Wonderful Life: The Burgess Shale and the Nature of History

by Stephen Jay Gould

  This conventional view has been assumed in essentially all the Burgess literature—not as an active argument explicitly supported by Burgess evidence, but as the dues that we all properly pay to traditional explanations when we make a side comment on a subject that has not engaged our primary attention. “Less severe competition” has been the watchword of interpretation. Whittington has written, for example: Conway Morris has also supported this traditional view. He wrote to me, in response to my defense of unconventional alternatives to follow: “I think that ecological conditions may have been sufficient to account for the observed morphological diversity.… Thus, perhaps the Cambrian explosion can be regarded as one huge example of ‘ecological release’” (letter of December 18, 1985).

  Presumably there was abundant food and space in the varied marine environments which were being occupied initially by these new animals, and competition was less severe than in succeeding periods. In these circumstances diverse combinations of characters may have been possible, as new ways of sensing the surroundings, of obtaining food, of moving about, of forming hard parts, and of behavior (e.g. predation and scavenging) were being evolved. Thus may have arisen strange animals, the remains of some of which we see in the Burgess Shale, and which do not fit into our classifications (1981b, p. 82).

  This argument is simply too sensible to dismiss. I haven’t the slightest doubt that the “empty ecological barrel” was a major contributor to Burgess disparity, and that such an explosion could never have occurred in a well-filled world. But I don’t for a minute believe that external ecology will explain the entire phenomenon. My main defense for this gut feeling relies upon scale. The Cambrian explosion was too big, too different, and too exclusive. I just can’t accept that if organisms always have the potential for diversification of this kind—while only the odd ecology of the Lower Cambrian ever permitted its realization—never, not even once, has a new phylum arisen since Burgess times. Yes, the world has not been so empty again, but some local situations have made a decent approach. What about new land risen from the sea? What about island continents when first invaded by new groups? These are not large barrels, but they are at least fair-to-middling bowls. I have to believe that organisms as well as environments were different in Cambrian times, that the explosion and later quiescence owes as much to a change in organic potential as to an altered ecological status.

  Ideas about organisms playing such active roles in channeling their own directions of evolutionary change (not merely supplying raw material for the motor of natural selection) have recently grown in popularity, as the strict forms of conventional Darwinism yield their exclusive sway, while retaining their large and proper influence. Evolution is a dialectic of inside and outside, not ecology pushing malleable structure to a set of adaptive positions in a well-oiled world. Two major theories, described in the next two sections, grant a more active role to organic structure.

  2. A directional history for genetic systems. In the traditional Darwinian view, morphologies have histories that constrain their future, but genetic material does not “age.” Differences in rates and patterns of change are responses of an unchanging material substrate (genes and their actions) to variations in environment that reset the pressures of natural selection.

  But perhaps genetic systems do “age” in the sense of becoming “less forgiving of major restructuring” (to cite a phrase from J. W. Valentine, who has thought long and deeply about this problem). Perhaps modern organisms could not spawn a rapid array of fundamentally new designs, no matter what the ecological opportunity.

  I have no profound suggestions about the potential nature of this genetic “aging,” but simply ask that we consider such an alternative. Our exploding knowledge of development and the mechanics of genetic action should provide, within a decade, the facts and ideas to flesh out this conception. Valentine mentions some possibilities. Were Cambrian genomes simpler and more flexible? Has the evolution of multiple copies for many genes, copies that then diverge into a range of related functions, tied up genomes into webs of interaction not easily broken? Did early genes have fewer interactions with others? Did ancient organisms develop with more direct translation of gene to product, permitting such creatures to interchange and alter their parts separately? Most important, do increased complexity and stereotypy of development from egg to adult put a brake upon potential changes of great magnitude? We cannot, for now, go much beyond such crude and preliminary suggestions.

  But I can present a good argument against the usual reason for dismissing such ideas in favor of conventional control by external environment. When evolutionists observe that several unrelated lineages react in the same way at the same time, they usually assume that some force external to the genetics of organisms has provoked the common response (for the genetic systems are too unlike, and a similar push from outside seems the only plausible common cause). We have always viewed the creatures that made the Cambrian explosion as unrelated in just this profound way. After all, they include representatives of nearly all modern phyla, and what could be more different, one from the other, than a trilobite, a snail, a brachiopod, and an echinoderm? These morphological designs were as distinct in the Cambrian as they are today, so we assume that the genetic systems were equally unlike—and that the common evolutionary vigor of all groups must therefore record the external push of ecological opportunity.

  But this argument assumes the old view of a long, invisible Precambrian history for creatures that evolved skeletons during the Cambrian explosion. The discovery of the Precambrian Ediacara fauna, with the strong possibility that this first multicellular assemblage may not be ancestral to modern groups (see pages 312–13), suggests that all Cambrian animals, despite their disparity of form, may have diverged not long before from a late Precambrian common ancestor. If so—if they had been separate for only a short time—all Cambrian animals may have carried a very similar genetic mechanism by virtue of their strictly limited time of separate life. No ties bind so strongly as the links of inheritance. In other words, the similar response of Cambrian organisms may reflect the homology of a genetic system still largely held in common, and still highly flexible, not only the analogy of response to a common external push. Of course, life needed the external push of ecological opportunity, but its ability to respond may have marked a shared genetic heritage, now dissipated.

  3. Early diversification and later locking as a property of systems. My friend Stu Kauffman of the University of Pennsylvania has developed a model to demonstrate that the Burgess pattern of rapid, maximal disparity followed by later decimation is a general property of systems, explicable without a special hypothesis about early relaxed competition or a directional history for genetic material.

  Consider the following metaphor. The earthly stage of life is a complex landscape with thousands of peaks, each a different height. The higher the peak, the greater the success—measured as selective value, morphological complexity, or however you choose—of the organisms on it. Sprinkle a few beginning organisms at random onto the peaks of this landscape and allow them to multiply and to change position. Changes can be large or small, but the small shifts do not concern us here, for they only permit organisms to mount higher on their particular peak and do not produce new body plans. The opportunity for new body plans arises with the rarer large jumps. We define large jumps as those that take an organism so far away from its former home that the new landscape is entirely uncorrelated with the old. Long jumps are enormously risky, but yield great reward for rare success. If you land on a peak higher than your previous home, you thrive and diversify, if you land on a lower peak or in a valley, you’re gone.

  Now we ask, How often does a large jump yield a successful outcome (a new body plan)? Kauffman proves that the probability of success is quite high at first, but drops precipitously and soon reaches an effective zero—just like the history of life. This pattern matches our intuitions. The first few species are placed on the landscape at random. This means t
hat, on average, half the peaks are higher, half lower, than the initial homes. Therefore, the first long jump has a roughly 50 percent chance of success. But now the triumphant species stands on a higher peak—and the percentage of still loftier peaks has decreased. After a few successful jumps, not many higher peaks remain unoccupied, and the probability of being able to move at all drops precipitously. In fact, if long jumps occur fairly often, all the high peaks will be occupied pretty early in the game, and no one has anyplace to go. So the victors dig in and evolve developmental systems so tied to their peaks that they couldn’t change even if the opportunity arose later. Thereafter, all they can do is hang tough on their peak or die. It’s a difficult world, and many meet the latter fate, not because ecology is a Darwinian log packed tight with wedges, but because even random extinctions leave spaces now inaccessible to everyone.

  Kauffman could even quantify the precipitous decline of possibilities for successful jumps. The waiting time to the next higher peak doubles after each successful jump. (Stu told me that a mountain of athletic data shows that when a record is fractured, the average time to the next break doubles.) If your first success needed only two tries on average, your tenth will require more than a thousand. Soon you have effectively no chance of ever getting anywhere better, for geological time may be long, but it is not infinite.

  THE DECIMATION OF THE BURGESS FAUNA

  We need no more than the descriptive pattern of Burgess disparity and later decimation to impose a major reform upon our traditional view of life. For the new iconography (see figure 3.72) not only alters but thoroughly inverts the conventional cone of increasing diversity. Instead of a narrow beginning and a constantly expanding upward range, multicellular life reaches its maximal scope at the start, while later decimation leaves only a few surviving designs.

  But the inverted iconography, however notable, does not have revolutionary impact by itself because it does not exclude the possibility of a fallback to conventionality. Remember what is at stake! Our most precious hope for the history of life, a hope that we would relinquish with greatest reluctance, involves the concepts of progress and predictability. Since the human mind arose so late, and therefore threatens to demand interpretation as an accidental afterthought in a quirky evolutionary play, we are incited to dig in our heels all the harder and to postulate that all previous life followed a sensible order implying the eventual rise of consciousness. The greatest threat lies in a history of numerous possibilities, each sensible in itself after the fact, but each utterly unpredictable at the outset—and with only one (or a very few) roads leading to anything like our exalted state.

  Burgess disparity and later decimation is a worst-case nightmare for this hope of inevitable order. If life started with a handful of simple models and then moved upward, any replay from the initial handful would follow the same basic course, however different the details. But if life started with all its models present, and constructed a later history from just a few survivors, then we face a disturbing possibility. Suppose that only a few will prevail, but all have an equal chance. The history of any surviving set is sensible, but each leads to a world thoroughly different from any other. If the human mind is a product of only one such set, then we may not be randomly evolved in the sense of coin flipping, but our origin is the product of massive historical contingency, and we would probably never arise again even if life’s tape could be replayed a thousand times.

  But we can wake up from this nightmare—with a simple and obvious conventional argument. Granted, massive extinction occurred and only a few original designs survived. But we need not assume that the extinction was a crap shoot. Suppose that survivors prevailed for cause. The early Cambrian was an era of experimentation. Let a bunch of engineers tinker, and most results don’t work worth a damn: the Burgess losers were destined for extinction by faulty anatomical construction. The winners were best adapted and assured of survival by their Darwinian edge. What does it matter if the early Cambrian threw up a hundred possibilities, or a thousand? If only half a dozen worked well enough to prevail in a tough world, then these six would form the rootstocks for all later life no matter how many times we replayed the tape.

  This idea of survival for cause based on anatomical deftness or complexity—“superior competitive ability” in the jargon—has been the favored explanation, virtually unchallenged, for the reduction of Burgess disparity, and indeed for all episodes of extinction in the history of life. This traditional interpretation is tightly linked with the conventional view for the origin of Burgess disparity as a filling of the empty ecological barrel. An empty barrel is a forgiving place. It contains so much space that even a clap-trap disaster of anatomical design can hunker down in a cranny and hang on without facing competition from the big boys of superior anatomy. But the party is soon over. The barrel fills, and everyone is thrown into the maelstrom of Darwinian competition. In this “war of all against all,” the inefficient survivors from gentler times soon make their permanent exit. Only the powerful gladiators win. Thumbs up for good anatomy!

  You will read this interpretation in textbooks, in articles of science magazines, even in the Yoho National Park Highline, the official newsletter for the home of the Burgess Shale (1987 edition). Under the headline “Yoho’s Fossils Have World Significance,” we are told: “The first animals moved into the environment devoid of competition. Later, more efficient life forms held sway only to be supplanted again and again as changing conditions and evolution took its course.” And when, in 1988, Parks Canada put out the first tourist brochure for its nation’s most famous fossils (“Animals of the Burgess Shale”), they wrote that all creatures outside the bounds of modern phyla (the weird wonders of my text) “appear to have been evolutionary dead ends, destined to be replaced by better-adapted or more efficient organisms.”

  Whittington and colleagues did not, until recently, challenge this comforting view. It makes too much sense. For example, in the summary comments of his monograph on Wiwaxia, Conway Morris explicitly linked the two traditional scenarios—barrel filling as a cause of disparity followed by stringent competition as the source of later extinction:

  It may be that diversification is simply a reflection of the availability of an almost empty ecospace with low levels of competition permitting the evolution of a wide variety of bodyplans, only some of which survived in the increasingly competitive environments through geological time (1985, p. 570).

  Briggs made the same point for a French popular audience:

  Perhaps this [disparity] is the result of an absence of competition before all the ecological niches of Cambrian seas were filled. Most of these arthropods rapidly became extinct, no doubt because the least well adapted animals were replaced by others that were better adapted (1985, p. 348).*

  Whittington also made the almost automatic equation between survival and adaptive superiority:

  The subsequent eliminations among such a plethora of metazoans, and the radiations of the forms that were best adapted, may have resulted in the emergence of what we recognize in retrospect as phyla (1980, p. 146).

  Conway Morris and Whittington put the matter most directly in an article for Scientific American—probably the best-read source on the Burgess Shale:

  Many Cambrian animals seem to be pioneering experiments by various metazoan groups, destined to be supplanted in due course by organisms that are better adapted. The trend after the Cambrian radiation appears to be the success and the enrichment in the numbers of species of a relatively few groups at the expense of the extinction of many other groups (1979, p. 133).

  Words have subtle power. Phrases that we intend as descriptions betray our notions of cause and ultimate meaning. I suspect that Simon and Harry thought they were only delineating a pattern in this passage, but consider the weight of such phrases as “destined to be supplanted” and “at the expense of.” Yes, most died and some proliferated. Our earth has always worked on the old principle that many are called and few chosen. But the
mere pattern of life and death offers no evidence that survivors directly vanquished the losers. The sources of victory are as varied and mysterious as the four phenomena proclaimed so wonderful that we know them not (Proverbs 30:19)—the way of an eagle in the air, the way of a serpent upon a rock, the way of a ship in the midst of the sea, and the way of a man with a maid.

  Arguments that propose adaptive superiority as the basis for survival risk the classic error of circular reasoning. Survival is the phenomenon to be explained, not the proof, ipso facto, that those who survived were “better adapted” than those who died. This issue has been kicking around the courtyards of Darwinian theory for more than a century. It even has a name—the “tautology argument.” Critics claim that our motto “survival of the fittest” is a meaningless tautology because fitness is defined by survival, and the definition of natural selection reduces to an empty “survival of those who survive.”

  Creationists have even been known to trot out this argument as a supposed disproof of evolution (Bethell, 1976; see my response in Gould, 1977)—as if more than a century of data could come crashing down through a schoolboy error in syllogistic logic. In fact, the supposed problem has an easy resolution, one that Darwin himself recognized and presented. Fitness—in this context, superior adaptation—cannot be defined after the fact by survival, but must be predictable before the challenge by an analysis of form, physiology, or behavior. As Darwin argued, the deer that should run faster and longer (as indicated by an analysis of bones, joints, and muscles) ought to survive better in a world of dangerous predators. Better survival is a prediction to be tested, not a definition of adaptation.