The Lying Stones of Marrakech
Barghoorn and colleagues dispelled a century of frustration by looking in a different place, where cellular remains of bacteria might be preserved—in chert beds. Chert has the same chemical formula (with a different molecular arrangement) as quartz: silicon dioxide. Paleontologists rarely think of looking for fossils in silicate rocks—for the perfectly valid and utterly obvious reason that silicates form by the cooling of volcanic magmas and therefore cannot contain organic remains. (Life, after all, doesn’t flourish in bubbling lavas, and anything falling in gets burnt to a crisp.) But cherts can form at lower temperatures and be deposited amid layers of ordinary sediments in oceanic waters. Bacterial cells, when trapped in this equivalent of surrounding glass, can be preserved as fossils.
This cardinal insight—that we had been searching in the wrong venue of ordinary (and barren) sediments rather than in fruitful cherts—created an entire field of study: collecting data for the first two-thirds or so of life’s full history! Forty years later, we may look back with wonder at the flood of achievement and the complete overturn of established wisdom. We now possess a rich fossil record of early life, extending right back to the earliest potential source for cellular evidence. (The oldest rocks on earth that could preserve such data do contain abundant fossils of bacterial organisms. These 3.5-to-3.6-billion-year-old rocks from Australia and South Africa are the most ancient strata on earth that have not been sufficiently altered by subsequent heat and pressure to destroy all anatomical evidence of life.)
Such ubiquity and abundance has forced a reversal of the old view. The origin of life at simplest bacterial grade now seems inevitable rather than improbable. As a mantra for memory, may I suggest: “Life on earth is as old as it could be.” I realize, of course, that an earliest possible appearance builds no proof for inevitability. After all, even a highly improbable event might occur, by good fortune, early in a series of trials. (You might flip those fifty successive heads on your tenth attempt—but don’t count, or bet, on it!) Nonetheless, faced with the data we now possess—that life appeared as soon as environmental conditions permitted such an event and then remained pervasive forever after—our thoughts must move to ideas about almost predictive inevitability. Given a planet of earthly size, distance, and composition, life of simplest grade probably originates with virtual certainty as a consequence of principles of organic chemistry and the physics of self-organizing systems.
But whatever the predictability of life’s origin, subsequent pathways of evolution have run in mighty peculiar directions, at least with respect to our conventional hopes and biases. The broadest pattern might seem to confirm our usual view of generally increasing complexity, leading sensibly to human consciousness: after all, the early earth sported only bacteria, while our planet now boasts people, ant colonies, and oak trees. Fair enough, but closer scrutiny of general timings or particular details can promote little faith in any steady pattern. If greater size and complexity provide such Darwinian blessings, why did life take so long to proceed “onward,” and why do most of the supposed steps occur so quirkily and so quickly? Consider the following epitome of major events:
Fossils, as stated above, appear as soon as they possibly could in the geological record. But life then remains exclusively at this simplest so-called prokaryotic grade (unicells without any internal organelles, that is, no nuclei, chromosomes, mitochondria, and so on) for about half its subsequent history. The first unicells of the more complex eukaryotic grade (with the conventional organelles of our high school textbook pictures of an amoeba or paramecium) do not appear in the fossil record until about two billion years ago. The three great multicellular kingdoms of plants, fungi, and animals arise sub-sequently (and, at least for algae within the plant kingdom, more than once and independently) from eukaryotic unicells. Fossils of simple multicellular algae extend back fairly reliably to about one billion years, and far more conjecturally to as many as 1.8 billion years.
But the real enigma—at least with respect to our parochial concerns about the progressive inevitability of our own lineage—surrounds the origin and early history of animals. If life had always been hankering to reach a pinnacle of expression as the animal kingdom, then organic history seemed in no hurry to initiate this ultimate phase. About five-sixths of life’s time had elapsed before animals made their first appearance in the fossil record some 600 million years ago. Moreover, the earth’s first community of animals, which held nearly exclusive sway from an initial appearance some 600 million years ago right to the dawn of the Cambrian period 543 million years ago, consisted of enigmatic species with no clear relation to modern forms.
These so-called Ediacaran animals (named for the locality of first discovery in Australia, but now known from all continents) could grow quite large (up to a few feet in length), but apparently contained neither complex internal organs, nor even any recognizable body openings for mouth or anus. Many Ediacaran creatures were flattened, pancakelike forms (in a variety of shapes and sizes), built of numerous tubelike sections, complexly quilted together into a single structure. Theories about the affinities of Ediacaran organisms span the full gamut—from viewing them, most conventionally, as simple ancestors for several modern phyla; to interpreting them, most radically, as an entirely separate (and ultimately failed) experiment in multicellular animal life. An intermediate position, now gaining favor—a situation that should lead to no predictions about the ultimate outcome of this complex debate—treats Ediacaran animals as a bountiful expression of the range of possibilities for diploblastic animals (built of two body layers), a group now so reduced in diversity (and subsisting only as corals, jellyfishes, and their allies) that living representatives provide little understanding of full potentials.
Modern animals—except for sponges, corals, and a few other minor groups—are all triploblastic, or composed of three body layers: an ectoderm, forming nervous tissue and other organs; mesoderm, forming reproductive structures and other parts; and endoderm, building the gut and other internal organs. (If you learned a conventional list of phyla back in high school biology, all groups from the flatworms on “up,” including all the “big” phyla of annelids, arthropods, mollusks, echinoderms, and vertebrates, are triploblasts.) This three-layered organization seems to act as a prerequisite for the formation of conventional, complex, mobile, bilaterally symmetrical organisms with body cavities, appendages, sensory organs, and all the other accoutrements that set our standard picture of a “proper” animal. Thus, in our aimlessly parochial manner (and ignoring such truly important groups as corals and sponges), we tend to equate the problem of the beginning of modern animals with the origin of triploblasts. If the Ediacaran animals are all (or mostly) diploblasts, or even more genealogically divergent from triploblast animals, then this first fauna does not resolve the problem of the origin of animals (in our conventionally limited sense of modern triploblasts).
The story of modern animals then becomes even more curious. The inception of the Cambrian period, 543 million years ago, marks the extinction, perhaps quite rapidly, of the Ediacara fauna, and the beginning of a rich record for animals with calcareous skeletons easily preserved as fossils. But the first phase of the Cambrian, called Manakayan and lasting from 543 to 530 million years ago, primarily features a confusing set of spines, plates, and other bits and pieces called (even in our technical literature) the SSF, or “small shelly fossils” (presumably the disarticulated fragments of skeletons that had not yet evolved to large, discrete units covering the entire organism).
The next two phases of the Cambrian (called Tommotian and Atdabanian, and ranging from 530 to about 520 million years ago) mark the strangest, most important, and most intriguing of all episodes in the fossil record of animals— the short interval known as the “Cambrian explosion,” and featuring the first fossils of all animal phyla with skeletons subject to easy preservation in the fossil record. (A single exception, a group of colonial marine organisms called the Bryozoa, make their appearance at the beginning of
the next or Ordovician period. Many intriguing inventions, including human consciousness and the dance language of bees, have arisen since then, but no new phyla, or animals of starkly divergent anatomical design.)
Time charts for major events in the history of life (left) and for details of the Cambrian Explosion and other events in the origin of multicellular animals (right).
Haeckel’s theoretical drawings of ancestral animals (left) compared with fossils of a Precambrian embryo (below).
The Cambrian explosion ranks as such a definitive episode in the history of animals that we cannot possibly grasp the basic tale of our own kingdom until we achieve better resolution for both the antecedents and the unfolding of this cardinal geological moment. A major discovery, announced in February 1998, and also based on learning to look in a previously unsuspected place, has thrilled the entire paleontological community for its promise in unraveling the previously unknown history of triploblast animals before the Cambrian explosion.
If the Cambrian explosion inspires frustration for its plethora of data—too much, too confusing, and too fast—the Precambrian history of triploblast animals engenders even more chagrin for its dearth. The complex animals of the explosion, so clearly assignable to modern phyla, obviously didn’t arise ex nihilo at their first moment of fossilization, but who (and where) are their antecedents in Precambrian times? What were the forebears of modern animals doing for 50 million prior years, when Ediacaran diploblasts (or stranger creatures) ruled the animal world?
Up to now, we have engaged in much speculation, while possessing only a whiff or two of data. Ediacaran strata also contain trails and feeding traces presumably made by triploblast organisms of modern design (for the flattened and mostly immobile Ediacaran animals could not crawl, burrow, or feed in a manner so suggestive of activities now confined to triploblast organisms). Thus, we do have evidence for the existence, and even the activities, of precursors for modern animals before the Cambrian explosion, but no data at all about their anatomy and appearance—a situation akin to the frustration we might feel if we could hear birdsong but had never seen a bird.
A potential solution—or at the very least, a firm and first source of anatomical data—has just been discovered by applying the venerable motto (so beloved by people, including yours truly, of shorter-than-average stature): good things often come in small packages, or to choose a more literary and inspirational expression, Micah’s statement (5:2) taken by the later evangelists as a prophecy of things to come: “But thou, Bethlehem … though thou be little among the thousands of Judah, yet out of thee shall he come forth unto me that is to be ruler in Israel.”
In short, paleontologists had been looking for conventional fossils in the usual (and visible) size ranges of adult organisms: fractions to few inches. But a solution had been lurking at the smaller size of creatures just barely visible (in principle) but undetectable in conventional practice—in the domain of embryos. Who would ever have thought that delicate embryos might be preserved as fossils, when presumably hardier adults left no fragments of their existence? The story, a fascinating lesson in the ways of science, has been building for more than a decade, but has only just been extended to the problem of Precambrian animals.
Fossils form in many modes and styles—as original hard parts preserved within entombing sediments, or as secondary structures formed by impressions of bones or shells (molds) that may then become filled with later sediments (casts). But original organic materials may also be replaced by percolating minerals—a process called petrifaction, or literally “making into stone,” a phenomenon perhaps best represented in popular knowledge by gorgeous specimens from the Petrified Forest of Arizona, where multicolored agate (another form of silicon dioxide) has replaced original carbon so precisely that the wood’s cellular structure can still be discerned. (Petrifaction enjoys sufficient public renown that many people mistakenly regard such replacement as the primary definition of a fossil. But any bit of an ancient organism qualifies as a fossil, whatever the style of preservation. In almost any circumstance, a professional would much prefer to work with unaltered hard parts than with petrified replacements.)
In any case, one poorly understood style of petrifaction leads to replacement of soft tissues by calcium phosphate—a process called phosphatization. This style of replacement can occur within days of death, thus leading to the rare and precious phenomenon of petrifaction before decay of soft anatomy. Phosphatization might provide a paleontologist’s holy grail if all soft tissues could thus be preserved at any size in any kind of sediment. Alas, the process seems to work in detail only for tiny objects up to about two millimeters in length (26.4 millimeters make an inch, so we are talking about barely visible dots, not even about bugs large enough to be designated as “yucky” when found in our dinner plates or beds).
Still, on the good old principle of not looking gift horses (or unexpected bounties) in the mouth (by complaining about an unavailable better deal), let us rejoice in the utterly unanticipated prospect that tiny creatures—which are, after all, ever so abundant in nature, however much they may generally pass beneath our exalted notice—might become petrified in sufficient detail to preserve their bristles, hairs, or even their cellular structure. The recognition that phosphatization may open up an entire world of tiny creatures, previously never considered as candidates for fossilization at all, may spark the greatest burst of paleontological exploration since the discovery that two billion years of Precambrian life lay hidden in chert.
The first hints that exquisite phosphatization of tiny creatures might resolve key issues in the early evolution of animals date to a discovery made in the mid-1970s and then researched and reported in one of the most elegant, but rather sadly underappreciated, series of papers ever published in the history of paleontology: the work of two German scientists, Klaus J. Müller and Dieter Walossek, on the fauna of distinctive upper Cambrian rocks in Sweden, known as Orsten beds. In these layers of limestone concretions, tiny arthropods (mostly larvae of crustaceans) have been preserved by phosphatization in exquisite, three-dimensional detail. The photography and drawings of Walossek and Müller have rarely been equaled in clarity and aesthetic brilliance, and their papers are a delight both to read and to see. (For a good early summary, consult K.J. Müller and D. Walossek, “A remarkable arthropod fauna from the Upper Cambrian ‘Orsten’ of Sweden,” Transactions of the Royal Society of Edinburgh, 1985, volume 76, pages 161–72; for a recent review, see Walossek and Müller, “Cambrian ‘Orsten’-type arthropods and the phylogeny of Crustacea,” in R. A. Fortey and R. H. Thomas, eds., Arthropod Relationships, London: Chapman and Hall, 1997.)
By dissolving the limestone in acetic acid, Walossek and Müller can recover the tiny phosphatized arthropods intact. They have collected more than one hundred thousand specimens following this procedure and have summarized their findings in a recent paper of 1997:
The cuticular surface of these arthropods is still present in full detail, revealing eyes and limbs, hairs and minute bristles, … gland openings, and even cellular patterns and grooves of muscle attachments underneath…. The maximum size of specimens recovered in this type of preservation does not exceed 2 mm.
From this beginning, other paleontologists have proceeded backward in time, and downward in growth from larvae to early embryonic stages containing just a few cells. In 1994, Xi-guang Zhang and Brian R. Pratt found balls of presumably embryonic cells measuring 0.30 to 0.35 millimeter in length and representing, perhaps, the earliest stages of adult trilobites also found in the same Middle Cambrian strata (Zhang and Pratt, “Middle Cambrian arthropod embryos with blastomeres,” Science, 1994, volume 266, pages 637–38). In 1997, Stefan Bengston and Yue Zhao then reported even earlier phosphatized embryos from basal Cambrian strata in China and Siberia. In an exciting addition to this growing literature, these authors traced a probable growth series, from embryos to tiny near adults, for two entirely different animals: a species from an enigmatic extinct group, t
he conulariids; and a probable segmented worm (Bengston and Zhao, “Fossilized metazoan embryos from the earliest Cambrian,” Science, 1997, volume 277, pages 1645–48).
When such novel technologies first encounter materials from a truly unknown or unsuspected world, genuinely revolutionary conclusions often emerge. In what may well be regarded by subsequent historians as the greatest paleontological discovery of the late twentieth century, Shuhai Xiao, a postdoctoral student in our paleontological program, Yun Zhang of Beijing University, and my colleague, and Shuhai Xiao’s mentor, Andrew H. Knoll, have just reported their discovery of the oldest triploblastic animals, preserved as phosphatized embryos in rocks from southern China estimated at 570 million years in age—and thus even older than the best-preserved Ediacaran faunas, found in strata about 10 million years younger (see Xiao, Zhang, and Knoll, “Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite,” Nature, 1998, volume 391, pages 553–58). These phosphatized fossils include a rich variety of multicellular algae, showing, according to the authors, that “by the time large animals enter the fossil record, the three principal groups of multicellular algae had not only diverged from other protistan [unicellular] stocks but had evolved a surprising degree of the morphological complexity exhibited by living algae.”
Still, given our understandably greater interest in our own animal kingdom, most attention will be riveted upon some smaller and rarer globular fossils, averaging half a millimeter in length, and found phosphatized in the same strata: an exquisite series of earliest embryonic stages, beginning with a single fertilized egg and proceeding through two-cell, four-cell, eight-cell, and sixteen-cell stages to small balls of cells representing slightly later phases of early development. These embryos cannot be assigned to any particular group (as more distinctive later stages have not yet been found), but their identification as earliest stages of triploblastic animals seems secure, both from characteristic features (especially the unchanging overall size of the embryo during these earliest stages, as average cell size decreases to pack more cells into a constant space), and uncanny resemblance to particular traits of living groups. (Several embryologists have told Knoll and colleagues that they would have identified these specimens as embryos of living crustaceans had they not been informed of their truly ancient age!)