Basal Cambrian soft-bodied segmented bilaterians preserved as microbial pseudomorphs
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eLife Assessment
This manuscript describes valuable new material of small, unusually preserved fossils from deep in the Cambrian of China and argues they represent very early bilaterian animals such as annelids or panarthropods. The authors present convincing evidence of the fossilisation of specimens as microbial pseudomorphs, however, the fossils show few details and it is difficult to assess their affinity. The broader claims made about the timing and nature of the Cambrian explosion are inadequately supported by the material, given that bilaterians were already known to exist during that period.
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Abstract
Before Cambrian Stage 3, unambiguous body fossils of segmented bilaterians were rare, severely hampering our understanding of the early history of such important animals. Here we report a variety of microfossils with quintessential features such as paired appendages, dorsoventral and anteroposterior differentiations from the basal Cambrian Fortunian of South China, representing the earliest known three-dimensional body fossils of segmented bilaterians. These fossils were all microbial pseudomorphs built up by secondarily phosphatized bacteria aggregations, testifying microbial pseudomorph could serve as a novel and important pathway to preserve tiny, fragile bilaterian progenitors. This finding unveils a diversified segmented bilaterian world at the very beginning of Cambrian and would arouse a more comprehensive perspective on the early evolution of bilaterian body plans.
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eLife Assessment
This manuscript describes valuable new material of small, unusually preserved fossils from deep in the Cambrian of China and argues they represent very early bilaterian animals such as annelids or panarthropods. The authors present convincing evidence of the fossilisation of specimens as microbial pseudomorphs, however, the fossils show few details and it is difficult to assess their affinity. The broader claims made about the timing and nature of the Cambrian explosion are inadequately supported by the material, given that bilaterians were already known to exist during that period.
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Reviewer #1 (Public review):
Summary:
A description of small phosphatised fossils from the Kuanchuanpu, formations that are claimed to represent unequivocal early segmented bilaterians with limbs, ie annelids or panarthropods. All material from the Kuanchuanpu is of interest, and the mode of preservation is certainly striking.
However, few details apart from bilateral symmetry and paired protrusions are present. In addition, fragments of potential progenitors such as anabaritiids cannot be entirely ruled out. In addition, the broader claims about the nature of the Cambrian explosion, the gap between the fossil record and molecular clocks, and what various authors have said about them are either inadequate or incorrect. For example, Budd and Jackson did not at all make the claim that the earliest bilaterians were soft-bodied and tiny. …
Reviewer #1 (Public review):
Summary:
A description of small phosphatised fossils from the Kuanchuanpu, formations that are claimed to represent unequivocal early segmented bilaterians with limbs, ie annelids or panarthropods. All material from the Kuanchuanpu is of interest, and the mode of preservation is certainly striking.
However, few details apart from bilateral symmetry and paired protrusions are present. In addition, fragments of potential progenitors such as anabaritiids cannot be entirely ruled out. In addition, the broader claims about the nature of the Cambrian explosion, the gap between the fossil record and molecular clocks, and what various authors have said about them are either inadequate or incorrect. For example, Budd and Jackson did not at all make the claim that the earliest bilaterians were soft-bodied and tiny. Glaessner (1958) is a very out-of-date reference to use. We know that bilaterians certainly existed by the time of Kuanchuanpo.
Even so, it is possible that these fragments do represent internal moulds of taxa such as lobopod-like organisms, even if the evidence is not totally persuasive.
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Reviewer #2 (Public review):
This manuscript by Yang et al. describes a variety of bilateral and segmented microfossils from the basal Cambrian (Fortunian Stage) Kuanchuanpu Formation, South China. During the Fortunian Stage, body fossils are scarce, and key evidence for the presence of different clades relies on exceptionally preserved microfossils of embryos and larvae. The authors interpret the described microfossils as segmented bilaterians, with anteroposterior and dorsoventral differentiation and paired appendages. The implication of this interpretation is that the microfossils represent important evidence for early bilaterian evolution.
The strength of the manuscript is the convincing presentation of the material's bilateral and segmented nature and its taphonomy. The combined use of scanning electron microscopy and X-ray …
Reviewer #2 (Public review):
This manuscript by Yang et al. describes a variety of bilateral and segmented microfossils from the basal Cambrian (Fortunian Stage) Kuanchuanpu Formation, South China. During the Fortunian Stage, body fossils are scarce, and key evidence for the presence of different clades relies on exceptionally preserved microfossils of embryos and larvae. The authors interpret the described microfossils as segmented bilaterians, with anteroposterior and dorsoventral differentiation and paired appendages. The implication of this interpretation is that the microfossils represent important evidence for early bilaterian evolution.
The strength of the manuscript is the convincing presentation of the material's bilateral and segmented nature and its taphonomy. The combined use of scanning electron microscopy and X-ray computed tomography to illustrate the material convincingly supports the argument of a bilaterian affinity. Likewise, the visualization of the cemented vesicles composed of phosphate nanocrystals that make up the fossils' internal molds supports the proposed taphonomic pathway.
The weakness of the manuscript is the further biological interpretations. While the manuscript presents a convincing argument that the molds derive from overall segmented (metameric) body plans, it does not fully explore which cavities/organs are actually molded. Instead, it assumes without discussion that the molds reflect the cuticle with a loss of fine external structures (e.g., setae). While external sclerites and cuticles are convincingly displayed in one case (Figure Supplement 5), more options exist for the rest of the material. Here, molds could perhaps represent other cavities, such as guts (including diverticula) or perivisceral cavities, both consistent with a lack of fine external details as well as an endogenous taphonomic pathway. A proper exploration of what these molds actually represent is, therefore, crucial to interpreting the ecological and evolutionary implications of the fossils.
Despite its weakness, the manuscript demonstrates convincing evidence of bilaterian microfossils in the Fortunian Stage. This evidence, in itself, contributes valuable information on the Cambrian animal radiation.
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