Wonderful Life: The Burgess Shale and the Nature of History

by Stephen Jay Gould

  In my recent studies I concluded that the pattern of maximal early breadth is a general characteristic of lineages at several scales and times, not only of major groups at the Cambrian explosion. In fact, we have proposed that this “bottom-heavy” asymmetry may rank among the few natural phenomena imparting a direction to time, thus serving as a rare example of “time’s arrow” (Gould, Gilinsky, and German, 1987; Morris, 1984). In our study, we portrayed evolutionary lineages and taxonomic groups as the traditional “spindle diagrams” of paleontology—read intuitively with the vertical dimension as time, and the width at any time proportional to the number of representatives in the group then living (figure 5.4). These diagrams may be bottom-heavy, top-heavy, or symmetrical (with maximum representation in the middle of the geological range). If bottom-heavy lineages characterize the history of life, then the Burgess pattern has generality across scales (for most of our spindle diagrams portray groups of low taxonomic rank, usually genera within families). If symmetrical lineages predominate, then the shape of diversification gives no direction to time.

  We measure degree of asymmetry by the relative position of the diagram’s center of gravity. This statement may sound like a mouthful, but our measure is intuitive and easy to grasp. Lineages with centers of gravity less than 0.5 (bottom-heavy in our terminology) reach their greatest diversity before their halfway point—that is, they follow the Burgess pattern. Lineages with centers of gravity above 0.5 attain their greatest representation past the halfway point of their geological lifetimes (see figure 5.4).

  5.4. Centers of gravity in paleontological spindle diagrams. (A) A bottom-heavy diagram, with center of gravity less than 0.5. (B) A symmetrical diagram, with center of gravity at 0.5. (C) A top-heavy diagram, with center of gravity greater than 0.5.

  In this way, we surveyed the entire history of marine invertebrate life—708 separate spindle diagrams at the level of genera within families. We found only one pattern of statistically significant departure from symmetry. Lineages that arose early in the history of multicellular life, defined as during the Cambrian or Ordovician periods, have average centers of gravity less than 0.5. Lineages that arose later cannot be distinguished from 0.5 in their mean values. The Burgess pattern is therefore affirmed across all groups of the conventional fossil record for marine invertebrates with hard parts. The early history of multicellular life is marked by a bottom-heavy signature for individual lineages; later times feature symmetrical lineages.

  Moreover, we found the same pattern as a generality for groups in early phases of expansion. The bottom-heavy signature is not an oddity of Cambrian invertebrate life, but a general statement about the nature of evolutionary diversification. For example, mammalian lineages that arose during the Paleocene epoch, the initial period of explosive diversification following the demise of dinosaurs, tend to be bottom-heavy, while lineages arising later are symmetrical.

  We may interpret this bottom-heavy pattern in several ways. I like to think of it as “early experimentation and later standardization.” Major lineages seem able to generate remarkable disparity of anatomical design at the outset of their history—early experimentation. Few of these designs survive an initial decimation, and later diversification occurs only within the restricted anatomical boundaries of these survivor—later standardization. The number of species may continue to increase, and may reach maximal values late in the history of lineages, but these profound diversifications occur within restricted anatomies—nearly a million described species of modern insects, but only three basic arthropod designs today, compared with more than twenty in the Burgess.

  However we interpret this bottom-heavy pattern, it strongly reinforces the case for contingency, and validates the principal theme of this book. First, the basic pattern is a disproof of our standard and comfortable iconography—the cone of increasing diversity. The thrall of this iconography and its underlying conceptual base prevented Walcott from grasping the true extent of Burgess disparity, and has continued to portray the controlling pattern of evolution in a direction opposite to its actual form. Second, maximal initial disparity and later decimation give the broadest possible role to contingency, for if the current taxonomic structure of life records the few fortunate survivors in a lottery of decimation, rather than the end result of progressive diversification by adaptive improvement, then a replay of life’s tape would yield a substantially different set of surviving anatomies and a later history making perfect sense in its own terms but markedly different from the one we know.

  MASS EXTINCTION

  If we could move continuously from the small to the large in inferring the causes of evolution, then Darwinian processes of the here and now might construct the topologies of evolutionary trees by extension. Since Darwin himself read a message of progress, albeit fitfully and ambiguously, in this theme of extrapolation from small to large, any geologically based derailment of this accumulative model would remove the best available argument for predictable advance in the history of life.

  Mass extinctions have been recorded since the dawn of paleontology. These episodes mark the major boundaries of the geological time scale. Yet, two aspects of Darwinian tradition have led paleontologists, until the last decade, to incorporate mass extinctions into the accumulative model. First, one could try, as Darwin himself did, to portray mass extinctions as artifacts of an imperfect fossil record. Rates of dying may have been genuinely high in these times, but the extinctions were probably spread rather evenly over several million years, and only have the appearance of geological simultaneity because most times are not represented by any sediment, and the extended period of extinction may be compressed into a single bedding plane. Second, one could grant that such episodes were especially rapid, but argue that the enhanced stress only “turns up the gain” on Darwinian processes slated to yield progress: if competition in ordinary times gradually precipitates out the best, just think what the incomparably fiercer battles in an immeasurably tougher world might produce. Mass extinction should only accelerate the process of predictable advance.

  The subject of mass extinction has received a new life in excitement, novel ideas, and hard data during the past ten years. The initial stimulant was, of course, Alvarez’s theory of extinction triggered by extraterrestrial impact, but the discussion has moved well beyond errant asteroids to comet showers, putative 26-million-year cycles, and mathematical models for genuine catastrophe. An adequate account of this work would take a book in itself, but I do discern a general theme that can be epitomized in a statement with far-ranging implications: mass extinctions are more frequent, rapid, devastating in magnitude, and distinctively different in effect than we formerly imagined. Mass extinctions, in other words, seem to be genuine disruptions in geological flow, not merely the high points of a continuity. They may result from environmental change at such a rate, and with so drastic a result, that organisms cannot adjust by the usual forces of natural selection. Thus, mass extinctions can derail, undo, and reorient whatever might be accumulating during the “normal” times between.

  The main question raised by mass extinction has always been, Is there any pattern to who gets through and who doesn’t—and if so, what causes the pattern? The most exciting prospect raised by new views on mass extinction holds that the reasons for differential survival are qualitatively different from the causes of success in normal time—thus imparting a distinctive, and perhaps controlling, signature to diversity and disparity in the history of life. Such a distinctively geological, large-scale agent of pattern would disprove the old accumulative model that offered to the doctrine of progress its best remaining hope. Paleontologists are just beginning to study the causal structure of differential survival, and the jury will be out for some time. But we already have strong indications that two models of patterning by mass extinction—I call them the random and the different-rules model—not only make the case for distinctiveness but also greatly strengthen the theme of contingency.

  1. The random mo
del. I need hardly say that if a mass extinction operates like genuine lottery, with each group holding a ticket unrelated to its anatomical virtues, then contingency, and maximal range of possibilities in replaying life’s tape, have been proven. We have some indications that true randomness may play a role. Some of the events are so profound, and the pool of survivors so restricted, that chance fluctuations in small samples may come into play. David M. Raup, for example, has estimated species loss in the Permo-Triassic extinction, the granddaddy of all, at 96 percent. When diversity plummets to 4 percent of its former value, we must entertain the idea that some groups lose by something akin to sheer bad luck.

  In a more direct study, Jablonski (1986) has traced the role in mass extinction of features known either to promote survival or to enhance speciation for marine mollusks in normal times. Jablonski found that none of these factors was beneficial or detrimental to survival in the different conditions of a mass extinction. With respect, at least, to these important causal factors of normal times, mass extinctions preserve or annihilate species at random. Geographic range was about the only factor that Jablonski could correlate with probability of survival—the bigger the area inhabited by a group, the greater its chance of pulling through. Perhaps times are so tough at these moments that the more space you normally occupy, the better your chance of finding someplace to hide.*

  2. The different-rules model. I don’t, myself, believe that true randomness predominates in mass extinctions (though it probably plays some role, particularly in the most profound of the great dyings). I think that most survivors get through for specific reasons, often a complex set of causes. But I also strongly suspect that in a great majority of cases, the traits that enhance survival during an extinction do so in ways that are incidental and unrelated to the causes of their evolution in the first place.

  This contention is the centerpiece of the different-rules model. Animals evolve their sizes, shapes, and physiologies under natural selection in normal times, and for specifiable reasons (usually involving adaptive advantage). Along comes a mass extinction, with its “different rules” for survival. Under the new regulations, the very best of your traits, the source of your previous flourishing, may now be your death knell. A trait with no previous significance, one that had just hitchhiked along for the developmental ride as a side consequence of another adaptation, may now hold the key to your survival. There can be no causal correlation in principle between the reasons for evolving a feature and its role in survival under the new rules. (The key issue for testing this model therefore lies in establishing that new rules do, indeed, prevail.) A species, after all, cannot evolve structures with a view to their potential usefulness millions of years down the road—unless our general ideas about causality are markedly awry, and the future can control the present.

  We probably owe our own existence to such good fortune. Small animals, for reasons not well understood, seem to have an edge in most mass extinctions, particularly in the Cretaceous event that wiped out remaining dinosaurs. Mammals may therefore have survived that great dying primarily because they were small, not because they embodied any intrinsic anatomical virtues relative to dinosaurs, now doomed by their size. And mammals were surely not small because they had sensed some future advantage; they had probably remained small for a reason that would be judged negatively in normal time—because dinosaurs dominated environments for large terrestrial vertebrates, and incumbents have advantages in nature as well as in politics.

  Kitchell, Clark, and Gombos (1986) have worked out an interesting example based on diatoms, single-celled plants of the oceanic plankton. Paleontologists have long wondered why diatoms came through the Cretaceous extinction relatively unscathed, while most other elements of the plankton crashed. For growth and reproduction, diatoms rely upon the seasonal availability of nutrients rising to the surface from deeper waters in zones of upwelling. (These episodes of upwelling unleash so-called diatom “blooms.”) When these nutrients are depleted, diatoms can change their form to a “resting spore,” essentially shut down their metabolism and sink to deeper waters. A return of nutrients will terminate this period of dormancy. Kitchell and her colleagues attribute the success of diatoms in the Cretaceous extinction to an incidental side consequence of dormancy. The resting spores evolved as a strategy for dealing with predictable and seasonal fluctuations in nutrients, clearly not for environmental catastrophes of mass extinction. But the ability to hunker down in a dormant state may have saved the diatoms under the different rules of mass extinction, especially if the “nuclear winter” model proves valid for the Cretaceous event—for darkness would cut off photosynthesis and propagate extinctions up and down a food chain ultimately dependent upon primary production, while diatoms might ride out the dark storm as resting spores below the photic zone.

  The different-rules model therefore fractures the causal continuity that Darwin envisaged between reasons for success within local populations and the causes of survival and proliferation through long stretches of geological time. Hence, this model strongly promotes the role of contingency, viewed primarily as unpredictability, in evolution. If long-term success depends upon incidental aspects of features evolved for different reasons, then how could we possibly know, if we rewound life’s tape to a distant past, which groups were destined for success? Their performance and evolution during our observation would not be relevant. We might base some guesses on incidental features that usually imply survival through a mass extinction, but how could we do so with any confidence? In an important sense, these crucial features don’t even exist until the different rules of mass extinction make their incidental effects important—for extreme stress may be needed to “key up” these features, and animals may never experience such conditions during normal times. And how can we know, in our rich and multifarious world, what the next episode of mass extinction, somewhere down the road, will require? Unpredictability must rule if geological longevity depends upon lucky side consequences of features evolved for other reasons.

  I particularly welcome this demonstration that several general principles of large-scale evolution promote the importance of contingency. The generalization—on the bottom-heaviness of lineages and the properties of mass extinction—are the stuff of traditional nonhistorical science, the style that usually opposes, or at least downgrades, a historical principle like contingency. This reinforcement is a happy situation for scientific pluralism. I do not relish the idea of defending historical science by building a bunker and fighting for respect and self-determination. Better to move forward in partnership; general patterns of evolution imply the unpredictability of specific outcomes.

  SEVEN POSSIBLE WORLDS

  The collapse of the cone and the ladder opens the floodgates to alternative worlds that didn’t emerge, but might have arisen with slight and sensible changes in some early events. These unrealized universes would have been every bit as ordered and explainable as the world we know, but ever so different in ways that we can never specify in detail. The enumeration of unrealized worlds is a parlor game without end, for who can count the possibilities? The universe is not so tightly interconnected that the fall of a petal disrupts a distant star, whatever our poets sing. But most quirky changes of topography or environment, most appearances and disappearances of groups (if not of single species), can irrevocably alter the pathways of life in substantial ways. The playground of contingency is immeasurable. Let us consider just seven alternative scenarios, arranged in chronological order to home in on the biological object that most excites our parochial fancy—Homo sapiens.

  EVOLUTION OF THE EUKARYOTIC CELL

  Life arose at least 3.5 billion years ago, about as soon as the earth became cool enough for stability of the chief chemical components. (I do not, by the way, view the origin of life itself as a chancy or unpredictable event. I suspect that given the composition of early atmospheres and oceans, life’s origin was a chemical necessity. Contingency arises later, when historical complexity enters
the picture of evolution.)

  With respect to the old belief in steady progress, nothing could be stranger than the early evolution of life—for nothing much happened for ever so long. The oldest fossils are prokaryotic cells some 3.5 billion years old (see pages 57–58). The fossil record of this time also includes the highest form of macroscopic complexity evolved by these prokaryote—stromatolites. These are layers of sediment trapped and bound by prokaryotic cells. The layers may pile up one atop the other, as tides bury and re-form the mat—and the whole structure may come to resemble a cabbage in cross section (also in size).

  Stromatolites and their prokaryotic builders dominated the fossil record throughout the world for more than 2 billion years. The first eukaryotic cells (the complex textbook variety, complete with nucleus and numerous structures of the cytoplasm) appeared some 1.4 billion years ago. The conventional argument holds that eukaryotic cells are a prerequisite for multicellular complexity, if only because sexual reproduction required paired chromosomes, and only sex can supply the variation that natural selection needs as raw material for further complexity.

  But multicellular animals did not arise soon after the origin of eukaryotic cells; they first appeared just before the Cambrian explosion some 570 million years ago. Hence, a good deal more than half the history of life is a story of prokaryotic cells alone, and only the last one-sixth of life’s time on earth has included multicellular animals.