The Lying Stones of Marrakech (51 page)

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, the 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!)

Elso Barghoorn, Knoll's thesis adviser, opened up the world of earliest life by discovering that bacteria could be preserved in chert. Now, a full generation later, Knoll and colleagues have penetrated the realm of earliest known animals of modern design by accessing a new domain where phosphatization preserves minute embryonic stages, but no known process of fossilization can reliably render potentially larger phases of growth. When I consider the cascade of knowledge that proceeded from Barghoorn's first report of Precambrian bacteria to our current record spanning three billion Precambrian years and hundreds of recorded forms, I can only conclude that the discovery of Xiao, Zhang, and Knoll places us at a gateway of equal promise for reconstructing the earliest history of modern animals, before their overt evolutionary burst to large size and greatly increased anatomical variety in the subsequent Cambrian explosion. If we can thereby gain any insight into the greatest of all mysteries surrounding
the early evolution of animals—the causes of both the anatomical explosion itself and the “turning off” of evolutionary fecundity for generating new phyla thereafter—then paleontology will shake hands with evolutionary theory in the finest merger of talents ever applied to the resolution of a historical enigma.

A closing and more general commentary may help to set a context of both humility and excitement at the threshold of this new quest. First, we might be able to coordinate the direct evidence of fossils with a potentially powerful indirect method for judging the times of origin and branching for major animal groups: the measurement of relative degrees of detailed genetic similarity among living representatives of diverse animal phyla. Such measurements can be made with great precision upon large masses of data, but firm conclusions do not always follow because various genes evolve at different rates that also maintain no constancy over time—and most methods applied so far have made simplifying (and probably unjustified) assumptions about relatively even ticking of supposed molecular clocks.

For example, in a paper that received much attention upon publication in 1996, G. A. Wray, J. S. Levinton, and L. H. Shapiro used differences in the molecular sequences of seven genes in living representatives of major phyla to derive an estimate of roughly 1.2 billion years for the divergence time between chordates (our phylum) and the three great groups on the other major genealogical branch of animals (arthropods, annelids, and mollusks), and 1.0 billion years for the later divergence of chordates from the more closely related phylum of echinoderms (Wray, Levinton, and Shapiro, “Molecular evidence for deep Precambrian divergences among metazoan phyla,”
Science
, 1996, volume 274, pages 568–73).

This paper sowed a great deal of unnecessary confusion when several uncomprehending journalistic reports, and a few careless statements by the authors, raised the old and false canard that such an early branching time for animal phyla disproves the reality of the Cambrian explosion by rendering this apparent burst of diversity as the artifact of an imperfect fossil record (signifying, perhaps, only the invention of hard parts, rather than any acceleration of anatomical innovation). For example, Wray et al. write: “Our results cast doubt on the prevailing notion that the animal phyla diverged explosively during the Cambrian or late Vendian [Ediacaran times], and instead suggest that there was an extended period of divergence … commencing about a billion years ago.”

But such statements confuse the vital distinction, in both evolutionary theory and actual results, between times of initial branching and subsequent rates of anatomical innovation or evolutionary change in general. Even the most
vociferous advocates of a genuine Cambrian explosion have never argued that this period of rapid anatomical diversification marks the moment of origin for animal phyla—if only because we all acknowledged the evidence for Precambrian tracks and trails of triploblasts even before the recent discovery of embryos. Nor do these same vociferous advocates imagine that only one wormlike species crawled across the great Cambrian divide to serve as an immediate common ancestor for all modern phyla. In fact, I can't imagine why anyone would care (for adjudicating the reality of the explosion, though one would care a great deal for discussions of some other evolutionary issues) whether one wormlike species carrying the ancestry of all later animals, or ten similar wormlike species already representing the lineages of ten subsequent phyla, crossed this great divide from an earlier Precambrian history. The Cambrian explosion represents a claim for a rapid spurt of
anatomical innovation
within the animal kingdom, not an argument about times
of genealogical divergence
.

The following example should clarify the fundamental distinction between times of genealogical splitting and rates of change. Both rhinoceroses and horses may have evolved from the genus
Hyracotherium
(formerly called
Eohippus)
. A visitor to the Eocene earth about 50 million years ago might determine that the basic split had already occurred. He might be able to identify one species of
Hyracotherium
as the ancestor of all later horses, and another species of the same genus as the progenitor of all subsequent rhinos. But this visitor would be laughed to justified scorn if he then argued that later divergences between horses and rhinos must be illusory because the two lineages had already split. After all, the two Eocene species looked like kissing cousins (as evidenced by their placement in the same genus), and only gained their later status as progenitors of highly distinct lineages by virtue of a subsequent history, utterly unknowable at the time of splitting. Similarly, if ten nearly identical wormlike forms (the analogs of the two
Hyracotherium
species) crossed the Cambrian boundary, but only evolved the anatomical distinctions of great phyla during the subsequent explosion, then the explosion remains as real, and as vitally important for life's history, as any advocate has ever averred.