* This is Part 1 of a two-part installment of “Problematica.” It is, for once, actually about problematica! Part 1 explores the problematic fossils of the Burgess Shale, especially Opabinia regalis. (Longtime Extinct readers will recognize this critter as the thing Adrian is tickling in his cartoon portrait.) Part 2 concerns the Ediacaran biota, which I have previously written about here. The question these essays attempts to answer is twofold. First, why are the problematic fossils of the Burgess Shale no longer as problematic as they used to be? And second, why has the history of Ediacaran paleontology played out so differently? Read on! Problematica is written by Max Dresow…
About half a billion years ago, a strange creature wended its way through the waters of what is now western Canada. Its size was modest, even by Cambrian standards— about five centimeters long at maturity, maybe seven. Its body was segmented, with large swimming lobes projecting laterally from the segments. Each lobe was outfitted with a set of gills, which attached at the top of the lobe or perhaps near the back. In the rear of the animal still more lobes combined to form a V-shaped tail fan somewhat reminiscent of a lobster’s.
Opabinia regalis reconstructed. Incidentally, this might be my favorite piece of paleoart and I have no idea who made it. If you know, please reach out
The stranger part of the animal, however, was the front. Here one could find a hollow tube or “proboscis” that stretched another centimeter or so in front of the head. The tube was outfitted with a claw-like pincer that bristled with curved spines. Presumably these were used to snatch up food and deliver it to the mouth: a suggestion that gains in plausibility when it’s observed that the tube was striated like the hoses on some vacuum cleaners. Above the proboscis, no fewer than five eyes perched upon little stalks. All of them, it seems, pointed upwards. The whole setup is faintly ridiculous, and yet it is a real body plan, preserved in exquisite detail by some remarkable fossils. The challenge is to say what exactly the owner of the body plan was. Where does Opabinia regalis fit on the evolutionary tree of animals?
The identity of fossils like Opabinia was once a major problem in paleontology. It was the kind of problem for which conferences were convened and edited volumes organized. One such volume, edited by Alberto Simonetta and Simon Conway Morris, began thus:
Problematical taxa are one of the most intriguing, and most ignored, of the problems in biology. The tendency to relegate them to the sidelines of enquiry, and the dustbin of classification, is understandable, but such a treatment threatens to remove an area of great interest to evolutionary biology. (Simonetta and Conway Morris 1989, ix)
Stephen Jay Gould made a similar point in Wonderful Life (1989). There, “weird wonders” like Opabinia assumed almost metaphysical significance, capable of imparting a new view of life’s history with important consequences for our understanding of our place in the universe.
Left: the original dust jacket of Wonderful Life, which Gould wanted to title Ode to Opabinia (before, I assume, an editor intervened); and right: its author at the Walcott Quarry
Paleontologists no longer make such a fuss about problematic fossils. The reason, it seems, is that these fossils are not as problematic as they used to be. Opabinia, for example, is now regarded as a stem arthropod, which is to say, a member of the arthropod lineage that branched before the last common ancestor of all living arthropods. Most remaining problematica are likewise expected to find homes on the stems of extant groups. (As an expert on the Cambrian fauna once told me, these remaining problematica “give graduate students something to work on.” So much for problematica as one of the most intriguing problems in biology!)
This essay asks two big questions. The first is: what accounts for the change described in the previous paragraph? Why are problematica no longer the burning issue they were in the 1980s? After all, the fossils are the same— so what changed in the practice of paleontology to render problematic fossils a mere nuisance as opposed to a deep mystery? Here Opabinia, and indeed the Burgess Shale fauna more generally, provides a useful test case.
But it also prompts a second question. That is, what’s going on with those fossils that resist robust taxonomic placement, even today? Ages ago, I wrote an essay about the soft-bodied macrofossils of the Ediacaran biota. There I noted that these fossils, which have been heavily scrutinized since the 1950s, remain for the most part phylogenetically adrift. I put this down to a variety of factors, which I’ll rehearse in Part 2. But I didn’t consider why the methods and concepts that cut so much ice in the Cambrian cut so little in the Ediacaran. The comparison is instructive, and I’ll develop it here. I’ll also describe some of the strategies that have been formulated to deal with these outstanding problematic fossils. (Outstanding, I should say, in both senses of that word.)
That’s where all this is headed. I’ll tackle the first big question in Part 1, and the second in Part 2. But before we get to this, I want to spend some time getting to know Opabinia regalis. How did this little fossil become a mystery that strained the practice of paleontological classification to its breaking point?
* * *
The strange creature called Opabinia regalis was first described in 1912 by the finest paleontologist of the day, Charles Doolittle Walcott. It had been discovered a year earlier in a small quarry that Walcott had opened in the Canadian Rockies. The quarry was located “on the west slope of the ridge between Mount Field and Avapta Peak, 1 mile northeast of Burgess Pass, above Field, British Columbia.” The area is stunning, all towering peaks and fairy blue lakes fed by braided streams. It is the quarry of the middle Cambrian Burgess Shale.
Top: panorama of the Walcott Quarry, taken in 1910; and bottom: the view from the Burgess Shale outcrop, with Emerald Lake in the foreground and Emerald and Michael Peaks behind
For Walcott, Opabinia was an anostracan: a relative of the “fairy shrimp” in the class Branchiopoda. This made it a very primitive crustacean. Walcott described the basic features of the family Opabinidae as such:
Carapace absent; paired eyes pedunculate; antennae unknown, frontal appendage (proboscis) flexible, prehensile in male, bifid in female. Trunk limbs 16 pairs, the terminal joints of the feet broad and spatulate as in the Thamnocephalinse, Abdomen a simple plate, with two caudal, unsegmented furcal rami on the female. (Walcott 1912, 166)
Plate 28 from Walcott (1912), rotated 90 degrees for convenience. Here, Opabinia regalis is shown at the bottom, in dorsal view (i.e., from above). Also pictured are Nathorstia (image 2) and Naraoia (images 3 and 4)
The species Opabinia regalis he described as elongate and moderately wide, its body divided into a small head section, a trunk of sixteen somites, and a broad telson. “In front there [was] a short section from which a strong central appendage extend[ed] directly forward as viewed from above and curve[d] upward from the front lower side of the head when seen in profile” (Walcott 1912, 167). Two eyes perched upon little stalks. None of the specimens showed traces of antennae, mandibles, or maxillae: characteristic features of the modern crustacean head. As for the creature’s legs, it had them, Walcott thought, but the details of their structure could not be determined.*
[* Here’s what Walcott had to say about the legs: “The thoracic legs are shown both in side view and from below on a flattened specimen. They appear to be of a uniform character on all the 16 somites except the two anterior pairs, which may be smaller and have narrower terminal joints. The legs are formed of two or three rather strong, short joints followed by broad, flat, elongate-oval lobe-like joints” (Walcott 1912, 168).]
Another diagram from Walcott (1912). This one shows Opabinia on the branchiopod line of descent, along with some other Burgess Shale beasties
Walcott died in 1927. As long as he was alive, relatively few people set eyes on his prized specimens. But things began to move after his death; and so, in 1930, George Evelyn Hutchinson— future dean of American ecologists— came to re-examine Opabinia.
Hutchinson agreed with Walcott that Opabinia regalis was an anostracan. But he failed to find evidence of jointed appendages, and unlike Walcott, thought he could discern traces of an antenna.* The supposed gills in Walcott’s figure Hutchinson diagnosed as “marks made by irregular splitting of the shale” (Hutchinson 1930, 5). In any event, “no trace of them is to be found either in the well-preserved anterior appendages in specimen 57683 or in other relatively perfect specimens.” Standing back, Hutchinson figured Opabinia as a creature “considerably less generalised [which is to say, more specialized] than the modern Anostraca” (10). In addition, he thought that it probably swam with its dorsal side facing down, like a person doing the backstroke.
[* Hutchinson: “Walcott said that the appendages were jointed, but I can find no trace of joints, nor would such be expected in a foliaceous [leaf-like] appendage” (Hutchinson 1930, 5).]
G. E. Hutchinson’s reconstruction of Opabinia as a probably-antenna-bearing back-swimmer. Note the absence of jointed legs in the reconstruction
In order to “express the considerable differences existing between modern species of Anostraca and Opabinia and its [allies],” Hutchinson recommended dividing Anostraca into two suborders: the Euanostraca (“with 19 or more segments of which at least 11 are pedigerous [footed]…”) and the Palaeanostraca (“with not more than 17 segments, of which 11–15 are pedigerous…”) (Hutchinson 1930, 12). Opabinia belonged to the Palaeanostraca, which was an entirely extinct group.
Three decades passed before Opabinia again became an object of scientific interest. That was when Alberto Simonetta, a professor of zoology at the University of Camerino (and a bird specialist!), launched an ambitious re-examination of Walcott’s fossils. Simonetta began his “comprehensive review of the arthropods in the Smithsonian collection in 1960, in part with his colleague Laura Delle Cave.”
His description of Opabinia was included in his fourth paper on the non-trilobite arthropods from the Burgess Shale… Simonetta depicted Opabinia with a bifid proboscis, short antenna-like appendages, just two large compound eyes, a dorsal exoskeleton with lateral projections (pleurae) and biramous trunk appendages with a long segmented inner branch. (Briggs 2015, 5)
Alberto Simonetta’s reconstruction of Opabinia, featuring facial spikes and eyes reminiscent of a honey bees (compound, tear-shaped, without eye-stalks). Also, notice that the animal is here depicted with rows of jointed legs, which aligns with Walcott’s reconstruction but not with Hutchinson’s
Altogether it represented a major departure from Hutchinson’s reconstruction, with its reduced lateral lobes and jointed limbs. But the fuss over Opabinia was just beginning.
* * *
The bombshell burst in 1975. That was when Harry Whittington, a Cambridge paleontologist who had been working on the arthropods of the Burgess Shale since the mid-1960s, monographed Opabinia.* His approach was to examine all ten specimens then known, nine of which had been collected by Walcott.
He used a modified dental drill to prepare specimens in order to reveal features obscured by matrix or even by other parts of the animal. [He then] took photographs of the fossils under ultraviolet light, illuminating them from different angles to emphasize particular features. Most importantly, perhaps, he set a new standard by making detailed explanatory drawings, sometimes incorporating information from both part and counterpart, that served to inform and illustrate his interpretations. He achieved this using a camera lucida, an apparatus with prism and mirror that fits on a binocular microscope and projects an image of the specimen onto a sheet of paper where it can be traced. These drawings were published, as far as possible, alongside his photographs providing a clear explanation of the evidence for his interpretations. (Briggs 2015, 3)
[* Harry Whittington has the bad fortune of sharing a name with the Texas attorney that former vice president Dick Cheney shot in the face in 2006.]
Opabinia regalis in lateral view. Figures (a) and (b) are the part and counterpart (with the counterpart flipped horizontally to match (c)), and (c) is Whittington’s explanatory drawing, produced using the camera lucida technique. According to Derek Briggs: “(a) is illuminated from a low angle and (b) from a high angle to generate reflection in the eyes, for example, showing the method Whittington used to illustrate different features of the Burgess Shale specimens. The needle-marks evident in (a) show where Whittington prepared the specimen to reveal the terminal spines on the ‘flexible frontal process’ or proboscis which is flexed backwards underneath the body. (c) [is] Whittington’s camera lucida drawing and interpretation. L and R indicate features on the left and right sides of the body; i and o, inner and outer eyes; l, lateral lobes of the trunk, numbered from the anterior; f, blades of the tail fan; ds, dark stain representing material that has ‘leaked’ beyond the body.”
What he found was that many features of Simonetta’s reconstruction could not be supported. Opabinia evidently lacked antennae and jaws, as well as the jointed limbs that would ally it to the arthropods. Perhaps it was an annelid of some sort— at the time, annelids and arthropods were thought to be closely related. But Whittington could find no clear reason to assign Opabinia to the annelids. Oh, and the thing had five eyes, gills that looked nothing like trilobite gills, and preservational features suggestive of a bottom-dwelling habit. In a word, it was a freak. So he concluded that Opabinia was an animal of uncertain affinity, which on present knowledge could not be assigned to any living group. In his words, “this enigmatic animal exhibits features common to arthropods and annelids, but cannot be placed in any recognized group of either” (Whittington 1975, 41). (In case you’ve forgotten, anostracans are arthropods, so this also ruled out an anostracan affinity.)
Whittington’s reconstruction of Opabinia, bearing five stalked eyes and zero jointed appendages. Allegedly, when Whittington displayed a preliminary version of this reconstruction at the Paleontological Association meeting in 1972, he was greeted with bursts of laughter. So unfamiliar was the creature’s anatomical structure
Opabinia was not an outlier. As Whittington and his colleagues worked through the fauna, creature after creature fell between the taxonomic cracks. They were, in Gould’s words, “weird wonders”— creatures without close relatives in the modern ocean, or even, for that matter, the ocean of a quarter-billion years ago (Gould 1989). Hallucigenia was one such: a nightmare animal that teetered about on legs like sewing needles— or so the original reconstruction had it. Anomalocaris, with its pineapple ring mouth, was another. Then there was Yohoia and Wiwaxia, the latter looking like a warrior’s helmet, and more than a dozen others, each as strange as the next. So much anatomical diversity at the base of the Phanerozoic rock column— how could this be? That was the basic mystery of the Burgess Shale.
Three reconstructed animals of the Burgess Shale fauna, drawn by Marianne Collins for Gould’s Wonderful Life. On the left is Anomalocaris; on the top right Opabinia; and on the bottom right Hallucigenia
Many noticed the mystery, but it was Gould who took these ideas and ran with them. In his hands, the Burgess oddballs became more than taxonomic curiosities; they were the standard-bearers of a new view of history. Gould argued that during the Cambrian a wide range of body plans evolved, only to be culled in a subsequent “decimation.” The episode set evolution on a trajectory that led, after many twists and turns, to the modern fauna. But had a different set of body plans survived, evolution might have cascaded down a different path. The fossils of the Burgess Shale entered the argument as evidence that morphological diversity peaked in the wake of the diversification event known as the “Cambrian explosion.” Gould also argued, on morphological grounds, that the survivors of the decimation were not adaptively superior to the lineages that went extinct. This is why he called the decimation “random,” and why he regarded it as a contingent event of the first magnitude.
Left: Gould’s representation of the “conventional” (but allegedly false) iconography of evolution, which he terms “the cone of increasing diversity”; and right: “the revised model of decimation and diversification, suggested by the proper reconstruction of the Burgess Shale” (Gould 1989, 46]). Here you should imagine creatures like Opabinia and Hallucigenia on the shorter stalks— these are groups (body plans) that left no descendants in the modern oceans. And you should imagine groups like the arthropods and annelids on the longer stalks. These are the taxa that, following an indiscriminate decimation, inherited the earth
Opabinia epitomized the argument. Indeed, as Gould wrote in a masterpiece of exaggeration, “Whittington’s reconstruction of Opabinia in 1975 will stand as one of the great documents in the history of human knowledge.” The reason is that it “led directly on to a fundamentally revised view about the history of life.”
We are awestruck by Tyrannosaurus; we marvel at the feathers of Archaeopteryx; we revel in every scrap of fossil human bone from Africa. But none of these has taught us anywhere near so much about the nature of evolution as a little two-inch Cambrian odd ball invertebrate named Opabinia. (Gould 1989, 136)
Why was Opabinia so liberating? Before this, Whittington had monographed Marrella— the “lace crab”— and Yohoia— a rather Opabinia-like animal that Walcott placed in the anostracans. He placed them both in the phylum Arthropoda. But Opabinia was not an arthropod. And, to use Gould’s words, “it sure as hell wasn’t anything anyone else could specify either” (Gould 1989, 131). On close inspection, “nothing from the Burgess Shale seemed to fit into any modern group” (excepting the arthropods, which didn’t resemble any living arthropods). That was what was so liberating.
Opabinia did not have to conform to the demands of arthropod, or any other, design. Whittington could come as close as any paleontologist ever had to the unattainable ideal of Parsifal— the perfect fool, with no preconceptions. He could simply describe what he saw, however strange. (Gould 1989, 132)
Gould went on to describe Whittington’s procedure, paying special attention to how the use of less rigorous methods had led past investigators astray:
Whittington needed all his special methods of dissection, varied orientations, and part-counterpart to resolve the morphology of so peculiar a beast. He also discovered that a failure to appreciate these methods had provided a major argument to support the arthropod model. Walcott had confused part and counterpart in one important specimen. He thought that he was viewing the bottom surface of the animal; in fact, he was looking down upon the upper surface. [Percy] Raymond, accepting this upside down interpretation, had made the perfectly reasonable claim that the gills of Opabinia lay below the outer carapace— as in the standard arthropod arrangement, with gill branches as the upper limbs of biramous append ages located just under the carapace. But in the correct orientation, the gills lie above the body lobes in a most unarthropod-like orientation. (Gould 1989, 133)
He closed by hammering home the importance of Opabinia:
Marrella and Yohoia had challenged Walcott’s shoehorn, but these genera were only orphaned within the Arthropoda. With Opabinia, the game cranked up to another level, and changed unalterably and forever. Opabinia belonged nowhere among the known animals of this or any former earth. If Whittington had chosen to place it within a formal classification at all (he wisely declined), he would have been forced to erect a new phylum for this single genus. Five eyes, a frontal nozzle, and gills above lateral flaps! Walcott’s shoehorn had fractured. Whittington wrote with characteristic brevity in the passive voice: “Opabinia regalis is not considered to have been a trilobitomorph arthropod, nor is it regarded as an annelid.“ Harry may be a measured man, but he knew what Opabinia implied for the rest of the Burgess fauna. “The Burgess Shale,” he remarked laconically, “contains other undescribed segmented animals of uncertain affinities.” (Gould 1989, 136)
After all this, it seems almost callous to report that these animals are now mostly housed on the arthropod stem. But they are. Including that weirdest of wonders, Opabinia regalis.
* * *
So what happened? Here the story becomes complicated, but much credit goes to the adoption of phylogenetic systematics (cladistics) and its corollary, the stem group concept. I’ll say what these are in a moment. First, though, let me plug Keynyn Brysse’s excellent paper, “From weird wonders to stem lineages: the second reclassification of the Burgess Shale fauna” (2008). This gets the story just right, in my opinion, and what I say here is entirely in line with Brysse’s account.
Some cladistic concepts represented, including “synapomorphy” (an “apomorphy,” or derived feature, shared by two or more taxa and inferred to have evolved in their most recent common ancestor) and “homoplasy” (a feature that has evolved separately in two or more lineages)
Now what are phylogenetics systematics and the stem group concept?
To begin, phylogenetic systematics is an approach to classification that works by grouping taxa into monophyletic groups, or clades, comprising a common ancestor and all its descendants, living and extinct. It does this on the evidence of shared derived features, or synapomorphies, which are features shared by two or more taxa and inferred to have evolved in their most recent common ancestor.* Phylogenetic systematics began to make waves in the 1960s, but did not make inroads into paleontology until the mid-1970s (Hull 1988). That was also when the stem group concept received its canonical formulation, courtesy of the British paleontologist and student of early chordate evolution, Richard Jefferies (Jefferies 1979).
[* A researcher might infer that a derived feature is a synapomorphy if just two lineages have that feature, for example. But it’s obviously possible that the feature did not evolve in their most recent common ancestor. Models of character evolution help researchers make these determinations.]
Jefferies’s (1979) depiction of the stem-/crown-group distinction (see the text for a verbal description)
The stem group concept is awkward to state but easy to understand. Take a glace at the above image and you’ll intuitively grasp that the “stem group” of a clade includes all members of that clade outside the “crown group”— the group that includes the last common ancestor of the living members of the clade and all its descendants, living and extinct. Members of the stem group are, by definition, extinct, and are more closely related to members of the crown group than to members of the closest living sister group. This is true despite the fact that it’s often difficult to constrain basal taxa to a particular stem (as opposed to the stem of the closest sister group), since these taxa share the fewest synapomorphies with the crown.
The adoption of phylogenetic systematics and the stem group concept had far-reaching effects on paleontological practice. But when thinking about problematica, its main virtue was that it allowed paleontologists to avoid a devil’s choice. Previously, when a problematic fossil came under a paleontologist’s microscope, the researcher could do one of two things. The first was to include it in the least dissimilar living group— a procedure that involved changing the definition of that group to accommodate the troublesome fossil. We might call this the “accommodationist strategy.” (Recall Hutchinson’s treatment of Opabinia, which involved loosening the definition of an anostracan to include creatures with fewer than 19 body segments.) The other was to erect a new higher-level taxon to house the oddball— even a new phylum, if the creature’s morphology was strange enough. Call this the “let-a-thousand-flowers-bloom strategy.”
Which to choose? That was a real question, and for a while, it caused paleontological tempers to run hot. Consider Opabinia. Like many of its contemporaries, Opabinia lacked features that would ally it to living groups. Whittington, for example, could find no jointed legs that would indicate an affinity with the phylum Arthropoda. But since it also possessed features that suggested arthropod affinity (like differentiated body segments), it was possible to see it as an arthropod, albeit one that violated the definition of the group based its living members.
Comparative leg segmentation in arthropods. Featuring a trilobite leg (A), the fifth and sixth legs of a eurypterid (B), and the leg of a pycnogonid (C), arachnid (D), scorpion (E), crustacean (F), chilopod (G), diplopod (H, I) and insect (J). From Snodgrass (1958)
Two factors militated against the arthropod solution. First, jointed appendages are pretty important to the definition of an arthropod— the word arthropod means joint (arthro-) foot (-pod)! Definitions can be revised, it’s true. But here there was another factor to contend with: namely, Opabinia’s possession of features that are totally unique, like its bizarre vacuum cleaner nose. That was the kind of character that seemed to warrant taxonomic recognition, much like the arthropod’s limb. So— researchers were forced to ask— why should we change the definition of an arthropod when we’re dealing with an animal that both lacked jointed appendages and possessed a unique character of similar anatomical complexity and (we might reasonably assume) great functional importance? Wouldn’t it be more “natural” to erect a new higher-level taxon to house the oddball, perhaps even a new phylum?
Faced with questions like this, many researchers opted to let a thousand flowers bloom. Gould was of this persuasion. So, initially, was Simon Conway Morris. Yet it was never a consensus solution to the problem posed by problematic fossils. Always there was skepticism, always resistance. Martin Glaessner, to name one prominent critic, argued that “failures are not phyla”— the phylum is a success category, and extinct taxa with one or a few members are not success stories (Glaessner, 1984, 135). He thus favored the accommodationist strategy; but in response, others warned that this ran the risk of seriously distorting our picture of metazoan evolution (e.g., Bentson 1986, Gould 1989). Things seemed headed for a stalemate.
This is where the stem group concept did its work. In effect, it offered a third way to deal with fossils that both lacked features diagnostic of living groups and possessed features all their own. That is, a paleontologist could locate such creatures on the stem of a living clade (including but not limited to those clades recognized as phyla). At a stroke a major conceptual pinch was relieved. Extinct basal taxa are not expected to possess all the features characteristic of living groups. What’s more, they’re expected to possess features absent in living groups, including weird features like Opabinia’s proboscis (Budd 2003). Anyway, there’s no need to erect a new phylum-level taxon to accommodate Opabinia’s eccentricities. The creature was simply a stem arthropod despite its unusual body plan. Problem (apparently) solved.
Reconstruction of the Burgess Shale fauna, with Opabinia capturing a worm, Anomalocaris about to munch a trilobite, and Hallucigenia (along with Wiwaxia and Marrella) scuttling over the seafloor
The solution did not represent a straightforward triumph of the accommodationist strategy. That strategy worked by adjusting the definition of a group to accommodate aberrant material. Usually the group in question was a phylum, of which there are approximately thirty-five in the animal kingdom. Indeed, so important was the phylum that the definition of a problematic fossil was often given in terms of phylum membership— problematic fossils were those that “[could not] be recognized as belonging to a known phylum” (Bengtson 1986, 3).*
[* The phylum category was accorded special significance because each phylum was thought to possess a distinctive, and highly successful, complex of characters: a body plan. As George Simpson wrote in 1949: “at the base of each phylum lies the acquisition of some distinctive complex of characters which happened to be rich in evolutionary potentialities worked out, often in strikingly diverse ways, in the later members of the group” (Simpson 1949, 23).]
But what is a phylum to a cladist, anyway? Is it the total group of a large clade? The crown group? A useless vestige of an earlier system of classification? Paleontologists answered these questions in different ways; but the thing to notice is that nothing about the application of the stem-crown distinction hinged on the position one took on in this debate. As a consequence, two researchers could agree that Opabinia was a stem arthropod even if one saw the arthropod phylum as comprising the total group and the other as just the crown. Settling this question was, methodologically, beside the point. What mattered was that many problematic taxa were located on the stems of living clades, regardless of whether these clades deserved to be called “phyla.”
Now back to Opabinia one last time.
* * *
Wonderful Life hit bookshelves in 1989. The same year, Derek Briggs and Richard Fortey published the first cladistic analysis that ordered the Burgess arthropods using parsimony. Based on a relatively modest dataset of twenty-eight taxa and forty-six characters, they showed that the majority of Cambrian arthropods could be accommodated in a plausible monophyletic tree— even the weird ones. The authors also argued that the problematic taxa did not show “any remarkable morphological separation [from modern groups],” as Gould had so emphatically claimed (Briggs and Fortey 1989, 243). Certainly there was no warrant for recognizing perhaps two dozen new phylum-level groups in the Burgess sediments.
This was not yet the stem group concept at work, at least not explicitly. But the gauntlet had been thrown down. In the case of the Burgess arthropods, there was no reason to erect new taxa “of equivalent rank and independent origin from the major arthropod groups” (Briggs and Fortey 1989, 241). Even the aberrant forms did not stand apart from the rest. They were better interpreted as forms that “bridge[d] the major groups.” In effect, stem taxa.
A cladogram of Cambrian and other arthropods, from Briggs and Fortey (1989)
However, two Burgess icons were missing from Briggs and Fortey’s study. The first was Anomalocaris, the big baddie of the Cambrian seas. The other was Opabinia. The omission was intentional. Back in 1986, the arthropod specialist Jan Bergström had argued that Opabinia and Anomalocaris were closely related taxa (Bergström 1986). He also suggested that Anomalocaris possessed segmented limbs, leading him to claim that, “by definition [it] should be called an arthropod.” Bucking convention, he proposed to house Anomalocaris and Opabinia in an unnamed taxon of equivalent rank to the other arthropod subphyla, like Crustacea. This was an instance of the let-a-thousand-flowers-bloom strategy.
Briggs, writing with his PhD supervisor Harry Whittington, disagreed. After reviewing Bergström’s claims (and finding them all wanting) Briggs and Whittington concluded that “no new evidence [allies] either of these animals with the arthropods” (Briggs and Whittington 1987, 186). Opabinia and Anomalocaris were orphaned and homeless again.
But not for long. In 1994, an Englishman named Graham Budd completed his PhD under Simon Conway Morris (another Whittington student and a veteran of the Burgess Shale fauna). The subject of the dissertation was the Cambrian fossils of the Sirius Passet Lagerstätte in Northern Greenland, which had been discovered in 1984. Budd focused on the lobopods and in 1993 published an account of an early Cambrian lobopod called Kerygmachela kierkegaardi.* The animal possessed “lateral lobes along the body with dorsal gill-like structures attached to them”— very similar, Budd noted, to Opabinia (Budd 1993, 709). So, his head crammed with lobopods, Budd turned his attention to the puzzle of Opabinia itself.
[* Kerygma is a Greek word meaning “proclamation,” and has an intuitive pronunciation. Chela (keela) means claw. And Kierkegaard is after the Danish philosopher Soren Kierkegaard. So, the full name is pronounced kerygma-keela kierkegaard-y.]
Budd’s reconstruction of Opabinia, with some lobes redacted to reveal two rows of conical lobopod-like limbs
The crucial paper appeared under the title “The morphology of Opabinia regalis and the reconstruction of the arthropod stem-group” (1996). In it, Budd made the ambitious argument that Kerygmachela, Opabinia, and Anomalocaris “probably form a paraphyletic grouping at the base of the arthropods”— part of the arthropod stem (Budd 1996, 1). Following a restudy of known Opabinia specimens, Budd was able to confirm the basic features of Whittington’s 1975 reconstruction, with two exceptions. First, Whittington seems to have misdescribed the gills (the only feature of Bergström’s critique that Budd upheld). Second, and more speculatively, Budd thought that Opabinia possessed conical, lobopod-like limbs, probably tipped with diminutive claws. The latter inference was based on the presence of reflective areas on the surface of some specimens, which Budd described as “a series of fairly well defined, sub-triangular reflective structures, arranged in a segmental fashion” (5). These he interpreted as traces of the internal cavities of lobopod-like limbs. He continued:
[The] observation of limbs is central to the assessment of the systematic position of Opabinia and its probable relatives Kerygmachela and Anomalocaris. This group of animals appears to contain representatives that are relatively ‘arthropodized’ (Anomalocaris), with arthropod-like frontal appendages, and also animals that are more ‘lobopod’-like (Kerygmachela, Opabinia). (Budd 1996, 7)
Translated into evolutionary terms, Kerygmachela and Opabinia probably occupied more basal positions on the arthropod stem, whereas Anomalocaris was more derived (occupying a position closer to the crown). This implied that the process of “arthropodization” could be resolved into “an orderly series of morphological innovations”: first the development of lateral lobes, then the development of external segmentation, then the sclerotization of the limbs and the formation of the biramous appendage, and finally, the sclerotization of the cuticle (Budd 1996, 12).
Budd’s reconstruction of the arthropod stem and its implications for “arthropodization.” The original caption reads as follows: “A broad-scale reconstruction of the arthropod stem-group, mostly following Ramskold's (1992) 'morphocline'. This has been converted into a phylogeny by the polarization discussed in the text… Important synapomorphies: 1. The plexus of arthropod characters of Budd (1993). 2. Onychophoran autapomorphies. 3. Heteronomous annulation, nodes. 4. Node enlargement. 5. 'Armoured' nodes. 6. Spine enlargement, effacement, limb spine loss, slender limbs. 7. ?Oval head shield. 8. Secondary loss of nodes. 9. Lateral lobes. 10. Arthropodan segmentation (= loss of small trunk annulations). 11. Large compound eyes, differentiation of trunk to form tail fan, gut diverticulae. 12. Sclerotization of appendages, fusion of lateral lobes and limbs to form biramous limbs… 13. Sclerotization of ternites (CCT clade =crustaceans+ chelicerates+trilobites: possibly +insects).”
Very little of this has gone unchallenged. In particular, the inference that Opabinia possessed lobopod-like limbs has met with resistance (e.g., Zhang and Briggs 2007; but see Budd and Daley 2012). And yet even Zhang and Briggs, who find “no convincing evidence for the presence of lobopod limbs,” agree that Opabinia belongs “on the stem of euarthropods” (Zhang and Briggs 2007, 161). This means that they agree with Budd that Opabinia has something to tell us about the process of body plan assembly in the clade: in the event, something about the origin of biramous limbs.
Pause for a moment to appreciate the significance of this. Once, Opabinia was an outcast, the ultimate wallflower at the Cambrian mixer. This made it evidentially inert in relation to questions of arthropod evolution. (If Opabinia was not an arthropod, then it could hardly tell us anything about the process of body plan assembly in the arthropods!) And yet as soon as it was convincingly located on the arthropod stem its evidential standing was transformed. Suddenly, Opabinia could be enlisted in an evidentiary role in the project of reconstructing the process of arthropodization. Indeed, it became a key datum, which extended the nodal length of the arthropod stem and permitted a closer look at the step-wise evolution of the arthropod body plan (Legg et al. 2012).
Not a bad trick from the most wonderful of the Cambrian weirdos.
* * *
The story of Opabinia is the story of the Burgess Shale fauna in a nutshell. Ultimately, it’s a story of success. Although questions remain, many of the most confounding fossils have found homes on the stems of living clades. Opabinia and Anomalocaris were stem arthropods. Hallucigenia was a stem onychophoran. And so on.
But—looking ahead to our second question— why has the history of Ediacaran paleontology been so different? Why did the concepts and methods that worked so well in the Cambrian cut so little ice in the preceding Ediacaran Period? And what is currently being done to break this taxonomic stalemate? Those are the questions for Part 2 of this essay, for which a link will be placed here when it’s available.
References
* There is a reference list below. Before coming to it, I want to mention a few resources and videos about the Burgess Shale fauna. On the resources side, the Royal Ontario Museum has a really fantastic page on the history of the Burgess Shale, from 1883 to the present. They also have a nice page on the Burgess Shale (fauna) more generally. Ellis Yochelson has written a fine reflection on Walcott’s work with the Burgess fossils, which pushes back against Gould’s dimmer view of his efforts. Finally, if you want to read about a second probable opabinid species, click here.
I’ve also embedded two videos beneath the reference list. The first is Gould speaking on the Burgess Shale and a bunch of other stuff in 1993. The second is my graduate advisor, Alan Love, speaking about the Gould–Conway Morris dispute in Banff, Alberta.
Bengtson, S. 1986. The problem of the problematica. In A. Hoffman and M. H. Nitecki (eds.), Problematic Fossil Taxa, 3–11. Oxford: Oxford University Press.
Bergström J. 1986. Opabinia and Anomalocaris, unique Cambrian ‘arthropods’ Lethaia 19:241–246.
Briggs, D. E. G. 2015. Extraordinary fossils reveal the nature of Cambrian life: a commentary on Whittington (1975) ‘The enigmatic animal Opabinia regalis, Middle Cambrian, Burgess Shale, British Columbia.’ Philosophical Transactions of the Royal Society, Part B 370:20140313.
Briggs, D. E. G. & Fortey, R. A. 1989. The early radiation and relationships of major arthropod groups. Science 246:241–243.
Brysse, K. 2008. From weird wonders to stem lineages: the second reclassification of the Burgess Shale fauna. Studies in History and Philosophy of Biological and Biomedical Sciences 39:298–313.
Budd, G. E. 1993. Cambrian gilled lobopod from Greenland. Nature 364:709–711.
Budd, G. E. 1996. The morphology of Opabinia regalis and the reconstruction of the arthropod stem-group. Lethaia 29:1–14.
Budd, G. E. 2003. The Cambrian fossil record and the origin of the phyla. Integrative and Comparative Biology 43:157–165.
Budd, G. E. and Daley, A. C. 2012. The lobes and lobopods of Opabinia regalis from the middle Cambrian Burgess Shale. Lethaia 45:83–95.
Glaessner, M. F. 1984. The Dawn of Animal Life: A Biohistorical Study. Cambridge (UK): Cambridge University Press.
Gould. S. J. 1989. Wonderful Life: The Burgess Shale and the Nature of History. New York: W. W. Norton & Co.
Hull, D. L. 1988. Science as a Process: An Evolutionary Account of the Social and Conceptual Development of Science. Chicago: University of Chicago Press.
Hutchinson, G. E. 1930. Restudy of some Burgess Shale fossils. Proceedings of the United States National Museum 78 1–11.
Jefferies, R. P. S. 1979. The origin of chordates— a methodological essay. In M. R. House (ed.), The origin of major invertebrate groups, 443–447. London: Academic Press.
Legg, D. A., Sutton, M. D., Edgecombe, G. D. and Caron, J.-B. Cambrian bivalved arthropod reveals origin of arthrodization. Proceedings of the Royal Society, Part B 279:4699–4704.
Simonetta, A. M. 1970. Simonetta AM. 1970 Studies on non-trilobite arthropods of the Burgess Shale (Middle Cambrian). Palaeontographia Italica 66 35–45.
Simonetta, A. M. and Conway-Morris, S. 1989. The Early Evolution of Metazoa and the Significance of Problematic Taxa. Cambridge (UK): Cambridge University Press.
Simpson, G. G. 1949. The Meaning of Evolution: A Study of the History of Life and of Its Significance for Man. New Haven: Yale University Press.
Snodgrass, R. E. 1958. Evolution of Arthropod Mechanisms. Washington: The Smithsonian Institution.
Walcott, C. D. 1912. Cambrian geology and paleontology, II: Middle Cambrian Branchiopoda, Malacostraca, Trilobita, and Merostomata. Smithsonian Miscellaneous Collections 57:146–228.
Whittington, H. B. 1975 The enigmatic animal Opabinia regalis, Middle Cambrian, Burgess Shale, British Columbia. Philosophical Transactions of the Royal Society, Part B 271:1–43.
Zhang, X.–L. and Briggs, D. E. G. 2007. The nature and significance of the appendages of Opabinia from the Middle Cambrian Burgess Shale. Lethaia 40:161–173.
VIDEOS
