This is part four in a series by Keith Miller (earlier parts can be found on the sidebar). It is an updated extension of Miller and Campbell's 2003 essay “The ‘Cambrian explosion’: A challenge to evolutionary theory?” from the book Perspectives on an Evolving Creation: Grand Rapids, and it coincides with our Question, "Does the Cambrian Explosion pose a challenge to evolution?". A pdf version of Miller's full paper can be found here.
Before the “Explosion”: What went bang?
A very important question is what organisms existed before the Cambrian “explosion.” Were there Precambrian precursors, or did the Cambrian explosion really happen in a biological vacuum? Many critics of evolution claim that the Precambrian is devoid of fossils that could represent body plans ancestral to those of the Cambrian invertebrates.
The words of Darwin are often cited as evidence of the seriousness of the problem for evolution.
"There is another and allied difficulty, which is much more serious, I allude to the manner in which species belonging to several of the main divisions of the animal kingdom suddenly appear in the lowest known fossiliferous rocks. Most of the arguments which have convinced me that all the existing species of the same group are descended from a single progenitor, apply with equal force to the earliest known species."1
When Darwin published his model of descent with modification by means of natural selection, knowledge of the fossil record was in its infancy. In particular, the Precambrian and Early Cambrian fossil record was virtually unknown. Even the fossils of the now famous Burgess Shale and similar units were as yet undiscovered. After more than a century of paleontological work, the situation has changed dramatically. In keeping with evolutionary expectations, fossils are now known from the late Precambrian and early Cambrian that record several dramatic transitions in the history of life.
The presence of Late Precambrian animals was recognized in the 1950s and became widely publicized by the early 1970s. These are the famous Ediacaran fossils named for fossil-rich beds in the Ediacaran Hills of South Australia and now recognized at sites throughout the world. These organisms are typically preserved as impressions in sandstones and siltstones. Associated with these fossils are trails (Figure 1) and simple burrows of organisms that show a limited increase in complexity and diversity toward the Cambrian.
The record of life actually extends far beyond the Ediacaran fossils (~565-545 My) into the deep geologic past. Fossils of algae, protists, and bacteria (Figure 2) are present throughout much of the precambrian. The earliest convincing fossils of bacteria are recognized in rocks 3.5 billion years old, and chemical signatures point to the presence of life even earlier. Finely layered mounds (called stromatolites) produced by the activity of mat-building bacteria and algae appear at about this time and become relatively abundant by around 2.7 billion years ago. Evidence of eukaryotic algae, possessing membrane-bounded nuclei and internal organelles, dates to about 1500 million years ago, or earlier if chemical evidence is accepted. Multicellularity had appeared by 1000 million years ago in the form of diverse and relatively advanced seaweeds. The earliest fossils of metazoans (multi-celled animals) may be represented by simple disk-shaped fossils found in rocks 610-600 million years old.2
The earliest unambiguous indication of the rise of metazoan life is preserved in the spectacular phosphorite deposits of the Doushantuo Formation of China dating to at least 580 million years ago. Phosphate can preserve organisms and tissues in such great detail that individual cells can often be recognized. Where environmental conditions are ideal for this type of preservation, extraordinary fossil deposits may result. In the case of the Doushantuo, phosphatization has preserved not only a variety of algal remains, but also the cellular tissues of sponges and millimeter-sized tubes that might represent stem cnidarians.3 However, even more spectacular is the preservation of metazoan eggs and early embryos. These embryos (see Figure 3) are of uncertain affinities but may represent cnidarians or even bilaterians (animals with bilateral symmetry).4
The Ediacaran fossils provide the next window into the rise of metazoans. These fossil-bearing units span from about 575 million years to the base of the Cambrian, and are found in south Australia, Namibia, the White Sea coast of Russia, and Newfoundland. The enigmatic soft-bodied organisms were preserved as impressions, or molds, on the surfaces of sandstone and siltstone layers. These sediment layers accumulated in shallow-marine environments where the seafloor was covered by firm microbial algal mats. The microbial mats covering the seafloor appear to have been important in determining the lifestyles of the Ediacaran organisms, as well as their unique mode of preservation.5
Most soft-bodied impressions of the Ediacaran (or Vendian) can roughly be placed into three general groups -- disks, fronds, and flat-bodied, bilaterally-symmetric forms. The biological affinity of these fossils is very difficult to determine and highly debated.6 Disks are the earliest appearing, and most common, Ediacaran fossils. They have often been identified as medusoids (“jellyfish”) but many appear to have been attached to the bottom, and none bear clear structures that would place them in a living group. Some do clearly possess tentacles around their margins suggesting a stem or sister group relationship to the cnidarians. Some sack-shaped fossils might even be stem anthozoans (the cnidarian group that includes anemones and corals).7
A few disk-shaped fossils may be related to other living phyla. One such form appears to be a sponge that might be assignable to the modern class of hexactinellids.8 Another is a small disk that has a raised center with five radial grooves that has been interpreted as a stem echinoderm (the phylum that includes modern starfish and sea urchins) that lacked the characteristic porous calcareous plates and other diagnostic features of true echinoderms.9
The frond-shaped forms include organisms that were attached to the bottom by a stalk, and others that appear to have been free lying. These fossils have also been assigned by some workers to a group of modern cnidarians (the “sea pens”) or to ctenophores. However, like the disks, the fronds are fairly diverse and some may be unrelated to living phyla.10 Others, although likely not able to be placed into a living cnidarian group, may be stem cnidarians, or even stem anthozoans. The discovery of better preserved fronds in the Cambrian that closely resemble some of the Ediacaran fossils would seem to support this interpretation.11
The bilaterally-symmetric forms of the Ediacaran are the most diverse and most enigmatic fossils of the late Precambrian. Some of these fossils may represent early experiments on the pathway to the living phyla.12 For example, Dickinsonia (Figure 4) and the similar Yorgia are fairly large flat highly-segmented forms that some workers have interpreted as annelids or stem annelids, while others have seen resemblances to other worm phyla or even chordates. These organisms do appear to have been able to move about the bottom as seen by associated crawling and resting traces. Even if not members of a living phylum, these organisms appear to at least be mobile bilateral metazoans (or bilaterians). Another bilateral form that has been the subject of much recent attention is Kimberella (Figure 5). This 555 million year old fossil has been interpreted as a stem mollusk.13 Scratch marks found associated with Kimberella indicate that it had some form of feeding structure (though probably not a true mollusk radula) that enabled it to graze the abundant algal mats. Other bilateral fossils have been interpreted to bear similarities to arthropods, although these interpretations are disputed.
An important, but less attention-getting, component of the Ediacaran fossil record is the presence of trace fossils such as trails, burrows and feeding traces. Except in the few cases mentioned above, there are no body fossils preserved of the organisms that made these traces. These traces tend to be small unbranched sediment-filled burrows that run horizontally along the sediment surface or under the microbial algal mats. Somewhat more complex burrows appear toward the base of the Cambrian including irregularly branching burrows and shallow vertical burrows.14 These traces are important because they point to the existence of small worm-like organisms that were probably feeding on and in the algal mats that covered extensive areas of the seafloor. The biological identity of these organisms is unknown, although they were clearly bilateria.
There is one more set of fossils that are known from the late Ediacaran (550-543 million years) that reveal yet another aspect of the metazoan diversity before the Cambrian. These fossils include tiny calcified or phosphatized tubes, cones and goblet-shaped structures that record the presence of animals capable of producing mineralized skeletons. They are commonly embedded within algal buildups that formed reef-like structures, and may be quite abundant.15 These algal-metazoan reefs foreshadow the later algal reefs of the Cambrian. The very peculiar cm-sized goblet-shaped Namacalathus (found as calcified fossils) lived attached to the algal mounds by stalks (Figure 6). Although the preserved shape of these fossils is consistent with that of cnidarians, their biology is uncertain.
The cone-in-cone structures of Cloudina (Figure 7) , and the more tubular Sinotubulites could have been produced by various types of worms such as serpulids. However, as with the trace fossils, the identity of the actual tube formers remains unknown. A significant observation of the Cloudina fossils is that many of them are perforated by borings. These borings provide the first clear evidence of predation before the Cambrian.
It is clear from the above discussion of the latest Precambrian, that the Cambrian explosion did not occur in a biological vacuum. Although many of the fossil specimens are enigmatic and difficult to classify, they nonetheless show significant biological diversity. Furthermore, at least a few living phyla had already appeared by the beginning of the Cambrian, and other forms likely represented stem groups related to later-evolving phyla.
1. C. Darwin, 1872, On the Origin of Species by Means of Natural Selection, 6th ed., p 234-255.
2. Summaries of the early fossil record of life can be found in Schopf, J.W. (ed,), 1983, Earth’s Early Biosphere: Its Origin and Evolution, Princeton University Press; and Knoll, A.H., 2003, Life on a Young Planet: The First Three Billion Years of Evolution on Earth, Princeton University Press. During the writing of this essay, a new fossil discovery from Australia has indicated the presence of possible sponge-grade metazoans in rocks 640-650 million years ago. See Maloof, A.C., et al., 2010, “Possible animal-body fossils in pre-Marinoan limestones from South Australia,” Nature Geoscience doi:10.1038/ngeo934.
3. Li, C-W., J-Y Chen, and T-E Hua, 1998, “Precambrian sponges with cellular structures,” Science 279: 879-882. Xiao, S, X. Yuan, and A.H. Knoll, 2000, “Eumetazoan fossils in terminal Proterozoic phosphorites?,” Proceedings of the National Academy of Science 97(25): 13684-13689.
4. J-Y Chen, et al., 2000, “Precambrian animal diversity: Putative phosphatized embryos from the Doushanto Formation of China,” Proceedings of the National Academy of Science 97 (9): 4457-4462. Xiao, S., and A.H, Knoll, 2000, “Phosphatized animal embryos from the Neoproterozoic Doushantuo Formation at Weng’an, Guizhou, south China,” Journal of Paleontology 74 (5): 767-788. J-Y Chen et al., 2006, “Phosphatized polar lobe-forming embryos from the Precambrian of southwest China,” Science 312: 163-165. Xiao, S., J.W. Hagadorn, C. Zhou, and X. Yuan, 2007, “Rare helical spheroidal fossils from the Doushantuo lagerstatte: Ediacaran animal embryos come of age?,” Geology 35 (2): 115-118.
5. Seilacher, A., 1999, “Biomat-related lifestyles in the Precambrian,” Palaios 14: 86-93.
6. Fedonkin, M.A., 1992, “Vendian faunas and the early evolution of metazoa,” IN, J.H. Lipps and P.W. Signor (eds.), Origin and Early Evolution of the Metazoa, Plenum Press, New York, p.87-129. Jenkins, R.J.F., 1992, “Functional and ecological aspects of Ediacaran assemblages,” IN, J.H. Lipps and P.W. Signor (eds.), Origin and Early Evolution of the Metazoa, Plenum Press, New York, p.131-176.
7. Gehling, J.G., 1988, “A cnidarian of actinian-grade from the Ediacaran Pound Subgroup, South Australia,” Alcheringa 12:299-314.
8. Gehling, J. G., and Rigby, K., 1996, “Long expected sponges from the Neoproterozoic Ediacara fauna of South Australia,” Journal of Paleontology 70(2): 185-195.
9. Gehling, J.G., 1987, “Earliest known echinoderm -- a new Ediacaran fossil from the Pound Subgroup of South Australia,” Alcheringa 11:337-345.
10. Narbbonne, G.M., M. Laflamme, C. Greentree, and P. Trusler, 2009, “Reconstructing a lost world: Ediacaran rangeomorphs from Spaniard’s Bay, Newfoundland,” Journal of Paleontology 83(4): 503-523.
11. Conway Morris, S., 1993, “Ediacaran-like fossils in Cambrian Burgess Shale-type faunas of North America,” Palaeontology 36(3): 593-635.
12. Dzik, J., 2003, “Anatomical information content in the Ediacaran fossils and their possible zoological affinities,” Integrative and Comparative Biology 43: 114-126. Fedonkin, M.A., 2003, “The origin of the Metazoa in light of the Proterozoic fossil record,” Paleontological Research 7(1): 9-41.
13. Fedonkin, M.A., and Waggoner, B.M., 1997, “The later Precambrian fossil Kimberella is a mollusc-like bilaterian organism,” Nature 388:868-871.
14. Crimes, T.P., 1992, “The record of trace fossils across the Proterozoic-Cambrian boundary,” IN, J.H. Lipps and P.W. Signor (eds.), Origin and Early Evolution of the Metazoa, Plenum Press, New York, p.177-202. Zhu, M., 1997, “Precambrian-Cambrian trace fossils from eastern Yunnan, China: Implications for Cambrian explosion,” IN Junyuan Chen, Yen-nien Cheng, and H.V. Iten (eds.), The Cambrian Explosion and the Fossil Record, Bulletin of the National Museum of Natural Science No. 10 (Taichung, Taiwan, China), p. 275-312.
15. Chen, Z., S. Bengtson, C-M. Zhou, H. Hua, and Z. Yue., 2008, Tube structure and original composition of Sinotubulities: Shelly fossils from the late Neoproterozoic in southern Shaanxi, China, Lethaia 41: 37-45. Hofmann, H.J., and E.W. Mountjoy, 2001, Namacalathus-Cloudina assemblage in Neoproterozoic Miette Group (Byng Formation), British Columbia: Canada’s oldest shelly fossils, Geology 29: 1091-1094. Grotzinger, J.P., W.A. Watters, and A.H. Knoll, 2000, Calcified metazoans in thrombolite-stromatolite reefs of the terminal Proterozoic Nama Group, Namibia, Paleobiology 26(3): 334-359.