Wonderful Life: The Burgess Shale and the Nature of History (37 page)

Hou and colleagues describe a rich and well-preserved assemblage, including priapulid and annelid worms, several bivalved arthropods, and three new genera with “merostomoid” body form (Hou, 1987a, 1987b, and 1987c; Sun and Hou, 1987a and 1987b; Hou and Sun, 1988).

The Burgess phenomenon, then, goes right back to the beginning of the Cambrian explosion. In a preliminary report, based on admittedly uncertain dating, Dzik and Lendzion (1988) describe a creature like
Anomalocaris
and a soft-bodied trilobite from Eastern European strata
below
the first appearance of ordinary trilobites. We can no longer doubt that Walcott found products of the Cambrian explosion itself in his slightly later strata of British Columbia. Burgess disparity is astounding enough for a time just 30 to 40 million years after the beginning of the Cambrian. But we cannot even view the Burgess range as accumulating steadily during this relatively short period. The main burst occurred well down in the Lower Cambrian—and probably produced the full Burgess range, if the Chinese fauna proves to be as rich as preliminary accounts suggest. The Burgess Shale represents the slightly later period of stabilization for the products of the Cambrian explosion. But what caused the subsequent decimation, and the consequent pattern of modern life, marked by great gaps between islands of extensive diversity within restricted anatomical designs?

The Burgess revision poses two great problems about the history of life. These are symmetrically disposed about the Burgess fauna itself, one before and one after: First, how, especially in the light of our usual views about evolution as a stately phenomenon, could such disparity arise so quickly? And second, if modern life is a product of Burgess decimation, what aspects of anatomy, what attributes of function, what environmental changes, set the pattern of who would win and who would lose? In short, first the origin, second the differential survival and propagation.

In many ways, the first is a juicier problem for evolutionary theory. How in heaven’s name could such disparity have arisen in the first place, whatever the later fortunes of its exemplars? But the second problem is the subject of this book, for the decimation of the Burgess fauna raises the fundamental question that I wish to address about the nature of history. My key experiment in replaying the tape of life begins with the Burgess fauna intact and asks whether an independent act of decimation from the same starting point would yield anything like the same groups and the same history that our planet has witnessed since the Burgess maximum in organic disparity. Hence, I shall shamelessly bypass the first problem—but not without presenting a brief summary of possible explanations, if only because one aspect of the potential solution does bear crucially on the second problem of differential fate.

Three major kinds of evolutionary explanation are available for the explosion that led to Burgess disparity. The first is conventional, and has been assumed—largely
faute de mieux
—in almost all published discussions. The last two have points in common and represent recent trends in evolutionary thinking. I have little doubt that a full explanation would involve aspects of all three attitudes.

1.
The first filling of the ecological barrel
. In conventional Darwinian theory, the organism proposes and the environment disposes. Organisms provide raw material in the form of genetic variation expressed in morphological differences. Within a population at any one time, these differences are small and—more important for the basic theory—undirected.
*
Evolutionary
change
(as opposed to mere variation) is produced by forces of natural selection arising from the external environment (both physical conditions and interactions with other organisms). Since organisms supply only raw material, and since this raw material has been judged as nearly always sufficient for all changes occurring at characteristically stately Darwinian rates, environment becomes the motor for regulating the speed and extent of evolutionary alteration. Therefore, according to conventional theory, the maximal rates of the Cambrian explosion must indicate something odd about environments at that time.

When we then inquire about the environmental oddity that could have engendered the Cambrian explosion, an obvious answer leaps at us. The Cambrian explosion was the first filling of the ecological barrel for multicellular life. This was a time of unparalleled opportunity. Nearly anything could find a place. Life was radiating into empty space and could proliferate at logarithmic rates, like a bacterial cell alone on an agar plate. In the bustle and ferment of this unique period, experimentation reigned in a world virtually free of competition for the one and only time.

In Darwinian theory, competition is the great regulator. Darwin conceived the world in metaphor as a log with ten thousand wedges, representing species, tightly hammered in along its length. A new species can enter this crowded world only by insinuating itself into a crack and popping another wedge out. Thus, diversity is self-regulating. As the Cambrian explosion proceeded, it drove itself to completion by filling the log with wedges. All later change would occur by a slower process of competition and displacement.

This Darwinian perspective also addresses the obvious objection to the model of the empty barrel as the cause of the Cambrian explosion: Life has suffered some astounding mass extinctions since the Cambrian—the Permian debacle may have wiped out 95 percent or more of all marine species—yet the Burgess phenomenon of explosive disparity never occurred again. Life did rediversify quickly after the Permian extinction, but no new phyla arose; the recolonizers of a depleted earth all remained within the strictures of previous anatomical designs. Yet the early Cambrian and post-Permian worlds were crucially different. Five percent may not be a high rate of survivorship, but no mode of life, no basic ecology, was entirely wiped out by the Permian debacle. The log remained populated, even if the wedges had become broader or more widely spaced. To shift metaphors, all the big spheres remained in the barrel, and only the pebbles in the interstices needed a complete recharging. The Cambrian barrel, on the other hand, was flat empty; the log was unscathed, with nary a woodsman’s blow nor a lover’s knife scratch (see Erwin, Valentine, and Sepkoski, 1987, for an interesting, quantitative development of this general argument).

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).

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.