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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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In the paper
“(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
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- 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
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- 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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In the paper
“In addition, probe excess titrations of Hox gene transcripts show that only one of the five Hox genes is utilized in the midgastrula stage or in the earliest trochophore stage (unpublished measurements).”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“In echinoids displaying maximal indirect development the embryonic process produces a bilaterally organized micrometazoan organism in 3 days which is capable of a freeliving, motile existence for months.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“First, it follows from them and from elementary phylogenetic considerations that the latest stem-group bilaterian prior to diversification into the great bilaterian clades would have utilized some form of indirect development.”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
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In the paper
“The propositions above predict that the Hox gene cluster, as such, will not be utilized for Type 1 embryo-to-larva developmental processes, but will be expressed only in the context of the patterning processes that occur in set-aside cells and their progeny (Davidson et al., 1995).”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
What the sources say
- Not checked yetcites Davidson et al., 1995 source
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In the paper
“The evolution of direct development is not seen until the Late Cretaceous, when nine clades independently lost the larval stage.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“Emlet (1985) demonstrated that of the 10 apical plates found in the adult echinoid test, the crystal axes of 6 are determined by the crystal axes of the larval skeleton, while the other 4 are formed de novo.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
What the sources say
- Not checked yetcites Emlet, 1985 source
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In the paper
“Thus it is inescapable that the latest common ancestor of this genus was a maximal indirect developer”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“Genes of the panbilaterian Hox cluster affect adult body plan morphogenesis, specifically by intervening and/or participating in regional specification processes.”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
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In the paper
“The notion that significant similarities are shared by all deuterostome dipleurula larvae is further supported by new studies on Brachyury expression in enteropneust hemichordates”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“This is typically a bilaterally organized micrometazoan which is the product of 10 Ϯ 2 rounds of division after fertilization, consisting of single-cell-thick structures.These are composed of a small number of differentiated cell types, e.g., muscle cells, neurons, ectodermal cells, several gut cell types, and mesenchymal mesodermal cells.”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
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In the paper
“We thus proposed that the initial stem-group bilaterians were a micrometazoan fauna, whose grade of organization was that which could be constructed solely with Type 1 embryonic regulatory processes.”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
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In the paper
“In addition it would have expressed the Brachyury gene in its mesodermal set-aside cells (Peterson et al., 1999a,b), supporting the obvious morphological homology of these cells and their coelomic derivatives (Peterson et al., 1997).”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
What the sources say
- Not checked yetcites Peterson et al., 1999a,b
- Not checked yetcites Peterson et al., 1997 source
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In the paper
“Hence, there was a latest common ancestor of bilaterians which must antedate representatives of any of the three bilaterian clades.”
§ Bilaterian Origins: Significance of New Experimental Observations > PHYLOGENY
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In the paper
“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.”
§ Bilaterian Origins: Significance of New Experimental Observations > Abstract
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In the paper
“The experiment of Raff et al. (1999) shows that the evolution of direct development in the ancestors of H. erythrogramma involved the disabling of the genetic regulatory program required to generate the larva, which is rescued in the hybrid.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
What the sources say
- Not checked yetcites Raff et al., 1999 source
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In the paper
“Furthermore, the latest common ancestor of molluscs and annelids was also indirectly developing.”
§ Bilaterian Origins: Significance of New Experimental Observations > Abstract
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In the paper
“This suggests that the latest common ancestor of hemichordates and echinoderms (Fig. 2, node H) would also have expressed Brachyury in these regions of the gut.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“In summary, it is a clear and unambiguous conclusion that the latest common ancestors of all echinoids at node B of Fig. 2 were a maximally indirectly developing population.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“Given that all other eleutherozoan groups (i.e., asteroids, ophiuroids, echinoids, and holothurians, which is to say all modern echinoderm groups except crinoids) also have primary larval stages, the latest common ancestor of eleutherozoans (Fig. 2, node E) must have utilized maximal indirect development as well (see also Smith, 1997;Nielsen, 1998).”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
What the sources say
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In the paper
“and similarly that the latest common ancestor of lophotrochozoan spiralians utilized a trochophore-like larva.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“A reasonable interpretation is that the latest common ancestor of deuterostomes (and possibly lophotrochozoans) utilized a dipleurula larva in its development”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“Thus both hemichordate and echinoderm dipleurula larvae express the Brachyury gene in the oral and anal regions of the larval gut.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
What the sources say
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In the paper
“Modern bilaterian animals, excepting the most complex and specialized forms such as insects, vertebrates, and cephalopods, utilize for embryogenesis a common set of developmental regulatory mechanisms.”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
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In the paper
“The development of modern adult bilaterian body plans requires an elaborate genetic control apparatus, the capacities of which far exceed the regulatory repertoire of Type 1 embryogenesis.”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
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In the paper
“Therefore, indirect development of some kind should be primitive for Bilateria.”
§ Bilaterian Origins: Significance of New Experimental Observations > INTRODUCTION
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In the paper
“and this case illustrates the polarity of a transition to direct development in echinoids; the latest common ancestor of all echinoidans was also obviously an indirect developer (node A of Fig. 2).”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“Using all three lines of evidence, Jeffery (1997) showed that direct-developing forms appeared only recently in the geological history of echinoids.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
What the sources say
- Not checked yetcites Jeffery, 1997 source
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In the paper
“It is immediately apparent that on phylogenetic grounds alone maximal indirect development is likely to be primitive for echinoids.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“Second, the sea urchin results confirm the proposition that the Hox complex is specifically required for adult body plan formation”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“In many ways the dipleurula larva of deuterostomes and the trochophore larva of lophotrochozoans resemble one another, even though their morphology differs.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“It was assembled from a far more ancient set of regulatory genes”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“However, the forms after internode 3 would have still had to utilize regulatory mechanisms for constructing the platform upon which to mount and develop the progeny of their set-aside cells that were similar to those utilized by their ancestors at internodes 1 and 2.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“Their structures were axially organized”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“In post-Cambrian evolution the vectorial spatial regulatory capacity of the Hox complex has been repeatedly coopted, above and beyond its function in A-P axis specification.”
§ 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.
In the paper
“There are also expression data for another gene, Cnox2, which again is expressed dynamically in a single cell type (Shenk et al., 1993a,b)”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
What the sources say
- Not checked yetcites Shenk et al., 1993a,b
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In the paper
“The import of these results is that the Hox complex is used in patterning elements of the adult body plan rather than for development of the larva-specific structures.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“in amniotes it is used in the specification of axial positions in the urogeni-tal tract (Kondo et al., 1997;Taylor et al., 1997)”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“In addition to the Type 1 regulatory package for embryogenesis it now possessed regional specification mechanisms that could impose spatial regulatory status on relatively massive numbers of growing cells (compared to any of its ancestors).”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“Many of these interconnections remain, in their various forms, programmed into the genomic sequences of the modern Bilateria.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“A glance at Fig. 1 implies that this origin was the latest common ancestor of bilaterians.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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“The regulatory repertoire now approaches that shared by all extant bilaterian organisms (except for those individual clades of modern bilaterians that have lost portions of this ancestral repertoire”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
What the sources say
- Not checked yetcites Ruvkun and Hobart, 1998
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In the paper
“It is important to emphasize that the similarities in utilization of the Hox complex in annelid and echinoderm larvae are not due merely to the small size of the larvae.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“Hence, a Hox complex consisting of at least seven genes (de Rosa et al., 1999) appears to be a bilaterian invention.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
What the sources say
- Not checked yetcites de Rosa et al., 1999 source
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In the paper
“The trochoblasts are larva-specific cells which generate larva-specific features, and their provenance and regulatory circuitry in annelid and molluscan embryos can only indicate a common ancestry, not convergence.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“Thus our observations support the panbilaterian developmental function of the Hox gene cluster per se in adult body plan formation.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“A number of molecular divergence studies now indicate that the bilaterian crown group may have originated (solid circle) as much as 630 -1200 Mya (e.g., Wray et al., 1996;Ayala et al., 1997;Bromham et al., 1998;Gu, 1998;Lynch, 1999;Wang et al., 1999).”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
What the sources say
- Not checked yetcites Wray et al., 1996
- Not checked yetcites Ayala et al., 1997
- Not checked yetcites Wang et al., 1999 source
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In the paper
“It was assembled in stages, no doubt as external conditions rendered useful the potential developmental outcomes (see discussion in Knoll and Carroll, 1999).”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
What the sources say
- Not checked yetcites Knoll and Carroll, 1999 source
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In the paper
“The latest stem bilaterian after internode 3, represented by the solid dot in Fig. 4, was ancestral to the directly developing Ecdysozoa as well as to Lophotrochozoa and Deuterostomia”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“It follows that the latest common ancestor of annelids and molluscs (Fig. 2, node J) utilized a trochophore larva.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“The homologous early development of their mesoderm is among the most basic and fundamental mechanisms utilized for constructing the adult body plans of these taxa.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“In sum, the developmental processes by which the embryo gives rise to the larva and the set-aside cells to the adult body plan are likely to have a shared evolutionary origin.”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“but this appears to be a ParaHox gene related to Gsx and not a Hox gene (Bu ¨rglin, 1994).”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
What the sources say
- Not checked yetcites Bu ¨rglin, 1994
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In the paper
“Third, they suggest that the lophotrochozoan and the deuterostome embryo/larva are in some distant sense homologous”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“These features can hardly have arisen by convergence.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“First, they show that the regulatory apparatus required to build a bilaterally organized micrometazoan organism that is capable of free-living existence, and that is composed of fully differentiated cells, does not necessarily include the Hox complex per se”
§ Bilaterian Origins: Significance of New Experimental Observations > EXPRESSION OF THE Hox GENE CLUSTER IN MAXIMAL INDIRECT DEVELOPMENT
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In the paper
“First, it is important that cnidarians do not have a Hox cluster like that of bilaterians.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
What the sources say
- Not checked yetcites Finnerty and Martindale, 1998
- Not checked yetcites Martinez et al., 1998 source
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In the paper
“The use of larva-specific Type 1 differentiation processes and the generation of adult body plan structures from set-aside cells in lophotrochozoans as well as in deuterostomes may be homologous.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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In the paper
“The developmental hardwiring which defines the bilaterian genome did not “spring forth fully blown” to appear all at once in the “urbilaterian.””
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“Thus, for example, Damen and van Loon (1996) and Damen et al. (1997) showed convincingly that the trochophores of annelids and molluscs share detailed similarities in the genetic regulatory circuitry underlying the development of trochophore-specific features.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
What the sources say
- Not checked yetcites Damen and van Loon (1996)
- Not checked yetcites Damen et al. (1997) source
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In the paper
“With respect to the evolutionary stages indicated in Fig. 4, the Hox complex would have arisen between internodes 2 and 3.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
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In the paper
“The latest common ancestor of echinoderms (Fig. 2, node F), hemichordates (Fig. 2, node G), and echinoderms ϩ hemichordates (Fig. 2, node H) must thus have utilized maximal indirect development.”
§ Bilaterian Origins: Significance of New Experimental Observations > FIG. 1.
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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
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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.
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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
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. It may state two separate claims as one.
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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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Probably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds.
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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.
plaindirect- Asserted: passes — The authors put it forward as true.
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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
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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
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a 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
“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
boosteddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
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
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
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
“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
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
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.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a 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
“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
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a 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
“for which we conclude indirect development is primitive.”
§ Bilaterian Origins: Significance of New Experimental Observations > ORIGIN OF THE BILATERIANS
boosted- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
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.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
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.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
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
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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
Cites
Evidence for a clade of nematodes, arthropods and other moulting animals
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The origins and relationships of lower invertebrates
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Archetypal organization of the amphioxus Hox gene cluster
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Evidence from 18 S Ribosomal DNA that the Lophophorates Are Protostome Animals
Halanych, K. M., Bacheller, J. D., Aguinaldo, A. M. A., Liva, S. M., Hillis, D. M., & Lake, J. A. (1995) · Science · doi:10.1126/science.7886451 · Cited by 575
Research works printed but not linked: 3
- Haeckel, 1874, die Gastrea-Theorie, die phylogenetische Classification des Thierreichs und die Homologie der Keimblätter, Jena. Z. Naturw., 8, 1
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- Jablonski, 1986, Larval ecology and macroevolution in marine invertebrates, Bull. Mar. Sci., 39, 565
Cited by
Sorted by citations
Cardiac Chamber Formation: Development, Genes, and Evolution
Moorman, A. F. M., & Christoffels, V. M. (2003) · Physiological Reviews · doi:10.1152/physrev.00006.2003 · Cited by 739
Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite
Weiss, I. M., Tuross, N., Addadi, L., & Weiner, S. (2002) · Journal of Experimental Zoology · doi:10.1002/jez.90004 · Cited by 665
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Self-citationThe new animal phylogeny: Reliability and implications
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Evolution of the chordate body plan: New insights from phylogenetic analyses of deuterostome phyla
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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
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