Precambrian animal diversity: Putative phosphatized embryos from the Doushantuo Formation of China

Chen, Jun-Yuan; Oliveri, Paola; Li, Chia-Wei; Guiqing, Zhou; Gao, Feng; Hagadorn, James W.; Peterson, Kevin J.; Davidson, Eric H.

doi:10.1073/pnas.97.9.4457

Cited by 172 publications

(91 citation statements)

References 39 publications

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“…This in itself shows that the stage of metazoan evolution represented by these Doushantuo specimens postdates the last common bilaterian ancestor. This conclusion is in accord with other fossil studies (6,(19)(20), as well as conclusions drawn from molecular phylogeny, which places this ancestor in the late Cryogenian at 635 ma or greater and hence before the end of Snowball Earth (21)(22).…”

Section: Discussionsupporting

confidence: 80%

Complex embryos displaying bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng'an, Guizhou, China

Chen

Bottjer

et al. 2009

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

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Three-dimensionally preserved embryos from the Precambrian Ediacaran Doushantuo Formation, Weng'an, Guizhou, southern China, have attracted great attention as the oldest fossil evidence yet found for multicellular animal life on Earth. Many embryos are early cleavage embryos and most of them yield a limited phylogenetic signal. Here we report the discovery of two Doushantuo embryos that are three-dimensionally preserved and complex. Imaging techniques using propagation phase-contrast based synchrotron radiation microtomography (PPC-SR-CT) reveal that the organization of cells demonstrates several bilaterian features, including the formation of anterior-posterior, dorso-ventral, and right-left polarities, and cell differentiation. Unexpectedly, our observations show a noticeable difference in organization patterns between the embryos, suggesting that they represent two distinct taxa. These embryos provide further evidence for the presence of bilaterian animals in the Doushantuo biota. Furthermore, these bilaterians had already diverged into distantly related groups at least 40 million years before the Cambrian radiation, indicating that the last common ancestor of the bilaterians lived much earlier than is usually thought.early animal evolution ͉ early metazoan evolution ͉ nondestructive 3-D reconstruction ͉ precambrian ediacaran embryos ͉ Weng'an biota

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Section: Discussionsupporting

confidence: 80%

Complex embryos displaying bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng'an, Guizhou, China

Chen

Bottjer

et al. 2009

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

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“…However, they are lacking the mesoderm and possess only two germ layers, an outer ectoderm and inner endoderm that are separated by an acellular mesogloea. Cnidaria are a sister-group to the Bilateria (Figure 1), and the fossil record reveals that cnidarians are >500 Myr old (Chen et al, 2000(Chen et al, , 2002Conway Morris, 2000). They are of crucial importance for unravelling the origin and evolution of major signalling pathways in animal evolution.…”

Section: Cnidarians Are Genetically Complexmentioning

confidence: 99%

The Wnt code: cnidarians signal the way

et al. 2006

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Cnidarians are the simplest metazoans with a nervous system. They are well known for their regeneration capacity, which is based on the restoration of a signalling centre (organizer). Recent work has identified the canonical Wnt pathway in the freshwater polyp Hydra, where it acts in organizer formation and regeneration. Wnt signalling is also essential for cnidarian embryogenesis. In the sea anemone Nematostella vectensis 11 of the 12 known wnt gene subfamilies were identified. Different wnt genes exhibit serial and overlapping expression domains along the oral-aboral axis of the embryo (the 'wnt code'). This is reminiscent of the hox code (cluster) in bilaterian embryogenesis that is, however, absent in cnidarians. It is proposed that the common ancestor of cnidarians and bilaterians invented a set of wnt genes that patterned the ancient main body axis. Major antagonists of Wnt ligands (e.g. Dkk 1/2/4) that were previously known only from chordates, are also present in cnidarians and exhibit a similar conserved function. The unexpectedly high level of genetic complexity of wnt genes evolved in early multi-cellular animals about 650 Myr ago and suggests a radical expansion of the genetic repertoire, concurrent with the evolution of multi-cellularity and the diversification of eumetazoan body plans. Oncogene (2006Oncogene ( ) 25, 7450-7460. doi:10.1038 Keywords: Wnt signalling; regeneration; axis formation; Hydra; Nematostella; cnidaria Cnidarians are genetically complexThe Cnidaria is an ancient metazoan phylum of diploblastic animals including freshwater polyps and hydroids, sea anemones and corals, and jellyfish. All cnidarians share the same simple body plan that is reminiscent of an early bilaterian gastrula. However, they are lacking the mesoderm and possess only two germ layers, an outer ectoderm and inner endoderm that are separated by an acellular mesogloea. Cnidaria are a sister-group to the Bilateria (Figure 1), and the fossil record reveals that cnidarians are >500 Myr old (Chen et al., 2000(Chen et al., , 2002Conway Morris, 2000). They are of crucial importance for unravelling the origin and evolution of major signalling pathways in animal evolution.There are two major genetic model systems for cnidarians: the well-known freshwater polyp Hydra (Steele, 2006) and the starlet sea anemone Nematostella vectensis (Holland, 2004;Darling et al., 2005), which was introduced by the pioneering work of Cadet Hand (Hand and Uhlinger, 1992). Recent EST projects in these and some other cnidarian taxa have revealed an astonishing and unexpected genetic complexity of cnidarians. Analyses of ESTs from the anthozoans Acropora millepora and Nematostella vectensis have lead to the identification of 16 571 non-redundant ESTs and 12 547 predicted peptides across the two species (7484 from Nematostella and 5063 from Acropora (Miller et al., 2005;Technau et al., 2005). Both data sets are far from saturation and one can estimate that anthozoan genomes are likely to contain 25 000 genes, which is in the same range as vertebr...

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“…The earliest reported fossils of possible metazoan embryos and adults are in the Ediacaran Doushantuo Formation (∼570 Mya) in southern China (3)(4)(5). Small globular fossils, ∼200 μm in diameter, show remarkable cellular details and have been interpreted as cnidarian gastrulae and planulae as well as bilaterian gastrulae comparable with living molluscans and echinoderms (4).…”

Section: Fossil Recordmentioning

confidence: 99%

Evolution of centralized nervous systems: Two schools of evolutionary thought

2012

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

112

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Understanding the evolution of centralized nervous systems requires an understanding of metazoan phylogenetic interrelationships, their fossil record, the variation in their cephalic neural characters, and the development of these characters. Each of these topics involves comparative approaches, and both cladistic and phenetic methodologies have been applied. Our understanding of metazoan phylogeny has increased greatly with the cladistic analysis of molecular data, and relaxed molecular clocks generally date the origin of bilaterians at 600-700 Mya (during the Ediacaran). Although the taxonomic affinities of the Ediacaran biota remain uncertain, a conservative interpretation suggests that a number of these taxa form clades that are closely related, if not stem clades of bilaterian crown clades. Analysis of brain-body complexity among extant bilaterians indicates that diffuse nerve nets and possibly, ganglionated cephalic neural systems existed in Ediacaran organisms. An outgroup analysis of cephalic neural characters among extant metazoans also indicates that the last common bilaterian ancestor possessed a diffuse nerve plexus and that brains evolved independently at least four times. In contrast, the hypothesis of a tripartite brain, based primarily on phenetic analysis of developmental genetic data, indicates that the brain arose in the last common bilaterian ancestor. Hopefully, this debate will be resolved by cladistic analysis of the genomes of additional taxa and an increased understanding of character identity genetic networks.The fact that some of these building stones are universal does not, of course, mean that the organs to which they contribute are as old as these molecules or their precursors.von Salvini-Plawen and Mayr (1) A ny consideration of the evolution of centralized nervous systems is inextricably linked to an understanding of the phylogeny of living metazoans, their fossil history, the vast range of complexity in their nervous systems, and the development of these nervous systems. For this reason, any attempt to reconstruct the phylogeny of metazoan CNSs must be based on all lines of evidence available. The molecular phylogenetic studies of the last 20 y are particularly important in understanding metazoan interrelationships as well as the time frame in which these animals arose and radiated, and we now have increased insights into the genetics underlying the development of CNSs.First, I will review the fossil history of the earliest putative metazoans, and then, I will discuss different comparative approaches to analyzing both molecular and morphological data: the molecular clock hypothesis, which has yielded a range of possible dates for the origin and divergence of metazoans; developmental genetics and its contribution to our understanding of the patterning of metazoan bodies, particularly patterning of the CNS; and conclusions based on the first outgroup analysis of metazoan central neural characters. Finally, I will review two hypotheses concerning the morphological complexity of the ...

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Precambrian animal diversity: Putative phosphatized embryos from the Doushantuo Formation of China

Cited by 172 publications

References 39 publications

Complex embryos displaying bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng'an, Guizhou, China

Complex embryos displaying bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng'an, Guizhou, China

The Wnt code: cnidarians signal the way

Evolution of centralized nervous systems: Two schools of evolutionary thought

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