The Lying Stones of Marrakech
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.
This crucial distinction has been recognized by most commentators on the work of Wray et al. Geerat J. Vermeij, in his direct evaluation (Science, 1996, page 526), wrote that “this new work in no way diminishes the significance of the Vendian-Cambrian revolution.” Fortey, Briggs, and Wills added (BioEssays, 1997, page 433) that “there is, of course, no necessary correspondence between morphology and genomic change.” In any case, a later publication by Ayala, Rzhetsky, and Ayala (Proceedings of the National Academy of Sciences, 1998, volume 95, pages 606–11) presents a powerful rebuttal to Wray et al.’s specific conclusions. By correcting statistical errors and unwarranted assumptions, and by adding data for twelve additional genes, these authors provide a very different estimate for initial diversification in late Precambrian times: about 670 million years ago for the split of chordates from the line of arthropods, annelids, and mollusks; and 600 million years for the later divergence of chordates from echinoderms.
Haeckel’s theoretical ancestral animal (left) compared with a Precambrian fossil embryo (below).
We are left, of course, with a key mystery (among many others): where are Precambrian adult triploblasts “hiding,” now that we have discovered their embryos? An old suggestion, first advanced in the 1870s in the prolific and often highly speculative work of the German biologist Ernst Haeckel (who was nonetheless outstandingly right far more often than random guesswork would allow), held that Precambrian animals had evolved as tiny forms not much larger than, or very different from, modern embryos—and would therefore be very hard to find as fossils. (The similarity between Haeckel’s hypothetical ancestors and Xiao, Zhang, and Knoll’s actual embryos is almost eerie—see figures on pages 323 and 330.) Moreover, E. H. Davidson, K.J. Peterson, and R. A. Cameron (Science, 1995, volume 270, pages 1319–25) have made a powerful case, based on genetic and developmental arguments, that Precambrian animals did originate at tiny sizes, and that the subsequent Cambrian explosion featured the evolution of novel embryological mechanisms for substantially increasing cell number and body size, accompanied by consequent potential for greatly enhanced anatomical innovation. If Haeckel’s old argument, buttressed by Davidson’s new concepts and data, has validity, we then gain genuine hope, even realistic expectation, that Precambrian adult triploblasts may soon be discovered, for such animals will be small enough to
be preserved by phosphatization.
As a final point, this developing scenario for the early history of animals might foster humility and generate respect for the complexity of evolutionary pathways. To make the obvious analogy: we used to regard the triumph of “superior” mammals over “antediluvian” dinosaurs as an inevitable consequence of progressive evolution. We now realize that mammals originated at the same time as dinosaurs and then lived for more than 100 million years as marginal, small-bodied creatures in the nooks and crannies of a dinosaur’s world. Moreover, mammals would never have expanded to dominate terrestrial ecosystems (and humans would surely never have evolved) without the supreme good fortune (for us) of a catastrophic extraterrestrial impact that, for some set of unknown reasons, eliminated dinosaurs and gave mammals an unanticipated opportunity.
Does this essay’s tale from an earlier time—Ediacaran “primitives” versus contemporary Precambrian ancestors of modern animals—differ in any substantial way? We now know (from the evidence of Xiao, Zhang, and Knoll’s embryos) that animals of modern design had already originated before the Ediacara fauna evolved into full bloom. Yet “primitive” Ediacara dominated the world of animal life, perhaps for 100 million years, while modern triploblasts waited in the proverbial wings, perhaps as tiny animals of embryonic size, living in nooks and crannies left over by much larger Ediacaran dominants. Only a mass extinction of unknown cause, a great dying that wiped out Ediacara and initiated the Cambrian transition 543 million years ago, gave modern triploblasts an opportunity to shine—and so we have.
In evolution, as well as in politics, incumbency offers such powerful advantages that even a putatively more competent group may be forced into a long period of watchful waiting, always hoping that an external stroke of good luck will finally grant an opportunity for picking up the reins of power. If fortune continues to smile, the new regime may eventually gain enough confidence to invent a comforting and commanding mythology about the inevitability of its necessary rise to dominance by gradually growing better and better—every day and in every way.
22
The
Paradox of the
Visibly Irrelevant
AN ODD PRINCIPLE OF HUMAN PSYCHOLOGY, WELL known and exploited by the full panoply of prevaricators, from charming barkers like Barnum to evil demagogues like Goebbels, holds that even the silliest of lies can win credibility by constant repetition. In current American parlance, these proclamations of “truth” by Xeroxing fall into the fascinating domain of “urban legends.”
My favorite bit of nonsense in this category intrudes upon me daily, and in very large type, thanks to a current billboard ad campaign by a company that will remain nameless. The latest version proclaims: “Scientists say we use 10 percent of our brains. That’s way too much.” Just about everyone regards the “truth” of this proclamation as obvious and incontrovertible—though you might still start a barroom fight over whether the correct figure should be 10, 15, or 20 percent. (I have heard all three asserted with utter confidence.) But this particular legend can only be judged as even worse than false: for the statement is truly meaningless and nonsensical. What do we mean by “90 percent unused”? What is all this superfluous tissue doing? The claim, in any case, can have no meaning until we develop an adequate theory about how the brain works. For now, we don’t even have a satisfactory account for the neurological basis of memory and its storage—surely the sine qua non for formulating any sensible notion about unused percentages of brain matter! (I think that the legend developed because we rightly sense that we ought to be behaving with far more intelligence than we seem willing to muster—and the pseudoquantification of the urban legend acts as a falsely rigorous version of this legitimate but vague feeling.)
In my field of evolutionary biology, the most prominent urban legend—another “truth” known by “everyone”—holds that evolution may well be the way of the world, but one has to accept the idea with a dose of faith because the process occurs far too slowly to yield any observable result in a human lifetime. Thus, we can document evolution from the fossil record and infer the process from the taxonomic relationships of living species, but we cannot see evolution on human timescales “in the wild.”
In fairness, we professionals must shoulder some blame for this utterly false impression about evolution’s invisibility in the here and now of everyday human life. Darwin himself—though he knew and emphasized many cases of substantial change in human time (including the development of breeds in his beloved pigeons)—tended to wax eloquent about the inexorable and stately slowness of natural evolution. In a famous passage from The Origin of Species, he even devised a striking metaphor about clocks to underscore the usual invisibility:
It may be said that natural selection is daily and hourly scrutinizing, throughout the world, every variation, even the slightest; rejecting that which is bad, preserving and adding up all that is good; silently and invisibly working…. We see nothing of these slow changes in progress until the hand of time has marked the long lapse of ages.
Nonetheless, the claim that evolution must be too slow to see can only rank as an urban legend—though not a completely harmless tale in this case, for our creationist incubi can then use the fallacy as an argument against evolution at any scale, and many folks take them seriously because they just “know” that evolution can never be seen in the immediate here and now. In fact, a precisely opposite situation actually prevails: biologists have documented a veritable glut of cases for rapid and eminently measurable evolution on timescales of years and decades.
However, this plethora of documents—while important for itself, and surely valid as a general confirmation for the proposition that organisms evolve—teaches us rather little about rates and patterns of evolution at the geological scales that build the history and taxonomic structure of life. The situation is wonderfully ironic—a point that I have tried to capture in the title of this article. The urban legend holds that evolution is too slow to document in palpable human lifetimes. The opposite truth has affirmed innumerable cases of measurable evolution at this minimal scale—but to be visible at all over so short a span, evolution must be far too rapid (and transient) to serve as the basis for major transformations in geological time. Hence the “paradox of the visibly irrelevant”—or, “if you can see it at all, it’s too fast to matter in the long run!”
Our best and most numerous cases have been documented for the dominant and most evolutionarily active organisms on our planet—bacteria. In the most impressive of recent examples, Richard E. Lenski and Michael Travisano (Proceedings of the National Academy of Sciences, 1994, volume 91, pages 6808–14) monitored evolutionary change for ten thousand generations in twelve laboratory populations of the common human gut bacterium Escherichia coli. By placing all twelve populations in identical environments, they could study evolution under ideal experimental conditions of replication—a rarity for the complex and unique events of evolutionary transformation in nature. In a fascinating set of results, they found that each population reacted and changed differently, even within an environment made as identical as human observers know how to do. Yet Lenski and Travisano did observe some important and repeated patterns within the diversity. For example, each population increased rapidly in average cell size for the first two thousand generations or so, but then remained nearly stable for the last five thousand generations.
A cynic might still reply: fine, I’ll grant you substantial observable evolution in the frenzied little world of bacteria, where enormous populations and new generations every hour allow you to monitor ten thousand episodes of natural selection in a manageable time. But a similar “experiment” would consume thousands of years for multicellular organisms that measure generations in years or decades rather than minutes or hours. So we may still maintain that evolution cannot be observed in the big, fat, furry, sexually reproducing organisms that serve as the prototype for “life” in ordinary human consciousness. (A reverse cynic would then re
reply that bacteria truly dominate life, and that vertebrates only represent a latecoming side issue in the full story of evolution, however falsely promoted to centrality by our own parochial focus. But we must leave this deep issue to another time.)
I dedicate this essay to illustrating our cynic’s error. Bacteria may provide our best and most consistent cases for obvious reasons, but measurable (and substantial) evolution has also, and often, been documented in vertebrates and other complex multicellular organisms. The classic cases have not exactly been hiding their light under a bushel, so I do wonder why the urban legend of evolution’s invisibility persists with such strength. Perhaps the firmest and most elegant examples involve a group of organisms named to commemorate our standard-bearer himself—Darwin’s finches of the Galápagos Islands, where my colleagues Peter and Rosemary Grant have spent many years documenting fine-scale evolution in such adaptively important features as size and strength of the bill (a key to the mechanics of feeding), as rapid climatic changes force an alteration of food preferences. This work formed the basis for Jonathan Weiner’s excellent book, The Beak of the Finch—so the story has certainly been well and prominently reported in both the technical and popular press.