Mystery Fossil

Your whole creation is never silent and never ceases to praise you. The spirit of every man utters its praises in words directed to you; animals and material bodies praise you through the mouth of those who meditate upon them, so that our soul may rise out of its weariness toward you, supporting itself upon the things which you created, and then passing on to you yourself who made them marvelously.

—St. Augustine1

[At] the dawn of European civilization, with the Greek philosophers, there were two clear tendencies in this problem. Those are the Platonic and the Democritian trends, either the view that dead matter was made alive by some spiritual principle or the assumption of a spontaneous generation from that matter, from dead or inert matter.

The Platonic view has predominated for centuries and, in fact, still continues to exist in the views of vitalists and neovitalists.

The Democritian line was pushed in the background and came into full force only in the seventeenth century in the work of Descartes. Both points of view really differed only in their interpretation of origin, but both of them equally assumed the possibility of spontaneous generation.

Until not so long ago we thought that man had been specially created and that maggots arose from rotten cheese by spontaneous generation. It didn't matter, but now we believe that human beings have been evolved and it matters a very great deal. Thus, it is of the utmost importance that we should get to the truth of this matter.

—J. B. S. Haldane, introducing Oparin3

Coming across an arresting full-page illustration in the colorful TimeLife Nature Library, I became aware for the first time of the appeal of Ediacaran organisms. The illustration (figure 1.1), in stark black and white, showed an odd disc-shaped fossil, fringed by fine radial lines, with three curving arms at its center. The picture was the frontispiece for chapter 2, "The Origin of the Sea," and its caption was as telegraphic as a personals ad:

mystery fossil, first of its rare kind ever found, has no known relationship with any other creature living or dead. It is also one of the oldest ever found. It comes from Pre-Cambrian rock strata in South Australia.4

This image held my attention and years later, when I had an opportunity to study Precambrian fossils at the University of California at Santa Barbara, I already appreciated the appeal of Ediacaran paleontology. In fact, I embarked on a study of the Ediacaran fossils for my postgraduate work.

These fossils are still as mysterious as when Tribrachidium was illustrated by the Time-Life Nature Library in the 1960s. With the Ediacaran fossils, or Ediacarans, paleontologists work a complex interface between the knowable (but difficult to know) and the unknowable (and thus outside the realm of science). The fossils of Ediacara document the events leading up to most important event in the history of life on earth.

Figure 1.1: Tribrachidium.

Life has been part of this 4.45-billion-year-old planet for more than 3.5 billion years; calling Earth a living planet is more than just a poetic image. Life is now seen as both a process (a verb, in the view of Lynn Margulis and Dorion Sagan5) and an important geophysical and geo-chemical phenomenon. This sentiment was nicely stated by A. I. Oparin in 1965:

As a rule the attempt to discover the possibility of life on Mars, Venus and other places has been made by the following methods. Studies were made of the conditions prevailing on these planets, and the question was asked if under these conditions organisms resembling those on Earth could exist. This is a fallacious approach. Life is produced by a certain environment, and it changes and alters the environment to adapt itself to it and adapt the environment to itself.6

Oparin's words seem strikingly current in light of the recent interest in the possibility of life on Mars. We know two things about life's origin. First, as Oparin pointed out in 1924, life originated in the absence of life and in the absence of free oxygen. Second, the appearance of life on Earth was apparently not a lengthy process. The earliest bacteria appeared almost as soon as Earth's crust was cool enough to support life. Oparin felt that "a billion years are needed to realize"7 life's origin from inorganic precursors, but the geological record does not allow this much time for what might have been the first event of spontaneous generation. If the recent claims of ancient Martian life are true, then either life planet-skipped by some sort of phenomenon of panspermia or life is very easy to create under the proper physical and chemical conditions.

In our solar system at least, life could not get a foothold on a planet until the megacratering crisis had ended. This crisis was the period of early bombardment of planets by planetesimals (gigantic, subplanetary-sized meteors). An accretion of meteors such as these formed the planet in the first place. So much energy was released with each incoming rocky mass that the entire planetary surface was melted and presumably sterilized. This era of meltdowns has been called the "impact frustration of life" and ended on earth with the end of the intensive period of megacratering (as indicated by the ages of craters on the moon) about 3.8 billion years ago.

Rocks struck by meteoric impacts become pervasively fractured. When these fractures became fluid-filled, their surface areas expanded greatly, and thus may have become ideal sites,8 precisely the micro-

chemical factories needed for the origin of life. From a biological point of view, the fractures formed by incoming meteors represented a megacratering opportunity rather than a crisis.

The earliest life must have been microbial, the first forms probably being about .005 millimeter in diameter. A fascinating question concerning the origin of life is, "When did the first cell acquire the ability to distinguish self from nonself?" As A. G. Cairns-Smith argued in Seven Clues to the Origin of Life, life's origin may well have been as much a mineralogical phenomenon as a biochemical phenomenon.9 In his view, a crystalline form of life (Gene-1) gave rise to a fully "organic" form of life (Gene-2).

Cairns-Smith felt that there must have been some sort of inorganic scaffolding on which the earliest life would have started. He proposed clay as the living crystal of Gene-1. More recent research has shown that clay does not have the properties needed to act as the scaffolding of Gene-2. Nevertheless, the main biomolecular constituents of life (nucleic acids, proteins, and phospholipids) are the products of complex biochemical synthesis pathways that cannot have arisen, de novo, on their own. As with self-supporting stones in a stone archway, some sort of scaffolding must have supported the stones during construction.

The idea of earliest life lacking individualization, forming as something like a living crystal, an extended body form that permeated some special environment of Earth, is indeed attractive. But however the first cells came to be, life apparently remained unicellular for billions of years. Multicellular life, individuals composed of billions or trillions of cells, did not appear on the globe until long after life began.10

The earliest organisms thought to represent multicellular creatures are uninspiring as fossils, occurring as more or less shapeless organic films (carbonized impressions) on slabs of shale.11 The best that can be said about them, and this is by no means certain for all examples, is that they were eukaryotes, bearers of nucleated cells.

Eukaryotic cells are characterized by the presence of intracellular organelles, many of which were once free-living, and subsequently symbiotic, bacteria. This idea of a symbiotic origin for the organelles of eukaryotic cells gained momentum in the United States with Oparin's attendance at a conference in Wakulla Springs, Florida, in 1963. In the discussion session, Oparin presented the revolutionary idea of symbio-genesis, the thought that a new type of organism can emerge by the fusion of two unrelated types.12 This was the first time many of the Western conference participants had heard these ideas:

The American investigator Hans Ris, of Wisconsin, visited the Soviet Union and has advanced an idea similar to what was expounded several years ago in Russia by Mereshkovskii, namely, that a cell represents a symbiotic structure. They said that for the time being the idea was rather too audacious. But it is possible you could develop it in the direction of representing the formation of cells as a gradual association, aggregation of symbionts.

Hans Ris was Lynn Margulis's adviser in college; to my surprise, before I mentioned it to her in June 1996, she had never heard that he had visited Russia. There appears to be a fascinating and untold story about the development of symbiogenesis theory in Soviet Russia, a story that may have its share of Cold War intrigues. However, I am not surprised by Oparin's comments because he was one of the few scientists of his stature at the time to have had more than a passing familiarity with symbiogenesis theory. The only other was the great Russian geologist Vladimir Ivanovich Vernadsky (1863—1945), who studied under sym-biogeneticist Andrei S. Famintsyn, "founder of the Russian school of plant physiology, who demonstrated the possibility of photosynthesis in artificial light."13 Vernadsky used his knowledge of symbiogenesis to found the now burgeoning field of biogeochemistry. In Vernadsky's view, biological processes are so important for our planet that it may truly be said that "life makes geology."

As Douglas R. Weiner points out in his review of Liya Nikolaevna Khakhina's book Concepts of Symbiogenesis: A Historical and Critical Study of the Research of Russian Botanists (translated into English in 1992),14'15 symbiogenesis is integral to the Russian traditions in the history of science. Andrei S. Famintsyn (descended from a sixteenth-century Scottish immigrant whose name is the Russian translation of Thompson)16 sought to supplement Darwinism with symbiogenesis theory. Konstantin S. Mereshkovskii tried to displace Darwinism with his new symbiogenesis theory between 1900 and 1920. Boris M. Kozo-Polyanskii tried to incorporate symbiogenesis smoothly within the overall schema of Darwinian evolution. Khakhina explains the slow headway symbiogenesis theory made in most scientific circles outside Russia. She describes it in terms of the perception that through the 1950s, symbiogenesis did not accord with the prevailing explanations of evolution.

The idea of a symbiotic origin of organelles is now the accepted theory presented in biology courses throughout the world. Nevertheless, scientists who espouse symbiogenesis raise hackles among their colleagues in evolutionary biology. One response to the murmuring is to boldly point out that there are indeed problems with the 1950s explanation of evolution, commonly called the neo-darwinian modern synthesis. A strong case can be made that neo-darwinism is due for an intellectual shakeup, and we return to this debate in chapter 13. As we will see, the solutions to the mysteries of Ediacara will play an important role in updating the modern synthesis. We start at the beginning of the Ediacaran fossil record.

The first large, complex, unquestionably multicellular fossils appear about 600 million years ago in stratified rocks of northern Mexico (chapter 9). Complex life on land, recognized by my wife Dianna and me as the biogeophysical entity Hypersea, appears some 200 million years later.17

Hypersea is the sum of eukaryotic life on land and all its symbionts. Despite its geological youth, Hypersea overwhelms the marine biota in terms of both total biomass and total biodiversity. This happens because the fluid connections between eukaryotes on land (particularly the ones involving plants and their root or mycorrhizal fungi) lead to a pumping of nutrients from the soil up into the photosynthetic parts of plants, a phenomenon we call hypermarine upwelling. Oparin18 neatly anticipated our Hypersea theory, even hinting at hypermarine upwelling back in 1963: "Imagine that land life did not exist. From the standpoint of a jellyfish, life on dry land is sheer nonsense. Through a complex process of adaptation, of water exchange of circulation [sic], such a form of life was able to arise."

The first complex multicellulars and Hypersea are separated by the great divide in the geological time chart, the Precambrian-Cambrian boundary. This boundary is marked by what has been called the Cambrian breakthrough, the abrupt appearance of virtually all major types of skeleton-bearing animals. A robust and continuing evolutionary debate regarding this breakthrough19 involves two main questions. First, did all the skeletalized animals appear suddenly at this time (the bang hypothesis), or do they have long histories that happened to leave virtually no fossil record (the whimper hypothesis)? Some authors advocate the whimper,20 others the bang.21 The whimperers are forced to admit that there is a major evolutionary radiation at the beginning of the Cambrian, although they try to keep the perceived number of new phyla appearing at this time to a minimum. The bangers see the phyla developing rapidly, and some postulate an unusual genetic reorganiza tion that happens only at this time and is frozen into place (the green genes hypothesis, a version of the bang hypothesis).22 The main problem with this putative fixing of particular gene expressions is that it is difficult or impossible to test scientifically.

The main proponent of the green genes hypothesis, James W. Valentine of the University of California at Berkeley, does not support the more extreme statements of his idea, and says that the elaboration of early animal genes "may have been necessary, but . . . was not sufficient, to drive the evolutionary creativity of the Cambrian."23 His 25-year quest to explain the Cambrian explosion in terms of gene regulation has not yet met with unequivocal success.24 Each successive Valentine paper on this subject seems to say, "Here is the latest breakthrough in modern genetic research; it must have something to do with the Cambrian explosion!" However, I believe that the origin of the major gene complexes in animals, an interesting subject in itself, has no necessary connection to the Cambrian event, and in fact may have been completely decoupled from it, the major steps in the formation of the animal genetic code having been taken well before the Cambrian.25 There will be a better harvest for scientists among fossils and the ecological issues of the Garden of Ediacara.26

Bang or whimper, the Cambrian armored animals include many of familiar types that can be placed in still extant phyla. But for at least 50 million years before the Cambrian explosion, there existed a marine world of large27 and unusual creatures.

These organisms constitute the Ediacaran biota. They have also been called the Ediacaran fauna, but because the term fauna implies animals, and paleontologists are not confident that all of the Ediacaran forms were animals; prudence requires the less specific term Ediacaran biota, or simply Ediacarans.

Diverse communities of multicellular creatures appear with the first members of the Ediacaran biota. My recent find in Mexico of trace fossils associated with the oldest Ediacarans indicates that true animals were unquestionably part of the biota.28 Also present were the Ediacaran body fossil forms, less easily classified.

The Ediacaran biota seems at first glance to be another case of apparent spontaneous generation. Oparin's billion years are not evident here. My field research indicates that the Ediacarans sprang forth, fully formed, without a long record of evolution. This leads to the second question.

How could this happen? Furthermore, what kind of creatures are represented by the Ediacarans? Were they the first animals? They certainly

Figure 1.2: Seilacher's interpretation of the structure of Ediacarans. Left: Inflated, as in life. Right: Deflated, as in many fossil specimens. Note the rigid vertical walls.

From M. A. S. and D. L. S. McMenamin, The Emergence of Animals: The Cambrian Breakthrough (New York: Columbia University Press, 1990). Artwork by Dianna McMenamin.

seem to be associated with trace fossil evidence of the earliest animals, but in the view of German invertebrate paleontologist Adolf Seilacher, they are not animals at all. In 1983 Seilacher destabilized what had been the consensus viewpoint (that is, Ediacarans as early animals) by pointing out that they had a quilted body architecture (figure 1.2) totally unlike anything seen in animals. Following insights made by German paleobotanist Hans D. Pflug, Seilacher argued that Ediacaran forms were suigeneris, representatives of a group of high taxonomic rank29 that went extinct at the beginning of the Cambrian.

A well-known science writer, following Seilacher's story, called the Ediacaran forms "aliens here on earth," meaning that they represented an alien body form no longer represented in the world.30 Later work has demonstrated that these forms survived well into the Cambrian. However, the newer research has not settled the question of what these forms were, or how they fed. Many mysteries remain. The solutions may well involve a fuller understanding of the phenomenon of symbiogene-sis. The question of the origin of life is an enduring puzzle, but we are just as ignorant about the origin of complex life.


1. Book V:1, p. 90 in Saint Augustine of Hippo, The Confessions of St. Augustine, translated by R. Warner (New York: Mentor, 1963).

2. S. W. Fox, ed., The Origins of Prebiological Systems and of Their Molecular Matrices (New York: Academic Press, 1965).

4. The illustration of the fossil Tribrachidium heraldicum appears in L. Engel, The Sea (New York: Time-Life Books, 1969), 36-37.

5. L. Margulis and D. Sagan, What Is Life? (New York: Simon & Schuster, 1995).

6. See pp. 91-92 of A. I. Oparin, "History of the Subject Matter of the Conference," in S. W. Fox, ed., The Origins of Prebiological Systems and of Their Molecular Matrices (New York: Academic Press, 1965), 91-98.

7. See p. 345 in S. W. Fox, ed., The Origins of Prebiological Systems and of Their Molecular Matrices (New York: Academic Press, 1965).

8. Because of small-scale cation exchange and close association of clays, apatite, and other phosphate minerals.

9. A. G. Cairns-Smith, Seven Clues to the Origin of Life (Cambridge, England: Cambridge University Press, 1991).

10. At least a billion years after the origin of life.

11. H. J. Hofmann, "Paleocene #7 Precambrian Biostratigraphy," Geoscience Canada 14 (1987):135-154.

12. See p. 345 in S. W. Fox, ed., The Origins of Prebiological Systems and of Their Molecular Matrices (New York: Academic Press, 1965).

13. A. L. Yanshin and F. T. Yanshina, "The Scientific Heritage of Vladimir Vernadsky," Impact of Science on Society 151 (1988):283—296.

14. D. R. Weiner, "Book Reviews Feature Review," Isis 87 (1996):140-210.

15. L. N. Khakhina, Concepts of Symbiogenesis: A Historical and Critical Study of the Research of Russian Botanists, Lynn Margulis and Mark McMenamin, eds. (New Haven: Yale University Press, 1992).

16. M. B. Saffo, "Evolution of Symbiosis," BioScience 46 (1996):300-304.

17. C. Zimmer, "Hypersea Invasion," Discover 16, no. 10 (1995):76-87; M. A. S. McMenamin and D. L. S. McMenamin, Hypersea: Life on Land (New York: Columbia University Press, 1994).

18. See p. 92 in S. W. Fox, ed., The Origins of Prebiological Systems and of Their Molecular Matrices (New York: Academic Press, 1965).

19. L. M. Van Valen, "Review of The Emergence of Animals: The Cambrian Breakthrough by M. A. S. McMenamin and D. L. S. McMenamin, 1990, Columbia University Press," Evolutionary Theory and Review 10 (1992):172.

20. R. A. Fortey, D. E. G. Briggs, and M. A. Wills, "The Cambrian Evolutionary 'Explosion': Decoupling Cladogenesis from Morphological Disparity," Biological Journal of the Linnaean Society 57 (1996):13—33.

21. D. H. Erwin, J. W. Valentine, and D. Jablonski, "The Origin of Animal Body Plans," American Scientist85 (1997):126—137. My favorite parts of this article are the illustrations; note the menacing gaze of the stalking anomalocarid on the cover illustration. Note also the use of Marilyn Monroe as representative of our branch of the animal family tree (M. DeRose, "Letters to the Editors." American Scientist 85 [1997]:204).

22. M. A. S. McMenamin and D. L. S. McMenamin, The Emergence of Animals: The Cambrian Breakthrough (New York: Columbia University Press, 1990).

23. See p. 137 of D. H. Erwin, J. W. Valentine, and D. Jablonski, "The Origin of Animal Body Plans," American Scientist85 (1997):126—137.

24. See J. W. Valentine and C. A. Campbell, "Genetic Regulation and the Fossil Record," American Scientist63 (1975):673-680; J. W. Valentine, "Late Precambrian Bilaterians: Grades and Clades," Proceedings of the National Academy of Sciences USA 91 (1994):6751-6757. See also B. Holmes, "When We Were Worms: The Garden of Ediacara," New Scientist 156 (1997): 30-35.

25. These steps were essentially complete by 600 million years ago, as shown by the presence of trace fossils of this age in Mexico; see M. A. S. McMenamin, "Ediacaran Biota from Sonora, Mexico," Proceedings of the National Academy of Sciences USA 93 (1996):4990-4993.

26. M. A. S. McMenamin, "The Garden of Ediacara," Palaios 1 (1986): 178-182.

27. Some up to a meter or more long.

28. Trace fossils are the markings made in sediment by the burrowing or locomotion of animals.

29. Such as a phylum or kingdom.

30. R. Lewin, "Alien Beings Here on Earth," Science 223 (1984):39.

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