But when we turn to Parker’s compendium of living organisms, we find but three pages devoted to priapulids, with a leisurely description of each family. Priapulids just don’t contribute much to an account of organic diversity; zoologists have found only about fifteen species. For some reason, priapulids do not rank among the success stories of modern biology.
An examination of priapulid distribution provides a clue to their relative failure. All priapulids live in unusual, harsh, or marginal environments—as if they cannot compete in the shallow, open environments frequented by most “standard” marine organisms, and can hang on only where ordinary creatures don’t bother. Two priapulid families include worms grown so small that they live among sand grains in the rich and fascinating (but decidedly “unstandard”) world of the so-called interstitial fauna. Most priapulids belong to the family Priapulidae, larger worms (up to twenty centimeters) of the sea bottom. But these priapulids do not inhabit the richest environments of the shallow-water tropics. They live in the coldest realms—at great depths in tropical regions, and in shallow waters in the frigid climates of high latitudes. They can also tolerate a variety of unusual conditions—low oxygen levels, hydrogen sulfide, low or sharply fluctuating salinity, and unproductive surroundings that impose long periods of starvation. It does not strain the boundaries of reasonable inference to argue that priapulids have managed to keep a toehold in a tough world by opting for difficult places devoid of sharp competition.
We might assume that these striking differences between modern polychaetes and priapulids indicate something so intrinsic about the relative mettle of these two groups that their geological history should be an uninterrupted tale of polychaete prosperity and priapulid struggle. If so, we are in for yet another surprise from the redoubtable Burgess fauna. This first recorded beginning of modern soft-bodied life contains six genera of polychaetes and six or seven genera of priapulids. (See Conway Morris’s monographs on priapulids, 1977d and polychaetes, 1979.)
Furthermore, the Burgess priapulids are numerically a major component of the fauna and, along with anomalocarids and a few arthropods, the earth’s first important soft-bodied carnivores. Ottoia prolifica (figure 5.1), most common of the Burgess priapulids, swallowed its prey whole. Hyolithids (conical shelled creatures of uncertain affinity) were favored as food. Thirty-one specimens have been found in the guts of Ottoia, most swallowed in the same orientation (and, therefore, almost certainly hunted and consumed in a definite style). One Ottoia had six hyolithids in its gut. Another specimen had eaten some of its own—the earliest example of cannibalism in the fossil record.
By contrast, polychaetes (figure 5.2), though equal to priapulids in taxonomic diversity, are much rarer numerically. Conway Morris remarks: “In comparison with the situation in many modern marine environments, the Burgess Shale polychaetes had a relatively minor role.”
Obviously, something dramatic (and disastrous) has happened to priapulids since the Burgess. Once, they had no rivals for abundance among soft-bodied forms, exceeding even the proud polychaetes of current majesty. Now, they are few and forgotten, denizens of the ocean’s spatial and environmental peripheries. The entire modern world contains scarcely more genera of priapulids than the single Burgess fauna from one quarry in British Columbia—while Burgess priapulids occupied center stage, not the tawdry provinces. What happened?
5.1. The Burgess priapulid Ottoia in its burrow, with its proboscis half extended. Drawn by Marianne Collins.
We do not know. It is tempting to argue that polychaetes had some biological leverage from the start and were destined for domination, however modest their beginning. But we have no idea what such an advantage might be. Conway Morris makes the intriguing observation that Burgess polychaetes had no jaws and that these organs of successful polychaete predators did not evolve until the subsequent Ordovician period. Perhaps the origin of jaws gave polychaetes their edge over the previously more abundant priapulids?
This supposition is plausible and may be correct, but we do not know; and a correlation (jaws with the beginning of dominance) need not imply a cause. In any case, our hypothetical Burgess geologist would not have known that the modest polychaetes would evolve jaws fifty million years hence.
5.2. The Burgess polychaete Canadia. Drawn by Marianne Collins.
The distribution and scarcity of modern priapulids, relative to Burgess abundance, does indicate a basic failure, but who can reconstruct the whys or wherefores? And who can say that a replay of life’s tape would not yield a modern world dominated by priapulids, with a few struggling jawless polychaetes at a tenuous periphery? What did happen makes sense; our world is not capricious. But many other plausible scenarios would have satisfied any modern votary of progress and good sense, and priapulid dominance lies firmly among the might-have-beens.
Are these Burgess fancies common to life’s history throughout or an oddity of uncertain beginnings, superseded by later inexorability? Consider one more might-have-been: When dinosaurs perished in the Cretaceous debacle, they left a vacuum in the world of large-bodied carnivores. Did the current reign of cats and dogs emerge by predictable necessity or contingent fortune? Would an Eocene paleontologist, surveying the vertebrate world fifty million years ago, have singled out for success the ancestors of Leo, king of beasts?
I doubt it. The Eocene world sported many lineages of mammalian carnivores, only one ancestral to modern forms and not especially distinguished at the time. But the Eocene featured a special moment in the history of carnivores, a pivot between two possibilities—one realized, the other forgotten. Mammals did not hold all the chips. In 1917, the American paleontologists W. D. Matthew and W. Granger described a “magnificent and quite unexpected” skeleton of a giant predacious bird from the Eocene of Wyoming, Diatryma gigantea:
Diatryma was a gigantic bird, ground living and with vestigial wings. In bulk of body and limbs it equalled all but the largest of moas and surpassed any living bird.… The height of the reconstructed skeleton is nearly 7 feet. The neck and head were totally unlike any living bird, the neck short and very massive, the head of enormous size with a huge compressed beak (1917).
The gigantic head and short, powerful neck identify Diatryma as a fierce carnivore, in sharp contrast with the small head and long, slender neck of the more peaceful ratites (ostriches, rheas, and their relatives). Like Tyrannosaurus, with its diminutive forelimbs but massive head and powerful hind limbs, Diatryma must have kicked, clawed, and bitten its prey into submission.
Diatrymids, distant relatives perhaps of cranes but no kin to ostriches and their ilk, ranged over Europe and North America for several million years. The plum of dominant carnivory could have fallen to the birds, but mammals finally prevailed, and we do not know why. We can invent stories about two legs, bird brains, and no teeth as necessarily inferior to all fours and sharp canines, but we know in our heart of hearts that if birds had won, we could tell just as good a tale about their inevitable success. A. S. Romer, leading vertebrate paleontologist of the generation just past, wrote in his textbook, the bible of the profession:
The presence of this great bird at a time when mammals were, for the most part, of very small size (the contemporary horse was the size of a fox terrier) suggests some interesting possibilities—which never materialized. The great reptiles had died off, and the surface of the earth was open for conquest. As possible successors there were the mammals and the birds. The former succeeded in the conquest, but the appearance of such a form as Diatryma shows that the birds were, at the beginning, rivals of the mammals (1966, p. 171).
In all these speculations about replaying life’s tape, we lament our lack of any controlled experiment. We cannot instigate the actual replay, and our planet provided only one run-through. But the crucial Eocene pivot between birds and mammals provides more and different evidence. For once, our recalcitrant and complex planet actually performed a proper experiment for us. This particular tape did have a replay, in South America—and thi
s time the birds won, or at least held the mammals to a respectable draw!
South America was an island continent, a kind of super-Australia, until the Isthmus of Panama arose just a few million years ago. Most animals usually considered as distinctively South American—jaguars, llamas, and tapirs, for example—are North American migrants of postisthmian arrival. The great native fauna of South America is largely gone (or surviving as a poor, if fascinating, remnant of armadillos, sloths, and the “Virginia” opossum, among others). No placental carnivores inhabited this giant ark. Most popular books tell us that the native South American carnivores were all marsupials, the so-called borhyaenids. They often neglect to say that another prominent group—the phororhacids, giant ground birds—fared just as well, if not better. Phororhacids also sported large heads and short, stout necks, but were not closely related to Diatryma. In South America, birds had a second and separate try as dominant carnivores, and this time they won, as suggested in Charles R. Knight’s famous reconstruction of a phororhacid standing in triumph over a mammalian victim (figure 5.3).
5.3. A phororhacid bird of South America stands in triumph over its mammalian prey in this depiction by Charles R. Knight.
In our smug, placental-centered parochialism, we may say that birds could triumph in South America only because marsupials are inferior to placentals and did not offer the kind of challenge that conquered predacious ground birds in Europe and North America. But can we be so sure? Borhyaenids could also be large and fierce, ranging to bear size and including such formidable creatures as Thylacosmilus, the marsupial sabertooth. We might also sneer and point out that, in any case, phororhacids quickly snuffed it (along with borhyaenids) as soon as superior placentals flooded over the rising isthmus. But this common saga of progress will not wash either. G. G. Simpson, our greatest expert on the evolution of South American mammals, wrote in one of his last books:
It has sometimes been said that these and other flightless South American birds … survived because there were long no placental carnivores on that continent. That speculation is far from convincing.… Most of the phororhacids became extinct before, only a straggler or two after, placental carnivores reached South America. Many of the borhyaenids that lived among these birds for many millions of years were highly predacious.… The phororhacids … were more likely to kill than to be killed by mammals (Simpson, 1980, pp. 147–50).
We must conclude, I think, that South America does represent a legitimate replay—round two for the birds.
GENERAL PATTERNS THAT ILLUSTRATE CONTINGENCY
This story of worms and birds—the first part graced with the sweep of history from Burgess times to now, the second with the virtues of repetition by natural experiment—moves contingency from a general statement about history into the realm of tangible things. A single story can establish plausibility by example, but it cannot make a complete case. The argument of this book needs two final supports: first, a statement about general properties of life’s history that reinforce the claims of contingency; and second, a chronology of examples illustrating the power of contingency not for selected and specific cases alone, but for the most general pathways and probabilities of life on our planet. This section and the next present these final supports for my argument; an epilogue on an arresting fact then completes the book.
If geological time had operated exactly as Darwin envisioned, contingency would still reign, with perhaps a bit more of life’s general pattern thrown into the realm of predictability under broad principles. Remember that Darwin viewed the history of life through his controlling metaphors of competition and the wedge (see page 229): the world is full of species, wedges crowded together on a log, and new forms can enter ecological communities only by displacing others (popping the wedges out). Displacement proceeds by competition under natural selection, and the better-adapted species win. Darwin felt that this process, operating in the micro-moment of the here and now, could be extrapolated into the countless millennia of geological time to yield the overall pattern of life’s history. For example, in chapter 10 of the Origin of Species, Darwin labored mightily (if incorrectly, in retrospect) to show that extinctions are not rapid and simultaneous across large differences of form and environment, but that each major group peters out slowly, its decline linked with the rise of a superior competitor.* But by “better adapted,” Darwin only meant “more suited to changing local environments,” not superior in any general anatomical sense. The pathways to local adaptation are as likely to restrict as to enhance the prospects for long-term success (simplification in parasites, overelaboration in peacocks). Moreover, nothing else is as quirky and unpredictable—both in our metaphors and on our planet—as trends in climate and geography. Continents fragment and disperse; oceanic circulation changes; rivers alter their course; mountains rise; estuaries dry up. If life works more by tracking environment than by climbing up a ladder of progress, then contingency should reign.
I assert the powerful role of contingency in Darwin’s system not as a logical corollary of his theory, but as an explicit theme central to his own life and work. Darwin invoked contingency in a fascinating way as his primary support for the fact of evolution itself. He embedded his defense in a paradox: One might think that the best evidence for evolution would reside in those exquisite examples of optimal adaptation presumably wrought by natural selection—the aerodynamic perfection of a feather or the flawless mimicry of insects that look like leaves or sticks. Such phenomena provide our standard textbook examples for the power of evolutionary modification—the mills of natural selection may operate slowly, but they grind exceedingly fine. Yet Darwin recognized that perfection cannot provide evidence for evolution because optimality covers the tracks of history.
If feathers are perfect, they may as well have been designed from scratch by an omnipotent God as from previous anatomy by a natural process. Darwin recognized that the primary evidence for evolution must be sought in quirks, oddities, and imperfections that lay bare the pathways of history. Whales, with their vestigial pelvic bones, must have descended from terrestrial ancestors with functional legs. Pandas, to eat bamboo, must build an imperfect “thumb” from a nubbin of a wrist bone, because carnivorous ancestors lost the requisite mobility of their first digit. Many animals of the Galapagos differ only slightly from neighbors in Ecuador, though the climate of these relatively cool volcanic islands diverges profoundly from conditions on the adjacent South American mainland. If whales retained no trace of their terrestrial heritage, if pandas bore perfect thumbs, if life on the Galápagos neatly matched the curious local environment—then history would not inhere in the productions of nature. But contingencies of “just history” do shape our world, and evolution lies exposed in the panoply of structures that have no other explanation than the shadow of their past.
Thus, contingency rules even in Darwin’s world of extrapolation from organic competition within local communities chock-full of species. However, an exciting intellectual movement of the last quarter century has led us to recognize that nature is not so smoothly and continuously ordered; the large does not emerge from the small simply by adding more time. Several large-scale pattern—based on the nature of macroevolution and the history of environment—impose their own signatures on nature’s pathways, and also disrupt, reset, and redirect whatever may be accumulating through time by the ticking of processes in the immediate here and now. Most of these patterns strongly reinforce the theme of contingency (see Gould, 1985a). Let us consider just two.
THE BURGESS PATTERN OF MAXIMAL INITIAL PROLIFERATION
The major argument of this book holds that contingency is immeasurably enhanced by the primary insight won from the Burgess Shale—that current patterns were not slowly evolved by continuous proliferation and advance, but set by a pronounced decimation (after a rapid initial diversification of anatomical designs), probably accomplished with a strong, perhaps controlling, component of lottery.
But we must know if the Burgess represe
nts an odd incident or a general theme in life’s history—for if most evolutionary bushes look like Christmas trees, with maximal breadth at their bottoms, then contingency wins its greatest possible boost as a predominant force in the history of organic disparity. My feeling about the importance of this question has led me to devote much of my technical research during the past fifteen years to the prevalence of “bottom-heaviness” in evolutionary trees (Raup et al., 1973; Raup and Gould, 1974; Gould et al., 1977; Gould, Gilinsky, and German, 1987).
Paleontologists have long recognized the Burgess pattern of maximal early disparity in conventional groups of fossils with hard parts. The echinoderms provide our premier example. All modern representatives of this exclusively marine phylum fall into five major group—the starfishes (Asteroidea), the brittle stars (Ophiuroidea), the sea urchins and sand dollars (Echinoidea), the sea lilies (Crinoidea), and the sea cucumbers (Holothuroidea). All share the basic pattern of fivefold radial symmetry. Yet Lower Paleozoic rocks, at the inception of the phylum, house some twenty to thirty basic groups of echinoderms, including some anatomies far outside the modern boundaries. The edrioasteroids built their globular skeletons in three-part symmetry. The bilateral symmetry of some “carpoids” is so pronounced that a few paleontologists view them as possible ancestors of fishes, and therefore of us as well (Jefferies, 1986). The bizarre helicoplacoids grew just a single food groove (not five), wound about the skeleton in a screwlike spiral. None of these groups survived the Paleozoic, and all modern echinoderms occupy the restricted realm of five-part symmetry. Yet none of these ancient groups shows any sign of anatomical insufficiency, or any hint of elimination by competition from surviving designs. Similar patterns may be found in the history of mollusks and vertebrates (where the early jawless and primitively jawed “fishes” show more variation in number and order of bones than all the later birds, reptiles, and mammals could muster; outward variety based on stereotypy of anatomical design has become a vertebrate hallmark).*