Paleontologists James Valentine, Douglas Erwin, and David Jablonski distill the confusing welter of conflicting views about the Ediacaran fossils: “Although the soft-bodied fossils that appear about 565 million years ago are animal-like, their classifications are hotly debated. In just the past few years these fossils have been viewed as protozoans; as lichens; as close relatives of the cnidarians; as a sister group to cnidarians plus all other animals; as representatives of more advanced, extinct phyla; and as representatives of a new kingdom entirely separate from the animals.”20 What’s more, Valentine, Erwin, and Jablonski note that those paleontologists who do regard the Ediacaran fauna as animals rarely classify them the same way, underscoring their lack of clear affinities to any known animal groups. As they note, “Still other specialists have parceled the fauna out among living phyla, with some assigned to the Cnidaria and others to the flatworms, annelids, arthropods and echinoderms.”21 The uncertain standing of these fossilized forms is partly due to their early extinction, but it also stems from an absence of defining characteristics shared with known groups. They conclude: “This confusing state of affairs arose because these body fossils do not tend to share definitive anatomical details with modern groups, and thus the assignments must be based on vague similarities of overall shape and form, a method that has frequently proved misleading in other cases.”22
Other leading paleontologists also doubt that the Cambrian animals descended from these Ediacaran forms. In a phylogenetic diagram showing the evolutionary relationship of Precambrian and Cambrian fossils, Oxford biologists Alan Cooper and Richard Fortey depict the Ediacaran fauna as lying on a line of descent separate from the Cambrian animals rather than being ancestral to them.23 In another paper, Fortey asserts that the beginning of the Cambrian “saw the sudden appearance in the fossil record of almost all the main types of animals (phyla) that still dominate the biota today.” He concedes that there are a variety of fossils in older strata, but insist that “they are either very small (such as bacteria and algae) or their relationships to the living fauna are highly contentious, as is the case with the famous soft-bodied fossils from the late Precambrian Pound Quartzite, Ediacara, South Australia.”24
Similarly, paleontologist Andrew Knoll and biologist Sean B. Carroll have argued: “It is genuinely difficult to map the characters of Ediacaran fossils onto the body plans of living invertebrates.”25 Although many paleontologists initially showed interest in the possibility that the Cambrian animal forms might have evolved from the Ediacaran organisms, paleontologist Peter Ward explains that “later study cast doubt on the affinity between these ancient remains preserved in sandstones [the Australian Ediacaran] and living creatures of today” (that is, animals representing phyla that first arose in the Cambrian).26 As Nature recently noted, if the Ediacaran fauna “were animals, they bore little or no resemblance to any other creatures, either fossil or extant.”27
This absence of clear affinities has led an increasing number of paleontologists to reject ancestor-descendant relationships between all but (at most) a few of the Ediacaran and Cambrian fauna. Nevertheless, some have suggested that trace fossils may establish a link. In an authoritative 2011 paper in the journal Science, Douglas Erwin and colleagues described the discovery of Ediacaran trace fossils consisting of surface tracks, burrows, fecal pellets, and feeding trails, which, they argue, though small, could only have been made by animals such as worms with a relatively high degree of complexity.28 On the basis of these findings, Erwin and other paleontologists have argued that these trace fossils suggest the existence of organisms with a head and tail, nervous systems, a muscular body wall allowing creeping or burrowing, and a gut with mouth and anus.29 Other paleontologists suggest that these characteristics may indicate the presence of a Precambrian mollusk or a worm phylum.30
Graham Budd, a British paleontologist who works at Uppsala University in Sweden, and others, have disputed these associations. Budd and geologist colleague Sören Jensen argue that many alleged trace fossils actually show evidence of inorganic origin: “There are numerous reports of older trace fossils, but most can be immediately shown to represent either inorganic sedimentary structures or metaphytes [land plants], or alternatively they have been misdated.”31 Still others have suggested that surface tracks and trails could have been left by mobile single-celled organisms, including a known form of a giant deep-sea protist that leaves bilaterian-like impressions. As one paper explains, “Some such traces date back to 1.5 billion to 1.8 billion years ago, which outdates even the boldest claims of the time of origin of animal multicellularity and forces researchers to contemplate the possibility of an inorganic or bacterial origin.”32
Even the most favorable interpretations of these trace fossils suggest that they indicate the presence of no more than two animal body plans (of largely unknown characteristics). Thus, the Ediacaran record falls far short of establishing the existence of the wide variety of transitional intermediates that a Darwinian view of life’s history requires. The Cambrian explosion attests to the first appearance of organisms representing at least twenty phyla and many more subphyla and classes, each manifesting distinctive body plans. In a best case, the Ediacaran forms represent possible ancestors for, at most, four distinct Cambrian body plans, even counting those documented only by trace fossils. This leaves the vast majority of the Cambrian phyla with no apparent ancestors in the Precambrian rocks (i.e., at least nineteen of the twenty-three phyla present in the Cambrian have no representative in Precambrian strata).33
Third, even if representatives of four animal phyla were present in the Ediacaran period, it does not follow that these forms were necessarily transitional or intermediate to the Cambrian animals. The Precambrian sponges (phylum Porifera), for example, were quite similar to their Cambrian brethren, thus demonstrating, not a gradual transformation from a simpler precursor or the presence of an ancestor common to many forms, but quite possibly only an earlier first appearance of a known Cambrian form. The same may be true of whatever kind of worm may be attested by Precambrian tracks and burrows.
Moreover, even assuming, as some evolutionary biologists do,34 that later Cambrian animals had a sponge-like Precambrian ancestor, the gap in complexity as measured by the number of cell types alone, to say nothing of the specific anatomical structures and distinct modes of body plan organization that are present in later animals but not in sponges, leaves a massive discontinuity in the fossil record that requires explanation (much like the morphological gap between Spriggina and actual arthropods).
An Ediacaran Mini-Explosion
The Ediacaran fossils themselves provide evidence of a puzzling leap in biological complexity, though not one nearly great enough (or of the right kind) to account for the Cambrian explosion. Before organisms like Kimberella, Dickinsonia, and sponges appeared, the only living forms documented in the fossil record for over 3 billion years were single-celled organisms and colonial algae. Producing sponges, worms, and mollusks from single-celled organisms is a little like transforming a spinning top into a bicycle. The bicycle isn’t remotely as complex as the automobile sitting beside it, but it represents an enormous leap in technological sophistication over the spinning top. Likewise, although the humble Ediacaran biota look simple beside most of the Cambrian animals, they represent an enormous leap in functional complexity over the single-celled organisms and colonial algae that preceded them.
Thus, the Ediacaran biota attest to a separate sudden increase in biological complexity within a short window of geological time (about 15 million years), following roughly 3 billion years in which only single-celled organisms inhabited the earth.35 This leap in complexity, in a relatively short span of geological time, may well exceed the explanatory resources of natural selection working on random mutations. We will return to that question in Part Two.
The Ediacaran fossils therefore do not solve the problem of the sudden increase in biological form and complexity during the Cambrian. Instead, they represent an earlier
, if less dramatic, manifestation of the same kind of problem. To biology’s “big bang,”36 the Ediacaran biota add a significant “pow.” As paleobiologist Kevin Peterson, of Dartmouth College, and his colleagues note, these fauna represent “an apparent quantum leap in ecological complexity as compared with the ‘boring billions’ [of years] that characterize Earth before the Ediacaran,” even if these organisms are “still relatively simple when compared with the Cambrian,” which they characterize as another “quantum leap in organismal and ecological complexity.”37
Many paleontologists now refer to the Ediacaran radiation as an explosion in its own right.38 This Precambrian “pow” makes the problem of fossil discontinuity only more acute, since credible intermediates leading to the Ediacaran layers are completely nonexistent in the even more sparsely populated strata beneath them.
Finally, even if one regards the appearance of the Ediacaran fossils as evidence of a “fuse” leading to the Cambrian explosion as some have proposed,39 the total time encompassed by the Ediacaran and Cambrian radiations still remains exceedingly brief relative to the expectations and requirements of a modern neo-Darwinian view of the history of life. As I will explain in more detail in Chapter 8, neo-Darwinism is the modern version of Darwin’s theory that invokes random genetic changes called mutations as the source of much of the new variation upon which natural selection acts. Like classical Darwinism, the neo-Darwinian mechanism requires great stretches of time to produce novel biological form and structure. Yet, current studies in geochronology suggest that only 40 to 50 million years elapsed between the beginning of the Ediacaran radiation (570–565 million years ago) and the end of the Cambrian explosion (525–520 million years ago).40 To anyone unfamiliar with the equations of population genetics by which neo-Darwinian evolutionary biologists estimate how much morphological change is likely to occur in a given period of time, 40 to 50 million years may seem like an eternity. But empirically derived estimates of the rate at which mutations accumulate imply that 40 to 50 million years does not constitute anything like enough time to build the necessary anatomical novelties that arise in the Cambrian and Ediacaran periods. I will describe this problem in more detail in Chapter 12.
Until recently, radiometric studies had estimated the duration of the Cambrian radiation itself at 40 million years, a period of time so brief, geologically speaking, that paleontologists had already dubbed it an “explosion.” The relative suddenness of the Cambrian explosion, even on the earlier measure of its duration, had already raised serious questions about the adequacy of the neo-Darwinian mechanism; consequently, it had also raised questions about whether a Darwinian understanding of the history of life could be reconciled with the Cambrian and Precambrian fossil record. Thus, treating the Ediacaran and the Cambrian radiations as one continuous evolutionary event (itself an unrealistically generous assumption) only returns the problem to its earlier (pre-zircon redating) status.
For all these reasons, the late Precambrian fossils have not solved, but instead have deepened, the mystery of the origin of animal form. And few leading Cambrian paleontologists, of whom I was aware on that September evening in 2009 while preparing to answer questions at the University of Oklahoma, thought otherwise.
Ediacaran Exotica
So what about the claim that certain exotic Ediacaran fossils are plausible ancestors to the Cambrian animal forms, even if better-known Ediacaran forms such as Dickinsonia, Charnia, and Spriggina are probably not? Did these exotic forms solve the mystery of the Cambrian explosion?
Only a few years before my visit to the University of Oklahoma, I had written a scientific review article with research help from several colleagues, including a paleontologist and a marine biologist.41 (The latter was Paul Chien, who helped discover the Precambrian sponge embryos discussed in the previous chapter.) In our review article, I explained many of the problems with treating the Ediacaran as transitional intermediates discussed above. In the process of doing the research for that article, my colleagues and I encountered few paleontologists who thought that Parvancorina, Arkarua (see Fig. 4.2), or Vernanimalcula represented definitive ancestors of the Cambrian bilaterians, arthropods, or echinoderms. Could we have missed something?
In fact, leading Cambrian authorities have dismissed associations between these odd fossil forms and the Cambrian animals. Nevertheless, in his talk before the showing of our film, the local professor from the University of Oklahoma asserted that the rather indistinct fossil form found in the Ediacaran Hills called Parvancorina represented a plausible ancestor of the arthropods. Some have described Parvancorina as a shield-shaped fossil form with a raised anchor-shaped ridge impressed atop it, bearing a superficial resemblance in its shape to that of a trilobite—thus, the claim that it might have represented an early arthropod. Yet leading Cambrian paleontologists dispute this association. Cambrian expert James Valentine has argued that Parvancorina is not convincing as an arthropod ancestor, and for good reason. Parvancorina fossils lack a head, jointed limbs, and compound eyes, all distinctive features of arthropods. Thus, Valentine noted that Parvancorina fossils “have not been shown to share derived features” with arthropods.42
FIGURE 4.2
Figure 4.2a (left): Photograph of Arkarua fossil, courtesy Taylor & Francis, Ltd. Figure 4.2b (right): Photograph of Parvancorina fossil, courtesy Peterson, K. J., Cotton, J. A., Gehling, J. G., and Pisani, D., “The Ediacaran Emergence of Bilaterians: Congruence between the Genetic and the Geological Fossil Records,” Philosophical Transactions of the Royal Society B, 2008, 363 (1496): 1435–43, Figure 2, by permission of the Royal Society.
Valentine makes much the same point about the small disc-like imprint called Arkarua, one of the other Ediacaran forms cited by the University of Oklahoma professor that night at the Sam Noble Museum. Valentine points out that it too lacks many distinctive features of the animal phylum to which it is typically assigned. Indeed, those who propose Arkarua as an ancestor of the Cambrian animals usually claim that it represents an early echinoderm (as the professor in Oklahoma did). Echinoderms include starfish, sand dollars, and other animals with fivefold symmetry extending from a central body cavity.43 Some have perceived five tiny segmented divisions within the circular impressions left by Arkarua, making them seem roughly similar to some modern echinoderms. But that similarity has proven superficial at best. Other paleontologists observe that Arkarua lacks a stereom, or water vascular system, a definitive diagnostic feature of echinoderms; thus, its “echinoderm-specific features are not readily visible.”44 Valentine has argued that, absent such telltale features, the relationship of Arkarua to echinoderms “remains uncertain.”45
In the case of Vernanimalcula, the story is more complicated but equally problematic. Vernanimalcula is the name that Chinese paleontologists gave to an imprint in phosphorite sediment found in the Doushantuo Formation in 2004. They found the structure in 580-to 600-million-year-old rocks, making the impression even older than the Ediacaran strata. The paleontologist David Bottjer of the University of Southern California, and some Chinese paleontologists (at least, initially), speculated that the Vernanimalcula imprint might be the remains of an early bilaterian.46
Recall that bilaterians are animals whose parts found on one side of the body midline are also found in mirror image on the other (as opposed to, say, a radially symmetric animal47). Figure 4.3 shows a picture of the structure of Vernanimalcula first found in the Doushantuo Phosphorite formation. Some paleontologists think that Vernanimalcula exhibits such bilateral symmetry and thus might be ancestral to the bilaterian animals that later first appeared in the Cambrian period.
But problems have emerged with this argument. First, the form of the Vernanimalcula does not resemble any specific bilaterian animal. In addition, recent scientific analyses of these remains have questioned whether this imprint preserves the remains of animals and, therefore, bilaterians at all. For example, in 2004, Stefan Bengtson and Graham Budd, two paleontologists and Cambrian experts, published
a detailed chemical and microscopic analysis of these fossils in the journal Science.48 They concluded that the structures preserved in phosphorite rocks had undergone significant alteration by so-called diagenesis and taphonomic processes. Diagenesis refers mainly to processes of chemical alteration that occur after sediments are deposited and before sedimentary rocks are fully hardened, or “lithified.” Taphonomic processes are those that alter once living organisms after burial and preservation in sediments.
FIGURE 4.3
Photograph of Vernanimalcula fossil. Courtesy American Association for the Advancement of Science, from Chen, J.-Y., Bottjer, D. J., Oliveri, P., Dornbos, S. Q., Gao, F., Ruffins, S., “Small Bilaterian Fossils from 40 to 55 Million Years Before the Cambrian,” Science, 305 (July 9, 2004): 218–22, Figure 1b. Reprinted with permission from AAAS.
Based on their microscopic analysis, Bengtson and Budd rejected the hypothesis that these structures preserved the remains of an animal form. Instead, they argued that the phosphorite imprint exhibited distinctive features of the chemically altered remains of one-celled microfossils—microfossils that had been encrusted with layers of chemical residue from various diagenetic processes.49
More recently, in 2012, Bengtson and three other colleagues published another paper sharply critical of the view that Vernanimalcula represents an ancestor of the bilaterian animals—or even an animal. They show that the “structures key to animal identity are effects of mineralization that do not represent biological tissues.” For this reason they conclude: “There is no evidential basis for interpreting Vernanimalcula as an animal, let alone a bilaterian.”50
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