ASSESSMENT OF GENEALOGICAL RELATIONSHIPS FOR BURGESS ORGANISMS
This book, long enough already, cannot become an abstract treatise on the rules of evolutionary inference. But I do need to provide a few explicit comments on how paleontologists move from descriptions of anatomy to proposals about genealogical relationships—so that my numerous statements on this subject receive some underpinning and do not stand as undefended pronouncements ex cathedra.
Louis Agassiz, the great zoologist who founded the institution that now houses both me and the Raymond collection of Burgess Shale fossils, picked a superficially peculiar name that we retain with pride—the Museum of Comparative Zoology. (Anticipating the hagiographical urges of his contemporaries, he even explicitly requested that his chosen title be retained in perpetuity, and that the museum not be renamed for him upon his demise.) Experiment and manipulation may form the stereotype of science, Agassiz argued, but disciplines that treat the inordinately complex, unrepeatable products of history must proceed differently. Natural history must operate by analyzing similarities and differences within its forest of unique and distinctive products—in other words, by comparison.
Evolutionary and genealogical inferences rest upon the study and meaning of similarities and differences, and the basic task is neither simple nor obvious. If we could just compile a long list of features, count the likenesses and unlikenesses, gin up a number to express an overall level of resemblances, and then equate evolutionary relationship with measured similarity, we could almost switch to automatic pilot and entrust our basic job to a computer.
The world, as usual, is not so simple—and thank goodness, for the horizon would probably be a disappointing place anyway. Similarities come in many forms: some are guides to genealogical inferences; others are pitfalls and dangers. As a basic distinction, we must rigidly separate similarities due to simple inheritance of features present in common ancestors, from similarities arising by separate evolution for the same function. The first kind of similarity, called homology, is the proper guide to descent. I have the same number of neck vertebrae as a giraffe, a mole, and a bat, not (obviously) because we all use our heads in the same way, but because seven is the ancestral number in mammals, and has been retained by descent in nearly all modern groups (sloths and their relatives excepted). The second kind of similarity, called analogy, is the most treacherous obstacle to the search for genealogy. The wings of birds, bats, and pterosaurs share some basic aerodynamic features, but each evolved independently; for no common ancestor of any pair had wings. Distinguishing homology from analogy is the basic activity of genealogical inference. We use a simple rule: rigidly exclude analogies and base genealogies on homology alone. Bats are mammals, not birds.
Using this cardinal rule, we can go a certain distance with the Burgess Shale. The tail flukes of Odaraia bear an uncanny resemblance to functionally similar structures of some fishes and marine mammals. But Odaraia is clearly an arthropod, not a vertebrate. Anomalocaris may have used its overlapping lateral flaps to swim by undulation, much as certain fishes with continuous lateral fins or flattened body edges do—but this functional similarity, evolved from different anatomical foundations, indicates nothing about genealogical relationship. Anomalocaris remains a weird wonder, no closer to a vertebrate than to any other known creature.
But the basic distinction between homology and analogy will not carry us far enough. We must make a second division, among homologous structures themselves. Rats and people share both hair and a vertebral column. Both are homologies, structures inherited from common ancestors. If we are searching for a criterion that will properly unite rats and people into the genealogical group of mammals, we can use hair, but the shared vertebral column will not help us at all. Why the difference? Hair works because it is a shared-and-derived character, confined to mammals among the vertebrates. A vertebral column is no help because it is a shared-but-primitive character, present in the common ancestor of all terrestrial vertebrates—not just mammals—and most fish.
This distinction between properly restricted (shared and derived) and overly broad homologies (shared but primitive) lies at the core of our greatest contemporary difficulties with Burgess organisms.* For example, many Burgess arthropods have a bivalved carapace; many others share the basic “merostomoid” form, a broad head shield followed by numerous short and wide body segments capped by a tail spike. These two features are, presumably, genuine arthropod homologies—each bivalved lineage doesn’t start from scratch and develop the same complex structure, slowly and separately. But neither the presence of a bivalved carapace nor “merostomoid” body form can identify a genealogically coherent group of Burgess arthropods because both are shared-but-primitive characters.
Figure 3.71 should clarify the reason for rejecting shared-but-primitive traits as a guide to genealogy. This evolutionary tree represents a lineage that has diversified into three great groups—I, II, and III—by the time marked by the dashed line. A star indicates the presence of a homologous trait—call it five digits on the front limb—inherited from the distant common ancestor (A). In many branches, this trait has been lost or modified beyond recognition. Every loss is marked by a double-headed arrow. Note that at the selected time, four species (1–4) still retain the shared-but-primitive trait. If we united these four as a genealogical group, we would be making the worst possible error—missing the three true groups entirely, while taking members from each to construct a false assemblage: species 1 might be the ancestor of horses; species 2 and 3, early rodents; and species 4, an ancestor of primates, including humans. The fallacy of basing groups on shared-but-primitive traits should be apparent.*
3.71. A hypothetical evolutionary tree illustrating why shared-but-primitive traits must be rejected as guides in identifying genealogical groups. Lineages and branching points marked with a star possess the shared-but-primitive trait. Double-headed arrows mark the loss of this trait.
But the Burgess problem is probably even worse. In my five-act chronology, I often spoke of a grabbag of available arthropod characters. Suppose that such shared-but-primitive features as the bivalved carapace, unlike the starred trait of figure 3.71, do not indicate continuous lineages. Suppose that in this early age of unparalleled experimentation and genetic lability, such traits could arise, again and again, in any new arthropod lineage—not by slow and separate evolution for common function (for the traits would then represent classic analogies), but as latent potentials in the genetic system of all early arthropods, separately recruitable for overt expression in each lineage. Then traits like merostomoid body form and bivalved carapaces would pop up again and again all over the arthropod evolutionary tree.
I suspect that such a strange phenomenon did prevail in Burgess times, and that we have had so little success in reconstructing Burgess genealogies because each species arose by a process not too different from constructing a meal from a gigantic old-style Chinese menu (before the Szechuan, yuppie, and other gastronomical revolutions)—one from column A, two from B, with many columns and long lists in each column. Our ability to recognize coherent groups among later arthropods arises for two reasons: First, lineages lost this original genetic potential for recruitment of each major part from many latent possibilities; and second, the removal of most lineages by extinction left only a few survivors, with big gaps between (figure 3.72). The radiation of these few surviving lineages (into a great diversity of species with restricted disparity of total form) produced the distinct groups that we know today as phyla and classes.
3.72. A hypothetical evolutionary tree reflecting a view of life’s history suggested by the reinterpretation of the Burgess fauna. The removal of most groups by extinction leaves large morphological gaps among the survivors. The dashed line represents the time of the Burgess Shale, with disparity at a maximum.
I think that Derek Briggs had a model like this in mind when he wrote of the difficulty in classifying Burgess arthropods: “Each species has unique characteristics,
while those shared tend to be generalized and common to many arthropods. Relationships between these contemporaneous species are, therefore, far from obvious, and possible ancestral forms are unknown.” (1981b, p. 38).*
I also think that the model of the grabbag might be extended to all Burgess animals taken together, not only to the arthropods separately. What are we to make of the feeding appendages on Anomalocaris? They do seem to be fashioned on an arthropod plan, but the rest of the body suggests no affinity with this great phylum. Perhaps they are only analogous to arthropod limbs, separately evolved and truly devoid of any genetic continuity with the jointed structures of arthropods. But perhaps the Burgess grabbag extended across phyla. Perhaps jointed structures with a common genetic underpinning were not yet restricted to the Arthropoda. Their limited presence elsewhere would not imply close genealogical relationship with arthropods, but only a broad range of latent and recruitable structures that did not yet respect the later, unbridgeable boundaries of modern phyla. The jaws of Wiwaxia (recalling the molluscan radula) and the feeding organ of Odontogriphus (recalling the lophophore of several phyla) come to mind as other possible features from the mega-grabbag.
The model of the grabbag is a taxonomist’s nightmare and an evolutionist’s delight. Imagine an organism built of a hundred basic features, with twenty possible forms per feature. The grabbag contains a hundred compartments, with twenty different tokens in each. To make a new Burgess creature, the Great Token-Stringer takes one token at random from each compartment and strings them all together. Voilà, the creature works—and you have nearly as many successful experiments as a musical scale can build catchy tunes. † The world has not operated this way since Burgess times. Today, the Great Token-Stringer uses a variety of separate bags—labeled “vertebrate body plan,” “angiosperm body plan,” “molluscan body plan,” and so forth. The tokens in each compartment are far less numerous, and few if any from bag 1 can also be found in bag 2. The Great Token-Stringer now makes a much more orderly set of new creatures, but the playfulness and surprise of his early work have disappeared. He is no longer the enfant terrible of a brave new multicellular world, fashioning Anomalocaris with a hint of arthropod, Wiwaxia with a whiff of mollusk, Nectocaris with an amalgam of arthropod and vertebrate.
The story is old, and canonical. The youthful firebrand has become the apostle of good sense and stable design. Yet the former spark is not entirely extinct. Something truly new slips by now and then within the boundaries of strict inheritance. Perhaps his natural vanity finally got the better of him. Perhaps he couldn’t bear the thought of running such an exquisite play for so long, and having no chronicler to admire the work. So he let the token for more brain tumble from compartment 1 of the primate bag—and assembled a species that could paint the caves of Lascaux, frame the glass of Chartres, and finally decipher the story of the Burgess Shale.
THE BURGESS SHALE AS A CAMBRIAN GENERALITY
The chief fascination of the Burgess Shale lies in a paradox of human comprehension. The most stunning and newsworthy parts of the story involve the greatest oddities and strangest creatures. Anomalocaris, two feet long, and crunching a trilobite in its circular “jellyfish” jaw, rightly wins the headlines. But the human mind needs anchors in familiarity. The Burgess teaches us a general lesson, and reverses our usual view of life, because so much about this fauna has the clear ring of conventionality. Its creatures eat and move in ordinary ways; the entire community strikes a working ecologist as comprehensible in modern terms; key elements of the fauna also appear in other locations, and we learn that the Burgess represents the normal world of Cambrian times, not a bizarre marine grotto in British Columbia.
I emphasized throughout my five-act chronology that the discovery of conventional creatures, true crustaceans and chelicerates, was every bit as important as the reconstruction of weird wonders in forging a complete interpretation for the Burgess Shale. If we now take a larger look, and consider the entire fauna as a totality, as a functioning ecological community, the same theme holds with even more force. The anatomical oddness of the Burgess gains its meaning against a backdrop of global spread and conventional ecology for the fauna as a whole.
PREDATORS AND PREY: THE FUNCTIONAL WORLD OF BURGESS ARTHROPODS
In 1985, Briggs and Whittington published a fascinating article summarizing their conclusions on the modes of life and ecology of Burgess arthropods; (the focus of almost all their previous monographic work had been anatomical and genealogical). Taking all the arthropods together, they inferred a range of behaviors and feeding styles comparable with modern faunas. They divided the Burgess genera into six major ecological categories.
1. Predatory and scavenging benthos. (Benthic creatures live on the sea floor and do little or no swimming.) This large group includes the trilobites and several of the “merostomoid” genera—Sidneyia, Emeraldella, Molaria, and Habelia (figure 3.73D and F–K). All have biramous body appendages bearing strong walking branches with a spiny inner border on the first segment, facing the central food groove. The alimentary canal (where identified) curves down and backward at the mouth—indicating that food was passed from the rear forward, as in most benthic arthropods. The strong spines imply that relatively large food items were caught or scavenged, and passed forward to the mouth.
2. Deposit-feeding benthos. (Deposit feeders extract small particles from sediment, often by processing large quantities of mud; they do not select or actively pursue large food items.) Several genera fall into this category, primarily on the evidence of weak or absent spines on the inner borders of the food groove—Canadaspis, Burgessia, Waptia, and Marrella, for example (figure 3.74E and H–J). Most of these genera could probably either walk across the bottom sediment or swim weakly in the water column just above.
3. Scavenging, and perhaps predatory, nektobenthos. (Nektobenthonic creatures both swim and walk on the sea floor.) The genera in this category—Branchiocaris and Yohoia (figure 3.74D and F)—were not primarily benthic because they did not possess biramous appendages with strong walking branches. Yohoia has three biramous appendages on the head, but probably uniramous limbs with gill branches, used for respiration and swimming, alone on the body; Branchiocaris has biramous body appendages, but with short, weak walking branches. The absence of strong inner branches on the body appendages also suggests that these genera did not eat by passing food forward from the rear. But both genera possess large head appendages with claws at the tip, and probably brought discrete food items from the front end of the body directly to the mouth.
4. Deposit-feeding and scavenging nektobenthos. Like the genera of the preceding category, the members of this group have body appendages with weak or absent inner branches, implying little walking and food processing from the rear; stronger outer branches for swimming; and head appendages that could have gathered food directly. But these genera—Leanchoilia, Actaeus, Perspicaris, and Plenocaris (figure 3.74A–C and G)—do not have strong claws on the tips of their frontal appendages, and probably did not capture large food items; hence they are regarded as probable deposit feeders.
3.73. Burgess arthropods, all drawn to the same scale to show their relative sizes (Briggs and Whittington, 1985). (A) Odaraia. (B) Sarotrocercus. (C) Aysheaia. (D) Habelia. (E) Alalcomenaeus. (F) Emeraldella. (G) Molaria. (H) Naraoia. (I) Sidneyia. (J) The trilobite Olenoides. (K) The large soft-bodied trilobite Tegopelte.
3.74. From Briggs and Whittington, 1985. Additional Burgess arthropods, all drawn to the same scale. (A) Perspicaris. (B) Plenocaris.(C) Leanchoilia.(D) Branchiocaris.(E) Marrella.(F) Yohoia.(G) Actaeus.(H) Canadaspis.(I) Waptia.(J) Burgessia.
5. Nektonic suspension feeders. This small category—consisting of Odaraia and Sarotrocercus (figure 3.73A–B)—includes the true swimmers among Burgess arthropods. These genera either had no walking branches (Sarotrocercus) or possessed short inner branches that could not extend beyond the carapace (Odaraia). They had the biggest eyes among Burgess arthropods, and both probably sought
small prey for filter feeding.
6. Others. Every classification has a residual category for unusual members. Aysheaia (figure 3.73C) may have been a parasite, living among and feeding on sponges. Alalcomenaeus (figure 3.73E) bears strong spines all along the inner edges of its walking legs, not only on the first segment, adjoining the food groove. Briggs and Whittington conjecture that Alalcomenaeus may have used these spines either to grasp on to algae, or to tear carcasses in scavenging.
Briggs and Whittington include two excellent summary figures in their paper (figures 3.73 and 3.74). Each genus is shown in its probable habitat, and all are drawn to the same scale—so that the substantial differences in size among genera may be appreciated.
Each of the six categories crosses genealogical lines. The ensemble fills a set of ordinary roles for modern marine arthropods. The great anatomical disparity among Burgess arthropods is therefore not a simple adaptive response to a wider range of environments available at this early time. Somehow, the same basic scope of opportunity originally elicited a far greater range of anatomical experimentation. Same ecological world; very different kind of evolutionary response: this situation defines the enigma of the Burgess.
Wonderful Life: The Burgess Shale and the Nature of History Page 21