In 1998, Xiao, Zhang & Knoll dazzled the palaeontological world with spectacular fossil embryos from Doushantuo, China. To find soft-bodied embryos is noteworthy in its own right, but these embryos were from the late Precambrian (the early part of the Ediacaran Period) and were identified as belonging to animals. The search for animal signatures before the Cambrian (when there was an explosion of animal life) has been intense - for Darwin predicted that they would one day be discovered and their absence presented him with a dilemma. Multicellular ediacaran fossils have been found, but their affinities with cambrian animals has been controversial. For example, one of the most widely cited examples (Charnia interpreted as a sea pen) did not stand up to critical scrutiny (Antcliffe and Brasier, 2007). Consequently, to find animal embryos in the early Ediacaran was deemed to be worth heralding. Stephen Jay Gould put pen to paper straight away, saying that "Fossils of tiny embryos 570 million years old may well be the greatest paleontological discovery of our time." More recently, Butterfield (2011) put it like this:
"Ever since Darwin there has been a disturbing void, both paleontological and psychological, at the base of the Phanerozoic eon. If his theory of gradualistic evolution be true, then surely the pre-Phanerozoic oceans must have swarmed with living animals - despite their conspicuous absence from the early fossil record. Thus, the 1998 report of fossilized animal embryos in the early Ediacaran Doushantuo Formation of South China was met with almost palpable relief."
The Doushantuo embryos made an enormous impact (source here)
However, several researchers have found the "animal" interpretation unconvincing. The fossilised characters regarded as diagnostic of animals have been found in other types of organism. Other features that have been observed are not "animal" at all. The first major challenge came in 2007, when Bailey et al. documented similarities with a modern giant sulphur-oxidising bacteria going by the name Thiomargarita. However, there were still problems: this interpretation explained some, but not all, of the data. What was needed was more fundamental research in order to evaluate alternative hypotheses. The two most significant avenues of research have been: to probe the inner structure of the embryos using Synchrotron X-ray tomographic microscopy; and reappraising, using experimental taphonomy, what realistically can be preserved of biological tissue and how this can be distinguished from diagenetic mineralisation.
Hagadorn et al. (2006) used X-ray computed tomography and reported internal cellular structures that were suggested to be "fossilized nuclei, spindle bundles, or other organelles". This boosted the "animal" interpretation, but it was also consistent with the giant sulphur bacteria hypothesis.
Then came a bombshell. Huldtgren et al. (2011) showed internal features incompatible with multicellular metazoan embryos, instead, there was a good fit with the embryos belonging to protists, and the observations are of structures producing "propagules for dispersion".
In parallel with this research, an experimental taphonomy study was published by Cunningham et al. (2012). This tested the hypothesis that the embryos should be identified as giant sulphur bacteria. Distinct differences were found between the experimentally preserved and the fossilised forms. The authors concluded that the hypothesis is falsified. Kaplan's News report in Nature had this to say:
"Of the 450 fossils scanned, 14 were found to contain structures that look like nuclei. In one of these specimens, three of the eight structures even have the elongated or dumb-bell shape of modern nuclei about to replicate. This hints that the organism died during cellular division. "We were enthralled to find nuclear division preserved by fossilization. It confirmed that the fossil organisms were not bacteria, but we soon realized that they were not like animals either, as animal nuclei tend to lose their contours during cell division, and these nuclei did not," says Bengtson."
The expertise developed in this experimental approach to fossilisation has developed the knowledge base for distinguishing between preserved biological material and diagenetic mineralisation. This has allowed a more general evaluation of extant fossil material. One casualty has been Vernanimalcula guizhouena, also from the Doushantuo Formation, which has been interpreted as the earliest bilaterian animal. Now, the diagnostic animal features are regarded as the products of diagenesis (Bengtson et al., 2012).
This blog has been stimulated by a lecture on the Doushantuo microfossils by Dr John Cunningham of the University of Bristol and co-author of several of the research papers cited above. The lecture was very useful to me for putting into context the various contributions that have been made since 1998, and it made me think that its content should be more widely known. The lecture abstract gave the conclusion that "there is currently no convincing evidence for advanced animals with bilateral symmetry in the Doushantuo biota". This particular quest for animals preceding the Cambrian Explosion has drawn a blank. Needless to say, Darwin's dilemma remains in full force.
Links to the literature cited are provided above. The two most recent research papers are as follows:
Experimental taphonomy of giant sulphur bacteria: implications for the interpretation of the embryo-like Ediacaran Doushantuo fossils
J. A. Cunningham, C.-W. Thomas, S. Bengtson, F. Marone, M. Stampanoni, F. R. Turner, J. V. Bailey, R. A. Raff, E. C. Raff and P. C. J. Donoghue.
Proc. R. Soc. B, 7 May 2012, 279, 1857-1864 | doi: 10.1098/rspb.2011.2064
Abstract: The Ediacaran Doushantuo biota has yielded fossils interpreted as eukaryotic organisms, either animal embryos or eukaryotes basal or distantly related to Metazoa. However, the fossils have been interpreted alternatively as giant sulphur bacteria similar to the extant Thiomargarita. To test this hypothesis, living and decayed Thiomargarita were compared with Doushantuo fossils and experimental taphonomic pathways were compared with modern embryos. In the fossils, as in eukaryotic cells, subcellular structures are distributed throughout cell volume; in Thiomargarita, a central vacuole encompasses approximately 98 per cent cell volume. Key features of the fossils, including putative lipid vesicles and nuclei, complex envelope ornament, and ornate outer vesicles are incompatible with living and decay morphologies observed in Thiomargarita. Microbial taphonomy of Thiomargarita also differed from that of embryos. Embryo tissues can be consumed and replaced by bacteria, forming a replica composed of a three-dimensional biofilm, a stable fabric for potential fossilization. Vacuolated Thiomargarita cells collapse easily and do not provide an internal substrate for bacteria. The findings do not support the hypothesis that giant sulphur bacteria are an appropriate interpretative model for the embryo-like Doushantuo fossils. However, sulphur bacteria may have mediated fossil mineralization and may provide a potential bacterial analogue for other macroscopic Precambrian remains.
A merciful death for the "earliest bilaterian," Vernanimalcula
Stefan Bengtson, John A. Cunningham, Chongyu Yin, and Philip C.J. Donoghue.
Evolution & Development, 14(5), 421-427 (Sept/Oct 2012) | DOI: 10.1111/j.1525-142X.2012.00562.x [pdf here]
Summary: Fossils described as Vernanimalcula guizhouena, from the nearly 600 million-year-old Doushantuo Formation in South China, have been interpreted as the remains of bilaterian animals. As such they would represent the oldest putative record of bilaterian animals in Earth history, and they have been invoked in debate over this formative episode of early animal evolution. However, this interpretation is fallacious. We review the evidential basis of the biological interpretation of Vernanimalcula, concluding that the structures key to animal identity are effects of mineralization that do not represent biological tissues, and, furthermore, that it is not possible to derive its anatomical reconstruction on the basis of the available evidence. There is no evidential basis for interpreting Vernanimalcula as an animal, let alone a bilaterian. The conclusions of evolutionary studies that have relied upon the bilaterian interpretation of Vernanimalcula must be called into question.
The discovery of soft-bodied fossils located at the top of Precambrian sedimentary sequences was a landmark for palaeontology. Prior to finding these forms, there was nothing between single-celled fossils and the sophisticated animals in Lower Cambrian rocks. There was a 'gap' in the fossil record that was a dilemma for Charles Darwin when he discussed the matter in On the Origin of Species. (6th ed., p.286): "To the question why we do not find rich fossiliferous deposits belonging to these assumed earliest periods prior to the Cambrian system, I can give no satisfactory answer." Unfortunately, whilst these soft-bodied organisms are now widely known, they do not provide a transition to the animals of the Lower Cambrian. There are few (if any) connections that can be made across the Precambrian/Cambrian boundary. There is still uncertainty as to what these life forms actually are and where they fit into the larger picture. Three scenarios have been proposed in recent years: early ancestors of marine invertebrate phyla, giant marine protists, and lichenized fungi. It is the third of these options that has been boosted in newly reported work by Gregory Retallack.
Life on land in the Ediacaran? Dickinsonia: fossil marine worms or land-living lichen? (Source here).
The Ediacaran fossils have been widely regarded as a marine fauna. The rocks are associated with a variety of depositional environments, but all are marine. A relevant example is the type section for these fossils: the Ediacaran Member of the Rawnsley Quartzite, north of Adelaide, Australia. The following description of Selden and Nudds (2004) summarises the literature, and it illustrates the radical nature of reinterpreting the enclosed fossils as terrestrial.
"The Ediacaran Member consists of a series of siltstones and sandstones which represent pelagic to inter-tidal conditions. The implication is that there was a continental edge delivering sediment into deep water, at times by means of turbidite flows and occasionally as a delta which shallowed the water to sub- and inter-tidal levels. Some storm horizons can be seen. It is at these shallow levels, around the storm wave base, that the fossils occur." (Evolution of Fossil Ecosystems, page 12)
In 1994, Retallack formally proposed that some Ediacaran fossils should be identified as lichens. He has recently worked on the type section of Ediacaran strata and has published a reinterpretation: they are concluded to be non-marine (lagoonal-aeolian) with palaeosols (Retallack, 2012). On these surfaces, he maintains, lichens grew. It is not my purpose here to discuss these evidences, but it is worth drawing attention to Paul Knauth's News & Views contribution to Nature, where he encourages an openness to these controversial views:
"As is usual in sedimentology, observations can be construed in alternative ways, and interpretations for these strata have historically covered the gamut of geological possibilities - from lacustrine to lagoonal, coastal and open marine. It is appropriate that interpretations change or are superseded with the arrival of new observations, and that is why this publication is fascinating and timely and should be considered seriously. Although Retallack's ideas are at odds with the accepted dogma, these do not need to be mutually exclusive."
At very least, Retallack deserves to be taken seriously. He has made a strong case, addressing both sedimentological and palaeontological aspects. His ideas have developed over a 20 year period and, arguably, the hypotheses he has developed have been tested and upheld. Knauth is willing to approach these radical ideas with an open mind. His concluding words are to be applauded:
"So I say, until the forensic evidence for Ediacaran habitats becomes strongly compelling one way or the other, let multiple hypotheses thrive!"
The major interest to us in this blog is the question: what are the implications if Retallack is correct? First, the relationship of the Ediacaran life forms to the animals of the Cambrian Explosion will need to be reappraised. There is no way that land-based lichens could be ancestors of animals. This point is, naturally enough, brought out in media reports and other commentaries. We need only add that Darwin's dilemma is reinforced.
"This would mean that at least some Ediacarans lived on land, under the sky, perhaps in the manner of lichens, or microbial colonies that form soil crusts. The Ediacarans, then, would be the now-not-so-rare (and not at all mythical) creatures that first colonized the land - not just in puddles, but in soils indicative of a dry, cold desert. This is as far away as imaginable from the oceanic idyll that many have assumed for Ediacaran organisms, and have reconstructed as such in a million coffee-table books." (Editorial in Nature)
"This discovery has implications for the tree of life, because it removes Ediacaran fossils from the ancestry of animals," said Retallack, professor of geological sciences and co-director of paleontological collections at the UO's Museum of Natural and Cultural History. (ScienceDaily report)
Second, we should note the difficulties encountered by geologists in interpreting the depositional environment of the Ediacaran Member. Although there are many useful principles to guide interpretations, geologists also bring presuppositions and conceptual models that influence what they see and what they consider significant. The problem with the Precambrian is that it is not familiar territory. The rocks represent a history of the Earth that is not representative of the present day. Yet, uniformitarianism is a favoured dogma in the Earth sciences, and this is a problem because it restricts the range of options for interpretation. Retallack's review and evaluation of alternative interpretations is valuable, as is also his analysis of evidences supporting palaeosols in the Ediacaran Member.
Third, the colonisation of Earth by living things needs further consideration. The presently favoured scheme for interpreting Earth history is characterised by evolutionary transformation. All stories of Life on Earth appear to have evolution as the integrating theme. This always brings questions about ancestor/descendant relationships (as we have noted for the Ediacaran life forms). But does it have to be like this? An alternative perspective, discussed on numerous occasions in this blog, is a scheme based on colonisation. As a rough guide, the principle is that wherever conditions enable viable ecosystems, life forms appear to occupy those environments. The Ediacaran may be a good example: with the development of palaeosols in otherwise barren land, colonisation by lichen-like organisms took place. For other examples, follow this link.
Ediacaran life on land
Gregory J. Retallack
Nature, 493, 89-92, (03 January 2013) | doi:10.1038/nature11777
Ediacaran (635-542â€‰ million years ago) fossils have been regarded as early animal ancestors of the Cambrian evolutionary explosion of marine invertebrate phyla, as giant marine protists and as lichenized fungi. Recent documentation of palaeosols in the Ediacara Member of the Rawnsley Quartzite of South Australia confirms past interpretations of lagoonal-aeolian deposition based on synsedimentary ferruginization and loessic texture. Further evidence for palaeosols comes from non-marine facies, dilation cracks, soil nodules, sand crystals, stable isotopic data and mass balance geochemistry. Here I show that the uppermost surfaces of the palaeosols have a variety of fossils in growth position, including Charniodiscus, Dickinsonia, Hallidaya, Parvancorina, Phyllozoon, Praecambridium, Rugoconites, Tribrachidium and 'old-elephant skin' (ichnogenus Rivularites). These fossils were preserved as ferruginous impressions, like plant fossils, and biological soil crusts of Phanerozoic eon sandy palaeosols. Sand crystals after gypsum and nodules of carbonate are shallow within the palaeosols, even after correcting for burial compaction. Periglacial involutions and modest geochemical differentiation of the palaeosols are evidence of a dry, cold temperate Ediacaran palaeoclimate in South Australia. This new interpretation of some Ediacaran fossils as large sessile organisms of cool, dry soils, is compatible with observations that Ediacaran fossils were similar in appearance and preservation to lichens and other microbial colonies of biological soil crusts, rather than marine animals1, or protists.
Palaeontology: Fossils come in to land
Shuhai Xiao & L. Paul Knauth
Nature, 493, (3 January 2013) 28-29 | doi:10.1038/nature11765
Fossils found in rocks of the Ediacaran period in Australia have been previously characterized as early marine organisms. But a report suggests that these rocks are fossilized soils. So did some of these Ediacaran organisms in fact live on land, like lichens? A palaeontologist and a geologist weigh up the evidence.
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