Homology of Hox Genes and the Zootype Concept in Early Metazoan Evolution

Schierwater, Bernd; Kuhn, Kerstin

doi:10.1006/mpev.1998.0489

Cited by 90 publications

(50 citation statements)

References 32 publications

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“…In this respect they are simpler than most larvae of cnidarians, ctenophorans, and poriferans. The simplicity of placozoans has been used to argue that they are basal to Cnidaria, Ctenophora, and Bilateria (35,36). The present phylogenetic analysis contradicts this assertion and instead suggests that placozoans are secondarily simplified.…”

Section: Evolution: Collinsmentioning

confidence: 50%

“…The simplicity of the placozoan body appears to be mirrored by a relatively simple regulatory gene system. A recent study was able to identify just a single placozoan gene resembling Hox genes of the Antennapedia class (Trox2), whereas similar effort turned up five such genes each in hydrozoan and scyphozoan cnidarians (36). The authors concluded that homology could not be determined for these genes and those known in Bilateria, though others have attempted the difficult task of linking some homeobox genes of diploblasts with Hox genes of bilaterians (37).…”

Section: Evolution: Collinsmentioning

confidence: 99%

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Evaluating multiple alternative hypotheses for the origin of Bilateria: An analysis of 18S rRNA molecular evidence

Collins

1998

Proc. Natl. Acad. Sci. U.S.A.

238

137

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Six alternative hypotheses for the phylogenetic origin of Bilateria are evaluated by using complete 18S rRNA gene sequences for 52 taxa. These data suggest that there is little support for three of these hypotheses. Bilateria is not likely to be the sister group of Radiata or Ctenophora, nor is it likely that Bilateria gave rise to Cnidaria or Ctenophora. Instead, these data reveal a close relationship between bilaterians, placozoans, and cnidarians. From this, several inferences can be drawn. Morphological features that previously have been identified as synapomorphies of Bilateria and Ctenophora, e.g., mesoderm, more likely evolved independently in each clade. The endomesodermal muscles of bilaterians may be homologous to the endodermal muscles of cnidarians, implying that the original bilaterian mesodermal muscles were myoepithelial. Placozoans should have a gastrulation stage during development. Of the three hypotheses that cannot be falsified with the 18S rRNA data, one is most strongly supported. This hypothesis states that Bilateria and Placozoa share a more recent common ancestor than either does to Cnidaria. If true, the simplicity of placozoan body architecture is secondarily derived from a more complex ancestor. This simplification may have occurred in association with a planula-type larva becoming reproductive before metamorphosis. If this simplification took place during the common history that placozoans share with bilaterians, then placozoan genes that contain a homeobox, such as Trox2, should be explored, for they may include the gene or genes most closely related to Hox genes of bilaterians.Despite numerous speculations and analyses concerning the evolutionary relationships of the major animal clades, until recently only three distinct hypotheses have been offered concerning the phylogenetic position of Bilateria within the other basal metazoan groups (Fig. 1 A-C). Two of these hypotheses are commonly found in zoology textbooks. One view, an idea that goes back to Haeckel (1) and was championed by Hyman (2, 3), is that Bilateria is the sister group to Radiata (Cnidaria and Ctenophora). A second hypothesis, preferred by Harbison (4) and Wilmer (5), holds that Bilateria and Ctenophora share a more recent common ancestor than either does to Cnidaria. Recent cladistic studies based on morphological characters (6, 7) have supported this second view. A third alternative, which appears to have fallen out of favor, has Bilateria as a nonmonophyletic group, with both cnidarians and ctenophorans derived from flatworm ancestors (8). The strength of these hypotheses is difficult to weigh on morphological evidence alone. The diploblastic groups have disparate body plans with many derived features, only a few of which are potentially informative as to their relative phylogenetic positions. Furthermore, homoplasies are difficult to infer when dealing with such general features as mouths, mesoderm, and symmetry.Molecular sequence studies provide sets of characters that can be used to both evaluate previ...

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Section: Evolution: Collinsmentioning

confidence: 50%

Section: Evolution: Collinsmentioning

confidence: 99%

Evaluating multiple alternative hypotheses for the origin of Bilateria: An analysis of 18S rRNA molecular evidence

Collins

1998

Proc. Natl. Acad. Sci. U.S.A.

238

137

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“…In this scenario, the birth of Hox genes occurred in the evolutionary lineage leading to cnidarians and bilateria ns, after this lineage had diverged from sponges and ctenophores. The placozoan Trichoplax adhaerens could occupy a pivotal position in this important evolutionary transition, because current data indicates it contains just a single Hox/ParaHox-related gene, Trox-2 (Schierwater and Kuhn, 1998;Monteiro et al, 2006;Schierwater et al, 2008;Srivastava et al, 2008). This gene has a protein sequence similar to the ParaHox gene Gsx, but could conceivably be representative of the elusive progenitor gene, ancestral to Hox and ParaHox, denoted the ProtoHox gene.…”

Section: The Origin Of Hox Genes and Axial Patterningmentioning

confidence: 99%

Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell

et al. 2016

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Our understanding of the early evolution of animals will be greatly improved if a final solution can be found to the evolutionary relationships between Porifera, Placozoa, Ctenophora, Cnidaria, and Bilateria. There have been many recent attempts to solve this key issue at the base of the metazoan tree of life, and these have sparked heated discussions and highlighted fundamental analytical problems. We argue that solving this problem will necessitate analysis of disparate data types, including phylogenomic data, larger scale genomic characters, developmental data, and morphological characters. At the least, morphological and developmental data must be used to cross-validate phylogenomic conclusions, but ideally solutions should be sought to the problems of combining disparate data sources with appropriate character weighting and algorithm choice.

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“…Within the last years, a large number of diploblastic Antp-related genes have been isolated (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30)(31). Among those, cnidarian sequences related to Hox and paraHox genes were found (15, 17-19, 22, 23, 25, 28, 29, 31), but the characterization of diploblastic Hox families, as well as their possible relatedness to triploblastic families, remains unclear in several cases (26,32). Moreover, although the expression analyses suggested that several cnidarian Antp-class genes are involved in patterning (15,19,24,27,29), the developmental role of the cnidarian Hoxrelated genes at the time the oral͞aboral axis is defined remains confused.…”

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confidence: 99%

Evolution of Antp-class genes and differential expression ofHydra Hox/paraHoxgenes in anterior patterning

Gauchat

Mazet

Berney

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

176

125

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The conservation of developmental functions exerted by Antpclass homeoproteins in protostomes and deuterostomes suggested that homologs with related functions are present in diploblastic animals. Our phylogenetic analyses showed that Antp-class homeodomains belong either to non-Hox or to Hox͞paraHox families. Among the 13 non-Hox families, 9 have diploblastic homologs, Msx, Emx, Barx, Evx, Tlx, NK-2, and Prh͞Hex, Not, and Dlx, reported here. Among the Hox͞paraHox, poriferan sequences were not found, and the cnidarian sequences formed at least five distinct cnox families. Two are significantly related to the paraHox Gsx (cnox-2) and the mox (cnox-5) sequences, whereas three display some relatedness to the Hox paralog groups 1 (cnox-1), 9͞10 (cnox-3) and the paraHox cdx (cnox-4). Intermediate Hox͞paraHox genes (PG 3 to 8 and lox) did not have clear cnidarian counterparts. In Hydra, cnox-1, cnox-2, and cnox-3 were not found chromosomally linked within a 150-kb range and displayed specific expression patterns in the adult head. During regeneration, cnox-1 was expressed as an early gene whatever the polarity, whereas cnox-2 was up-regulated later during head but not foot regeneration. Finally, cnox-3 expression was reestablished in the adult head once it was fully formed. These results suggest that the Hydra genes related to anterior Hox͞paraHox genes are involved at different stages of apical differentiation. However, the positional information defining the oral͞aboral axis in Hydra cannot be correlated strictly to that characterizing the anterior-posterior axis in vertebrates or arthropods. T he discovery of structural and functional homologies between regulatory genes used by Drosophila and vertebrates during their development led to the hypothesis that animals would share a common set of genes for defining the head, trunk, and posterior regions at early developmental stages (1-6). The proposed genes were homeobox genes belonging either to the Antp class, like empty-spiracle (emx), even-skipped (evx), Hox genes, or to the Prd class, like orthodenticle (Otx), goosecoid. Phylogenetic analyses performed on a vast amount of Hox homeodomain (HD) sequences, including representatives from all classes of homeobox genes from animals, protozoa, fungi, and plants, confirmed the monophyly of the Antp class as well as its position as a sister group to the Paired class (7). Within the Antp class, the Hox gene organization is distinctive and enigmatic: the genes map in clusters, and the order of individual genes within a cluster correlates with their temporospatial expression pattern along the anterior-posterior body axis during development (8). Recently, it was proposed that the common bilaterian ancestor of protostomes and deuterostomes had at least seven Hox genes (9). However, the question of the composition of the ancestral HOX cluster remains open. Analysis of Hox homeobox sequences (10) suggested that the conserved HOX cluster emerged early in the evolution of metazoans from an original cluster harboring three ancestral g...

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Homology of Hox Genes and the Zootype Concept in Early Metazoan Evolution

Cited by 90 publications

References 32 publications

Evaluating multiple alternative hypotheses for the origin of Bilateria: An analysis of 18S rRNA molecular evidence

Evaluating multiple alternative hypotheses for the origin of Bilateria: An analysis of 18S rRNA molecular evidence

Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell

Evolution of Antp-class genes and differential expression ofHydra Hox/paraHoxgenes in anterior patterning

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