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Review
, 363 (1496), 1557-68

Deciphering Deuterostome Phylogeny: Molecular, Morphological and Palaeontological Perspectives

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Review

Deciphering Deuterostome Phylogeny: Molecular, Morphological and Palaeontological Perspectives

Billie J Swalla et al. Philos Trans R Soc Lond B Biol Sci.

Abstract

Deuterostomes are a monophyletic group of animals that include the vertebrates, invertebrate chordates, ambulacrarians and xenoturbellids. Fossil representatives from most major deuterostome groups, including some phylum-level crown groups, are found in the Lower Cambrian, suggesting that evolutionary divergence occurred in the Late Precambrian, in agreement with some molecular clock estimates. Molecular phylogenies, larval morphology and the adult heart/kidney complex all support echinoderms and hemichordates as a sister grouping (Ambulacraria). Xenoturbellids are a relatively newly discovered phylum of worm-like deuterostomes that lacks a fossil record, but molecular evidence suggests that these animals are a sister group to the Ambulacraria. Within the chordates, cephalochordates share large stretches of chromosomal synteny with the vertebrates, have a complete Hox complex and are sister group to the vertebrates based on ribosomal and mitochondrial gene evidence. In contrast, tunicates have a highly derived adult body plan and are sister group to the vertebrates based on the analyses of concatenated genomic sequences. Cephalochordates and hemichordates share gill slits and an acellular cartilage, suggesting that the ancestral deuterostome also shared these features. Gene network data suggest that the deuterostome ancestor had an anterior-posterior body axis specified by Hox and Wnt genes, a dorsoventral axis specified by a BMP/chordin gradient, and was bilaterally symmetrical with left-right asymmetry determined by expression of nodal.

Figures

Figure 1
Figure 1
Current deuterostome phylogeny, according to available molecular and morphological data. Dotted lines, clades of uncertainty where conflicting data have been obtained. I and II mark clades where the evidence for a monophyletic group is very high. (I) Ambulacraria is made up of hemichordates and echinoderms. Mitochondrial, ribosomal and genomic evidence are in accord for this grouping. The Ambulacraria develop similarly through gastrulation and share larvae that feed by ciliated bands, strengthening their sister group relationship. Genomic evidence suggests that xenoturbellids may be a sister group to the Ambulacraria, but it is also possible that they are an out-group to the rest of the deuterostomes. (II) Chordates are a monophyletic group that share a specific body plan, but mitochondrial and genomic evidence are in conflict about the position of the tunicates. Mitochondrial and ribosomal evidence place cephalochordates as sister group to the vertebrates, whereas genomic evidence places tunicates as the sister group to the vertebrates. Adapted from Zeng & Swalla (2005).
Figure 2
Figure 2
The fossil record of deuterostomes and molecular clock estimates of divergence times. Thick black lines, known occurrence; thin black lines, inferred range. Error bars=95% CIs on molecular estimates. Cambrian deuterostomes and possible deuterostomes as follows (not to scale): 1, Haikouichthys (Lower Cambrian craniate); 2, Cathaymyrus (Lower Cambrian cephalochordate); 3, Haikouella (Lower Cambrian chordate; possible stem-group craniate); 4, Rhabdopleura (Middle Cambrian pterobranch); 5, Stromatocystites (Lower Cambrian crown-group echinoderm); 6, Trochocystites (Middle Cambrian stem-group echinoderm); 7, Shankouclava (Lower Cambrian ?aplousobranch ascidian tunicate); 8, Phlogites (Lower Cambrian; possible stem-group ambulacrarian); 9, Vetulicola (Lower Cambrian problematica). Molecular dating for nodes A–C as follows. A, craniate–echinoderm split based on linearized gene tree (adapted from Ayala et al. 1998); B, craniate–tunicate split based on Bayesian relaxed clock model (adapted from Douzery et al. 2004); C, Echinoderm–hemichordate split based on linearized gene tree (adapted from Peterson et al. 2004). Grey bands are deposits with soft-bodied preservation: C, Chengjiang Formation; G, Guanshan Formation; B, Burgess Shale.
Figure 3
Figure 3
Summary of body axes determination in deuterostomata. A, anterior; P, posterior; a, animal; v, vegetal. Late embryonic expression of nodal is in red for all phyla. Dorsal in hemichordates is shown by BMP expression in yellow. In Echinodermata, the aboral (dorsal) axis is shown by a yellow strip, with later nodal expression marked red on the right side of the larvae, opposite of where the adult rudiment will form. Dorsal in chordates is marked in blue, while expression of chordin is shown during gastrulation in Cephalochordata, Tunicata and Craniata. The BMP–chordin axis is reversed in the chordates from the Ambulacraria. Note that later nodal expression is on the left side in the chordates, and on the right side in echinoderms. Expression patterns are adapted from Duboc et al. 2005 (urchin nodal), Lowe et al. 2006 (hemichordate chordin), Yu et al. 2007 (cephalochordate BMP and chordin), Darras & Nishida 2001 (ascidian chordin) and Sasai & De Robertis 1997 (frog BMP & chordin).

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