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Bilaterian Origins: Significance of New Experimental Observations
Open accessAbstract
Several recent laboratory observations that bear on the origin of the Bilateria are reviewed and interpreted in light of our set-aside cell theory for bilaterian origins. We first discuss new data concerning the phylogeny of bilaterian phyla. Next, we use systematic, molecular, and paleontological lines of evidence to argue that the latest common ancestor of echinoderms plus hemichordates used a maximal indirect mode of development. Furthermore, the latest common ancestor of molluscs and annelids was also indirectly developing. Finally, we discuss new data on Hox gene expression patterns which suggest that both sea urchins and polychaete annelids use Hox genes in a very similar fashion. Neither utilizes the complete Hox complex in the development of the larva per se, while the Hox complex is expressed in the set-aside cells from which the adult body plan is formed. Our current views on the ancestry of the bilaterians are summarized in phylogenetic terms, incorporating the characters discussed in this paper.
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51 Own interpretation · 32 Not checked yet · 11 No basis given · 4 Own result · 1 Own method
In the paper
“We showed that the larva develops exactly the same structures whether or not it contains the rudiment from which the adult derives (Davidson et al., 1995).”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
What the sources say
- Not checked yetcites Davidson et al., 1995 source
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“(A) The CH-Hox2 expression pattern in a L1-stage larva (see Irvine et al., 1999) seen in longitudinal section with the anterior end upward.The cells expressing the gene are in the posterior region occupied by the teloblasts, which generate the segmental tissues of the adult body.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
What the sources say
- Not checked yetcites Irvine et al., 1999
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In the paper
“More importantly, all of those Hox cluster genes so far investigated by in situ hybridization are indeed expressed in the progeny of the set-side cells, i.e., as elements that will give rise to structures of the juvenile”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
What the sources say
- Not checked yetcites Arenas-Mena et al., 1998 source
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In the paper
“(B) CH-Hox4 expression in an L2 larval stage.The plane of section is slightly oblique to the longitudinal axis and the gut appears almost in cross section.Like CH-Hox2, the cells expressing the Chv-Hox4 gene product are the progeny of the teloblastic set-aside cells.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“Expression of five different Hox genes in embryonic Chaetopterus, two of which are shown, occurs in the presumed germ band stem cells.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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“All of the eight Hox genes so far examined are expressed copiously during adult body plan formation (Arenas-Mena et al., 1998).”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
What the sources say
- Not checked yetcites Arenas-Mena et al., 1998 source
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In the paper
“The progeny of those cells form the pentamerally symmetric mesodermal components of the juvenile.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“So far no real surprises: the more shocking observation that emerged from this study was that 6 of the 8 Hox cluster genes examined by Arenas-Mena et al. (1998) are not significantly expressed at all until embryogenesis is complete.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
What the sources say
- Not checked yetcites Arenas-Mena et al. (1998) source
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In the paper
“So far at least, a correct statement is that in echinoids the Hox gene cluster is expressed in set-aside cell progeny during the early phases of adult body plan development.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“At the end of embryogenesis the set-aside cells are located in two prominent pouches of about 10 cells each, protruding on either side of the foregut.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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- It may state two separate claims as one. 26
- Probably not a substantial claim. 3
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In the paper
“It is immediately apparent that while maximal indirect development is conspicuously absent in ecdysozoans, it occurs in most deuterostome and lophotrochozoan clades.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“One gene is also expressed in the gut, and another in the protonephridia, but for the other three the locus of expression is exclusively in the set-aside cells and not in any cells constituting the bilateral structures of the feeding larva.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“As in amphioxus (Garcı ´a-Fernandez and Holland, 1994), there is a single Hox cluster, which includes at least 10 genes.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
What the sources say
- Not checked yetcites Martinez et al., 1999 source
plainSingle case- Asserted: passes — The authors put it forward as true.
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In the paper
“A second very important point for our present purposes, which is illustrated in Fig. 1, is that the Bilateria are monophyletic, the sister group of Cnidaria”
§ Bilaterian Origins: Significance of New Experimental Observations > PHYLOGENY
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In the paper
“In this case, however, numerous transitions to direct development must have occurred, since most of the clades marked on Fig. 1 also contain some direct developing forms.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“As this mode of early development is found in all invertebrate deuterostomes (including invertebrate chordates), and also in most protostome clades, it is concluded to be primitive for Bilateria.”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
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In the paper
“Finally, we discuss new data on Hox gene expression patterns which suggest that both sea urchins and polychaete annelids use Hox genes in a very similar fashion.Neither utilizes the complete Hox complex in the development of the larva per se, while the Hox complex is expressed in the set-aside cells from which the adult body plan is formed.”
§ Bilaterian Origins: Significance of New Experimental Observations > Abstract
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In the paper
“For present concerns the main point of Fig. 1 is that Lophotrochozoa, Ecdysozoa, and Deuterostomia are each monophyletic clades.”
§ Bilaterian Origins: Significance of New Experimental Observations > PHYLOGENY
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In the paper
“The only monophyletic group of genera that is entirely direct developing is the echinothuroids.To a greater or lesser extent all other clades include species that utilize planktotrophic larvae, which is to say they develop by maximal indirect processes.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“Significantly, H. erythrogramma shows vestiges of the larval skeleton and epaulettes (Emlet, 1995), as well as retaining some of the larval ectoderm cell lineage assignments of its relatives (Wray and Raff, 1990).”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
What the sources say
- Not checked yetcites Emlet, 1995 source
- Not checked yetcites Wray and Raff, 1990
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In the paper
“In maximal indirect development, as defined earlier (Davidson et al., 1995;Peterson et al., 1997), the embryo gives rise to a larva that bears little relation to the adult body plan, and the latter is formed by a separate postembryonic developmental process.”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
What the sources say
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In the paper
“The key difference between maximal indirect development and direct development is that in direct development regional specification processes are telescoped immediately onto Type 1 embryogenesis so that assembly of the adult body plan begins at once.”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
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In the paper
“Hence, the trochoblasts of annelid and molluscan embryos express the same lineage-specific gene, and expression is driven by the same set of transcription factors.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“Hence trochophore and trochophore-like larvae must be primitive for at least spiralians if not for all lophotrochozoans.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“Finally, both use set-aside cells for the construction of the adult body plan.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“In order to position the origin of the vectorial Hox gene regulatory system in early bilaterian evolution, we point out that it must have arisen following the appearance of set-aside cells (internode 2 of Fig. 4), since it would not have been useful before this, i.e., in the context of purely Type 1 embryonic process.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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- Rests on an assumption: The Hox complex is a vectorial patterning system composed of a linked set of genes encoding similar transcription factors.
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
“In this sense their development could now be termed indirect, because the adult forms were produced indirectly, and what had been the adult form after internode 1 has now become merely a developmental platform.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“Thus the ecdysozoan common ancestor per se must have lost the larval “form,” which was still preserved in the ancestor of all protostomes.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“But they fly in the face of the assumption that development of all bilaterian animal forms depends on Hox cluster function, since the free-living echinoid larva is such a form.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
plainSingle case- Asserted: passes — The authors put it forward as true.
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In the paper
“This process involved gene duplication and genomic organization, but above all the making and breaking of thousands upon thousands of intergenic regulatory connections.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“There can now be no question that the primitive echinoid condition was indirect development and that the polarity of the transitions which have frequently and independently occurred during echinoid evolution is always toward direct development.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“and in mammals even to provide a temporal rather than spatial regulatory sequence in hematopoietic differentiation (Care ` et al., 1994).”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
What the sources say
- Not checked yetcites Care ` et al., 1994
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In the paper
“and thus they deployed vectorial mechanisms in their spatial development, including organizer systems that secrete diffusible signaling factors, and also the Hox gene complex.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“This was established by measurements of Hox gene mRNA content per embryo, measurements which far exceed the sensitivity of in situ hybridization for this material and which detect transcripts down to the level of a few tenths of a molecule per average embryo cell.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
boosted- Asserted: passes — The authors put it forward as true.
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In the paper
“The animals utilizing these mechanisms built mesodermal layers and some form of CNS, at least in their adult phases.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“for which we conclude indirect development is primitive.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“Both utilize Type 1 embryogenesis (see Davidson, 1991;Davidson et al., 1995; and the data discussed above), which divides the cleavage-stage embryo into a set of polyclonal territories.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
What the sources say
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Moreover, the expression of one of these genes (Cnox1-Pc, a posterior-type gene; Martinez et al., 1998) is limited to a single cell type (Aerne et al., 1995), unlike Hox gene expression in bilaterians.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
What the sources say
- Not checked yetcites Martinez et al., 1998
- Not checked yetcites Aerne et al., 1995
plain- Asserted: passes — The authors put it forward as true.
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The paper relies on this without support.
The Hox complex is a vectorial patterning system composed of a linked set of genes encoding similar transcription factors.
“The Hox complex is essentially a vectorial patterning system consisting of a linked set of genes encoding similar transcription factors.”
The paper relies on this without support.
The developmental expression of Hox regulators in a linear positional array depends on their chromosomal order.
“The developmental expression of these regulators in a linear positional array depends in some way yet unclear on their chromosomal order.”
The paper relies on this without support.
Hox complex function is always to specify regulatory states in populations of growing cells.
“Hox complex function is always to specify regulatory states in populations of growing cells.”
Claims other papers make about this one
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In the citing paper
“Many lines of evidence show that for deuterostomes and lophotrochozoans maximal indirect development is primitive, and direct development is derived (36–38).”
From Precambrian animal diversity: Putative phosphatized embryos from the Doushantuo Formation of China (2000) · cites this paper as [37]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
“Damen and van Loon (1996) showed that this specificity is achieved through modular elements of the cis-regulatory system controlling the -tubulin gene.”
§ Bilaterian Origins: Significance of New Experimental Observations > References
“30. Damen, W. G. M., and van Loon, A. E. (1996). Multiple cis-acting elements act cooperatively in directing trochoblast-specific ex- pression of the ␣-tubulin-4 gene in Patella embryos.”
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
“e.g., Wray et al., 1996;Ayala et al., 1997;Bromham et al., 1998”
§ Bilaterian Origins: Significance of New Experimental Observations > References
“8. Ayala, F. J., Rzhetsky, A., and Ayala, F. J. (1998). Origin of the metazoan plyla: Molecular clocks confirm paleontological esti- mates.”
Citations
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Weiss, I. M., Tuross, N., Addadi, L., & Weiner, S. (2002) · Journal of Experimental Zoology · doi:10.1002/jez.90004 · Cited by 665
Peterson, K. J., & Eernisse, D. J. (2001) · Evolution & Development · doi:10.1046/j.1525-142x.2001.003003170.x · Cited by 529
Self-citationThe new animal phylogeny: Reliability and implications
Adoutte, A., Balavoine, G., Lartillot, N., Lespinet, O., Prud'homme, B., & de Rosa, R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4453 · Cited by 512
Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla
Cameron, C. B., Garey, J. R., & Swalla, B. J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4469 · Cited by 414
Metadata
- Authors
- Peterson, K. J., Cameron, R. A., & Davidson, E. H.
- Affiliations
- California Institute of Technology (US)
- ORCID
- Cameron, R.Andrew
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2000-03
- Volume
- 219
- Issue
- 1
- Pages
- 1-17
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W2022880235
- Cited by
- 133
- References
- 131
- Citations by year
- 2025: 1 · 2023: 2 · 2022: 2 · 2021: 3 · 2019: 1 · 2017: 2 · 2016: 2 · 2015: 3 · 2014: 1 · 2013: 1 · 2012: 1
- FWCI
- 1.47
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- National Science Foundation (9604454)
- Yale University
- California Institute of Technology
- State University of New York
- University of Washington
- National Institutes of Health
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD05753)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
- Keywords
- bilaterian origin, indirect development, Echinodermata, hemichordates, Mollusca, Annelida, Hox genes, sea urchins, Polychaeta, larval development, body plan evolution, common ancestor
- MeSH terms
- Animals, Annelida, Chordata, Nonvertebrate, Echinodermata, Biological Evolution, Genes, Homeobox, Multigene Family, Invertebrates, Models, Biological, Mollusca, Phylogeny, Gene Expression Regulation, Developmental
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
A language model drew the claims from the paper on 2026-10-06, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).
A second model labelled each claim on 2026-10-06 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).
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