phylogeny, RNA, Ribosomal, 18S, Software, Models, Statistical, Evolution, Molecular

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Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences

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