Bilaterian Origins: Significance of New Experimental Observations

The echinoid larva develops exactly the same structures whether or not it contains the adult rudiment.

“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).”

• cites Davidson et al., 1995 sourceNot checked yet

  Not checked in the free run.

In Chaetopterus L1-stage larvae, CH-Hox2 expression is in the posterior region occupied by teloblasts, which generate the segmental tissues of the adult body.

“(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.”

• cites Irvine et al., 1999Not checked yet

  Not checked in the free run.

All Hox cluster genes so far investigated by in situ hybridization are expressed in the progeny of set-aside cells.

“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”

• cites Arenas-Mena et al., 1998 sourceNot checked yet

  Not checked in the free run.

In Chaetopterus L2 larval stage, cells expressing CH-Hox4 are progeny of teloblastic set-aside cells.

“(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.”

Expression of five different Hox genes in embryonic Chaetopterus occurs in the presumed germ band stem cells.

“Expression of five different Hox genes in embryonic Chaetopterus, two of which are shown, occurs in the presumed germ band stem cells.”

All eight Hox genes examined so far are expressed copiously during adult body plan formation.

“All of the eight Hox genes so far examined are expressed copiously during adult body plan formation (Arenas-Mena et al., 1998).”

• cites Arenas-Mena et al., 1998 sourceNot checked yet

  Not checked in the free run.

The progeny of the set-aside cells form the pentamerally symmetric mesodermal components of the juvenile.

“The progeny of those cells form the pentamerally symmetric mesodermal components of the juvenile.”

Six of the eight Hox cluster genes examined are not significantly expressed until embryogenesis is complete.

“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.”

• cites Arenas-Mena et al. (1998) sourceNot checked yet

  Not checked in the free run.

In echinoids, the Hox gene cluster is expressed in set-aside cell progeny during the early phases of adult body plan development.

“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.”

At the end of embryogenesis, the set-aside cells are located in two pouches of about 10 cells each, protruding on either side of the foregut.

“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.”

Probe excess titrations show that only one of five Hox genes is utilized in the midgastrula stage or in the earliest trochophore stage.

“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).”

In echinoids with maximal indirect development, the embryonic process produces a bilaterally organized micrometazoan in 3 days that can live freely and move for months.

“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.”

The latest stem-group bilaterian prior to diversification into the great bilaterian clades would have utilized some form of indirect development.

“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.”

The Hox gene cluster is not used for Type 1 embryo-to-larva developmental processes but is expressed in the patterning processes that occur in set-aside cells and their progeny.

“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).”

• cites Davidson et al., 1995 sourceNot checked yet

  Not checked in the free run.

The evolution of direct development in echinoids is not seen until the Late Cretaceous, when nine clades independently lost the larval stage.

“The evolution of direct development is not seen until the Late Cretaceous, when nine clades independently lost the larval stage.”

Emlet (1985) demonstrated that of the 10 apical plates in the adult echinoid test, the crystal axes of 6 are determined by the larval skeleton, while the other 4 are formed de novo.

“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.”

• cites Emlet, 1985 sourceNot checked yet

  Not checked in the free run.

The latest common ancestor of the genus Heliocidaris was a maximal indirect developer.

“Thus it is inescapable that the latest common ancestor of this genus was a maximal indirect developer”

Hox genes of the panbilaterian cluster affect adult body plan morphogenesis by intervening in or participating in regional specification processes.

“Genes of the panbilaterian Hox cluster affect adult body plan morphogenesis, specifically by intervening and/or participating in regional specification processes.”

All deuterostome dipleurula larvae share significant similarities.

“The notion that significant similarities are shared by all deuterostome dipleurula larvae is further supported by new studies on Brachyury expression in enteropneust hemichordates”

• cites Tagawa et al., 1998 sourceNot checked yet

  Not checked in the free run.

• cites Peterson et al., 1999aNot checked yet

  Not checked in the free run.

• cites Shoguchi et al., 1999 sourceNot checked yet

  Not checked in the free run.

The larva in maximal indirect development is typically a bilaterally organized micrometazoan produced by 10±2 rounds of division after fertilization, consisting of single-cell-thick structures with a small number of differentiated cell types.

“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.”

The initial stem-group bilaterians were a micrometazoan fauna whose grade of organization could be constructed solely with Type 1 embryonic regulatory processes.

“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.”

The latest common ancestor of hemichordates and echinoderms would also have expressed Brachyury in its mesodermal set-aside cells.

“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).”

• cites Peterson et al., 1999a,bNot checked yet

  Not checked in the free run.

• cites Peterson et al., 1997 sourceNot checked yet

  Not checked in the free run.

There was a latest common ancestor of bilaterians that must antedate representatives of any of the three bilaterian clades.

“Hence, there was a latest common ancestor of bilaterians which must antedate representatives of any of the three bilaterian clades.”

The latest common ancestor of echinoderms plus hemichordates used a maximal indirect mode of development.

“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.”

The Raff et al. experiment shows that the evolution of direct development in the ancestors of H. erythrogramma involved disabling the genetic regulatory program required to generate the larva, which is rescued in the hybrid.

“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.”

• cites Raff et al., 1999 sourceNot checked yet

  Not checked in the free run.

The latest common ancestor of molluscs and annelids was also indirectly developing.

“Furthermore, the latest common ancestor of molluscs and annelids was also indirectly developing.”

The latest common ancestor of hemichordates and echinoderms would have expressed Brachyury in the oral and anal regions of the gut.

“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.”

The latest common ancestors of all echinoids at node B of Fig. 2 were a maximally indirectly developing population.

“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.”

The latest common ancestor of eleutherozoans (node E of Fig. 2) must have utilized maximal indirect development.

“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).”

• cites Smith, 1997 sourceNot checked yet

  Not checked in the free run.

• cites Nielsen, 1998 sourceNot checked yet

  Not checked in the free run.

The latest common ancestor of lophotrochozoan spiralians utilized a trochophore-like larva.

“and similarly that the latest common ancestor of lophotrochozoan spiralians utilized a trochophore-like larva.”

The latest common ancestor of deuterostomes, and possibly of lophotrochozoans, utilized a dipleurula larva in its development.

“A reasonable interpretation is that the latest common ancestor of deuterostomes (and possibly lophotrochozoans) utilized a dipleurula larva in its development”

Hemichordate and echinoderm dipleurula larvae both express Brachyury in the oral and anal regions of the larval gut.

“Thus both hemichordate and echinoderm dipleurula larvae express the Brachyury gene in the oral and anal regions of the larval gut.”

• cites Tagawa et al., 1998 sourceNot checked yet

  Not checked in the free run.

• cites Peterson et al., 1999aNot checked yet

  Not checked in the free run.

• cites Shoguchi et al., 1999 sourceNot checked yet

  Not checked in the free run.

Most bilaterian animals, except the most complex and specialized forms such as insects, vertebrates, and cephalopods, employ a shared set of developmental regulatory mechanisms during embryogenesis.

“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.”

The development of modern adult bilaterian body plans requires an elaborate genetic control apparatus whose capacities exceed those of Type 1 embryogenesis.

“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.”

Indirect development of some kind should be primitive for Bilateria.

“Therefore, indirect development of some kind should be primitive for Bilateria.”

The latest common ancestor of all echinoidans was an indirect developer (node A of Fig. 2).

“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).”

Using all three lines of evidence, Jeffery (1997) showed that direct-developing forms appeared only recently in the geological history of echinoids.

“Using all three lines of evidence, Jeffery (1997) showed that direct-developing forms appeared only recently in the geological history of echinoids.”

• cites Jeffery, 1997 sourceNot checked yet

  Not checked in the free run.

On phylogenetic grounds alone, maximal indirect development is likely primitive for echinoids.

“It is immediately apparent that on phylogenetic grounds alone maximal indirect development is likely to be primitive for echinoids.”

The sea urchin results confirm that the Hox complex is specifically required for adult body plan formation.

“Second, the sea urchin results confirm the proposition that the Hox complex is specifically required for adult body plan formation”

The dipleurula larva of deuterostomes and the trochophore larva of lophotrochozoans resemble one another despite differences in morphology.

“In many ways the dipleurula larva of deuterostomes and the trochophore larva of lophotrochozoans resemble one another, even though their morphology differs.”

The bilaterian developmental hardwiring was assembled from a far more ancient set of regulatory genes.

“It was assembled from a far more ancient set of regulatory genes”

Forms after internode 3 still had to use regulatory mechanisms for constructing the platform on which to mount and develop the progeny of their set-aside cells, similar to those used by ancestors at internodes 1 and 2.

“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.”

The structures of these animals were axially organized.

“Their structures were axially organized”

In post-Cambrian evolution, the vectorial spatial regulatory capacity of the Hox complex has been repeatedly coopted beyond its role in A-P axis specification.

“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.”

• AssumptionRests on an assumption: The Hox complex is a vectorial patterning system composed of a linked set of genes encoding similar transcription factors.

Cnox2 is expressed dynamically in a single cell type.

“There are also expression data for another gene, Cnox2, which again is expressed dynamically in a single cell type (Shenk et al., 1993a,b)”

• cites Shenk et al., 1993a,bNot checked yet

  Not checked in the free run.

The Hox complex is used in patterning elements of the adult body plan rather than for development of larva-specific structures.

“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.”

In amniotes, the Hox complex is used to specify axial positions in the urogenital tract.

“in amniotes it is used in the specification of axial positions in the urogeni-tal tract (Kondo et al., 1997;Taylor et al., 1997)”

• cites Kondo et al., 1997 sourceNot checked yet

  Not checked in the free run.

• cites Taylor et al., 1997 sourceNot checked yet

  Not checked in the free run.

Besides the Type 1 embryogenesis regulatory package, the latest common ancestor at internode 3 had regional specification mechanisms capable of imposing spatial regulatory status on relatively large numbers of growing cells compared with its ancestors.

“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).”

Many of these interconnections remain, in various forms, programmed into the genomic sequences of modern Bilateria.

“Many of these interconnections remain, in their various forms, programmed into the genomic sequences of the modern Bilateria.”

The shared evolutionary origin of these developmental processes was the latest common ancestor of bilaterians.

“A glance at Fig. 1 implies that this origin was the latest common ancestor of bilaterians.”

At internode 3, the latest common ancestor of bilaterians had a regulatory repertoire close to the one shared by all living bilaterians, except for lineages that lost parts of this ancestral repertoire.

“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”

• cites Ruvkun and Hobart, 1998Not checked yet

  Not checked in the free run.

The similarities in Hox complex utilization in annelid and echinoderm larvae are not due merely to the small size of the larvae.

“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.”

A Hox complex of at least seven genes appears to be a bilaterian invention.

“Hence, a Hox complex consisting of at least seven genes (de Rosa et al., 1999) appears to be a bilaterian invention.”

• cites de Rosa et al., 1999 sourceNot checked yet

  Not checked in the free run.

The provenance and regulatory circuitry of trochoblasts in annelid and molluscan embryos indicate common ancestry rather than convergence.

“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.”

The observations support a panbilaterian developmental function of the Hox gene cluster itself in adult body plan formation.

“Thus our observations support the panbilaterian developmental function of the Hox gene cluster per se in adult body plan formation.”

Molecular divergence studies indicate that the bilaterian crown group may have originated as much as 630-1200 million years ago.

“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).”

• cites Wray et al., 1996Not checked yet

  Not checked in the free run.

• cites Ayala et al., 1997Not checked yet

  Not checked in the free run.

• cites Wang et al., 1999 sourceNot checked yet

  Not checked in the free run.

The bilaterian developmental hardwiring was assembled in stages, as external conditions made potential developmental outcomes useful.

“It was assembled in stages, no doubt as external conditions rendered useful the potential developmental outcomes (see discussion in Knoll and Carroll, 1999).”

• cites Knoll and Carroll, 1999 sourceNot checked yet

  Not checked in the free run.

The latest stem bilaterian after internode 3 was ancestral to the directly developing Ecdysozoa, Lophotrochozoa, and Deuterostomia.

“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”

The latest common ancestor of annelids and molluscs used a trochophore larva.

“It follows that the latest common ancestor of annelids and molluscs (Fig. 2, node J) utilized a trochophore larva.”

The homologous early development of mesoderm is among the most fundamental mechanisms used to construct adult body plans in echinoderms and hemichordates.

“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.”

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.

“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.”

Cnox2 appears to be a ParaHox gene related to Gsx and not a Hox gene.

“but this appears to be a ParaHox gene related to Gsx and not a Hox gene (Bu ¨rglin, 1994).”

• cites Bu ¨rglin, 1994Not checked yet

  Not checked in the free run.

The lophotrochozoan and deuterostome embryo/larva are homologous in a distant sense.

“Third, they suggest that the lophotrochozoan and the deuterostome embryo/larva are in some distant sense homologous”

The shared trochophore-specific features of annelids and molluscs can hardly have arisen by convergence.

“These features can hardly have arisen by convergence.”

The regulatory apparatus required to build a bilaterally organized micrometazoan that can live freely and is composed of fully differentiated cells does not necessarily include the Hox complex itself.

“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”

Cnidarians lack a Hox cluster comparable to that of bilaterians.

“First, it is important that cnidarians do not have a Hox cluster like that of bilaterians.”

• cites Finnerty and Martindale, 1998Not checked yet

  Not checked in the free run.

• cites Martinez et al., 1998 sourceNot checked yet

  Not checked in the free run.

The use of larva-specific Type 1 differentiation and the generation of adult structures from set-aside cells in lophotrochozoans and deuterostomes may be homologous.

“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.”

The developmental hardwiring defining the bilaterian genome did not appear all at once in the urbilaterian.

“The developmental hardwiring which defines the bilaterian genome did not “spring forth fully blown” to appear all at once in the “urbilaterian.””

Annelid and molluscan trochophores share detailed similarities in the genetic regulatory circuitry that underlies trochophore-specific features.

“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.”

• cites Damen and van Loon (1996)Not checked yet

  Not checked in the free run.

• cites Damen et al. (1997) sourceNot checked yet

  Not checked in the free run.

The Hox complex arose between internodes 2 and 3 of Fig. 4.

“With respect to the evolutionary stages indicated in Fig. 4, the Hox complex would have arisen between internodes 2 and 3.”

The latest common ancestor of echinoderms, hemichordates, and the echinoderm-hemichordate clade must have used maximal indirect development.

“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.”