Evolutionary Scenario of the Early History of the Animal Kingdom: Evidence from Precambrian (Ediacaran) Weng’an and Early Cambrian Maotianshan Biotas, China Jun-Yuan Chen
Abstract
Late Proterozoic (Ediacaran) Weng’an (580 mya) and Early Cambrian Maotianshan (c. 530 mya) faunas of South China, illustrated here, document diverse body plans at phylum and subphylum level and confirm that bilaterians evolved well before the “Cambrian explosion”. The Weng’an faunas (from Guizhou), the oldest record of metazoans, consist mainly of embryos with possible affinities to living sponges, cnidarians, and bilaterians, but with adult specimens (though microscopic) of the same groups. The Maotianshan Shale faunas (from Yunnan), remarkably diverse at species level (over 100 species), have great diversity of metazoan body plans, many comparable with those of living groups. Because they occur at or near the evolutionary roots of many animal groups, intermediate forms are present. Evolution of Early Cambrian metazoans was surprisingly rapid. Worm-like ancestral euarthropods elucidate the evolutionary origins of the arthropods. The diverse Maotianshan vertebrates, representing “missing” history between an amphioxus-like ancestor and craniate vertebrates, provide an improved understanding of the early evolution of the vertebrates. Keywords
China • Guizhou • Yunnan • Chengjiang • Latest Precambrian (Ediacaran)– Early Cambrian • Doushantuo Formation • Weng’an phosphate member • Fossil embryos • Maotianshan Shale (Early Cambrian) • Panarthropod phylogeny • Origin of Chordata and vertebrates (Cristozoa) • Inception of vertebrate brain • Phylogeny of Deuterostomia
Introduction J.-Y. Chen () LPS Institute of Geology and Palaeontology of Academia Sinica, Nanjing 210008, People’s Republic of China Institute of Evolution and Developmental Biology, Nanjing University, Nanjing 210093, People’s Republic of China e-mail:
[email protected];
[email protected] The sudden appearance of animal fossils at the beginning of the Cambrian was of particular concern to Darwin (The Origin of Species, 1859, pp. 313–314); it seemed to be at odds with his theory of evolution through natural selection. He believed that the Cambrian trilobites may have descended from
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Precambrian ancestors long before the Cambrian. However, no Precambrian ancestor had yet been found at that time. The great evolutionary event called the Cambrian Explosion has been a great mystery and a highly controversial issue among researchers. Like a coin, the Cambrian explosion has two sides: the Cambrian above and the Precambrian below. The magnitude of the event can be understood based on the contrast between the biota and the degree of diversity of the fossils from both sides. Great advances have been made in Cambrian palaeontology over the past century (e.g., Whittington 1985), especially the discovery of the extraordinarily well-preserved soft-bodied fauna from the Middle Cambrian Burgess Shale (Briggs et al. 1994) and the Lower Cambrian Maotianshan Shale deposits (Chen 2004). The Cambrian side of the “Cambrian explosion” is richly illustrated and contrasts greatly with the Precambrian side, but it should be noted that with new finds, the diversity of both is increasing continuously. Compared with the Cambrian, our knowledge of Precambrian fossils is very limited. The discovery of the macroscopic Ediacaran biota in Australia in 1946 provided the first evidence of multicellular life before the Cambrian (Glaessner 1984). Members of the macroscopic Ediacaran biota are now found worldwide, and include enigmatic tubular and frondshaped sessile organisms. They emerged about 570 million years ago, flourished for a period of ca. 30 million years, and suddenly disappeared by the Precambrian/Cambrian transition 542 million years ago. The reasons for the extinction of the Ediacaran biota are not clear and are probably related to the advent of predators. The Ediacaran organisms have been described as metazoans with affinities to the Cnidaria (Glaessner 1959), molluscs (e.g. Kimberella Fedonkin and Waggoner 1997) and other bilaterians (Peterson et al. 2008), but most of the fossils are morphologically distinct from modern and even Cambrian life forms. Some palaeontologists do not agree that these creatures can be categorized using the currently accepted biological classification scheme (Seilacher 1989; Seilacher et al. 2003). Because it is difficult to deduce the evolutionary relationships among these Ediacaran organisms, some palaeontologists have suggested that they represent completely extinct lineages and established the kingdom Vendozoa (Seilacher 1984), now renamed the Vendobionta phyllum (Seilacher 1989). Because these
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enigmatic organisms predominantly left no descendants, the strange forms have been interpreted by some authors as “failed experiments” in multicellular life. The sudden appearance of metazoan diversity in the Cambrian with a great multiplicity of body plans in the animal groups at the phylum and subphylum levels remains a great mystery. Searching for metazoan fossils from Precambrian times is a challenging task. Once the efficient preservation of soft tissues, as well as bacteria (e.g. Bailey et al. 2007), in phosphate deposits was understood, palaeontologists began to look for metazoan fossils in Precambrian phosphate deposits. In 1998, two parallel teams found fossil embryos and sponges in the Precambrian Duoshantou phosphate deposit in Weng’an, Guizhou, southern China (Li et al. 1998; Xiao et al. 1998; Xiao and Knoll 1999, 2000). The Weng’an fauna, named after the fossil locality, is the oldest fossil record of metazoans and predominantly includes diverse embryos with affinities to living sponges, cnidarians, and bilaterians. In addition to the fossil embryos, the Weng’an fauna has yielded adult specimens of microscopic metazoans representing sponges, cnidarians, and bilaterians. The fauna lived in the early Ediacaran, immediately after the Snow Ball event, at least 580 million years ago, suggesting that metazoan life, including sponges, cnidarians, and bilaterians, flourished long before the Cambrian explosion and is indeed very deeply rooted. The great advances in Precambrian palaeontology, especially the intensive study of the Weng’an biota during the past 10 years, have significantly changed our view of the Cambrian explosion. However, the contrast between the Precambrian and Cambrian faunas remains great and the explosive Cambrian evolutionary event remains an enigma. The recently discovered fossil fauna from the Lower Cambrian Maotianshan Shale deposits in the Chengjiang, Haikou, and Anning areas near Kunming, China, documents the sudden appearance of a diversity of metazoans. These are not only remarkably diverse at the species level, including over 100 species, but illustrate a great morphological diversity of metazoan body plans. Many of these are comparable to those of living groups at the phylum and subphylum levels or were short lived and soon extinct (Gould 1989; Hou et al. 2004; Chen 2004). The close affinities between the 530-million-year-old Maotianshan Shale biota and the 505-million-year-old Burgess Shale biota suggest that
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these forms were geologically widespread and evolutionarily conserved following the Cambrian explosion. Because the intermediate forms were not well established and few survived, they appear only near the evolutionary roots of the related animal groups, becoming extinct soon after the new, advanced forms emerged. The fauna of the Maotianshan Shale lies close to the roots of many animal groups and intermediate forms living at that time. The discovery of many intermediate forms not only satisfies Darwin’s prediction but also casts new light on the evolutionary origins of the animal groups, especially the vertebrates and arthropods. The body plans (or body forms) of animals are essentially blueprints for the way the body of the organism is laid out (Raff 1996; Hall 1998; Chen 2009). The blueprint is shared by a group of animals ranked together at higher taxonomic levels, including superphyla, phyla, subphyla, classes, and orders. It is characteristic of a unique anatomical body organization that it is evolutionarily conserved and deeply rooted. The sudden appearance of the high animal diversity in the Cambrian corresponds to the sudden appearance of the diverse body plans of the animal groups at the phylum and subphylum levels. There are many living representatives of animals with these body plans, including vertebrates, ascidians, priapulids, sipunculans, arrow worms, possible molluscs, possible annelids, phoronida, and brachiopods (Chen 2004; Hou et al. 2004), many having changed little since the Cambrian (e.g. the ctenophores, priapulids, sipunculans, chaetognaths, tunicates, and inarticulate brachiopods). On the contrary, crest animals (the Cristzoa), including the extinct precraniates and living vertebrates (craniates), evolved rapidly and now include diverse and very distinct nested body plans that emerged later in evolution. The origin of the vertebrates has long been obscure and controversial, with a lack of fossil evidence for the first vertebrates and the very beginnings of vertebrate evolution. The fossils from the Maotianshan Shale, including Yunnanozoon, Haikouella, and Haikouichthys, are representatives of the missing history of early vertebrate evolution. The study of these fossils contributes to a new understanding of the evolutionary origin of the vertebrates, their heads, brains, head sensorial organs, branchial arches, backbones, and feeding behaviour.
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The limb-bearing segmented animals known as panarthropods have been diverse and abundant since the Early Cambrian and include diverse nested body plans representing different stages of evolution. Most of these different body plans appeared in the Early Cambrian, emerging one after another near the root of the evolutionary history of the panarthropods. Their appearance is a remarkable and rare phenomenon, shedding light on the evolutionary origins of various aspects of the arthropods, including the evolution of the head, limbs, and brain. The affinities of numerous Cambrian animals remain controversial. However, the body plans of these animal groups, especially the stalked sessile and pelagic medusiform lophophore-bearing animals and the vetulicolian organisms, offer clues to their possible affinities with extant animals. The regulatory network architecture is critical for establishing the body parts and body plan of the animals (Davidson 2006). The evolution of animal body plans provides us with interesting suggestions of how the genomic internal architectures and developmental processes that directed the course of evolution. The sudden birth of the diverse animal body plans suggests that the Cambrian explosion was marked with the diversification event of regulatory network architectures that regulate developmental processes of the animals.
The Oldest Fossil Evidence for the First Occurrence of Animal Life on Earth Molecular data predict that the divergence of the metazoans (including the calcisponges, cnidarians, and bilaterians) and the separation of the major bilaterian clades (the deuterostomes, ecdysozoans, and lophotrochozoans) occurred deep in time, either within the Ediacaran, following the Cryogenian Marinoan glaciation ending about 635 mya (Hoffman et al. 2004; Condon et al. 2005; Peterson and Butterfield 2005), or 100–200 million years before the Marinoan (Douzery et al. 2004). Recent discovery of possible sponge graded metazoan fossils in pre-Marinoan limestones from South Australia (Maloof et al. 2010) together with evidence from sponge biomarkers indicates that metazoans originated pre-Marinoan time, with a robust presence throughout the Ediacaran (Love et al. 2009).
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Fig. 1 Main localities producing the oldest known metazoans: the Wusi, Baishakan, and Nantuo quarries (adapted from Chen et al. 2009a)
Chen (2009) in discussing the appearance of diverse animal body plans during the Cambrian explosion states that “The Ediacaran Doushantuo phosphate deposits in Weng’an, Guizhou (Fig. 1) yield diverse metazoans, including sponges (Li et al. 1998), cnidarians (Chen et al. 2000, 2002a; Xiao et al. 2000), and bilateral animals and their related embryos (Chen et al. 2004b; Chen et al. 2006)”. This incredible 580-million-year-old Weng’an biota has received great attention because it is the oldest fossil evidence yet found for animal life on Earth.
Geological Setting of the Weng’an Biota The Doushantuo Formation is widely distributed in southern China and in areas of N. W. China. It is underlain by a glacial deposit known as the Nantuo Formation, laid down during the Marinoan glaciation and thus represents the first deposit after the last extensive glaciation of Snowball Earth. The Doushantuo Formation in Weng’an, Guizhou, crops out along the
axis of the Mt Beidou anticline (Fig. 1). It is well exposed in the Wusi quarry (Fig. 1), where the thickness is 49 m, consisting of five different lithological units (Fig. 2). The Weng’an phosphate member of the Doushantuo Formation varies laterally in thickness and lithology on a scale of metres to tens of metres (see Fig. 2). The Doushantuo Formation has been intensively quarried for phosphates at the Wusi, Baishaikang, and Nanbao quarries. All the specimens examined in the study come from the black and grey facies of the Weng’an phosphate member in these quarries. The quality of preservation varies among the three sites. Wusi (Fig. 3a) and Baishakan (Fig. 3b, c) are the best sites for metazoic embryos (Wusi and Baishakan) and microscopic adults (Baishakan). However, with extensive mining activity, these three quarries have suffered disastrous destruction by extreme sliding activity and have been deeply buried by massive rocks from the overlying strata (Fig. 3d, e). The Weng’an county government had recognized the fossil treasures at this site and erected a monument at the Baishakan quarry (Fig. 3c).
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Fig. 2 Natural and diagrammatic profiles of the lithologic sequence of the Ediacaran Doushatuo Formation in the Mt. Beiduoshan area, Wengan, Guizhou. The lithologic profile was photographed from the western part of the Baishakan quarry;
the thickness of lithologic units was measured in the Wusi quarry. WPM1 is the black facies, WPM2 the gray facies of the Weng’an Phosphate Member. MDM = Middle Dolomite Member; LPM = Early Phosphate Member
In the Yangtze Gorges area, about 600 km northeast of Weng’an (Fig. 2), the Lower Dolomite Member of the Doushantuo Formation, interpreted as a cap carbonate, contains an ash bed that has been dated as 635.23 ± 0.57 Ma using U–Pb dating techniques (Condon et al. 2005; Zhu et al. 2007). The top of the Doushantuo Formation in the Yangtze Gorges area contains another ash bed with a U–Pb age of 551.07 ± 0.61 Ma (Condon et al. 2005). Within the Doushantuo Formation at Weng’an, above the basal dolomite, are a lower and an upper phosphorite interval, separated by the Middle Dolomite Member with a minor hiatus above. The upper phosphorite interval, containing the rich Weng’an microfossil fauna, has been interpreted as younger than 580 million years by carbon isotopic and sequence stratigraphic analyses (Condon et al. 2005). However, the upper Doushantuo Formation corresponding to the Weng’an phosphate member has yielded a Pb–Pb age of 599 ± 4 (Barfod et al. 2002). A Pb–Pb age of 576 ± 14 million years has been calculated for the upper phosphate member (Chen et al. 2004a), providing additional evidence that the Doushantuo fauna predates the Ediacaran biota and is thus the oldest record of animal fossils currently
known. In summary, the balance of evidence indicates that the Doushantuo microfossils are older than 580 million years and hence are the earliest fossil assemblage displaying affinities to diverse metazoan groups.
Affinities of the Metazoan Embryos and Related Adults It is not easy to interpret the Doushantuo microfossils using traditional methods, either in petrographic thin sections (one per specimen) or with external scanning electron microscopy (SEM). Many of the microfossils, especially the embryos, are too simple in form to convey significant morphological information insofar as they resemble eggs or very early cleavage stages, although intriguing insights have been made into their early development (e.g. Chen et al. 2006). The diversity represented by these fossils has not yet been fully documented. A recent technological approach known as propagation phase contrast synchrotron X-ray microtomography (PPC-SR-μCT) provides a unique
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Fig. 3 Sites at the Wusi and Baishakan quarries producing the oldest known metazoans were well exposed several years ago but are now deeply buried by massive rock fall from the upper slope. A and B, photographed in 1997 and 2003, respectively, show well-exposed outcrops of the fossil-bearing beds in the Wusi (a) and Baishakan quarries (b) several years ago; (c), shows a
stone monument at the Baishakan quarry with illustrations of the Weng’an fauna about the evolutionary dawn of the animal life (photograph taken 2007); d and e show outcrops at the Wusi (d) and Baishakan quarries (e), now deeply buried by massive rocks shed from the upper slope (photographs taken by ZJ Yin in 2010)
analytical tool that is increasingly used in studying the Weng’an fossils (Chen et al. 2006, 2009a, b; Donoghue et al. 2006). Microtomography permits the non-destructive computational examination of specimens from any vantage point, the visualization of their internal characters in virtual sections in any plane, and virtual three-dimensional depictions of their internal structures. This technique reveals many structures that are invisible or barely visible with classical absorption contrast-based microtomography (Tafforeau et al. 2006; Chen et al. 2006, 2009a). In the case of the Weng’an fossils, it can show the complex internal features of structures that might previously have been ignored or misinterpreted because of their deceptive exterior forms (Fig. 4). Perhaps most importantly, it facilitates the analysis of the small minority of Doushantuo embryos that retain intrinsically complex structures and large numbers of cells.
The study of the Doushantuo microfossils was initially directed towards algae and acritarchs (Zhang 1989; Zhang and Yuan 1992) and intense interest has been generated in the metazoan embryos and adult forms since 1998 (Xiao et al. 1998; Li et al. 1998). The diversity of the animal forms represented in the microfossil assemblage and their possible phylogenetic affinities are increasing as our knowledge of the faunas continues to expand (Chen et al. 2000). More recently, great interest has been taken in the discovery of a microscopic putative adult bilaterian, Vernanimalcula (Chen et al. 2004a), with a general bilateral antero-posterior organization, a triploblastic structure, and bilateral symmetry. A pair of prominent coelomic structures lies symmetrically on each side of the prominent gut (Fig. 5). An anterior mouth is ventrally directed, followed by a thick pharynx with a multilayered wall and probable muscularity. The pharynx
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Fig. 4 PPC-SR-μT external view of a “soccer ball”-like 4-cell embryo (a) with chorionate cover consisting of large chorion cells (b); PPC-SR-μT is an external view of the chorionate cover
(c) and internal digital section (d) of an 8-cell embryo (adapted from Chen et al. 2009a)
opens posteriorly into a large stomach or intestine. The wall of the stomach or intestine is always composed of two tightly apposed, thin, phosphatized layers of tissue. These two layers are separated by a continuous thin partition, interpreted as the remains of a basement membrane. The endodermal layers bounding the stomach (or intestine) are continuous, with a thickened region of the external body wall at the posterior end, i.e. the anus (Fig. 5). Vernanimalcula is small but structurally complex, representing the earliest adult organism with a bilaterian form so far found in the fossil record. Its simple external morphology and lack of obvious appendages conform to the morphological and developmental predictions of the blueprint of an adult, triploblastic, coelomate animal.
The exquisite preservation of Vernanimalcula, however, has led some authors (e.g. Bengtson and Budd 2004) to suspect that these fossils are not real arguing that the authors “fail to take into full account taphonomy and diagenesis”. Chen et al. (2004c) believe that Bengston and Budd’s argument is not supported by sufficient evidence by counter-arguing that the open spaces in the animal, including its coeloms and the lumina of the mouth and oesophagus, are filled with black amorphous material derived from an organic sedimentary matrix that permeated through the pores of the fossilized wall of the animal while the sediment was still soft and hydrated (Fig. 5a). This indicates that the animal fossilization process began prior to the sediments becoming fully dehydrated. The firstgeneration cavity fillings in Vernanimalcula resulted
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Fig. 5 A–C, image in transmitted light (a), illustration (b), and restoration (c) of a microscopic bilaterian adult Vernanimalcula guizhouena from the Precambrian Doushantuo Formation, Weng’an, Guizhou, showing paired coeloms extending the length of the gut, syn-sedimentary organic micritic fillings in
the coeloms and late diagenetic vuggy fillings in the rear of the body. (d) a coelogastular embryo with possible cnidarian affinities showing organic micrite filling and whitish sparry diagenetic filling in shrinkage fractures (created by dewatering of internal sediments within the spacious blastocoel). Scale bar = 100 μm
from “internal sedimentation” while the matrix was still hydrated. The structures of Vernanimalcula were fossilized before internal cementation occurred, arguing against secondary diagenetic noise, and are primarily biological. However, early diagenesis did occur when the filling structure within the interspaces formed as the internal sediments dehydrated, and these usually appear between the fossilized biological wall and the internal sediments (Fig. 5a). A similar diagenetic history can be widely observed in the preservation of the Weng’an-type fossils. The early diagenetic products usually occur as a coating on either the outer or inner surface of the biological wall structure, as
diagenetic filling in the narrow interspaces formed by the dehydration of the sediments, or as internal sediments within the biological cavities. A later diagenetic product can also be seen in the specimens examined, as a clean, whitish dolomite filling the voids (Fig. 5a). The voids in the matrix and fossils were probably produced by freshwater dissolution in a late diagenetic stage, destructive in terms of fossil preservation. In addition to Vernanimalcula, the microscopic adult forms in the Weng’an fauna also include sponges, with a tabulate anthozoan form recorded in both thin section (Chen et al. 2002a; Xiao et al. 2000a, b) and with SEM (Xiao et al. 2000a, b) (Fig. 6b–f), and a
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Fig. 6 Microscopic cnidarian adults from the Precambrian Doushantuo Formation, Weng’an, Guizhou. (a, b) restoration (a) and transmitted-light photograph (b) of Eohydiania wenganense
(holotype); (c–f), restoration (c) and transmitted-light photograph (d–f) of coral-like cnidarian adult Sinocyclocylicus guizhouensis (Xue et al. 1992). Scale bar = 100 μm
hydroid-like form (Fig. 6a, b). Cross-sections of possible anthozoan polyps and stalks of similar sie and morphology have also been reported by Chen et al. (2002a) and Chen (2004), and exactly the same forms were discovered earlier by Xiao et al. (2000a, b). Microscopic (
