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Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA
Open accessAbstract
We studied the evolutionary relationships among basal metazoan lineages by using complete large subunit (LSU) and small subunit (SSU) ribosomal RNA sequences for 23 taxa. After identifying competing hypotheses, we performed maximum likelihood searches for trees conforming to each hypothesis. Kishino–Hasegawa tests were used to determine whether the data (LSU, SSU, and combined) reject any of the competing hypotheses. We also conducted unconstrained tree searches, compared the resulting topologies, and calculated bootstrap indices. Shimodaira–Hasegawa tests were applied to determine whether the data reject any of the topologies resulting from the constrained and unconstrained tree searches. LSU, SSU, and the combined data strongly contradict two assertions pertaining to sponge phylogeny. Hexactinellid sponges are not likely to be the basal lineage of a monophyletic Porifera or the sister group to all other animals. Instead, Hexactinellida and Demospongia form a well-supported clade of siliceous sponges, Silicea. It remains unclear, on the basis of these data alone, whether the calcarean sponges are more closely related to Silicea or to nonsponge animals. The SSU and combined data reject the hypothesis that Bilateria is more closely related to Ctenophora than it is to Cnidaria, whereas LSU data alone do not refute either hypothesis. LSU and SSU data agree in supporting the monophyly of Bilateria, Cnidaria, Ctenophora, and Metazoa. LSU sequence data reveal phylogenetic structure in a data set with limited taxon sampling. Continued accumulation of LSU sequences should increase our understanding of animal phylogeny.
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TL;DR
Complete LSU and SSU rRNA sequences for 23 taxa were used to test competing hypotheses of basal metazoan phylogeny. The data strongly reject Hexactinellida as basal within a monophyletic Porifera or as sister to all other animals, support a Silicea clade of Hexactinellida plus Demospongia, and reject Ctenophora as closer to Bilateria than Cnidaria in SSU and combined analyses.
Key findings
- LSU, SSU, and combined data reject two sponge hypotheses: Porifera monophyletic with Hexactinellida basal (KH P = 0.021, 0.002, 0.000 for SSU, LSU, combined) and Hexactinellida sister to all other Metazoans (KH P = 0.028, 0.005, 0.000). Instead, Hexactinellida and Demospongia form a well-supported Silicea clade (ML bootstraps 95 and 100); whether Calcarea is closer to Silicea or to nonsponge animals remains unclear.
- SSU and combined data reject Bilateria being more closely related to Ctenophora than to Cnidaria (KH P = 0.022 and 0.033), whereas LSU alone does not (P = 1.000).
- LSU and SSU agree in supporting monophyly of Bilateria, Cnidaria, Ctenophora, and Metazoa; ML bootstraps were 100 except Cnidaria (77 and 62) and Metazoa (63 and 63), and combined data raised Cnidaria and Metazoa support to 98 and 99.
- LSU and combined data reject Hydrozoa as sister to other cnidarians (KH P = 0.004 and 0.016; SH LSU P = 0.036), and SSU data reject Choanoflagellida as sister group to Metazoa (KH P = 0.049).
Methods
- Compiled complete LSU and SSU rRNA sequences for 23 taxa; 17 LSU and 3 SSU sequences were new. LSU was sequenced from mainly nonbilaterian animals (one mesomycetozoan, two choanoflagellates, four sponges, five cnidarians, three ctenophores, two bilaterians); SSU from three cnidarians; three fungi served as outgroup.
- Final alignment contained 4,003 characters (SSU 1,595; LSU 2,408), with 1,779 variable and 1,216 parsimony-informative sites combined. Secondary structure was encoded and ambiguous regions excluded; model selection used nested likelihood ratio tests in modeltest, and analyses used paup*.
- Constrained ML searches for a priori hypotheses were compared with Kishino–Hasegawa tests; unconstrained ML and MP searches (2:1 transversion:transition weighting) were compared with Shimodaira–Hasegawa tests; support estimated with 100 ML and 1,000 MP bootstrap pseudoreplicates and Bremer indices; analyses repeated excluding D. tigrina.
Limitations
- Stated: taxon sampling is relatively limited, particularly outside the fungal/animal divergence, and may be inadequate to resolve the closest relatives of animals; bilaterian taxa have the longest branches, so the position of Bilateria in any topology may be artifactual.
- Stated: SSU rRNA data have limitations including nucleotide compositional bias, among-site rate variation, and heterogeneous rates across lineages; LSU may share similar limitations because of similar functional constraints and genetic linkage.
- Evident from the text: the SH test did not yield many significant P-values, and SSU data did not refute any hypotheses under SH; LSU alone failed to reject the Ctenophora-sister-to-Bilateria hypothesis.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The combined and SSU data reject the hypothesis that Ctenophora is more closely related to Bilateria than is Cnidaria.”
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“A poorly supported (bootstrap < 50) monophyletic Porifera is the sister to all other animals, which are broadly arranged as seen in the SSU topology.”
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Our data unequivocally contradict this hypothesis and the proposal that Calcarea and Demospongia form a clade, leaving two hypotheses pertaining to sponge phylogeny for further consideration.”
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In the paper
“In contrast, the SSU topology has Hexactinellida plus Demospongia as the sister group to all other animals, Calcarea as the sister to nonsponge animals (Eumetazoa), and Ctenophora as the sister group to Cnidaria plus Bilateria.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“They are consistent in suggesting monophyletic Choanoflagellida, Metazoa, Bilateria, Cnidaria, and Ctenophora, with ML bootstraps of 100 except for Cnidaria (77 and 62) and Metazoa (63 and 63).”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“LSU and SSU data agree in supporting the monophyly of Bilateria, Cnidaria, Ctenophora, and Metazoa.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The SH test, which was applied to all hypotheses that resulted from the constrained and unconstrained tree searches, did not yield many significant P-values.”
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The combined tree agrees with the LSU topology in having Anthozoa as sister to the medusa-bearing cnidarians.”
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In the combined ML topology, Mesomycetozoa plus Choanoflagellida compose the sister group to Metazoa.”
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The SSU data do not refute any hypotheses by using this test.”
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- It may state two separate claims as one. 10
- Probably not a substantial claim. 6
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Finally, the layout among cnidarians differs between the two topologies, with Hydrozoa being the sister group of Anthozoa plus Scyphozoa in the SSU topology and Anthozoa as the sister group to the medusa-bearing cnidarians in the LSU topology.”
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Within each gene, the loops were markedly more A-T rich than the stems.”
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The symmetric difference, or the number of clades present in only one of two trees being compared, is 6 between the combined ML topology and the SSU tree, whereas the symmetric difference between the combined and LSU trees is 10.”
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“For instance, relatively accelerated substitution rates in both genes are evident for the bilaterian taxa whereas rates are relatively low for cnidarians and ctenophores.”
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“By combining the data, bootstrap support for monophyly of Cnidaria and Metazoa increased to 98 and 99, respectively.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“However, the SSU data do not refute either of the competing hypotheses, and the LSU and combined data both strongly contradict the hypothesis that Hydrozoa is sister to the other cnidarian groups.”
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In the paper
“The KH test is often inappropriately used to discern among hypotheses chosen a posteriori (33).”
What the sources say
- Not checked yetcites [33] Goldman N, Anderson J P, Rodrigo A G. Syst Biol. 2000;49:652–670. doi: 10.1080/106351500750049752. [DOI] [PubMed] [Google Scholar]
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In the paper
“Moreover, LSU is much larger than SSU and contains a greater proportion of variable regions.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✗ Based: failsProbably not a substantial claim. The paper may give no reason why it holds. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Nevertheless, three independent sets of molecular data show sponges to be paraphyletic—SSU, LSU, and Protein Kinase C—implying that this alternative is most likely.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“If true, then an animal with sponge characteristics is in the direct ancestry of nonsponge animals.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Cladistic analyses of morphology tend to suggest a step-wise arrangement where either Porifera or Placozoa diverge first, then Cnidaria, and finally Ctenophora, from the lineage leading to Bilateria (19, 20).”
What the sources say
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Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesProbably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The LSU data also reject the SSU ML topology, presumably because it contains the cnidarian hypothesis that is rejected.”
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
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In the paper
“Agreement has also developed for the proposal that Deuterostomia is a clade composed of just Chordata, Urochordata, Hemichordata, and Echinodermata (17, 18).”
What the sources say
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None of the sources cited for this claim have been checked yet.
In the paper
“Among the limitations noted are nucleotide compositional bias, among site rate variation, and heterogeneous rates of evolution across lineages (12–16).”
What the sources say
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The authors state this as an assumption.
Comparative zoology is predicated on the assumption of a phylogenetic history.
“Comparative zoology is predicated on the assumption of a phylogenetic history.”
The paper relies on this without support.
The best measure of the validity of any hypothesis is provided by the accord or incongruence of alternative lines of evidence.
“Nevertheless, the best measure of the validity of any hypothesis is provided by the accord or incongruence of alternative lines of evidence.”
The paper relies on this without support.
Determining orthologs is not problematic for ribosomal genes because of the mechanisms of concerted evolution.
“Unlike for some protein coding genes, determining orthologs is not problematic for ribosomal genes because of the mechanisms of concerted evolution.”
The paper relies on this without support.
The best available model of sequence evolution selected by likelihood ratio tests is adequate for phylogenetic analysis.
“We performed nested likelihood ratio tests (LRT) by using modeltest version 3.0 (30) to determine the best available model of sequence evolution for the SSU, LSU, and combined data, as well as the stem and loop regions of each gene.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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 Medina et al., 2001
In the citing paper
“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 Medina et al., 2001
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Metadata
- Authors
- Medina, M., Collins, A. G., Silberman, J. D., & Sogin, M. L.
- Affiliations
- Marine Biological Laboratory (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2001-08-14
- Volume
- 98
- Issue
- 17
- Pages
- 9707-9712
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC55517
- OpenAlex
- W2028169893
- Semantic Scholar
- f694ef75b9f27240d665cb7d43dedb376b9ed7f2
- Cited by
- 395
- References
- 46
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 5 · 2023: 4 · 2022: 2 · 2021: 11 · 2020: 5 · 2019: 4 · 2018: 5 · 2017: 4 · 2016: 10 · 2015: 7 · 2014: 9 · 2013: 10 · 2012: 16
- FWCI
- 23.98
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Smithsonian Digital Repository (Smithsonian Institution) (submittedVersion)
- Funders
- National Science Foundation (9814845)
- National Aeronautics and Space Administration
- Florida International University
- National Institutes of Health (5r01gm032964-17, GM32964)
- National Institute of General Medical Sciences (GM32964)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- sponge phylogeny, Hexactinellida, Demospongiae, Silicea, calcareous sponges, sponges, Bilateria, Ctenophora, Cnidaria, monophyly, large subunit rRNA, small subunit rRNA, phylogenetic incongruence
- MeSH terms
- Animals, Animal Population Groups, Aplysia, Cnidaria, Echinodermata, Fungi, Models, Biological, Molecular Sequence Data, Phylogeny, Platyhelminths, Porifera, RNA, Fungal, RNA, Ribosomal, Sequence Homology, Nucleic Acid, Species Specificity, Urochordata, Xenopus laevis, Polymerase Chain Reaction, Sequence Alignment, Sequence Analysis, RNA, Evolution, Molecular
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