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THE : A MIRROR FOR MODERN EVOLUTIONARY

by

Keynyn Alexandra Ripley Brysse

A submitted in conformity with the requirements

for the degree of

Institute for the History and Philosophy of Science and Technology

University of Toronto

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While these forms may be included Bien que ces formulaires in the document page count, aient inclus dans la pagination, their removal does not represent il n'y aura aucun contenu manquant. any loss of content from the thesis. Canada The Burgess Shale: A Cambrian Mirror for Modern Keynyn Alexandra Ripley Brysse

Doctor of Philosophy

Institute for the History and Philosophy of Science and Technology University of Toronto 2008 Abstract The Burgess Shale, discovered in 1909, contains the fossilized remains of unusual marine from shortly after the . This thesis delineates three distinct phases in Burgess Shale research. It examines why the Burgess Shale has inspired such dissimilar interpretations and asks what the consequences of these different views are for our understanding of the tempo and mode of and the place of in evolutionary biology.

The Burgess Shale were initially classified by Charles Doolittle Walcott as primitive members of modern groups. Later, in the 1960s, Cambridge (UK) paleontologists, led by Harry Whittington, came to think of the Burgess creatures as unique evolutionary experiments, unrelated to modern phyla. This "weird wonders" view was taken to its extreme by . Gould used the Burgess fossils to advance a highly distinctive theory of the tempo and mode of evolution, and to argue that morphological disparity has decreased over time, not increased as commonly believed. Gould held to this view until his death. The third phase, initiated by and in the 1980s, gives a very different interpretation to the Burgess Shale. On this new understanding, disparity has not decreased, and the Burgess creatures are no longer weird

ii wonders deserving unique status, but are now seen as "stem groups" on the evolutionary paths leading up to the modern phyla.

This thesis investigates the motivations of the protagonists in this debate. Briggs and

Conway Morris each arrived at their Phase 3 view for different reasons. Briggs credited the adoption of , a new method of classification. Conway Morris credited the increased information provided by the discovery of new fossils, and the re-interpretation of known fossils. Despite the fact that Gould and Conway Morris both dismissed cladistics as an inadequate tool for the study of biological diversity, they held radically divergent views about the diversity of the Burgess Shale. This dissertation will show that these men had different theories of the tempo and mode of evolution; therefore, each saw the Burgess fossils in the light of his own theories, assumptions, and goals.

iii Quotations

"Fossils provide just enough data to fuel a debate but not enough to resolve it."1

"It becomes clear that there has been a battle underway to monopolize the Cambrian explosion and impose a story that fits a triumphant set of preconceived notions. So who owns the Burgess Shale now?"2

1 Andrew Berry, "Wonderful crucible," Review of The Crucible of Creation: The Burgess Shale and the Rise of Animals by Simon Conway Morris (Oxford: Oxford University Press, 1998) Evolution vol. 52, no. 5 (October 1998), 1529. 2 Jeffrey Levinton, "Who owns the Cambrian explosion?" Review of The Crucible of Creation: The Burgess Shale and the Rise of Animals by Simon Conway Morris (Oxford: Oxford University Press, 1998) The Quarterly Review of Biology vol. 74, no. 2 (June 1999): 201-204.

IV Acknowledgments

I would like to thank my supervisor, Denis Walsh, for his excellent advice and tremendous support: intellectual, psychological, and financial. Special thanks are also due to the rest of my dissertation committee, Polly Winsor and Marga Vicedo, and my other final examiners, David Sepkoski and Paul Thompson, who were all kind, supportive, and full of excellent suggestions. Jean-Bernard Caron, Curator of Invertebrate at the Royal Ontario Museum, and Allison Daley, a paleontology student currently writing her dissertation on the Burgess Shale, have been frequent and extremely friendly sources of information and encouragement. Athena McKown, who recently received her Ph.D. in botany from the University of Toronto, provided helpful information about the evolution of C4 photosynthesis in plants, and was a valuable source of insight into modern phylogenetic and other scientific practices. She has also been, and continues to be, a huge source of comfort and advice, usually served with tea. I am grateful to John Henry at the , who first suggested that the Burgess Shale reclassifications might make a good dissertation topic, and to Christian Baron, a Ph.D. candidate at the University of Copenhagen, who made me aware of Sidnie Manton's connection to the German idealistic morphology tradition. Thanks are also due to Trevor Levere and Isaac Record, Editor-in-Chief and Editorial Assistant ofAnnals of Science, who kindly let me use the Annals scanner to upload images for my thesis. I am also very grateful for the assistance, advice, and support of Denise Horsley and Muna Salloum, who have both reassured and rescued me countless times over the past five years. I would also like to thank the staff of the General and Zoology Library at the British Museum of Natural History, who let me examine and photograph their collection of Sidnie Manton's correspondence.

Finally, and most profoundly, I am especially indebted to Derek Briggs, , Simon Conway Morris, , and Harry Whittington for so kindly and generously taking the time to discuss with me their work on the Burgess Shale. Their ideas, spoken and written, published and unpublished, are the subject of the research described in these pages, and as such my work would not have been possible without their support and very generous assistance. Briggs and Fortey even allowed me to read and photocopy materials of interest from among their unpublished notes and correspondence, which have proven indispensible for my work.

v My Ph.D. studies were supported by a Doctoral Fellowship from the Social Sciences and Humanities Research Council of Canada (SSHRC), and also by a Margaret and Nicolas Fodor Fellowship, two travel grants and a bursary fromth e School of Graduate Studies, and two travel grants from the Institute for History and Philosophy of Science and Technology, all at the University of Toronto. I am very grateful for this financial assistance, as well as the income provided by several teaching and research assistantships and an instructorship, without which I would not have been able to conduct my research.

vi Table of Contents

Abstract ii

Quotations iv

Acknowledgments v

Table of Contents vii

List of Tables , viii

List of Figures ix

List of Appendices xi

Chapter 1 Introduction: "The Single Most Important Discovery Ever Made" 1 Chapter 2 Cladistics and Stem Groups: "Building a Phylogeny from the Bottom Up" 59

Chapter 3 Conway Morris's Reclassifications: "Fishing in the Cambrian Sea" 120

Chapter 4 The Occupation and Navigation of Morphospace 157

Chapter 5 "The Golden Age of Body Plans:" Phyla in the Burgess Shale 200

Chapter 6 Conclusion: The "Battle" for the Burgess Shale 253

Bibliography 260

Appendix A 289

vii List of Tables

Table 1. Appendage Distributions in Modern vs. Burgess Shale 22

Table 2. The Three Phases of Burgess Shale Research 52

Table 3. Changing Classifications of Burgess Shale 53

viii List of Figures

Figure 1. Location of Three Main Burgess Shale Quarries 3

Figure 2. Geological Time Scale ..8

Figure 3. Four Major Body Plans 19

Figure 4. Biramous Arthropod Appendage 20

Figure 5. Marretta splendens. 23

Figure 6. Yohoia tenuis 24

Figure 7. regalis 26

Figure 8. Nectocaris pteryx... 29

Figure 9. sparsa (Conway Morris, 1977) 30

Figure 10. corrugata 31

Figure 11. canadensis - The Complete Animal 32

Figure 12. Two Models of Morphological Disparity through Time 40

Figure 13. Whittington's Phylogenetic Lawn Diagram 63

Figure 14. The First Burgess Shale 65

Figure 15. Synapomorphies and Shared Ancestry 74

Figure 16. Cladogram vs. Phylogenetic Tree 76

Figure 17. The Stem Group Concept 93

Figure 18. Classification of Three Burgess Genera 95

Figure 19. Classification of Three Burgess Genera-Phase 1 96

Figure 20. Classification of Three Burgess Genera-Phase 2 97

Figure 21. Classification of Three Burgess Genera-Phase 3 98

Figure 22. Stem-Group Arthropods from the Burgess Shale 99

ix Figure 23. Hattucigenia sparsa (Ramskdld, 1992)..... 132

Figure 24. sinicum. 133

Figure 25. pedunculata 134

Figure 26. Halkieria evangelista 139

Figure 27. Two Hypotheses of Lophotrochozoan Phylogeny.... 141

Figure 28. Anomalocaris canadensis -The Original Fossil.... 142

Figure 29. nathorsti. 143

Figure 30. Appendage F 146

Figure 31. kierkegaardi. 150

Figure 32. A Geometrically Impossible Shell 190

Figure 33. Waddington's Epigenetic Landscape 192

x List of Appendices

Appendix A Species Known fromth e Burgess Shale.... 289

xi Chapter 1 "The Single Most Important Fossil Discovery Ever Made"1

This thesis explores a recent debate in paleontology and evolutionary biology, over the classification and interpretation of an ancient set of invertebrate animal fossils, found in the Burgess Shale of British Columbia, Canada. It is important to paleontologists to achieve an accurate and complete (or as complete as possible) reconstruction of the on

Earth, and the Burgess fossils, as some of the oldest and most exquisitely preserved animals known, can certainly shed light on this issue. But there is much more at stake in this debate, and much more to be gained, than simply an appreciation of the fossils themselves. The

Burgess Shale has been interpreted and appropriated in very distinct ways by different scientists, to support vastly different theories about the history and significance of life on

Earth, the nature and operation of evolution, and even the meaning of our own existence.

In addition to the specific controversy over the Burgess fossils themselves (which includes the question of how and when the major groups or phyla of animals arose), evolutionary biology and paleontology have experienced several important debates in (and leading up to) the 20th century, all of which are reflected in the changing perceptions of the

Burgess Shale. These debates include: the importance of structuralism versus functionalism in determining organic form, the proper methods and goals of systematics, the importance of contingency in the history of life, and the tempo and mode of evolution. In a sense the

Burgess Shale is a microcosm of, or testing ground for, these other conflicts, and as we will

1 Ellis L. Yochelson, "Discovery, collection, and description of the Middle Cambrian Burgess Shale biota by Charles Doolittle Walcott," Proceedings of the American Philosophical Society vol. 140, no. 4 (December 1996), 470.

1 2

see in the following pages, scientists who hold different views on these other issues have

arrived at vastly different interpretations of the Burgess Shale.

The Burgess Shale - Setting and Significance

The Burgess Shale is a set of fossil beds located on the slopes of Mount Stephen and

on Fossil Ridge, a rocky outcrop stretching between Mount Field and Mount Wapta, in Yoho

National Park, British Columbia, close to the B.C. - border. (Figure 1) These beds

contain some of the most exquisitely preserved remains known of marine invertebrate

animals, ranging in size from less than a millimetre, to over a metre in length. Recent

estimates date the Burgess Shale to 505 million years ago, in the Middle Cambrian

geological period. This means the Burgess Shale represents a time shortly after the rapid

(and as yet unexplained) appearance and diversification of most (if not all) of the animal phyla, known as the Cambrian explosion, which took place from approximately 530 to 520 million years ago,2

Scientific references to the Burgess Shale often seem confusing, for there are various names for the different Burgess Shale quarries (geographical locations), the rock beds within the quarries (geological sections), and the stratigraphic formations and members

(geochronological units) to which the rocks in the quarries belong. Thus it can be difficult

for the non-expert to make distinctions between, and correlations among, these various types of units. I shall lay out the basic terms here. In summary, the Burgess Shale is an informal name for a set of fossil beds, including the and the Beds (also known as the Ogygopsis Shale), which are found within the Burgess Shale Formation, and

2 Jean-Bernard Caron, and Community Analysis of the Middle Cambrian Greater Phyllopod Bed, Burgess Shale (PhD. thesis. University of Toronto, 2005), 1. Wapta Mountain

Fossil Ridge

Walcott Quarry

Mount Field

Mount Stephen

Town of Field Collins Quarry

Trilobite Beds/ Ogygopsis Shale

1000 m Figure 1. Location of Three Main Burgess Shale Quarries Hatched line is Canadian Pacific Railway line; grey line is Kicking Horse River; thick black line is Trans-Canada Highway. Grey rectangle in map inset in upper right corner indicates location of main map area. Modified from Fletcher and Collins, 1824. 4 which have been excavated in several quarries including the , the Raymond

Quarry, and the Collins Quarry.

The Trilobite Beds, which are located on Mount Stephen, were discovered in 1886 by

Richard G. McConnell, a geologist with the Geological Survey of Canada (GSC). Charles

Doolittle Walcott, an American geologist, visited this site in the early 1900s and proposed to call it the "Ogygopsis Shale," after the most common trilobite found within its rocks.

In 1909, Walcott discovered another, extremely rich, fossil locality on the nearby Fossil

Ridge. This quarry was later named the Walcott Quarry, after its discoverer. The particular rock layers exposed in this quarry are part of a series of bedding layers which Walcott named the Phyllopod Bed, after a particular group of with leaf-shaped limbs commonly found within.3 The name "Burgess Shale" was originally given, by Walcott, to the series of rocks containing the Phyllopod Bed; the name was only later extended to the Trilobite

Beds/1Ogygopsis Shale which had been discovered earlier. Thus Walcott is credited with having discovered the Burgess Shale.4

Later expeditions dug additional quarries above (e.g. the Raymond Quarry, twenty metres higher, first excavated in 1930) and below Walcott's original quarry (e.g. several quarries dug by the Royal Ontario Museum (ROM) beginning in the 1970s), and the beds exposed in all of these quarries on Fossil Ridge are collectively known as the Greater

Phyllopod Bed.5 Further collecting has also been done in and around the Trilobite

Beds/'Ogygopsis Shale of Mount Stephen; for example, the Collins Quarry (named after

Desmond Collins, then Curator of Invertebrate Paleontology at the ROM, who led several

3 Harry B. Whittington, The Burgess Shale (New Haven: Press, 1985), 19. 4 Harry B. Whittington, "The Burgess Shale: history of research and preservation of fossils," in Proceedings of the North American Paleontological Convention, Part 1: Extraordinary Fossils. 1170-1201 (Lawrence: Allen Press, Inc., 1971), 1171. 5 Caron, 5. 5

expeditions to the Burgess Shale in the late 1970s and 80s) is located several meters below

and to the west of the Trilobite Beds.6 All of these localities, on Mount Stephen, Fossil

Ridge, and between, are collectively contained within the Burgess Shale.

The history of the Burgess Shale has been even more confusing in terms of

geological units and chronostratigraphy. The rocks containing the Burgess Shale were

formerly thought to belong to the , but geologists now recognize it as a

separate Burgess Shale Formation.7 (This formation includes several different geological members which do not bear on the present discussion.) Estimates of the age of the Burgess

Shale have also shifted dramatically over time. Walcott thought the Burgess Shale was about

15 million years old;8 by the late 1970s this estimate had radically increased to 530 million years.9 Current dating techniques have reduced the estimated age slightly, to 505 million years.10

The Burgess Shale, then, is an informal term for a series of fossil beds, approximately

105 metres in total thickness, found on and around Mount Stephen and Fossil Ridge in Yoho

National Park, which are approximately 505 million years old.11 These fossil beds are unique in their exquisite preservation of extremely ancient marine organisms. The Burgess

6 Terence P. Fletcher and Desmond H. Collins, "The Burgess Shale and associated Cambrian formations west of the Fossil Gully Fault Zone on Mount Stephen, British Columbia," Canadian Journal of Earth Sciences vol. 40 (2003), 1828. 7 William H. Fritz, "Geological setting of the Burgess Shale," in Proceedings of the North American Paleontological Convention, Part 1: Extraordinary Fossils. 1155-1170 (Lawrence: Allen Press, Inc., 1971), 1157. 8 Ellis L. Yochelson, Secretary, Charles Doolittle Walcott (Kent and London: The Kent State University Press, 2001), 82. 9 See for example Simon Conway Morris, "The Burgess Shale (Middle Cambrian) fauna," Annual Review of Ecology andSystematics vol. 10 (1979), 327. 10 Desmond Collins, "To be or not to be: that is the evolutionary question," Review of The Crucible of Creation: The Burgess Shale and the Rise of Animals by Simon Conway Morris (Oxford: Oxford University Press, 1998) Literary Review of Canada vol. 7, no. 9 (June 1999), 26. 11 James W. Hagadorn, "Burgess Shale: Cambrian explosion in full bloom," in Exceptional Fossil Preservation: A Unique View on the Evolution of . David J. Bottjer, Walter Etter, James W. Hagadorn, and Carol M. Tang, eds. 61-89 (New York: Columbia University Press, 2002), 62. 6

Shale contains the remains of organisms which lived in, on, and above a set of mudbanks at

the base of an ancient limestone mound known as the Cathedral Escarpment (a sort of reef,

not built by , which hadn't evolved yet, but by calcareous algae).12 Many discussions

of the Burgess Shale suggest that the Burgess organisms were caught in a mudslide and

carried some distance before being buried.13 However, recent work, notably by Jean-Bernard

Caron, the current Curator of Invertebrate Paleontology at the ROM, suggests that the

Burgess Shale was an autochthonous community — in other words, that the organisms were

fossilized in the place where they had lived.14 In either case, however, the general lack of

organic decay, the general absence of trace fossils, and the fact that most specimens seem to

be randomly oriented with respect to the substrate suggest that the event which created the

Burgess Shale was a sudden, energetic mudflow which tossed the organisms around and then buried them quickly, killing them rapidly and sealing out oxygen and microscopic organisms which would otherwise have caused decomposition. Both hard and soft parts of organisms

are preserved, though the original organic components have typically been replaced by other minerals. The fossils thus usually occur as hydrous aluminosilicate or pyrite films

compressed between the bedding planes of the mud, now hardened into shale.15 A few

specimens are found at angles to the bedding planes (meaning that "dissecting" through the

rock layers will reveal different parts of the fossil).16

The fossils of the Burgess Shale are so exquisitely preserved that paleontologists refer to it as a "konservat-Lagerstatte," a name firstuse d by German paleontologist Adolf

12 Hagadarn, 63. 13 See for example Simon Conway Morris, "Middle Cambrian polyehaetes fromth e Burgess Shale of British Columbia," Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, vol. 285, no. 1007 (23 March 1979), 236 and Hagadorn, 65. 14 Caron, 261. 15 Hagadorn, 67. 16 Whittington, "The Burgess Shale: history of research and preservation of fossils," 1185. 7

Seilacher, in 1970, to describe a "deposit containing fossils that are so exceptionally preserved... that it warrants special exploitation" by scientists. These fossil Lagerstatten are extremely rare; the Burgess Shale is one of fewer than one hundred fossil sites worldwide which are "products of the fortuitous co-occurrence of unique biological, chemical, and sedimentary conditions" leading to the preservation of soft tissues.17 The abundance of exquisitely preserved soft-bodied organisms, which would not be fossilized under normal circumstances, and their extreme antiquity, have led paleontologists to regard this site as one of the most important, if not the most important, fossil discoveries of all time. Collins wrote, for example, "[the] Burgess Shale fossils give us our best look at the first animals to evolve on Earth. They are therefore extraordinarily important to our knowledge of early life on

Earth, and to our understanding of how life has evolved since."18 Invertebrate paleontologist and popular science writer Stephen Jay Gould called it "the most precious and important of all fossil localities,"19 and Walcott's biographer, Ellis Yochelson, believed it was "the single most important fossil discovery ever made."20

Since the 1980s, several other sites containing Cambrian fossils have been discovered, the most important and well-known of which are the Chengjiang fauna in the

Yunnan Province of China, and the fauna of Peary Land, Greenland. Both are approximately fifteen million years older than the Burgess Shale. (Figure 2) The

Chengjiang fossils are comparable in preservational quality to those of the Burgess Shale;

17 David J. Bottjer, Walter Etter, James W. Hagadorn, and Carol M. Tang, "Fossil-Lagerstatten: jewels of the fossil record," in Exceptional Fossil Preservation: A Unique View on the Evolution of Marine Life. David J. Bottjer, Walter Etter, James W. Hagadorn, and Carol M. Tang, eds. 1-10 (New York: Columbia University Press, 2002), 2. 18 Collins, 'To be or not to be," 26. 19 Stephen J. Gould, Wonderful Life: The Burgess Shale and the Nature of History (New York and London: W. W. Norton & Company, 1989), 13. 20 Yochelson, "Discovery, collection, and description of the Middle Cambrian Burgess Shale," 470. 8

Time Eon Era Period Faunas of Interest Cenozoic Quaternary 65 Tertiary Mesozoic Cretaeeous 250 Paleozoic 488 Cambrian Late

501 Phanerozoi c Middle ••• Burgess Shale (-505) 510 Early — Sirius Passet (~518) *l— Chengjiang (~525)

542 Neoproterozoic Mesoproterozoic Paleoproterozoic "Precambri an" Proterozoi c

Figure 2. Geological Time Scale Relative (and approximate absolute) ages of the three best-known Burgess Shale-type faunas are indicated. Numbers indicate millions of years ago. Modified from Valentine, On the Origin of Phyla, 170, Carroll, Grenier, and Weatfierbee, 4, and Gee, 4. Relative sizes of time units as drawn do not reflect their actual durations. those at Sirius Passet are of slightly lower quality, but all still qualify as konservat-

Lagerstatten.21 Paleontologists, including some of those who also worked on the Burgess

Shale, began to publish papers reporting studies of the Chengjiang and Sirius Passet fossils in

21 Graham E. Budd, "The morphology and phylogenetic significance of Kerygmachela kierkegaardi Budd (, Lower Cambrian, N Greenland)," Transactions of the Royal Society of Edinburgh: Earth Sciences vol. 89, no. 4 (1999), 250-251. 9 the late 1980s. (This work will be discussed in more detail in Chapter 3.) I turn now to a

more detailed discussion of the discovery of the Burgess Shale, and the three distinct phases

of interpretation of its fossils.

Phase 1: The Early History of the Burgess Shale

When he discovered the Burgess Shale, Walcott was the Director of the USGS, and was also an acknowledged expert on Cambrian and paleontology in general, and in particular. Later (beginning in 1907) he became the Secretary (i.e., Director) of the Smithsonian Institution in Washington, D.C. Walcott, who had an arrangement with the

GSC to collect, describe, and publish on Canadian paleontological materials that the GSC had neither the money nor the qualified personnel to handle themselves, discovered his first

Burgess Shale fossils (including three unusual arthropod genera, Waptia, , and

Naraoia) on August 30th or 31st, 1909, at the advanced age of 59, while on a collecting expedition in the British Columbia Rockies with his family.22 They remained in the area, collecting further specimens, until September. According to Gould, Walcott was quickly able to trace the isolated blocks in which he found these specimens to the quarry higher up

from which they had fallen, but was unable to excavate more fossils from this quarry because the team had not brought dynamite with them that season. They returned the following

summer, however, and began excavation within the main Burgess Shale site, which Walcott referred to as the Phyllopod Bed, and which later became known as the Walcott Quarry.

Walcott, with a team of workers consisting of family members and a handful of American

and Canadian geologists and general labourers, excavated in the Walcott Quarry from 1910

Yochelson, Smithsonian Institution Secretary, 84,434. 10 through 1913, returning for one final field season in 1917.23 In all, he collected some 60,000 fossil specimens, which he shipped back to the Smithsonian Institution's National Museum of Natural History (now the National Museum).24

Walcott published a few preliminary reports on Burgess Shale organisms between

1911 and 1927, but was never able to find enough time away from his administrative duties

(which, in addition to running the Smithsonian, included membership or leadership of various geological, institutional, and government committees, some of which reported to the

President of the United States) to examine the Burgess fossils as closely as he wished.25 The brief descriptions which were all Walcott managed before his death were clearly meant as temporary, initial treatments upon which he hoped to later expand. Yochelson explained that

"Walcott's primary goal [with his brief Burgess Shale publications] was to produce illustrations and descriptions in a timely fashion, without waiting for monographic treatment."26 Walcott clearly hoped to devote his later years to more in-depth work on the

Burgess Shale; when he planned his retirement for May of 1927, he stated his intention to withdraw from "all executive and administrative work" because he had "writing to do that w[ould] take all [his] energy up to 1949."27 Walcott never got a chance even to begin this estimated twenty-year opus, however; he died in February of 1927, while still in office.

23 Gould, Wonderful Life, 71-75. 24 Whittington, The Burgess Shale, 6. Gould (Wonderful Life, 75), puts the figurea t 80,000 specimens. 25 See for example Charles Doolittle Walcott, "Middle Cambrian Merostomata," Smithsonian Miscellaneous Collections, vol. 57, no. 2 (1911): 17-40, "Middle Cambrian holothurians and Medusae," Smithsonian Miscellaneous Collections, vol. 57, no. 3 (1911): 41-68, "Middle Cambrian Annelida," Smithsonian Miscellaneous Collections, vol. 57, no. 5 (1911): 109-144, "Middle Cambrian Brancbiostomata, , Trilobita, and Merostomata," Smithsonian Miscellaneous Collections, vol. 57, no. 6 (1912): 145-228, "Cambrian trilobites," Smithsonian Miscellaneous Collections, vol. 64, no. 3 (1916): 157-258, and "Cambrian and Ozarkian Irilobites," Smithsonian Miscellaneous Collections, vol. 75, no. 3 (1925): 61-146. 26 Yochelson, Smithsonian Institution Secretary, 97. 27 Excerpt from Walcott's diary, qtd. in Yochelson, Smithsonian Institution Secretary, 490. 11

Gould wrote a bestselling book about the Burgess Shale in 1989, entitled Wonderful

Life: The Burgess Shale and the Nature of History, in which he distinguished two phases of

Burgess Shale research. (The third phase, which others have identified, was not yet fully underway at the time this book was published.) Gould referred to the firstphas e as

"Walcott's shoehorn," in which the busy director classified what few Burgess creatures he

had time to examine as primitive members of modern phyla and classes.28 Gould argued that

Walcott did not appreciate the true diversity and uniqueness of the Burgess Shale, for two

reasons: first, the Secretary of the Smithsonian was too busy with administrative

commitments to have time to examine the Burgess fossils as closely as was needed; second,

he, like other paleontologists of his day, was committed to a view of ancient fossils as generalized and primitive ancestors of modern groups. This commitment, according to

Gould, required him to classify the Burgess fossils as primitive representatives of modern phyla. Gould noted that Walcott classified every Burgess species he examined within a modern group of organisms. If Walcott thought any of the Burgess animals had unusual

features, no such puzzlement was apparent in his notes or his classification scheme.

There has been some debate over whether Walcott's perception of the Burgess fossils

actually constituted a "shoehorn" as Gould suggested; Gould's term implies a forcing to fit

preconceived notions, without a careful study of the features which would reveal true

relationships, and not everyone agrees that Walcott was so blind and prejudiced as this.

Derek Briggs and Richard Fortey, in a 1992 book chapter, and Desmond Collins, in a 1996

article, both acknowledged that Walcott and other paleontologists of his day did attempt to fit

their fossil specimens into modem groups, but did not speculate about the theoretical

presuppositions which might underlie this attempt. Briggs and Fortey referred to the first

28 Gould, Wonderful Life, 244. 12 phase as the "lumping approach" to Cambrian classification; and Collins noted that this phase "encompassed attempts to classify the animals of the Burgess Shale within classes and phyla of animals living today."30

Yochelson objected vehemently to any slur on Walcott's name, and was particularly incensed by the charge, first made in Harry Whittington's 1971 monograph on the arthropod

Marrella splendens and repeated in Gould's Wonderful Life, that Walcott was so determined to see diagnostic features of modern groups in his Burgess fossils that he actually fabricated them, adding details to his drawings and retouched photographs that were not actually present in the fossils themselves. Yochelson argued hotly:

Another myth of the Burgess Shale is that photographs were so heavily retouched that body features were modified and that Walcott even added non­ existent structures. These are serious accusations; restudy of Walcott's original specimens has destroyed them. He described what was present, and he did not change the morphology - period!31

Yochelson did not specify precisely which of Walcott's original specimens and photographs he studied and therefore felt he had cleared of suspicion, and Whittington and his Cambridge colleagues must be allowed the final word, as they actually examined and further prepared Walcott's specimens, comparing them detail by detail to his drawings and

Derek E.CBriggs, and Richard A. Fortey, The early Cambrian radiation of arthropods," in Origin and early evolution of the Metazoa. Jere H. Lipps and Philip W. Signor, eds., 335-373 (New York and London: Plenum Press, 1992), 350. 30 Desmond Collins, "The 'evolution' of Anomalocaris and its classification in the arthropod Class Dinocarida (nov.) and Order (nov.)," Journal of Paleontology vol. 70, no. 2 (1996), 292. 31 Yochelson, Smithsonian Institution Secretary, 79.1 must confess I found it hard to take Yochelson's pronouncements in this biography seriously. His two-volume biography of Walcott consists almost entirely of snippets culled fromWalcott' s diary entries, strung together with very little in the way of analysis, and with long and very odd chapter titles such as "The 'Normalcy' Years (May 1919-May 1921): Time Flies Like an Arrow, But Fruit Flies Like a Banana - One Contribution to the Silly Season." Silly indeed. Richard Fortey agrees; in a 2001 review of the second volume, he described Yochelson's account as "almost bruisingly detailed — we findou t what Walcott did on virtually every day of his life, stopping only at the lavatory door." Fortey also noted that "Yochelson tends to settle all accounts in Walcott*s fevour,an d the reader gets the impression that his admiration for this prototype Washington mandarin borders on idolization." Richard A. Fortey, "The American dream personified?" Review of Smithsonian Institution Secretary, Charles Doolittle Walcott by Yochelson, Nature vol. 414, no. 6859 (1 November 2001): 19-20. 13 photographs. Whittington wrote with some aspersion, "Several [of Walcott's illustrations]

are heavily retouched to the point of falsification of certain features, notably the representation of the supposed mandible, maxilla, and maxillula."32 This fabrication is highly significant, as the presence of these three post-oral pairs of appendages are diagnostic of trilobites - the group into which Walcott classified Marrella. Whittington's discovery that these appendages were not actually present, along with several other anomalous features, forced him to revoke Walcott's classification in his 1971 restudy of Marrella (more on this below).

In his biography of Walcott, Yochelson defended the busy director by arguing that his classification of Burgess species was not an unthinking accommodation to the whiggish, progressive view of evolution of his day, "virtually without constraint from [the] Burgess data," as Gould claims.33 In fact, Yochelson argued, when compared to contemporary taxonomic schemes and practices, Walcott's interpretation of the Burgess fauna is actually daring and unconventional. As Yochelson explained, Walcott worked on the Burgess fauna at a time when it was not acceptable - or even conceivable - practice among systematic paleontologists to erect higher taxa based solely on extinct forms. "Tinkering with higher categories was not the fashion at the end of the nineteenth century, or for many years thereafter," Yochelson asserted, and added that even in the mid-twentieth century, the highly influential paleontologist George Gaylord Simpson "argued that there were no extinct phyla and virtually no extinct classes."34 Viewed in this context, Gould's "shoehorn" no longer fits: while it is true that Walcott did not erect any new phyla or classes for his Burgess Shale

32 Harry B. Whittington, "Redescription of Marrella splendens (Trilobitoidea) from the Burgess Shale, Middle Cambrian, British Columbia," Geological Survey of Canada Bulletin vol. 209 (1971), 20. 33 Gould, Wonderful Life, 244. 34 Yochelson, Smithsonian Institution Secretary, 547. 14

organisms, he "consistently used the concept of new families and new orders to convey how

different these fossils were." This reluctance among biologists to recognize new phyla or

classes of extinct organisms was only weakened, according to Yochelson, by the new studies

of the Burgess Shale in the 1960s, which revealed organisms that seemed to utterly defy

conventional classification.35

After Walcott's death, the Burgess Shale was not studied in any depth for forty years.

Percy Raymond, a geologist and trilobite expert at Harvard University, excavated in the

Walcott Quarry both shortly before and after Walcott's death, and Yochelson included in his biography a letter from Walcott's widow, Mary Vaux Walcott, to Charles Greeley Abbot,

Walcott's successor as Smithsonian Secretary, expressing concern over Raymond's presumption. She wrote,

You know in Dr. Walcott's collection there were a number of undescribed specimens, and these are what are causing me uneasiness. I think these should be described & named, as Raymond is an uncertain quantity, with Harvard swelled head, and I should very much dislike him to have any credit from our quarry which should belong to Dr. Walcott.36

In addition to removing five boxes' worth of specimens fromth e Walcott Quarry, Raymond also began another excavation about twenty metres higher up on Fossil Ridge, which is now known as the Raymond Quarry. Raymond brought his fossils back to the Museum of

Comparative Zoology at Harvard, where they, like Walcott's specimens at the Smithsonian,

languished virtually unexamined until the 1960s. The chief exception to this was the work of

Norwegian paleontologist Leif St0rmer, whose contribution to the Treatise on Invertebrate

Paleontology of 1959 required him to describe and reclassify the Burgess arthropods.

35 The question of when and whether it has been appropriate to erect higher taxa for extinct organisms will be discussed in more detail in Chapter 5. 36 Letter from Mary Vaux Walcott to Charles Greeley Abbot, August 9,1930 (SIA, RU 46, Box 103, Folder 10), qtd. in Yochelson, Smithsonian Institution Secretary, 504. 15

Stermer created a new class, the Trilobitoidea, which he placed alongside the trilobites proper (Class Trilobita) in a new , the Trilobitomorpha, within the Phylum

Arthropoda.37 The Trilobitoidea, which included most of the Burgess arthropod genera, contained animals that were clearly arthropods, and which possessed limbs similar to those of trilobites, but could not be accommodated within the trilobites proper. As Gould explained,

"Instead of spreading the Burgess arthropods widely among groups throughout the phylum

[Arthropoda, as Walcott had], he [St0rmerj brought most of them together in allegiance with the trilobites themselves." This strategy, in Gould's estimation, was merely a different version of the shoehorn: "Both Walcott's scattering into a broad range of known groups, and

Stormer's gathering together as the Trilobitoidea remained fully faithful to the rule of the shoehorn - all Burgess genera belong in established groups."38 I would argue that Stermer's method does make them more distinct that Walcott's; notwithstanding Gould's sleight-of- hand in dismissing the significance of the Trilobitoidea, the fact remains that the

Trilobitoidea is a new class, and as such represents a novel higher taxon into which Stormer placed several Burgess species. It appears, then, that by the end of the 1950s, the "shoehorn" was already cracking. When the Burgess fossils were re-studied in the late 1960s and 1970s, a new interpretation took hold, as we will see.

Yochelson and Gould suggest several reasons for the forty-year lag in Burgess Shale research, including the lack of funds during the Great Depression; the advent of World War

II; the growth of the oil industry and its focus on younger rocks; the possessiveness expressed by Walcott's widow (as illustrated in the above letter); the inaccessibility of

37 Leif Stermer, "Trilobitomorpha," in Treatise on Invertebrate Paleontology, Part O, Arthropoda 1. Raymond C. Moore, ed. 022 (Lawrence: Geological Society of America and University of Kansas Press, 1959), and Leif Stermer, "Trilobitoidea," in Treatise on Invertebrate Paleontology, Part O, Arthropoda 1. Raymond C. Moore, ed. 023 (Lawrence: Geological Society of America and University of Kansas Press, 1959). 3$ Gould, Wonderful Life, 112-113. 16

Walcott's specimens (they were stored out of sight in the top drawers of high cabinets, in a

building that lacked air conditioning); and finally the "tacit assumption" by other Cambrian

geologists/paleontologists that Walcott had done a sufficient job on the Burgess Shale and

little more real work was required.39 Forty years later, Whittington and his team would

realize that the real work was just getting started.

Phase 2: The "Cambridge Campaign "40

By the mid-1960s, the GSC's project of mapping Canadian geology had brought them

to the particular stretch of the that included the Burgess Shale, and it

seemed logical to begin a new study of these ancient organisms. The GSC invited

Cambridge trilobite expert Harry B. Whittington, then in his fifties, to head the paleontological aspects of this mission (the geological aspects were supervised by GSC

geologist James Aitken). New excavations were conducted in the summers of 1966 and

1967, and Whittington brought the collected fossils back to Cambridge for study.

Whittington focused his attention on the trilobites and trilobite-like fossils. Two other

English paleontologists, David Bruton and Christopher Hughes, were brought in to work on the - and merostomoid or -like Burgess arthropods. Whittington invited two graduate students at Cambridge, Derek Briggs and Simon Conway Morris, to handle the bivalved arthropods and Burgess worms (, priapulids, and other worm­ like fossils), respectively. Bruton had participated in the field work in 1967, but the other members of the "Cambridge campaign," as Conway Morris has referred to this episode in

Burgess history, were brought in after excavation was complete - Briggs and Conway Morris

39 Gould, Wonderful Life, 111, and Yochelson, Smithsonian Institution Secretary, 541. 40 Simon Conway Morris, The Crucible of Creation: The Burgess Shale and the Rise of Animals (Oxford: Oxford University Press, 1998), 45. did not begin work until late 1972. As well as preparing and studying the new material from

the 1966-67 field seasons, the Cambridge team also made several trips to the Smithsonian

Museum in Washington, D.C., to study Walcott's original specimens.41

Though I shall refer to these five men as "the Cambridge team," for the sake of

simplicity and to distinguish them fromothe r scientists who have worked on the Burgess

Shale, they did not really function as a team at all. As we have seen, they began their work on the Burgess Shale at different times, and at different stages of their respective careers.

Further, each man independently studied his own designated group of fossils and came up with his own conclusions. Though they collaborated on a few joint publications about the

Burgess Shale, these too were, for the most part, conceived independently. The Atlas of the

Burgess Shale, for example, edited by Conway Morris and published in 1982, contains individual sections written independently by each of the different team members; Conway

Morris simply requested contributions fromth e others, compiled them, and sent the lot to the publisher. Nor, when their detailed examination of their respective fossils began to reveal highly unusual combinations of characters that made classification extremely difficult, did they get together as a team and come up with a unified theory to account for these oddities.42

Four of the fivetea m members (i.e., all but Conway Morris) were needed to cover the various groups of arthropods because the vast majority of Burgess fossils were found to be arthropods (as are the vast majority of extant species). Arthropods are distinguished from other animal groups primarily by their possession of a sclerotized exoskeleton, and by their jointed appendages. (The word "arthropod" literally means "jointed foot.") Traditionally, arthropods were thought to have descended from bilaterally symmetrical, serially segmented

41 Conway Morris, Crucible of Creation, 45. 42 Simon Conway Morris, Interview by author, 10 January 2007 (Cambridge, England, MP3 recording). 18 ancestors, and the classification of the arthropods was based on the many alterations they appear to have made to the basic segmented body plan.43 (Figure 3) In the arthropods, adjacent segments of particular body regions have been modified, often through fusion, into functionally cohesive units (the units are known as tagmata, and the process of fusion is tagmosis). Thus in many arthropods, three basic tagmata can be recognized: the head, the trunk, and the tail (these may be given different names in different arthropod groups).

Each tagma often bears associated appendages that have also been modified for the particular function of that body part. The ancestor of the arthropods presumably bore identical biramous (double-branched) appendages on each of its identical body segments.44

(Figure 4) The upper branch of each appendage would probably have been modified into a gill, for respiration, while the lower branch would have been a more familiar-looking walking leg. Evolutionary modification of these ancestrally biramous limbs has often involved the loss of one of the two leg branches (thus leaving a uniramous appendage) and/or morphological changes in the remaining branch(es). For example, arthropod trunk segments often bear biramous limbs with gill and walking leg segments, while the head appendages have often been modified into uniramous anterior antennae and ventral feeding appendages.

It is important to note that in the case of the biramous arthropod appendage, the two parts of the appendage originate from a shared protuberance called a coxa; they do not arise

43 Traditional phytogeny would name the annelids (segmented worms) as the ancestors of the arthropods. More recent work suggests the arthropods may he more closely related to the nematodes or roundworms, as members of the Superphylum . (See Anna Maria A. Aguinaldo, et al., "Evidence for a of nematodes, arthropods and other moulting animals,"Nature vol. 387, no. 6632 (May 29,1997): 489-493.) In either case, however, the classification of the groups within the Arthropoda remains essentially unchanged, and the onychophorans and remain the closest relatives of the arthropods (these are typically classified as either basal arthropods or as the sister groups of the arthropods). 44 R.A.Robison, and R.L. Kaesler, "Phylum Arthropoda," in Fossil Invertebrates, R.S. Boardman, A.H. Cheetham, & A.J. Rowell, eds., 205-269 (: Blackwell Scientific Publications, 1987), 205-210. 19

Figure 3. Four Major Arthropod Body Plans A. Trilobitomorpha, B. Insecta (a sub-group of the Uniramia, on Manton's classification), C. Crustacea, D. . Different groups of arthropods have evolved different tagmata or regions of fused body segments, each with characteristic numbers and types of appendages. Modified from Steamer, "Arthropoda - general features," 05. 20

Figure 4. Biramous Arthropod Appendage Many arthropods possess biramous limbs, or limbs with two distinct branches which arise from a common segment called the coxa. Typically, the upper (dorsal) branch is a gill, while the lower (ventral) branch is a walking leg. The biramous limbs of different arthropods, or those attached to different segments of the same arthropod body, may be heavily modified. For example, in the head appendages, the gill branch may be lost, and the walking leg may have been altered to become a feeding appendage. Modified from Steamer, "Arthropoda - general features," 09.

independently of each other from the body wall, but are truly two parts of a single

appendage.

In the mid 20th century, most biologists recognized four major groups of arthropods:

the Trilobitomorpha, the Chelicerata, the Crustacea, and the Uniramia.45 These groups were

generally defined based on the two main criteria just discussed: numbers and types of tagmata, and associated appendages.46 By examining their patterns of tagmosis, and the

45 e.g. Derek E.G. Briggs, "Early arthropods: dampening the Cambrian explosion," in Arthropod . Short Courses in Paleontology, No. 3. D.G. Mikulic, ed., 24-43 (Knoxville: The Paleontological Society, 1990), 24. 46 Robison and Kaesler, 212. 21 numbers, arrangements, and types of appendages, scientists were able to classify all known arthropods, living and fossil, into one of these four groups. Then came the new work on the

Burgess Shale, begun in the late 1960s.

The Burgess Shale contains arthropods with combinations of tagmata and appendage numbers, types, and positions that had never been encountered before. Many of the Burgess

Shale arthropods proved almost impossible to classify because they are undeniably arthropods (they possess the characteristic features, including jointed limbs and an exoskeleton), and yet, because of their unique combinations of tagmata and specialized appendages, they could not be placed within any of the known arthropod groups.47 (Table 1)

Still other Burgess organisms seemed to be so strange that their affiliation with any known phylum was uncertain; they seemed to possess entirely unique body plans. When the

Cambridge team began their work on the Burgess Shale, they soon encountered creatures that seemed impossible to classify.

Whittington confronted such difficulties immediately, when he chose Marrella splendens, a small but plentiful arthropod with two pairs of large spines on its head shield, as his starting point in the new Burgess studies. (Figure 5) Walcott had classified Marrella as a trilobite. In 1959, in the new Treatise on Invertebrate Paleontology, Stermer had revised this classification, placing Marrella in a new Class Trilobitoidea, as a close relative of the true

Class Trilobita, both grouped together within a new Subphylum Trilobitomorpha. Starmer

47 Jonathan Bard, "The fifth day of creation," BioEssays vol. 12, no. 6 (June 1990), 304. 48 The story of the initial descriptive work done by the Cambridge team has been recounted elsewhere, most notably in Gould, Wonderful Life. I do not repeat the entire story here, therefore, but restrict my examples to those descriptions that are particularly illustrative of the shift between Phases 2 and 3, and those that I was able to supplement with unpublished material. 22

Arthropod Head; Pre-Oral Head: Post-Oral Body Previously-Known Arthropods Uniramia 1 per segment None or 1 per segment Chelicerata 1 5 1 UR or BR per segment Crustacea 2 3 1 UR or BR per segment Trilobita 1 3 1 BR per segment Burgess Shale Arthropods or Possible Arthropods Anomalocaris 1 None None? Burgessia 1 3 BR 7 BR Leanchoitia 1 2 BR 1 BR per segment Marrella 2 None 1 biramous per segment Odaraia None 1 1 BR per segment None 1 1 per segment; segments 5-9 BR Yohoia 1 3 1 BR, segments 1-10 only

Table 1. Appendage Distributions in Modern vs. Burgess Shale Arthropods UR = uniramous; BR = biramous. ? indicates information not available at the time of generic diagnosis. Data from Bard, 304, and Collins, "The 'evolution' of Anomalocaris" 285. described the Trilobitomorpha as "Aquatic Arthropoda with preoral antennae and remaining appendages of typical or modified trilobite type, biramous appendages characterized by presense of a lateral gill branch attached to very base [coxa] of walking leg."49

Whittington initially accepted the classification of Marrella as trilobite-like, but as he began his examination of Marrella, he began to note many departures from typical trilobite morphology. These details had not been observed by earlier scientists because they had not examined all specimens closely, nor had they appreciated the wealth of detail afforded by preparing specimens and examining those preserved in various orientations to the bedding plane of the shale. Whittington realized that he could gain new insights into each creature's three-dimensional structure by "dissecting" through layers of sediment and overlying

Stermer, "Trilobitomorpha," 022. 23

Figure 5. Marrella splendens Modified from Briggs and Fortey, "The early radiation and relationships of the major arthropod groups," 242. Originally drawn by P. Baldaro. fossil to reveal hidden features, and by comparing different specimens preserved in different orientations.50 Marrella had many jointed biramous appendages, like trilobites, but its walking legs had only six segments, not eight as in almost all trilobites. Marrella also turned out to have different head appendages than trilobites (not including the unusual head spines, which were not appendages): Marrella bore two pre-oral pairs of antennae, and no post-oral appendages (e.g. no mandibles or maxillae), while trilobites have one pre-oral pair of antennae and three pairs of biramous post-oral appendages.51

Whittington was thus faced with a dilemma: while bearing a general resemblance to trilobites, Marrella did not possess the defining features of all trilobites, nor did it fit into any other known arthropod group. Though he kept Marrella in Stormer's Trilobitoidea in his first published description of the unusual 'lace crab' as Marrella was informally known,

Whittington, "Redescription of Marrella splendens," 1-5. Whittington, "Redescription of Marrella splendens," 1. Whittington "knew it was a bust": Marretta was too different to fit into any known group of arthropods, but he did not know where Marretta did fit.

Whittington's next project was Yohoia tenuis, another arthropod that Walcott had placed within the branchiopod crustaceans, and Steamer had included in his Trilobitoidea.

(Figure 6) Whittington discovered that Yohoia possessed three pairs of post-oral head appendages, like trilobites, but they were uniramous, not biramous, indicating substantial evolutionary modification from the trilobite body plan. Further, Yohoia lacked pre-oral antennae, and had instead a pair of large grasping pre-oral ventral appendages, with spiny tips. No other known trilobite or crustacean, or indeed any known arthropod, possessed appendages like these. Yohoia's trunk appendages were also very unusual, being flattened, lobe-like, and covered with hair-like fringes.53 Whittington had examined only two Burgess species so far, and both seemed too unusual - lacking in some requisite features and possessing other, unique, features - to fit into established groups.

Figure 6. Yohoia tenuis Modified from Briggs and Fortey, '"The early radiation and relationships of the major arthropod groups,' 242. Originally drawn by P. Baldaro.

52 Whittington qtd. in Gould, Wonderful Life, 121. 53 Harry B. Whittington, "Yohoia Walcott and Plenocaris n. gen., arthropods fromth e Burgess Shale, Middle Cambrian, British Columbia," Geological Survey of Canada Bulletin vol. 231 (1974), 4. 25

The next Burgess organism Whittington tackled was Opabinia regalis, which Walcott had classified as another branchiopod crustacean, probably quite primitive as its long segmented body with simple appendages struck him as not too far removed from its supposed annelidan ancestor.54 (Figure 7) Walcott could not find any of the various head appendages that characterize all known arthropods, except for a nozzle-like structure at the front of the head. Opabinia was particularly unusual in lacking antennae. Previous workers, including

St0rmer and Simonetta, claimed to have seen a medial line running down the length of the frontal nozzle, and thought therefore that it might represent a fused pair of antennae.

Whittington, however, could find no evidence of this line in any of the specimens he examined.55

Several paleontologists, including Walcott himself, G. Evelyn Hutchinson (who reviewed some of Walcott's Burgess specimens in 1931) and Alberto Simonetta (who undertook his own review of known Burgess specimens in the 1960s and 70s), interpreted the flattened and fringed lobes of the thorax as gill limbs, and expected that walking legs would be found underneath them, giving Opabinia true biramous arthropod limbs. These walking legs had not yet been found, however; so Whittington, with his new appreciation for the three-dimensional preservation of the Burgess fossils, carefully "dissected" through the gill­ like appendages. He found nothing. The trunk of Opabinia did seem to have two types of

"appendages" - a series of flattened overlapping lobes, and overlying all but the first lobe on each side, a flattened,sheet-lik e gill. But the lobes were not jointed like true walking

54 Gould, Wonderful Life, 127. 55 Harry B. Whittington, "The enigmatic animal Opabinia regalis, Middle Cambrian, Burgess Shale, British Columbia," Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences vol. 271, no. 910 (1975), 32-33. 26

Figure 7. Opabinia regalis Modified from Gould, Wonderful Life, 126. Originally drawn by Marianne Collins. legs, and, crucially, the gill and lobe of each body segment did not arise from a common coxa, but instead each gill and each lobe arose independently from the body wall. The lobes and gills of Opabinia were therefore nothing like the appendages of true arthropods.

Opabinia also turned out to have five eyes - two paired and one central (Walcott had only observed one pair of eyes).56 Once again, Whittington was faced with a creature that defied known classification - only the situation was even more bizarre than before. While

Marrella and Yohoia could not be placed within any known group of arthropods, they were at least recognizably arthropods. Opabinia, with its lack of the typical jointed head and body appendages, could not be classified within the Arthropoda at all, nor indeed in any known group of animals. In the conclusion to his monograph on Opabinia, Whittington wrote:

Whittington, "The enigmatic animal Opabinia regalis" 2. "This enigmatic animal thus exhibits features common to arthropods and annelids... but cannot be placed in any recognized group of either."57

While Whittington was working on these three species, his colleagues were making unusual discoveries of their own. Hughes's study of Burgessia bella proved it to be neither a merostome nor a crustacean but another arthropod of uncertain affinities, possessing "a mixture of characters... many of which are to be found in modern arthropods of various groups." Briggs came to a similar conclusion in his analysis of Branchiocaris pretiosa.

Briggs was assigned the Burgess arthropods with bivalved carapaces to study, and expected them all to be crustaceans, since all modern bivalved arthropods are crustaceans. Some, like

Perspicaris and , did meet these expectations, but some did not. In addition to their bivalved carapace, crustaceans are also characterized by the possession of five pairs of head appendages, two pre-oral (usually antennae) and three post-oral (usually feeding appendages). Briggs discovered that Branchiocaris was "externally more crustacean-like," in that it possessed a "bivalved carapace, lamellate trunk appendages, and a pair of uniramous antennae."59 However, it also possessed an unusually robust pair of post-oral head appendages. These were not antennae, but instead possibly grasping arms ending in pincers, and like nothing Briggs had seen before. Once again, a Burgess arthropod had been discovered whose features matched no known arthropod group.60

Conway Morris had been given the Burgess worms as his assignment, but was unable to start immediately due to illness (he developed appendicitis, followed by

57 Whittington, "The enigmatic animal Opabinia regalis," 41. 58 Christopher P. Hughes, "Rediscription of Burgessia bella fromth e Middle Cambrian Burgess Shale, British Columbia," Fossils and Strata, vol. 4 (1975), 434. 59 Derek E.G. Briggs, Unpublished notes for a presentation at the 1979 meeting of the Paleontological Society entitled "A short course on arthropods," part of the Geological Society of America Meeting in San Diego. Non- archived personal notes in possession of Derek Briggs, Yale University, 9 (hereafter "Briggs Notes"). 60 Gould, Wonderful Life, 157-163. 28

septicemia).61 As he recovered, his observation of his colleagues' discoveries of unusual

creatures led him to suspect that not all of his own specimens awaiting study would fit comfortably into established annelid groups. Conway Morris therefore set out deliberately to find any oddballs among his assigned specimens. This search revealed several highly unusual species, including Nectocaris pteryx, Hallucigenia sparsa, Laggania cambria, and

Wiwaxia corrugata.

Nectocaris was one of the many Burgess species which Walcott had discovered, but did not have time to name or describe. (Figure 8) This creature, known only from a single specimen, was unusual in that it seemed to have the head of an arthropod, but the body of a . The head appeared to be enclosed in an arthropod-like carapace, and bore stalked eyes. It also carried at least one pair of appendages (probably pre-oral, as in crustaceans), but these did not appear to be jointed, as in true arthropods. Also, the body, while apparently segmented, did not bear jointed appendages; instead, it seemed to have two fins, one dorsal and one ventral, both supported by fin rays, as in . The Phylum Chordata includes humans and all other animals, and is not thought to be closely related to the

Phylum Arthropoda, so this apparent mixture of chordate and arthropod characters was very puzzling. Conway Morris concluded that Nectocaris could not be classified within the arthropods but also "cannot be shown to have a greater affinity with any other fossil or recent phylum." Nectocaris remained a mystery, classified in "Phylum Uncertain."62

Conway Morris, Crucible of Creation, 50. 62 Simon Conway Morris, "Nectocaris pteryx, a new organism fromth e Middle Cambrian Burgess Shale of British Columbia," Neues Jahrbuchfiir Geologie und Paldontologie vol. 12 (1976), 712. Figure 8. Nectocaris pteryx Modified from Gould, Wonderful Life, 146. Originally drawn by Marianne Collins.

One of the most famous Burgess creatures is one studied and re-named by Conway

Morris: Hallucigenia sparsa. (Figure 9) Walcott originally named this creature Canadia sparsa, and classified it as a worm, but Conway Morris saw immediately that it was very different from Walcott's other Burgess , such as Canadia spinosa, and in fact, resembled nothing Conway Morris had ever seen. His "dissections" of various specimens showed that the creature then known as Canadia sparsa had no immediately identifiable head, paired rows spikes on one side of the body, and a row of tentacle-like structures on the other. Conway Morris surmised that the creature walked on the paired spikes and fed with the various tentacles, each of which probably therefore led independently to the gut, and he (in collaboration with a friend, trilobite paleontologist Ken McNamara) 30

Figure 9. Hallucigenia sparsa (Conway Morris, 1977) Conway Morris's initial reconstruction of Hallucigenia sparsa showed it walking on paired spikes (sunk a few millimetres into the seabed) and bearing a single row of dorsal tentacles. Conway Morris speculated that the tentacles were hollow, each acting as a separate mouth and leading independently to the gut. Modified from Conway Morris, "A new metazoan fromth e Cambrian Burgess Shale," 628. renamed the unusual creature Hallucigenia "as a tribute to its dream-like appearance."

Hallucigenia was, at the time, one of the most obviously unique Burgess creatures, and was yet another to be given "Phylum Uncertain" status.

Another of Walcotfs polychaete worms to be restudied by Conway Morris was

Wiwaxia. (Figure 10) Conway Morris discovered that Wiwaxia lacked the hair-like setae and body segmentation of true polychaetes, and possessed unusual scale-like sclerites, spines, and a pair of tiny "jaws." Though the jaw apparatus somewhat resembled the radula or feeding apparatus of molluscs, Conway Morris viewed Wiwaxia's anatomy on the whole as strange enough to dissociate it from this, or any other, known phylum.64

Simon Conway Morris, "A new metazoan fromth e Cambrian Burgess Shale of British Columbia," Palaeontology vol. 20, no. 3 (1977), 624. 64 Gould, Wonderful Life, 189-193. 31

Figure 10. Wiwaxia corrugata Modified from Conway Morris, "The Middle Cambrianmetazoan Wiwaxia corrugata" 560.

Perhaps the best known weird wonder of the Burgess Shale is the creature Anomalocaris, a free-swimming predator much larger than any other Burgess organism (perhaps more than a metre in length). (Figure 11) The first Anomalocaris canadensis specimen was discovered in 1886 by Canadian geologist R. G. McConnell in the trilobite beds of Mount Stephen, near but not in the then-unknown Burgess Shale. This specimen was described in 1892 by Joseph

Whiteaves, chief paleontologist for the GSC, as the headless carapace of a crustacean.

Further expeditions over the next eighty years, by Walcott and by the Cambridge team, failed to turn up any complete specimens of this supposed crustacean, although some speculated that its front half might be Tuzoia, another crustacean-like fragmentary fossil. During this Figure 11. Anomalocaris canadensis - The Complete Animal Modified from Whittington and Briggs, "The largest Cambrian animal, Anomalocaris," 595. time several other unusual organisms were discovered and named, including the

Peytoia, and the baglike Laggania, interpreted by Walcott as a , and redescribed by Conway Morris in 1978 as a .

It was not until 1981 that a new specimen revealed that three of these four "genera" were in fact different body parts of a single organism: the bulbous Laggania was the body, the jellyfish-like Peytoia was its mouth, and the -like Anomalocaris was actually an isolated frontal feeding appendage (Tuzoia was found to be unrelated). These results were published by Whittington and Briggs in 1982 and 1985. Once again, the Burgess Shale had yielded a creature so strange it could not be placed within any known group of animals.

By the end of the 1970s, it seemed clear to the Cambridge team that the Burgess

Shale contained representatives of several hitherto unknown phyla, very different from modern animals, as well as some representatives of modern phyla. Whittington wrote in

1979: "The Burgess Shale forms include three trilobites with appendages, early crustaceans, and a possible uniramian ancestor; the remainder represent separate lines of descent apparently unrelated to major taxa."65 Whittington declined to classify the problematic

Burgess arthropods to a rank higher than the family level, but admitted they did not seem to show any particular relationship to each other or to modern arthropods.66 He also included a diagram which depicted dozens of independent groups of arthropods, in addition to the four groups already known, evolving in parallel through the Paleozoic. This diagram is recognized as depicting a taxonomic concept known as a "phylogenetic lawn," and will be discussed in much more detail in Chapter 2.

In a short paper for a 1981 conference, Whittington stated that " evolution may have been as complex as that of the Phanerozoic," and referred to "The many distinct lines of descent that are recognizable in the Early Cambrian [which] are the product of this pattern." He then speculated that not just the arthropods, but indeed the metazoa

(animals) as a whole might be polyphyletic.67 For Whittington then, the Burgess Shale did not show the relationships of fossil animals to each other and to modern groups, but instead demonstrated that these fossils represented many unique lines of descent unrelated to each other or to modern animals.

Harry B. Whittington, "Early arthropods, their appendages and relationships," in The Origin of Major Invertebrate Groups. The Systematics Association Special Volume No. 12. M.R. House, ed., 253-268 (London: Academic Press, 1979), 253. 66 Whittington, "Early arthropods, their appendages and relationships," 261. 67 Harry B. Whittington, "The Burgess Shale fauna and the early evolution of metazoan animals," in Short Papers for the Second International Symposium on the Cambrian System. Michael E. Taylor, ed., 239. (U.S. Department of the Interior, Geological Survey Open-File Report 81-743,1981), 239. Briggs and Conway Morris were coming to the same realization. The Cambridge team collaborated in 1982 to publish an Atlas of the Burgess Shale.6* This atlas included brief descriptions of twenty-three Burgess species. Among the twenty-three were four species classified only as "" (i.e., of uncertain taxonomic position), and nine classified as arthropods of uncertain position. Given that the Arthropoda at that time was considered to be an informal group comprising of several phyla which had all achieved

'arthropodization' independently, this list of twenty-three species actually includes thirteen potentially new phyla.69

In 1985 Conway Morris and Whittington published another general report on the

Burgess Shale. In this report, they wrote:

Although the various species in the Burgess Shale that can be placed in a particular phylum may be very different from their descendants alive today, there is usually no difficulty in recognizing the underlying bodyplan. There are, however, quite a large number of species with such a unique anatomy that it seems impossible to place them in any known phylum.70

In another article published in 1985, Whittington wrote, "As detailed investigations of particular fossils have confirmed and emphasized strange morphologies, we are having to admit that strange body plans that have become extinct were part of the early radiation of metazoans."71

Though the Cambridge team were reluctant to formally establish a new phylum for each apparently unique Burgess genus, their inability to place these unusual genera within known phyla did imply that such a drastic measure might be necessary. As in Walcott's day,

Simon Conway Morris, ed., Atlas of the Burgess Shale, (Silverstone: Palaeontological Association, 1982). 69 Conway Morris, ed., Atlas of the Burgess Shale, 1. 70 Simon Conway Morris, and Harry B. Whittington, Fossils of the Burgess Shale: A National Treasure in Yoho National Park, British Columbia, (Geological Survey of Canada Miscellaneous Report 43,1985), 21. 71 Harry B. Whittington, "Introduction," Extraordinary Fossil Biotas: Their Ecological and Evolutionary Significance. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences vol. 311,no. 1148 (1985), 3. 35 paleontologists were initially reluctant to erect higher taxa based solely on fossils.

Additionally, biologists and paleontologists expect that a higher taxon will show a certain minimum level of diversity: a phylum should contain multiple classes; each class should contain several orders; each order should contain several families; each family should include many genera, and each genus should comprise several species. To establish a new phylum, class, order, family and genus for a single unusual species seemed ludicrous, initially. But as more and more bizarre fossils were discovered, with no discernible relationship to each other or to modern organisms, this ludicrous step began to seem like the only possible solution. As a sort of compromise, the Cambridge team began to apply terms like "Phylum Uncertain" and "incertae sedis" to the problematic Burgess taxa.

According to Yochelson, the category of incertae sedis is useful in two ways: first, it prevents one from forcing a species into a higher category in which it does not really belong; and second, it serves to flag the problematic group for further study, instead of concealing its difficulties behind a conventional label.72 The term "Phylum Uncertain" plays a comparable role in classification. Though the Cambridge team at first seemed to make use of these categories as mere placeholders, as time went on and they were forced to apply these labels to more and more Burgess taxa, they eventually began to speculate that these unusual forms really did represent novel phyla. Not knowing where things belonged began to feed doubts that anything belonged.

Whittington's Cambridge team discovered that most Burgess specimens contained a puzzling and unique mixture of familiar and bizarre characters. The unusual morphologies of the Burgess creatures prevented them from being "shoehorned" into modern groups, and a

72 Ellis L. Yochelson, "Agmata, a proposed extinct phylum of early Cambrian age," Journal of Paleontology vol. 51, no. 3 (May 1977), 438. 36 belief arose that many new classes and even phyla of animals must be proposed to accommodate the incredible diversity of the Burgess Shale fossils.73 Collins described this as a phase which "postulates that Cambrian animals that cannot be classified in modern groups are members of classes and phyla that have become extinct." Briggs and Fortey called this phase the "multiple polyphyly approach," and described it as encompassing the belief that "the various Cambrian arthropods were surmised to have had separate 'soft- bodied' ancestors," and "there was no indication of whether any one arthropod is more closely related to any other." Briggs and Fortey credit Sidnie Manton as the chief inspiration for this interpretation. These Phase 2 beliefs were expressed in the published papers of each member of the Cambridge team, including Briggs, Conway Morris, and Whittington.

Whittington envisioned the evolution of the arthropods as a phylogenetic lawn, based on his re-descriptions of the Burgess fossils, and the influence of his mentor, Sidnie Manton.

Manton, the greatest carcinologist and one of the greatest functional morphologists of the

20th century, proposed in mid-century that the arthropods comprise several unrelated groups which had each arisen independently from different ancestors, inspiring the belief, widely held in the 1970s and early 1980s, that many more classes and phyla of animals existed in the

Cambrian than have survived to the present day. (Manton's classification and influence will be discussed below.)

The idea that the disparity of organic form was vastly greater in the Cambrian Period than it is now has significant implications for the history of life and the tempo and mode of

73 "Walcott's shoehorn" and "weird wonders" were the names that Gould gave to the two phases of Burgess Shale research discussed in his book Wonderful Life (e.g. 110,188). The phrase "weird wonders" has been taken up by other paleontologists, and has become "a common term for a fossil organism that lacks obvious similiarities to any living taxon. In a cladistic sense, a weird wonder is an organism with numerous ; an organism is not a weird wonder if it is only poorly preserved or poorly known." (Benjamin J. Waggoner, "Phylogenetic hypotheses of the relationship of arthropods to Precambrian and Cambrian problematic fossil taxa," Systematic Biology vol. 45, no. 2 (June 1996), 191-192.) evolution. Evolutionists since Darwin have believed that both diversity (number of species or other taxa) as well as morphological disparity (amount of morphological difference between groups of organisms) have increased steadily over time. Darwin referred to this

slow, stately increase as the Principle of Divergence, demonstrated by the one illustration in

On the Origin of Species: a tree with a narrow trunk at the base, and ever-spreading and ramifying branches above.74

The fossils of the Burgess Shale seem to contradict this Principle, however. If the

Burgess Shale contains species of such great morphological uniqueness that they deserve to be classified as unique phyla, that would mean that morphological disparity was at a maximum in the Cambrian Period, and that it has since decreased, not increased as Darwin

(and evolutionists for 150 years after him) believed. These and other radical implications of the Burgess oddballs were presented in their most extreme form by Gould, in his 1989 book

Wonderful Life. Gould has played two commingled roles in the story of the Burgess Shale; he wrote the first historical treatment of it, and was the first author to discuss distinct phases of Burgess research and their implications. However, Gould is also himself a player in the

Burgess Shale debate; until his death in 2002 he was the staunchest defender of the Phase 2 view, which he called the "weird wonders" view. When Briggs and Conway Morris changed their minds about the interpretation of the Burgess fossils, forging the new, Phase 3, view, they were placed in the uncomfortable position of not just contradicting their own earlier published statements, but having to denounce the bestselling story of their triumphant

74 Charles Darwin, On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. 2nd ed. (London: John Murray, 1860 (1st ed. 1859)), 96-97. 38

"discoveries," as penned by Gould. This was especially difficult for Conway Morris, whom

Gould had lionized as the hero of the Phase 2 view.75

Based on the work of the Cambridge team in the 1970s and early 1980s, Gould predicted that the Burgess Shale contained, in addition to representatives of the four known arthropod classes and of most of the thirty or so known animal phyla, more than twenty new arthropod classes76 and at least fifteen to twenty new phyla.77 This news was astonishing, to say the least. Gould used this prediction as a platform on which to base a radical revision of the very nature of evolution: first, Gould proposed that morphological disparity, as measured by distinctness of body plans (where each body plan is called a phylum), reached a maximum early in the history of life and has declined ever since. This, Gould said, leads to his second claim, which is that the operation of evolution has been and is highly contingent. I shall discuss both claims below.

First, Gould claimed that the weird wonders of the Burgess Shale indicate that morphological disparity, was highest in the Cambrian period and has been declining ever since, with speciation occurring as mere variation on those few body plans remaining after a random (and unexplained) decimation. Diversity may still be increasing, in that the number of species may be getting larger, but most of these species may (and do) share the same basic body plan - so diversification is merely minor alteration to established morphology.

Disparity, on the other hand - a measure of major morphological difference - will not necessarily increase along with it, and Gould argued that in fact, disparity has decreased over time. Gould argued:

More on this in Chapter 3. Gould, Wonderfiil Life, 106,209. Gould, Wonderful Life, 99. The sweep of anatomical variety reached a maximum right after the initial diversification of multicellular animals [during the Cambrian explosion, shortly before the time of the Burgess Shale]. The later history of life proceeded by elimination, not expansion. The current earth may hold more species than ever before, but most are iterations upon a few basic anatomical designs.78

In a later paper, Gould phrased things more dramatically: "The Burgess Shale... does not contain many species; but, paradoxically, these few species express a wider range of design than one million living species do today."79 The traditional cone of increasing diversity, in which morphological difference increases steadily over time, is thus disproved, Gould asserted; instead, we have an inverted cone or bush, in which the greatest morphological difference occurs near the bottom and is subsequently pruned by . (Figure 12)

In addition to his arguments about diversity, Gould made a claim about contingency: if the animal phyla alive today are merely the randomly-chosen survivors of a once much greater number of phyla, then the history of life on Earth has been largely contingent, since other groups might have survived than the ones that actually did. Gould used the metaphor of 'replaying the tape of life' to express his view of evolution as highly contingent:

You press the rewind button, making sure you thoroughly erase everything that actually happened... Then let the tape run again [from the time of the Burgess Shale] and see if the repetition looks at all like the original. If each replay strongly resembles life's actual pathway, then we must conclude that what actually happened pretty much had to occur. But suppose that experimental versions all yield sensible results strikingly different from the actual history of life? What could we then say about the predictability of self- conscious intelligence? or of mammals? or of ? or of life on land? or simply of multicellular persistence for 600 million difficult years?80

78 Gould, Wonderful Life, 47. 79 Stephen Jay Gould, "Redrafting the tree of life," Proceedings of the American Philosophical Society vol. 141, no. 1 (March 1997), 51. 80 Gould, Wonderful Life, 48-50. 40

This contingency goes hand-in-hand with Gould's argument for maximal disparity in the

Cambrian, as I mentioned above. In Gould's theory of evolution, "The maximum range of anatomical possibilities arises with the first rush of diversification" - very early in the

Figure 12. Two Models of Morphological Disparity through Time A. the "cone of increasing diversity."81 According to the traditional view of evolution, morphological disparity was low in the early history of life and has increased steadily over time. The same phenomenon is illustrated by Darwin's Principle of Divergence. B. Gould's inverted cone, illustrating his model of diversification and decimation. In both diagrams, the vertical axis represents time, increasing upwards, and the horizontal axis measures morphological diversity, increasing outwards. On Gould's theory, morphological disparity reached a maximum in the Cambrian Period, early in the history of life (the widest part of the "bush" diagram, and has declined ever since, as existing body plans went extinct and new body plans failed to arise. Modified from Gould, Wonderful Life, 46. history of anirnitl life. Many of these init&l body plans then become extinct, not because they are inferior to those that survive, but for reasons of pure luck - "extinction by lottery,"

in Gould's phrase. "Later history," Gould concludes, "is a tale of restriction, as most of these

early experiments succumb and life settles down to generating endless variants upon a few

surviving models."82 We will return to Gould's theory of evolution, particularly the crucial notion of how life becomes "restricted" or "settles down," in Chapter 5. Here, it will suffice

81 Gould explicitly decouples diversity ("number of distinct species in a group") from disparity ("difference in body plans"), yet confusingly names his diagram depicting traditional beliefs about disparity the "cone of increasing diversity." Wonderful Life, 46-49. 82 Gould, Wonderful Life, 47. 41 to conclude that Gould used the Cambridge team's work, in the 1970s and early 1980s, to argue that the weird wonders of the Burgess Shale represented many new phyla of animals, and then used this hypothesis to launch his own theory of evolution as a highly contingent and punctuational process of initial diversification followed by extinction, and then stabilization or settling down of the remaining groups.83

Phase 3: A New View of the Burgess Shale

Even as Whittington and Conway Morris were admitting that they saw no way to fit the Burgess Shale oddballs into the known animal phyla, Derek Briggs, working with trilobite paleontologist Richard Fortey, was exploring a new method of classification that allowed them to start making sense of the relationships between the Burgess creatures, as well as their relationships with modern organisms. Then Conway Morris, upon examining new fossils from Sirius Passet and Chengjiang, as well as re-examining several Burgess fossils, also began to revamp many of his initial classifications, now affiliating Burgess oddballs with modern phyla. Finally, a new generation of paleontologists began to study and interpret the Burgess Shale fossils. Excavation of the Burgess Shale was taken over in the late 1970s and early 1980s by Desmond Collins, whose team collected over a hundred

Gould chose the name "decimation" for this phenomenon of extinction, defining it as the "random elimination of most lineages," {Wonderful Life, 47) and also referred repeatedly to a "lottery" or contest decided by "Lady Luck" (e.g., 48). He never provided any independent evidence mat this decimation actually occurred, and the closest he came to proposing a mechanism for it in the entire book is the vague suggestion that "Perhaps the grim reaper works during brief episodes of mass extinction, provoked by unpredictable environmental catastrophes (often triggered by impacts of extraterrestrial bodies)" (48). I findi t highly interesting that Gould can make such an ad hoc and unsupported claim, even in a work of popular science, and even more so that it has gone virtually unchallenged (see Daniel C. Dennett, Darwin's Dangerous Idea: Evolution and the Meanings of Life (New York, Simon & Schuster, 1995), 299-312, for the only published criticism of mis specific claim that I am aware of). I am intrigued by the thought mat this claim might have seemed unremarkable, even self-evident, in the general excitement over the Alvarez impact hypothesis and related periodic impact/ extinction hypothesis that swept the scientific community in the 1980s. But this is a story for another time. thousand new specimens now housed at the ROM. These specimens are now being studied by Collins's former student Jean-Bernard Caron, the ROM's current Curator of Invertebrate

Paleontology, who has already published reclassifications of several Burgess taxa. Finally,

Conway Morris's former student Graham Budd is focusing his attention on the fossils of

Sirius Passet. With the combined efforts of all these scientists, paleontologists now suspect that the weird wonders of the Burgess Shale aren't so weird after all.

Anomalocaris is now recognized as an arthropod, albeit in a unique class, the

Dinocarida (proposed by Collins in 1996). A few other former Burgess oddballs have also been placed in this class, including Opabinia. and Wiwaxia have recently been recognized as ancestral lophotrochozoans (a taxonomic group including the molluscs, annelids, and bracbiopods); their feeding apparatus turned out to be radulae after all.85 And

Hallucigenia, once the poster child of Burgess oddballs, has also found a home within a modern phylum: reoriented with the spikes up and the "tentacles" down, it is now recognized as an onychophoran, one of a group of fleshy-lobed creatures that are either primitive arthropods or the immediate sister group to them. As early as 1983, in an analysis of early crustacean relationships, Briggs wrote: "it seems unlikely that many of the groups [of crustacean-like Burgess Shale species]... are of separate origin." For some paleontologists at least, the Phase 2 view, in which Burgess taxa were unique phyla unrelated to modern organisms, had begun to give way. But why? As we will see, Briggs and Conway Morris both came to support the Phase 3 view, but independently and for totally different (indeed, conflicting) reasons. Gould, on the other hand, remained an outspoken defender of the Phase

84 Jean-Bernard Caron, Curator of Invertebrate Paleontology, ROM, personal communication, November 2004. 85 Caron, Jean-Bernard, A. Scheltema, C. Schander, and David Rudkin, "A soft-bodied mollusc with radula from the Middle Cambrian Burgess Shale," Nature vol. 442, no. 7099 (2006), 159. 86 Derek E.G. Briggs, "Affinities and early evolution of the Crustacea: the evidence of the Cambrian fossils." in Crustacean phytogeny. Frederick Schram, ed., 1-22. (Rotterdam: A. A. Balkema, 1983), 20. 43

2 view until his death. Why did these men hold such radically different views of the Burgess

Shale, and what are the implications of their different views? The answers to these questions form the basis of this dissertation.

Collins describes the third phase as a series of "attempts to demonstrate that most

Cambrian animals probably do belong in extant phyla, but some are in, as yet, unrecognized extinct classes. The third perception," Collins concluded, "thus falls in the spectrum between the extremes of the other two, visualizing a Cambrian world significantly different from the present but not quite so different as Gould proposed (1989)."87 Briggs and Fortey called their third phase the "cladistic approach," crediting their own application of this new systematic method with the changing perception of the Burgess Shale.88 Gould did not discuss a third phase in his 1989 book, presumably for two reasons. First, the third phase was still in its infancy when Gould was writing his book, and second, Gould did not agree with the Phase 3 interpretation of the Burgess Shale. However, a few years later, in a 1992 paper discussing the relocation of the Burgess genus Hallucigenia from "Phylum Uncertain" to a place within the onychophorans,89 Gould introduced a new taxonomic "tradition,"

"related" to the shoehorn, which he called "the straightening rod." The shoehorn and the straightening rod were presented as two incorrect philosophies of classification, in contrast to a third, correct, philosophy (the one held by Gould himself). Gould wrote: "The straightening rod tries to push a jutting thumb of oddness back into a linear array by designating the small and peculiar group as intermediary between two large and conventional

87 Collins, "The 'evolution' ofAnomalocaris," 292. 88 Briggs and Fortey, "The early Cambrian radiation of arthropods," 350. The application of cladistics to the study of the Burgess Shale, and its implications, are discussed in Chapter 2. 89 The , or velvet worms, are variously classified a subphylum or class within the arthropods, or their most closely related sister phylum. Their exact taxonomic position changes depending on the source one consults, but most if not all biologists and paleontologists agree that they are either arthropods or the closest sister group to them. See for example Richard CBrusca and Gary J. Brusca, Invertebrates (Sunderland: Sinauer Associates, Inc., 1990), 464. categories." In other words, the straightening rod "change[s] life's geometry from a tree to a line," by (falsely) placing Cambrian groups in positions where they anchor and connect existing branches of the tree, instead of representing separate and new branches of their own.91 Gould argues that both the shoehorn and the straightening rod are "misleading and restrictive," whereas his weird wonders approach captures the genuine disparity and uniqueness of the Cambrian fossils. He does not accuse anyone in particular of using the straightening rod, and calls it a taxonomic tradition (the better to highlight his own new and improved methods, no doubt), but from his description it seems to be meant to capture the new (Phase 3) view which had arisen to rival his own view. Certainly he only lists three ways to classify things - the shoehorn, the straightening rod, and his own way - so if one wanted to apply one of these labels to the Phase 3 understanding, it would have to be the straightening rod, by default. To his death in 2002 Gould continued to defend his weird wonders (Phase 2) interpretation of the Burgess Shale.

Interlude: A Return to Arthropod

As mentioned above, in Phases 1 and 3 the arthropods were classified as members of a single phylum, but for a brief period at the height of Phase 2, they were thought (by many paleontologists and biologists, including the Cambridge team) to comprise several different phyla, which had thus all achieved "arthropodization" independently (i.e., the resemblances they shared were accidents, not indications of close relationship). The classification of the arthropods - the most abundant animals in the fossil record and in the modern world - and

90 Stephen J. Gould, "The reversal of Hallucigenia? in Eight Little Piggies: Reflections in Natural History, 342- 352 (New York: W.W. Norton & Company, 1993), 344. 91 Gould, "The reversal of Hallucigenia," 345. 45 their perceived relationships with each other, have important implications for understanding the Burgess Shale, the modern biosphere, and the nature of evolution.

In terms of numbers alone, the same fossils were counted as one phylum in Phases 1 and 3 and as fifteen or more phyla in Phase 2, just because of the different rank assigned to arthropod groups at these different periods. Likewise the perceived relationships among arthropod groups have deep implications for the history of life and the operation of evolution: if the many arthropod groups constitute one phylum which evolved from a single common ancestor, then morphological disparity is reduced, and evolution is perceived as more conservative. If, on the other hand, several arthropod-like phyla arose independently, then disparity is high and evolution might be perceived as more flexible (since it would have created the same arthropod-like features in groups from different genetic and phylogenetic backgrounds). The possibility of multiple independent origins for many different animal phyla leads directly to Whittington's phylogenetic lawn, and is highly compatible with

Gould's interpretation of the Burgess Shale. The implications of arthropod classification and evolution will be discussed more fully in later chapters; here I provide a short history of the classification of the arthropods, since the mid-19th century, as a background for later discussion.

The Arthropoda was first recognized as a phylum by Karl von Siebold and Friedich

Hermann Stannius in 1848. The past 150 years have seen some major debates over the relationships among the various arthropod groups, and the reality of the Arthropoda itself as a unified group has been questioned several times. According to historian of evolution Peter

Bowler, until the early 1900s, classifications were argued primarily on the basis of evidence from embryology and comparative anatomy of extant organisms, not on the basis of fossil evidence. The privileging of extant over extinct affected not only the characters used to make the classification, but the classes themselves. Bowler asserts that the 1890s were the heyday of arthropod polyphyly, in that it was almost universally accepted that there had been

at least two separate origins for the major arthropod groups. Zoologists including Anton

Dohrn divided the arthropod-like animals into the Branchiata (crustaceans and trilobites) and the Tracheata (onychophorans, myriapods, , and ), believing that each of these two groups had arisen separately from a different annelidan ancestor, and had each evolved their defining arthropodan characters (e.g., sclerotized exoskeleton, jointed limbs) independently.

Bowler reported a brief shift towards a more conservative, monophyletic arthropod in the first half of the twentieth century, which can be seen in Walcott's and

Starmer's use of the Phylum Arthropoda in their classifications of Burgess fossils. However, this new shift was prevented from taking a firm hold by Sidnie Manton (1902-1979), an

English zoologist who took a functional morphological approach to classification. In a series of highly influential papers published fromth e 1950s through the 1970s, she argued for a separate origin for three major groups of arthropods: the uniramians, biramians, and chelicerates. Manton argued that the organs of the various arthropods, especially the head appendages, were so different in appearance and function in each of the major groups that they could not possibly have a common origin. It was this view of arthropod taxonomy - polyphyletic, and in which unique structures were perceived as markers of unique origin - that the Cambridge team learned and applied to their initial work on the Burgess Shale.

Whittington, Briggs, Bruton, and Hughes - the four members of the team working on the

92 Peter J. Bowler, Life's Splendid Drama: Evolutionary Biology and the Reconstruction of Life's Ancestry, 1860-1940, ( and London: The Press, 1996), 97-102. 93 Conway Morris, The Crucible of Creation, 171. arthropods of the Burgess Shale - each corresponded with Manton in the 1970s, to ask her

advice on the reconstruction and interpretation of the Burgess arthropods, and they each thanked her for her advice in the acknowledgments of their Burgess monograhps.94 Frederick Schram noted, in a review of Manton's 1977 textbook, her influence on the Cambridge team:

[T]he many papers that are appearing by several workers on the restudy of the Burgess Shale fauna are solidly in the Mantonian tradition. Many is the time I have listened to revelations of some new information on a Burgess arthropod when the conversation closed with the reverent amen- "Of course we've checked this out with Sidnie."95

Manton had very clear ideas about the value of neontological versus paleontological data for taxonomy. In a letter to Whittington dated 27 November 1976, Manton wrote:

"Palaeontologists can presumably do what [they] like with the , a group of heterogeneous extinct arthropods, but they should not interfere with the Leptostraca, created

for modern crustaceans, even if some extinct ones fit into this group." The point was made again in a letter from Manton to Briggs, dated 21 January 1977: "You can do what you like, by you I mean palaeontologists in general, with Phyllocarida, but you can't monkey with

Leptostraca, a group now a sub-class erected for extant crustaceans. If some fossils really fit

Correspondence between Whittington and Manton began, according to the letters present in the archive, in August 1971. The firstdate s of correspondence between Manton and Hughes, Bruton, and Briggs are 3 August 1973, and 12 July 1974 (this is the date of the firstletter s frombot h Bruton and Briggs). Sidnie Manton Collections - Correspondence, Manton Papers, Natural History Museum General and Zoology Library, London, Correspondence M-Z, box 2, Envelope: Whittington, H.B. 1971-1975, and Sidnie Manton Collections - Correspondence, Manton Papers, Natural History Museum General and Zoology Library, London, Correspondence A-L, box 1, Envelopes: Br - Bu, and Ho - Hu (Hereafter "Manton Correspondence"). In several of their early papers, members of the Cambridge team thanked Manton for valuable discussion. See for example Whittington, "The enigmatic animal Opabinia regalis" 3, and "The Middle Cambrian trilobite Naraoia, Burgess Shale, British Columbia," Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 280, no. 974 (31 August 1977), 440; Derek E.G. Briggs, "The morphology, mode of life, and affinities of Canadaspis perfecta (Crustacea: Phyllocarida), Middle Cambrian, Burgess Shale, British Columbia," Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 281, no. 984 (23 January 1978), 484; and David L. Bruton, "The arthropod Sidneyia inexpectans Middle Cambrian, Burgess Shale, British Columbia." Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 295, no. 1079 (18 December 1981), 651. 95 Frederick R. Schram, "Manton on arthropods," Review of The Arthropoda: Habits, Functional Morphology, and Evolution by Sidnie M. Manton (Oxford: Clarendon Press, 1977) Paleobiology vol. 5, no. 1 (Winter 1979), 65. in there, well and good, but you can't change Leptostraca. Finally, in a review of

Manton's 1977 textbook, fellow carcinologist Frederick Schram wrote: "Dr. Manton had never felt comfortable with fossils nor phylogenetic interpretations derived from them, and this is unfortunately too evident in the book."97 These examples show that Manton believed fossils, no matter how well preserved, may fit into modern categories or not, but cannot be used to revise the modern categories - these stand based on extant, not fossil, evidence.

Sidnie Manton's functional morphological approach to arthropods was a huge influence on 20th-century arthropod systematics, and also on Whittington and Briggs's interpretations of the Burgess Shale arthropods. In fact, an argument can be made that the

Phase 2 interpretation of the Burgess Shale follows naturally from Manton's arthropod classification. Though Manton did some embryological studies of arthropods, her series of highly detailed papers on arthropod locomotion (eleven papers, 1950-1973) and feeding mechanisms (two papers, 1963-1964) were better known, and she is most famous for her arguments regarding the evolutionary relationships of the arthropods, most explicitly articulated in her great textbook The Arthropoda: Habits, Functional Morphology, and

Evolution (1977).98 Whittington and the other Cambridge team members working on

Burgess arthropods wrote to Manton often for her guidance in interpreting their fossil specimens, particularly in terms of functional morphology.

96 Manton was in very poor health by the mid 1970s, and cataracts in both eyes prevented her fromseein g well. Those of her letters which she typed or wrote herself (as opposed to those dictated to her assistant) often contained numerous typographical errors, including transposition of letters, incorrect punctuation, and extra or missing letters. I have corrected these, for ease of reading, in my quotations, but have been careful not to change any actual words or the meaning of any material quoted. 97 Schram, "Manton on arthropods," 63. 98 Sidnie M. Manton, The Arthropoda: Habits, Functional Morphology, and Evolution (Oxford: Clarendon Press, 1977). Manton was influenced by the German idealistic morphology school of systematics.

Though Briggs argues that Manton's particular systematic methodology was not shared by

Harry Whittington, it is clear that Whittington was greatly influenced by the results of

Manton's systematics - i.e., by her classification of the arthropods. Manton, like

Whittington, was very skeptical of cladistics. Zoologist Anthony A. Fincham, in a 1978 review of Manton's The Arthropoda, wrote that while the "monophyleticists" who supported arthropod monophyly were "willing to accept hypothetical ancestors... Dr. Manton accepts only the evidence based on facts from embryology, functional anatomy and fossils and dismisses existing theories which 'depend upon the assumption of functionally impossible ancestral stages'." For this reason, Fincham wrote, Manton's book represents a "clash... inevitably head-on with the Hennigian school which seeks to describe all phylogenies in terms of monophyletic groups."100

Manton, as we have seen, privileged the data from extant over extinct arthropods in her classification scheme. She recognized three phyla of modern arthropods, which had all achieved the arthropod grade of organization independently. These were the Chelicerata,

Crustacea, and Uniramia. Manton also allowed that the extinct Trilobita might represent a group of equivalent rank, but just as paleontologists were not allowed to mess with her modern groups, she did not intrude on their territory by presuming to classify their fossil groups (and, indeed, believed that the state of knowledge of fossil arthropods was not yet

99 Frederick R. Schram, "The British School: Caiman, Cannon, and Manton and their effect on carcinology in the English speaking world," in History of Carcinology. Frank Truesdale, ed., 321-348 (Rotterdam: A.A. Balkema/Rotterdam/Brookfield, 1993). I thank Christian Baron, a Ph.D. candidate at the University of Copenhagen, for making me aware of Manton's connection to the German idealistic morphology tradition. (Baron, personal communication, July 2007). 100 Anthony A. Fincham, "Monument to evolution," Times Higher Education Supplement, 7 April 1978. Copied in Briggs Notes, Folder "Manton." sufficient for their higher-level classification). Despite her reluctance to erect formal taxonomic ranks within fossil groups, Manton's belief in multiple polyphyletic origins for various arthropod groups had definite implications for the history of arthropods. In this context, the Cambridge group's initial decision, in Phase 2, to classify several Burgess organisms as "uncertain arthropods" and "uncertain phyla" becomes less startling. If the already-known arthropod classes had evolved independently, then at the same time one would naturally view any unique characteristics as evidence for a separate origin, while believing that any similarities between species might be mere convergences - as the arthropod-like features must be, having apparently arisen independently in several independent arthropod-like groups.102

Following Manton's death in 1979, however, and with the advent of molecular systematics which showed a clear genetic relationship among arthropod groups, the popularity of arthropod polyphyly declined once more, and the proponents of arthropod monophyly began to number among the majority of biologists and paleontologists. As arthropod groups in general were once again seen as closely related to each other, the

Burgess arthropods also were perceived as having closer evolutionary ties, to each other and to modern arthropods, than they had had under the Phase 2 polyphyletic approach. Thus

Manton's work was a major factor in shaping the Phase 2 interpretation of the Burgess Shale, and the decline of her arthropod classification following her death, and the advent of molecular phylogenetic data, were likewise significant factors in allowing the rise of the

Phase 3 interpretation.

101 See for example Manton, 495, and Manton and Anderson, 269. m Somewhat ironically, then, the Phase 2 view, which Gould used to argue for a theory of evolution as highly contingent, thus also leads to an increased incidence of convergences. This is problematic if contingency and convergence are seen as opposites, which is how they were construed by Gould and Conway Morris. The contingency versus convergence debate is discussed in detail in Chapter 4. 51

The Three Phases of Burgess Shale Research

As discussed above, I follow Stephen Jay Gould, Desmond Collins, and Derek Briggs and Richard Fortey, in distinguishing three distinct phases in the understanding of Burgess and other Cambrian animals, though I do not adopt unconditionally the exact divisions or chronology of any of them. Neither do I wish to imply that the shift from one phase to the next necessarily involved scientific progress; in fact a chief argument of this thesis is that the shift from Phase 2 to Phase 3 did not always provide better answers, but in fact simply changed many of the questions. Gould identified three phases or philosophies of Burgess classification, but the definitions he gave are problematic, and many paleontologists do not now support the conclusions that follow from his (Phase 2) interpretation. While Collins listed three phases in his article, he made no attempt to elucidate the reasons behind their occurrence, nor why one shifted to another. Briggs and Fortey described their third approach to Cambrian taxonomy as the adoption of cladistic methods, but did not elaborate on how or why this adoption occurred.103 In this thesis I shall go beyond the simple identification and naming of phases to explore the reasons for the transition between them. In particular, my intention is to explore the second phase shift, and to contrast the second and third phases, which has not been previously examined by any historian of science. Table 2 summarizes the chronology and terminology of the three phases identified by Gould, Briggs and Fortey, and

Collins:

103 In fairness to Collins, Briggs, and Fortey, it must be stated that the historical analysis of different phases of Burgess research was not the purpose of their papers - they simply mention these phases in order to point out that things have changed, and (in the case of the Briggs and Fortey paper) to preface their discussion of current methods of research. 52

Phase 1 Phase 2 Phase 3 Gould 1989; "Walcott's 1909-1975(7) "weird "coalesced" "straightening ? Gould 1992 shoehorn" wonders" 1975-1978 rod" Briggs and "lumping e.g. Stormer "multiple e.g. "cladistic e.g. Fortey 1992 approach" 1944 & 1959 polyphyly Whittington approach" Briggs approach" 1979 1983 Collins 1996 "first 1892-1979 "second 1975-1985 "third phase" 1989- phase" phase" Present

Table 2. The Three Phases of Burgess Shale Research The table lists the names that Gould, Briggs and Fortey, and Collins have given to the three phases of Burgess Shale studies which they each recognize. Chronological delimitation of the phases, if any was indicated in the original source, is also given. Data from Gould, Wonderful Life, and "The reversal of Hallucigenia," Briggs and Fortey, "The early Cambrian radiation of arthropods," and Collins, "The 'evolution' of Anomalocaris."

The changing classifications of particular Burgess Shale species will be discussed in detail in the chapters to follow. Walcott named ninety genera from the Burgess Shale,104 and published descriptions and classifications of seventy of them, all of which he grouped within modern phyla.105 In 1971, Whittington reported that approximately 150 species in ninety- five genera were then known from the Burgess Shale.106 Subsequently, in a 1994 book,

Briggs and colleagues reported 124 genera (including 171 species) known from the Burgess

Shale.107 Their list includes twenty-four species named by Walcott but since relocated to new or different genera, and thirteen species named by Walcott but since found to be identical to other species (therefore the thirteen duplicates are subsumed under their synonyms). The list also includes twelve new species named by members of the Cambridge team, one of which was later found to be identical to a species that Walcott had named earlier. Of the eleven remaining new species, one was named by Whittington (Sarotrocercus

104 Charles Doolittle Walcott, "The Cambrian and its problems in the Cordilleran region," in Problems of American Geology: A Series of Lectures Dealing With Some of the Canadian Shield and of the Cordilleras, 162-233 (New Haven: Yale University Press, 1915), 211. 105 , "Charles Doolittle Walcott: paleontologist-1850-1927," Science vol. 65, no. 1689 (13 May 1927), 457. 106 Whittington, "The Burgess Shale: history of research and preservation of fossils," 1171. 107 Derek E.G. Briggs, Douglas H. Erwin, and Frederick J. Collier, The Fossils of the Burgess Shale (Washington and London: Smithsonian Institution Press, 1994), 217-221. See Appendix A for the fall list of 124 genera known from the Burgess Shale in 1994. 53 oblitd), one by Briggs (Perspicaris recondita), one by Briggs and Collins { uncatd), and eight by Conway Morris (including Odontogriphus omalus and Nectocaris pteryx). In the third phase of Burgess studies, many of these species have been reclassified yet again, and new species have been described and classified.

The following table charts the changing classification of a number of Burgess species through each phase of understanding. The particular species listed are included because they figure largely in the coming discussion; though other Burgess species have undergone taxonomic revision as well, those included here have had the most varied histories.

Species Name Phase 1 Phase 2 Phase 3 Anomalocaris Phylum Arthropoda Phylum Uncertain Phylum Arthropoda canadensis Class Crustacea (Whittington and Class Dinocarida Subclass Branchiopoda Briggs 1985) Order Radiodonta Order Notostraca (Collins 1996) (Walcott 1912) Aysheaia Phylum Annelida Phylum Uncertain, Phylum Arthropoda pedunculata Class Polychaeta or possibly Phylum Class Onychophora (Walcott 1911) Onychophora Order Protonychophora (Whittington 1978) (Robison 1985) Branchiocaris Phylum Arthropoda Grade: Arthropod Phylum Arthropoda Class pretiosa Class Crustacea Phylum Uncertain Crustacea Subclass Malacostraca (Briggs 1976) Subclass Malacostraca (Walcott 1912) (Briggs and Clarkson 1990) Burgessia Phylum Arthropoda Grade: Arthropod Phylum Arthropoda bella Class Crustacea Phylum Uncertain Stem group chelicerate Subclass Branchiopoda (Hughes 1975) (Waggoner 1996) Order Notostraca (Walcott 1912) Canadaspis Phylum Arthropoda Grade: Arthropod (no revisions to Phase 2 perfecta Class Crustacea Phylum Crustacea classification as yet) Subclass Malacostraca Subclass Order Hymenocarina Malacostraca (then Hymenocaris Order Canadaspidida obliqua, Walcott 1912) (Briggs 1978) 54

Hallucigenia Phylum Annelida Phylum Uncertain Phylum Arthropoda OR sparsa Class Polychaeta (Conway Morris Phylum Onychophora Order Miskoiida 1977) Stem group (then Canadia sparsa, onychophoran Walcottl911) (Ramskold and Hou 1991) Laggania Phylum Echinoderaiata Phylum Porifera Phylum Arthropoda cambria Class Holothuroidea AND Phylum Class Dinocarida (Walcottl911) Order Radiodonta (Conway Morris (Collins 1996) 1978) Marrella Phylum Arthropoda Grade: Arthropod Phylum Arthropoda splendens Class Crustacea Phylum Uncertain (Arachnomorpha) Subclass Trilobita (Whittington 1971) Class Marrellomorpha Order Marrellida Order Marrellida (Walcott 1912) (Garcia-Bellido and Collins 2006) Nectocaris (unknown) Phylum Uncertain Phylum pteryx (Conway Morris (Simonetta 1988) 1976) Odaraia alata Phylum Arthropoda Grade: Arthropod Phylum Arthropoda Class Crustacea Phylum Uncertain Class Crustacea Subclass Malacostraca (Briggs 1981) Subclass Branchiopda Order Hymenocarina Order Odaraiida (Walcott 1912) (Simonetta and Delle Cave 1975) Odontogriphus (unknown) Phylum Uncertain Phylum omalus (Conway Morris Stem group mollusc 1976) (Caronetal2006) Opabinia Phylum Arthropoda Phylum Uncertain Phylum Arthropoda regalis Class Crustacea (Whittington 1975) Class Dinocarida Subclass Branchiopoda Order Opabiniida Order Anostraca (Collins 1996) (Walcott 1912) Peytoia Phylum Cnidaria Phylum Uncertain Phylum Arthropoda nathorsti Class Schyphozoa (Conway Morris and Class Dinocarida (Walcott 1911) Robison 1982) Order Radiodonta (Collins 1996) Sidneyia Phylum Arthropoda Grade: Arthropod Phylum Arthropoda inexpectans Class Crustacea Phylum Uncertain Stem group chelicerate Subclass Merostomata (Bruton 1981) (Waggoner 1996) Order Limulavida (Walcott 1911) 55

Wiwaxia Phylum Annelida Phylum Uncertain Superphylum corrugata Class Polychaeta (Conway Morris Lophotrochozoa (Walcottl911) 1985) Stem group mollusc, or stem group of annelids and (Conway Morris and Caron 2007) Yohoia tenuis Phylum Arthropoda Grade: Arthropod Phylum Arthropoda Class Crustacea Phylum Uncertain Stem group chelicerate Subclass Branchiopoda (Whittington 1974) (Chen etal. 2007) Order Anostraca (Walcott 1912)

Table 3. Changing Classifications of Burgess Shale Species Names and dates in brackets refer to the major publication in which the given classification appeared (see Bibliography for full references). Note that in Phases 1 and 3 the arthropods were considered to be a single phylum, whereas in Phase 2 they were thought to comprise several unrelated phyla which had each achieved the grade of "arthropodization" independently.

Structure of Chapters to Follow

I will not discuss the first phase, or the shift to Phase 2, in much greater detail than I have already done, both for reasons of space and because these topics have been covered elsewhere.108 The debate which forms the basis for this thesis, which has not previously been the subject of historical or philosophical analysis, was fought between those scientists who hold the interpretation which characterizes the second phase of Burgess studies, and those who have come to hold the interpretation which characterizes the third phase.

The third phase, which began slowly in the early 1980s and built to a head by the end of the decade, applied new systematic methodologies - cladistics, and its corollary the stem group concept - to a great influx of new fossils from the Burgess Shale, and from other

Cambrian fossil faunas in Greenland and China, to forge a place for the Burgess oddballs in a

108 See for example Gould, Wonderful Life, Yochelson, "Discovery, collection, and description of the Middle Cambrian Burgess Shale," 469-545, and Yochelson, Smithsonian Institution Secretary. system of classification that could also accommodate modern animals. Proponents of this new view also disputed Gould's claims as presented in Wonderful Life; in a series of papers published from the late 1980s through the early 2000s, Derek Briggs, his colleague Richard

Fortey, and their Ph.D. student Matthew Wills (who also wrote his dissertation on the subject) challenged Gould's claim of maximal disparity in the Cambrian,109 while Simon

Conway Morris wrote two books presenting his own interpretation of the Burgess Shale and challenging Gould's arguments about the tempo and mode of evolution.110 Both Briggs and

Conway Morris, at approximately the same time but independently and for different reasons, experienced a shift in their understanding of the Burgess Shale, from a Phase 2, weird wonders view to the new understanding characteristic of Phase 3. Using published articles, reviews, and books, unpublished notes and correspondence, and interviews with the key figures of Burgess research, I explore the shift from Phase 2 to Phase 3 and the reasons behind it.

In Chapter 2,1 discuss the work of Derek Briggs, and his adoption of cladistic methodologies, which were the chief cause of the shift in his perception of the Burgess Shale fossils and their relationships to each other and to modern animals. Briggs's use of cladistics can be contrasted with Whittington's commitment to the traditional school of evolutionary systematics, and to the particular classification of arthropods proposed by Sidnie Manton. I

See for example: Derek E.G. Briggs, Richard A. Fortey, and Matthew A. Wills, "Morphological disparity in the Cambrian," Science vol. 256, no. 5064 (19 June 1992): 1670-1673, Matthew A. Wills, The Cambrian Radiation and the Recognition of Higher Taxa. (Ph.D. thesis, , 1994), Matthew A. Wills, Derek E.G. Briggs, and Richard A. Fortey, "Disparity as an evolutionary index: a comparison of Cambrian and recent arthropods," Paleobiology vol. 20, no. 2 (Spring 1994): 93-130, Richard A. Fortey, Derek E.G. Briggs, and Matthew A. Wills, "The Cambrian evolutionary 'explosion': decoupling cladogenesis frommorphologica l disparity," Biological Journal of the Linnean Society vol. 57 (1996): 13-33, Matthew A. Wills, Derek E.G. Briggs, and Richard A. Fortey, "Evolutionary correlates of arthropod tagmosis: scrambled legs," in Arthropod Relationships, Systematics Association Special Series 55, Richard A. Fortey and R.H. Thomas, eds., 57-65 (London: Chapman & Hall, 1998), and Matthew A. Wills and Richard A. Fortey, "The shape of life: how much is written in stone?" BioEssays vol. 22, no. 12 (2000): 1142-1152. 110 Conway Morris, The Crucible of Creation, and Life's Solution: Inevitable Humans in a Lonely Universe (Cambridge: Cambridge University Press, 2003). will show that these commitments lead directly to a Phase 2 understanding of the Burgess

Shale (which Whittington held), while a commitment to cladistics leads to the view characteristic of Phase 3 (which Briggs adopted).

Chapter 3 focuses on the re-classification of three particular fossil groups, which

Conway Morris collectively credits for his shift in the understanding of the Burgess Shale.

The discovery of similar fossils in the Sirius Passet fauna of Greenland and the Chengjiang fauna of China helped Conway Morris to understand the Burgess Shale specimens which had long puzzled him, and other scientists, leading him to turn away from the Phase 2 understanding, and towards a Phase 3 view, of the Burgess Shale.

Chapter 4 uses an analysis of adaptive landscape models and theoretical morphospaces as a framework through which to examine the Conway Morris - Gould debate over the tempo and mode of evolution. Gould and Conway Morris have framed this debate as a dispute over the significance of contingency versus convergence as factors influencing evolution. The argument is this, but it is also much more, and an examination of the very different ways in which Gould and Conway Morris define and use adaptive landscapes (after

Simpson, 1944) and theoretical morphospaces (after Raup^ 1966) highlights what else is at stake.

In Chapter 5,1 examine the history of the phylum and body plan concepts, and explore how they have been applied by Burgess Shale scientists in an attempt to understand these enigmatic fossils and their relationships to modern organisms. I show also how Gould and Conway Morris can be recast as but the latest antagonists in a two-hundred-year-old debate between structuralists and functionalists. I discuss the work of Gould, Briggs, and

Conway Morris, as well as that of Conway Morris's former Ph.D. student Graham Budd, 58

who has been chiefly responsible for applying the stem versus distinction to the

fossils of the Cambrian. The stem group concept, a corollary of cladistics, has provided a

new and valuable way to appreciate the relationships between ancient and modern animals.

Interestingly, these tools are not perceived by everyone to have the same value. Conway

Morris is not a cladist but thinks the stem versus crown group distinction has been important;

Briggs is a cladist but dismisses the stem versus crown group concept as mere semantics.

Gould shared Conway Morris's opinion of cladistics, but disagreed with him on everything

else pertaining to the Burgess Shale.

An exploration of these debates and disagreements will shed light on the scientific understanding of the Burgess Shale, the history of life on Earth, and the patterns and processes of evolution. Chapter 2 Cladistics and Stem Groups: "Building a Phylogeny from the Bottom Up"111

"Curiously, Gould hardly mentions the new discipline of cladistics, which was being developed at exactly the same time as Conway Morris, Briggs and Whittington were patiently chipping out Burgess oddities. The cladistic method works by analysing shared similarities, and produces a classification based on derived, homologous characters; and it does not make value judgments about 'disparity.' ...Scientific discussion will centre on the of particular characters, which is always controversial in arthropods. But sorting out such complex questions provides more constructive insights into the classification of these arthropods than simply saying: 'Gee isn't that weird - it must be a new class!' ."m

"How can anyone make a claim about Burgess versus modern disparity with a chart [i.e., a cladogram] that has eliminated all the unique tagmoses of the Burgess taxa and does not acknowledge the spiny carapace of Marrella, the three-pronged tail fluke of Odaraia, and the remarkable (and different) frontal appendages of and Yohokrt"m

The debate in the mid twentieth century between the followers of the old method of

classification (evolutionary systematics) and the first enthusiastic converts to the new method

(cladistics, or phylogenetic systematics) was presented, at the time of its occurrence and in

the few histories written since, as an argument over proper methodology. If systematics or biological classification is to be regarded as a science, it should follow a method that is

explicit, logical, and universally applicable; it should produce hypotheses of relationship that

are reproducible and testable, and there should be a clear-cut, empirical method for choosing

among the proposed hypotheses. The cladists argued that their method met all these criteria,

while the method of the evolutionary systematists - which involved the subjective

111 Derek E.G. Briggs and Richard A. Fortey, "Wonderful strife: systematics, stem groups, and the phylogenetic signal of the Cambrian radiation," Paleobiology vol. 31, no. 2 (Spring 2005), 96. 112 Richard A. Fortey, "The collection connection," Review of Wonderful Life: The Burgess Shale and the Nature of History by Stephen J. Gould (New York: W.W. Norton & Company, 1989) Nature vol. 342, no. 6247 (16 November 1989), 303. 113 Stephen J. Gould, "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis: why we must strive to quantify morphospace," Paleobiology vol. 17, no. 4 (Autumn 1991), 415.

59 60 application of the intangible result of academic experience, along with perhaps equally subjective weighting of the biological and evolutionary importance of particular characters, to the organisms to be classified, most emphatically did not. These accusations were well- founded, and evolutionary systematics eventually lost out to cladistics on these methodological grounds.

What has not been appreciated, however - neither by participants in nor by historians of the debate - is that evolutionary systematics and cladistics were not, as one might assume, two methods of doing the same thing. These two schools had very different systematic objectives, and when cladistics won the day, the systematic community as a whole adopted a new set of systematic goals along with their new set of systematic methods. The goal of evolutionary systematics is to produce natural groups, where "natural" means biologically real, and overall similarity is an important determinant of biological reality. Evolutionary systematists depict these natural groups using evolutionary trees, which include ancestors and descendants. The goal of cladistics, by contrast, is to organize taxa according to recency of common ancestry, or in other words, to produce a sequence of evolutionary events. A natural group for a cladist is one that is united by this sequence of events, regardless of overall similarity. This method produces a cladogram, which does not show ancestors and descendants, but only terminal taxa, and the sequence of particular events which occurred in their evolution. These very different goals have deep implications for the project of classification in general, and the understanding of the relationships and significance of the

Burgess Shale fossils in particular, and these implications form the basis of this chapter.

In this chapter, I will explore one major cause of the shift to the third phase of

Burgess Shale studies: the adoption of cladistic methodology. The shift to Phase 3, for Derek 61

Briggs at least, occurred primarily because of a concurrent shift in systematic methodology

among paleontologists more generally, in the 1980s. This new methodology was then

imported into Burgess Shale studies, primarily through the work of Briggs and his frequent

co-author, invertebrate paleontologist Richard Fortey. The adoption of cladistics, and its

corollary, the stem group concept (applied to the Burgess Shale primarily by Conway

Morris's former student Graham Budd), has forged a new understanding of the Burgess Shale

- but has it also changed the questions we are allowed to ask? While many paleontologists,

including Briggs and Fortey, have celebrated cladistics as the tool which allowed them to

finally make taxonomie sense of the Burgess creatures, others do not agree that it has been so

crucial. Conway Morris has also shifted to a Phase 3 view of the Burgess Shale, but gives

different reasons for doing so, and does not think that cladistics is a particularly appropriate tool to use on the Burgess Shale organisms in particular, or in biology in general. (Conway

Morris's views will be discussed in Chapter 3.) Gould remained the staunchest supporter of the Phase 2 view, and has engaged in a protracted debate with Conway Morris over the tempo and mode of evolution, yet he agreed with Conway Morris about the limitations of cladistics - even if they agreed about nothing else. This chapter will describe the rise of

cladistics, in paleontology generally and in Burgess Shale studies more specifically, and then

contrast the views of the cladistic advocates (Briggs, Fortey, and their former student

Matthew Wills) with those of its main detractors, Stephen Jay Gould and Simon Conway

Morris. Picturing the Problem: The Phylogenetic Lawn vs. the Oculogram

The change that occurred between Phase 2 and Phase 3 with the importation of

cladistics can be seen most clearly by comparing two diagrams of arthropod relationships

characteristic of each phase: Harry Whittington's phylogenetic lawn diagram, illustrative of

the Phase 2 understanding held chiefly by Whittington and Gould; and Briggs and Fortey's

cladogram, which ushered in the Phase 3 understanding, championed by them (and, for

different reasons, by Conway Morris as well).

Whittington's diagram, published in the proceedings of a symposium of the

Systematics Association held at the University of Hull, 19-21 April, 1978, purports to

illustrate the pattern of evolution in arthropods throughout the Phanerozoic Eon.114 (Figure

13) The four main groups of arthropods known before the Burgess Shale was discovered are presented: the extinct Trilobita, and the three groups with living representatives: the

Chelicerata (including and insects), Crustacea (including crabs and ), and

Uniramia (including centipedes and millipedes). More striking than the illustration of these

groups as independent lineages, however, are the dozens of parallel lines around them, some

marked by thickened areas. The thickened portions represent known genera, mainly from the

Burgess Shale, which cannot be accommodated within any of the four major arthropod

groups. The rest of the thin parallel lines, which are numerous, represent Whittington's

prediction that many more unusual arthropods remained to be discovered.

In the second phase of Burgess Shale studies, exemplified by Whittington's phylogenetic lawn diagram, Burgess organisms with unusual features were seen as members

of previously unknown phyla because of those umisual features. Amiskwia was excluded

from the chaetognath worms by its unusual tentacles; Yohoia, Branchiocaris, and Opabinia

114 Whittington, "Early arthropods, their appendages and relationships," 262. 63

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S:.;:j A j 1 fc;:;;:i.:;| r;:;j A If I::::":;;:! '"; 1; f 1 I J !:::::::.! |.:::.:j oc " H t:::.;::| tu i^;t**: J & :" =I ! 1 |:.:;::3 a. ' F: i;;: 1 3 1 i::::'i O I;-!:: * I 1 o ' l::;; O • '. T m 1 I jf j TO j u< — """ s j _J 1 < 1 w' < s *- f a. £ 1 w i ;*0 » I o 1 1 P j j f ' f ' ' j 1 !H 1 IIH llll J '1 II i 1 • 1 H 1 .III II ; | ? 1 1 1 ...... X FIG. 2. Diagram of the pattern of evolution in arthropods. Shapes of areas of each major group indicate range in time audi increase or decrease in numbers of kinds in time, not scaled in proportion to numbers; dense stipple indicates marine habitat Jess dense the contmental habim. The many thin, parallel lines show the supposed range in time of known and unknown genera and families of other arthropods. These other genera are known mainly from the middle Cambrian and lower Devonian (indicated by thicker portion of line) and are forms which did not have a mineralized exoskeleton.

Figure 13. Whittington's Phylogenetic Lawn Diagram Arthropod groups, known and hypothesized, are represented as lines or shaded areas. Note that none of the lines converge, indicating no knowledge of the relationships among the different groups. Modified from Whittington, "Early arthropods, their appendages and relationships," 262. were excluded from the branchiopod crustaceans by their unusual head appendages (and, in

Opabinia's case, possession of five eyes); Marrella was removed from the trilobites because

of its unusual arrangement of appendages and bizarre paired head spines; and Hallucigenia

and Anomalocaris were so unusual in almost every aspect that they could not even be

reconstructed correctly, initially. As we have seen, this view, characteristic of the second phase of Burgess Shale research, reached its pinnacle with Gould who predicted that the

Burgess Shale contained twenty new arthropod classes115 and fifteen to twenty new phyla,116

over and above the fossil representatives of the modern four arthropod classes and thirty or

so phyla.

Whittington's phylogenetic lawn diagram can be contrasted with the first cladogram of Burgess arthropods, published in the proceedings of another conference, the Second

International Symposium on the Cambrian System, held in Golden, Colorado, 9-13 August

11*7 1981. (Figure 14) The most immediately striking difference between this cladogram and

Whittington's phylogenetic lawn diagram is its root: the cladogram shows all of the arthropods in question arising from a single common ancestor. As Gould later pointed out, the fact that a cladogram shows a single common ancestor for the taxa it groups is not a conclusion for which the cladogram gives evidence, but an assumption that is made before the cladogram is generated.

As well, the cladogram suggests closer relationships within this group of arthropods:

for example, Actaeus and Yohoia are grouped together because they have both lost the inner branch of their trunk appendages. This loss is a derived or new character shared by these two genera and no others, and the fact that they share it suggests that they are more closely 115 Gould, Wonderful Life, 106,209. 116 Gould, Wonderful Life, 99. 117 Briggs and Whittington, "Relationships of arthropods," 41. 65

FkfsmlL Qm hypothesis of interrelationships of Cambrian arthropod genera. Key to synepomorpbies as follows: 1, Serial seornentatlon, paired appendages 2. Jointed exottceieton I, Caphaik: aH»id (dotted DnBt indicate raUitionihip (« und«ehl»d} 4. Carapsca (extending poatwiorly beyond cephaton), ter^itsa lacking 5. Carapace bivalved 6. Telaon processes (Mi character la almost certainly convergent and therefore Invalid) 7. Oistlnetlon between thorax ami abdomen S. Peddle-«heped llrnba in caudal 9. Incorporation of Uri^ (not anternae) Irtto head posteriorly, radut^ aecond antenne 10, Phyilocsrid trunk segmentation II, Tergitea «^th pleurse following cephalic shield 12. Incorporation of llrnba (not antennee} Into head poaterioriy IX Two poatarlor cephalic limbt M» Three poat«rior cephalic limb* 15. Unresolved 16. Fused pottarior ahleld or pygidiutn 17. Low of pre-telson appendages 19. Four posterior cephalic limbs, specialization of cephalic limb* diatally, flat psddleilke teten 19. Unresolved 20, Loss of irmer rami of trunk limbs

Figure 14. The First Burgess Shale Cladogram Modified from Briggs and Whittington, "Relationships of arthropods from the Burgess Shale," 41. 66

related to each other than either is to any other genus (or in other words, they are sister

groups). Similarly, Perspicaris and Canadaspis are shown to be closely related because they

both possess trunk appendages characteristic of phyllocarid crustaceans. The evolution of

these characteristic trunk appendages is hypothesized to have occurred at the node labeled

"20" in Whittington and Briggs's original caption. The cladogram does not say exactly when

(in absolute time) this happened, nor which fossil species first evolved this character and was

thus the ancestor of Perspicaris and Canadaspis, but it does hypothesize that these two

species are sister groups, because they share this derived character. The implications of these

groupings, definitions, and methods will be discussed below.

This cladogram was intended as a very preliminary attempt to classify the Burgess

Shale arthropods; Briggs noted many difficulties and uncertainties encountered in the

generation of the cladogram, which made it difficult to decide which characters should be

viewed as indicative of close relationship, and which might have arisen independently in multiple groups, thus giving no indication of close relationship despite causing morphological resemblance.118 Nevertheless, it provides at the least a clearly stated scientific hypothesis of proposed relationships, which can now be tested against available evidence.

For this reason, Briggs regarded the cladistic approach, however flawed, as a distinct

improvement over the phylogenetic lawn view, which, as he and Fortey later noted, "merely pushes the problem of relationships back into the Precambrian (and denies the possibility of

solving it by the scientific method)."119

Others agreed; paleontologist Richard Jefferies, for example, said in response to the presentation of Whittington's phylogenetic lawn interpretation at the 1978 Systematics

Briggs and Whittington, "Relationships of arthropods," 40. Briggs and Fortey, "The early Cambrian radiation of arthropods," 351. Association meeting that "he thought it was terrible that Whittington and his group had presented an interpretation requiring either agnosticism or Special Creation."120 Fortey, in a

1989 review of Gould's Wonderful Life, pointed out that a cladistic approach, which focuses on classifying groups according to the characters shared among them, is much more useful than Gould's weird wonders approach (equivalent to the phylogenetic lawn), in which we get hung up on the unusual characters of each group and therefore view them as unique and unrelated.121

Yet Whittington, and Gould, continued to argue against the cladistic approach.

Though Whittington's name appeared as coauthor on the 1981 paper giving the first cladogram of Burgess Shale arthropods, it is clear from his letters to Briggs while Briggs was writing the paper that Whittington had deep reservations about the implications of applying cladistics to the study of the Burgess organisms. For example Whittington wrote on 24

February 1981:

I don't accept the idea of a common origin - we assume it for purposes of this exercise, but there is no evidence either way - you don't have to have the bottom part of the cladogram! - or rather they [= the common features shared by the grouped taxa] need not have occurred only once.122

Also, in a separate paper published in the same 1981 volume as the cladistic analysis,

Whittington firmly stated his continued allegiance to the phylogenetic lawn: "The Cambrian pattern of evolution thus shows many discrete, parallel lines of descent."123 His main argument against the cladistic approach, thus expressed, was his belief that the Burgess

120 Richard P. S. Jefferies, qtd, in M. R. House, "Discussion on the origin of major invertebrate groups," in The Origin of Major Invertebrate Groups, Proceedings of a symposium held at the University of Hull, The Systematics Association Special Volume No. 12, MR. House, ed. (London: Academic Press, 1979), 488. 121 Fortey, "The collection connection," 303. 122 Letter from Whittington to Briggs, 24 February 1981, Non-archived personal correspondence in possession of Derek Briggs, Yale University (hereafter "Briggs Correspondence"). 123 Whittington, "The Burgess Shale fauna," 239. arthropods did not share a common origin but instead comprised several groups which had each evolved their arthropod-like characters independently.124

Gould argued even more vehemently against the applicability of cladistics to the

Burgess Shale, arguing that the cladistic methodology, by its very nature, could not answer what he saw as the most important questions about the Burgess Shale: how morphologically different the Burgess creatures were from each other and frommoder n groups, and therefore what this level of morphological disparity says about the very nature of evolution.

What did Gould mean? What is cladistics, and why did its adoption so radically change the way the Burgess Shale fossils were classified, and understood? Why did paleontologists in general and Briggs in particular convert to the new method of cladistics?

And did this change really lead to a genuinely new understanding of the Burgess Shale and its place in the history of life, or was the new understanding merely a methodological artifact? The answers to these questions are key in characterizing the different interpretations of the Burgess Shale and its place in the history of life in Phase 2 and Phase 3. To answer these questions, we must begin with an in-depth look at the methods of classification used by paleontologists and biologists. How was cladistics different from evolutionary systematics - the system of classification it replaced?

Evolutionary Systematics vs. Cladistics: Different Methods with Different Objectives

Following the publication of Darwin's theory of evolution in 1859, the project of biological classification was reconceived as the grouping of taxa which were related by descent. There has been much debate, however, over which specific methods are best to

124 As discussed in Chapter 1, Whittington was greatly influenced in this belief by the work of functional morphologist Sidnie M. Manton, who had published a series of papers arguing for arthropod polyphyly. determine this common descent, and then construct groups. This debate came to a head in

the last third of the 20* century, when three competing schools of systematics arose. One of

these schools, numerical taxonomy, was quite short-lived and will not be discussed here,

largely because it did not play a significant role in the classification or interpretation of the

Burgess Shale or other Cambrian animals. The debate between the other two schools, by

contrast, had and continues to have deep implications for the understanding of the Burgess

Shale. Most of the battle between these schools was fought over the particular taxonomic

methods, groups, and definitions employed by the two camps, but underlying all this was an

unstated but nonetheless real and crucial dispute over the goals of systematics itself- and as

we shall see, these goals are very different for these two schools of systematics.

In the first half of the 20th century, most paleontologists and other biologists followed

a system of classification known as evolutionary systematics. This system was heartily

endorsed by the great paleontologist and Evolutionary Synthesist George Gaylord Simpson,

as well as by the equally famous ornithologist, systematist, and fellow Synthesis architect

Ernst Mayr. A comparatively recent rival system, cladistics (also known as cladism or phylogenetic systematics), was proposed by the German zoologist Willi Hennig, who published a groundbreaking book on the subject in 1950. This book was not translated into

English until 1966,125 and while some biologists embraced cladistics immediately, others

resisted it while vehemently defending the traditional evolutionary systematics.

A principal subject of contention between evolutionary systematists and cladists was

the correct way to delineate natural, biologically real groups of organisms. Before Darwin,

groups were recognized on the basis of morphological similarities and differences; to this

125 Willi Hennig, Phylogenetic Systematics (Urbana: University of Illinois Press, 1966). This firstEnglis h edition was not merely a translation but also a substantial revision of his 1950 German book. basis Darwin added commonality of descent. Cladists wish to construct groups using only

common descent (phylogeny); evolutionary systematists wish to do this and more besides,

retaining the amount of morphological difference as another factor in the recognition of

natural groups. The two schools can thus be distinguished by their approach to

morphological difference. In cladistics, differences and degrees of differences really don't matter; only similarity (indeed, only a particular kind of similarity) counts, as we shall see below. In evolutionary systematics, by contrast, both the fact and the degree of difference do

count. There are big differences and little differences, and the big ones count for a lot in

defining groups. These distinct approaches highlight the disparate goals of the two schools:

cladists seek to reconstruct sequences of evolutionary events, while evolutionary systematists

seek to identify natural biological groups.

What Counts as a Character?

In evolutionary systematics, as we have seen, classification is based on notions of phylogeny and the similarity of the organisms being classified, with some characters being deemed of greater biological significance than others, though all have a place in the analysis.

In cladistics, it is phylogeny alone, or specifically monophyly, as measured by recency of common ancestry, that counts. And if one is attempting to reconstruct the recency of common ancestry, only one particular kind of character gives evidence of such events: shared derived characters, or synapomorphies. Thus, a crucial difference between evolutionary systematists and cladists is the type of characters they use in their respective analyses.

Evolutionary systematists classify based on overall similarity and/or subjective weighting of characters: how many features (usually morphological, but sometimes also developmental, 71 ecological, behavioural, etc.) do the organisms in question share? Are any of these features of sufficient biological importance that they should be taken as defining features of the group?

The basic rule in evolutionary systematics is that, barring superficial similarity through convergence, those taxa which share the most overall similarity are probably the most closely related and should be grouped together. On this scheme, groups possessing highly unusual features are often excluded from association with groups lacking the unusual features, even if they share other characters in common. On this view, for example, the Burgess genus

Marrella would be seen as unique because of its unusually large paired cephalic spines.

Cladists, by contrast, do not employ overall similarity as a basis for classification, and in fact argue that overall similarity is inherently misleading. Instead, cladists distinguish two main types of characters, primitive and derived, and argue that only derived characters (more specifically, shared derived characters or synapomorphies) are useful in phylogenetic analysis. A key aspect of assessing primitive versus derived characters for cladistic analysis is determining the polarity of character states. For each character - wings, placentas, or eyes, for example - there are two or more character states or particular configurations in which the character may be found, such as presence, absence, and/or particular sizes, shapes, numbers, or components. Polarity means determining which character state came first, and which evolved later. The former is the primitive state; the latter the (or a) derived state. Primitive character states (plesiomorphies) don't set the group in question apart from its ancestor because the ancestor has that character state too; only the derived character states

(apomorphies) set descendants apart from ancestors, and only shared derived states

(synapomorphies) show which descendant groups are more closely related to each other than 72 to others. This is why only synapomorphies can be used to construct natural groups (or , in proper cladistic terminology).

A derived character is one that is only present in a particular group, inherited from the closest common ancestor, which first developed that character. Typically a clade is distinguished by its possession of a unique combination of several shared derived characters

(all of which are given equal weight, or importance, in the analysis). This suite of shared derived characters can be used as the basis of classification because it sets apart the group which possesses it from all other groups, each of which possesses its own different suite of shared derived characters. Sister groups - groups which share a more recent common ancestor with each other than with any other group - are recognized by cladists because they share evolutionary novelties with each other, more than they share with any other group.

According to Eldredge and Cracraflt, the realization that only synapomorphies can and should be used to distinguish real biological groups was Hennig's greatest insight and contribution. They note that Hennig realized that

evolutionary similarities shared by a [holophyletic] group are of two sorts: those held over from some remote common ancestor (e.g. two pairs of limbs in mammals) vs. those held only by members of that group (e.g. three inner ear bones in mammals), Hennig pointed out that older evolutionary novelties can be retained in a sporadic manner; consequently their utility for defining and recognizing clusters of organisms is only appropriate to the hierarchical level at which they represent true evolutionary novelties.126

Similarities of the first kind are primitive; those of the second kind are derived. A primitive character is one that was inherited from an ancestor of the group, and will probably also be found in other descendants of the same ancestor. The character is not unique to the group in question, and therefore is not useful in defining that group. Even though all members of the

126 Niles Eldredge and Joel Cracraft, Phylogenetic Patterns and the Evolutionary Process: Method and Theory in Comparative Biology (New York: Columbia University Press, 1980), 10. 73 group may share this characteristic, it cannot be used to define the group because other groups share it too, so the character actually does nothing to demarcate that one group to the exclusion of all others. (Figure 15) For example, while all horses have hair, this character is not useful in defining the horse family, Equidae, within the mammals, because all mammals share this character; it does not help delineate horses as a group within the mammals because it is primiti ve to the mammals. This character is useful, however, in distinguishing mammals from fishes, for example. While having hair is a primitive character within the mammals, it is a derived character when considering the evolution of the Mammalia as a whole: the distinction between primitive and derived is entirely relative to the level of analysis. Mayr emphasized that the key difference between evolutionary systematists and cladists "is in the treatment of autapomorph characters. Instead of automatically giving sister groups the same rank, the evolutionary taxonomist ranks them by considering the relative weight of their autapomorphies as compared to their synapomorphies."127 This examination,

Mayr asserted, gave a much more complete and realistic way of understanding not just the evolutionary history, but also the evolutionary significance, of the groups in question:

127 , "Biological classification: toward a synthesis of opposing methodologies," Science vol. 214, no. 4520 (30 October 1981), 514. 74 M

fish mouse zebra horse

Figure 15. Synapomorphies and Shared Ancestry A cladogram is constructed to analyze the relationships among four taxa (a fish, a mouse, a zebra, and a horse). The way the lines extending downward fromth e taxa connect to each other indicates hypotheses of relationship. The horse and the zebra are grouped most closely together because they share a derived character found in neither the mouse nor the fish: four hooves, each formed from a single digit. This trait must have evolved sometime in the shared common ancestry of the zebra and the horse (but not the mouse or the fish); this synapomorphy is labeled H. B represents the evolution of body hair, a character found in the mouse, zebra and horse, but not the fish. B is a synapomorphy which unites the mouse, zebra, and horse (but not the fish) into a monophyletic group (M). However, B is a primitive character (a plesiomorphy) with respect to determining relationships within M. In other words, the presence of B alone does not tell us whether the horse is more closely related to the mouse or to the zebra, because they all share this character - they all have hair. In order to determine relationships within M, a synapomorphy at a higher level is needed - a derived character found in only two of the taxa, not all three. H (hooves) is such a character, and only a character like H - a shared, derived character - will provide the evidence required to determine recency of common ancestry. Similarity per se is not evidence of recency of common ancestry; synapomorphies are.

The taxonomic task of the eladist is completed with the cladistic character analysis. The genealogy gives him [sic] the classification directly, since for him classification is nothing but genealogy. The evolutionary taxonomist carries the analysis one step further. He is interested not only in branching, but, like Darwin, also in the subsequent fate of each branch. ...Among two related groups, derived from the same nearest common ancestor, one may hardly differ from the ancestral group, while the other may have entered a new adaptive zone and evolved into a novel type. Even though they are sister groups in the terminology of cladistics, they may deserve different categorical rank, because their bi61ogical characteristics differ to such an extent as to affect any comparative study.

Mayr, "Biological classification," 513. 75

The sister group relationship is key in cladistics; cladists argue that it is the only relationship that can be determined with confidence in phylogenetic analysis. This is a major break from evolutionary systematics, which seeks to identify ancestors and descendants. The identification of sister groups versus ancestors is one thing that makes a cladogram (a diagram of relationships constructed by cladists) very different from an evolutionary tree (the preferred diagram of evolutionary systematists).

Cladograms vs. Phylogenetic Trees

Another source of confusion and even animosity between evolutionary systematists and cladists is the question of whether and how to draw evolutionary trees. It is crucial to realize, as the earliest cladists most especially emphasized, that a cladogram is not a phylogenetic tree. (Figure 16) define sister groups - taxa that are thought to be each other's closest relative - but do not show ancestors and descendants. Rather than showing a tree of relationships among groups, a cladogram depicts a sequence of evolutionary events. Evolutionary trees show ancestors and descendants, but cladograms

(branching diagrams generated by cladistic analysis) do not. Cladograms show branching patterns, and the taxa occurring at the ends of branches. One taxon on a cladogram might possibly be ancestral to others, but this relationship is not depicted or inferred because, cladists argue, there is not enough factual evidence to support this type of supposition.

Cladists typically use sophisticated computer programs to compile lists of species (or other taxa) and the various character states they possess. The computer program then constructs a cladogram based on the distribution of the various character states among the 76

. B

B C

A b.

A B C

Figure 16. Cladogram vs. Phylogenetic Tree The cladogram (a) shows tot among three related taxa, A, B, and C, B and C are more closely related to each other than either is to A. There is no evidence, however, to dinstinguish among the possible ancestor- descendant relationships among the three taxa. For example, A might have evolved into B, and then into C (b); A might have evolved into C and then into B (c); B and C might both be descendants of A (d); A and B might be descendants of a common ancestor, with B evolving into C (e); A and C might be descendants of a common ancestor, with C evolving into B; or finally, B and C might have evolved from a common ancestor which itself shares a common ancestor with A. As these examples amply illustrate, the cladogram is not an expression of ancestor-descendant relationships; it is not a phylogenetic tree. The fact mat at least six trees can be drawn from a single cladogram is evidence that the correct tree is underdetermined by the cladistic data. As cladists argue, then, there is only enough reliable information available to construct cladograms, not trees. taxa in question. The best cladogram is often chosen according to the criterion of parsimony:

the cladogram which groups the taxa with the fewest convergences (i.e., by invoking the

fewest independent evolutionary origins of the same character state) is generally considered

to be the best one. More recently, some cladists have begun to use Bayesian methods to

choose the most likely cladogram. Whichever method is employed, the point to note here is

that there are objective, well-defined, and quantifiable methods for determining which of

several proposed cladograms best fits the data in hand. There is no such rigorous and

quantifiable method for choosing among the trees of evolutionary systematists. An

evolutionary systematist may, from his experience and knowledge, have a "feel" for which

tree is "right," but this sort of vague notion is problematic when one's goal is to be as

scientific as possible. As Jim Endersby notes, "cladists... aim to create a taxonomy based on

a rigorous, objective methodology for assessing phylogeny."129 The rigor and objectivity of

their system, in contrast with evolutionary systematics, are among the chief strengths cited by

cladists, and were the major reason why cladistics eventually won out over the more intuitive

and subjective school of evolutionary systematics. Evolutionary systematists could not

articulate an objective methodology, and in contrast to the rigor of cladistics, their a priori

weighting of some characters as more biologically important than others looked like "voodoo

paleontology," in the memorable words of British paleontologist and popular science writer

Henry Gee.130

This new method of cladistics, especially its emphasis on shared derived characters, had profound effects on the classification - and therefore the interpretation - of the Burgess

Jim Endersby, "'The realm of hard evidence': novelty, persuasion, and collaboration in botanical cladistics,' Studies in History and Philosophy of Biological and Biomedical Sciences vol. 32, no. 2 (2001), 349. 130 Henry Gee, In Search of Deep Time: Beyond the Fossil Record to a New History of Life (New York and London: The Free Press, 1999), 131. Shale organisms, which began to be felt in the 1980s and which, I argue, was a major cause of the shift from Phase 2 to Phase 3. At the same time that paleontologists in general were gradually becoming converted to cladistics, Derek Briggs was realizing that his Burgess

Shale arthropods might be amenable to phylogenetic analysis by this new method of taxonomic practice.

The Problem ofMonophyly

Another contested area in the debate between evolutionary systematists and cladists was the proper way to define a natural group. The debate over what constitutes a natural group is reflected in a disagreement over terminology between the two schools. Both evolutionary systematists and cladists agree that real biological groups should contain lineages descended from a common ancestor, and should not contain lineages that do not descend from that common ancestor (i.e., that are more closely related to lineages outside the group than those within it). The latter type is called a polyphyletic group, and is not valid in either school. An example of a polyphyletic group would be one that unites dolphins and ichthyosaurs (but not other mammals). These two fast^swimming, streamlined, air-breathing marine creatures share many morphological similarities, but they do not constitute a natural group because they are not each other's sister groups. Dolphins share a more recent common ancestor with other mammals than they do with ichthyosaurs, so it is not natural to remove them from a mammal group and join them with ichthyosaurs instead.

The former type of group, however, is problematic. Evolutionary systematists call a group that contains a common ancestor and only its descendants monophyletic, and believe that real biological groups must be monophyletic. Cladists agree that the only real biological groups are monophyletic - but they define monophyletic groups (or clades, in their terminology) as those containing a common ancestor, only its descendants, and all of those

descendants. This stricter form of monophyly is only a requirement of cladistics, not of

evolutionary systematics. Evolutionary systematists call this stricter form "holophyly" to

distinguish it from their less strict version of monophyly, while cladists retain the word monophyly for the stricter form, and refer to the less strict (and to them, unacceptable) version as . In summary, then, paraphyletic groups are not allowed in cladistics but permitted in evolutionary systematics; holophyletic groups are required in cladistics but not required in evolutionary systematics.m It was evolutionary systematist Peter Ashlock who proposed to replace Hennig's "monophyly" with the word "holophyly," arguing that his definition of monophyly (the less strict one) was the correct one as it had been in use by evolutionary systematists for many decades. It was Hennig, he said, who had redefined monophyly in a new and too narrow sense. Thus, a group composed of the nearest common ancestor and all its descendants would now be called holophyletic. Ashlock then proposed to use "monophyletic" to designate a group composed of the nearest common ancestor and some, but not all, of its descendants. As Ashlock explained, "Holophyly and monophyly, then, become two aspects of the more general concept, monophyly."132 This redefinition of terms had the effect of allowing evolutionary systematists to preserve their cherished groups like reptiles and fish while seeming to adhere to the increasingly popular cladistic credo of monophyly.

131 In the remainder of this thesis, I will use the terms "holophyly" and "holophyletic" to refer to the kinds of groups acceptable to cladists. I adopt the evolutionary systematists' terms not to indicate that I take their side, but because in a discussion which involves both schools of thought, the words "monophyly" and "monophyletic" become ambiguous, whereas "holophyly" and "holophyletic" do not 132 Peter D. Ashlock, "Monophyly and associated terms," Systematic Zoology vol. 20, no. 1 (1971), 65. 80

But why do these two schools require different levels of monophyly, and what are the implications of these different requirements? This problem goes back to the tenets of

Darwinism upheld by each school: both privilege commonality of descent, but evolutionary systematists also recognize the importance of Darwin's Principle of Divergence. They wish to acknowledge high levels of morphological divergence by recognizing the divergent morphologies as distinct biological groups. In other words, they believe it is reasonable and desirable to remove a descendant from a monophyletic group if it has achieved sufficient morphological distinctness that it deserves recognition as its own, separate, group. Ernst

Mayr defended this practice in his grand opus The Growth of Biological Thought:

From Haeckel to 1950 the sequence of operations [in systematics] had always been first to delimit a taxon on the basis of phenetic considerations and then to test whether it was monophyletic. The cladists simply combine all inferred descendants of a given species into a 'monophyletic' taxon, even if they are as different as birds and crocodiles.133

Mayr's sequence of operations is justified in a system of classification based on divergence as well as phylogeny, but is not justified in a purely phylogenetic classification, since it would result in a paraphyletic group. The consequence of this goal is that some taxa which are valid in evolutionary systematics are not valid in cladistics. This consequence is most visible in the classification of certain problematic fossil groups.

Paleontologists long suspected - and in the second half of the twentieth century, have demonstrated conclusively - that birds arose from a particular group of reptiles, the theropod dinosaurs. Evolutionary systematists recognize reptiles and birds as taxa of equivalent rank

(classes) within the Phylum Chordata, because they are well-defined groups which seem to each possess a comparable level of organization, and this classification has stood for

133 Ernst Mayr, The Growth of Biological Thought: Diversity, Evolution, and Inheritance (Cambridge and London: The Belknap Press of Harvard University Press, 1982), 228. 81

hundreds of years. However, according to cladists, because birds descended from reptiles,

they should be classified as lower-ranking taxa within a larger taxon, the Reptilomorpha. On

the cladistic view, the reptiles minus the birds should not be recognized as a valid group,

because it is paraphyletic, and is only defined as a group based on the retention of primitive

characters. In cladistics, such paraphyletic groups are not valid. The shared features which

connect snakes and crocodiles also connect snakes and birds, so any natural group containing

snakes and crocodiles must also include birds. The exclusion of birds from this group is

artificial; they share the same common ancestor and inherited the same plesiomorphies as

snakes and crocodiles, but are excluded only because they have become very different, morphologically and ecologically, fromthei r seemingly more "reptilian" relatives. This move is acceptable in evolutionary systematics, which gives systematic weight to difference, but unacceptable in cladistics, which uses only recency of common ancestry to construct

groups.

While paleontologists can recognize the theoretical validity of constructing groups based on holophyly, it is difficult to enforce this rule in paleontological practice. The

cladistic restriction of higher taxon designation to the most inclusive groups is also highly problematic: for evolutionary systematists, at least, there is a real sense in which groups like birds, mammals, reptiles, and fish seem to be of equal biological importance: they each comprise many orders, families, genera, and species, all of which appear to be variations on a basic body plan particular to each larger group. To an evolutionary systematise the fact that the reptiles have collectively retained a suite of primitive characteristics and its accompanying mode of life is of major biological significance. Their particular characters and mode of life are sufficient to warrant their designation as a cohesive group, the Reptilia, distinct from other groups (such as Aves) that have evolved very different characters and modes of life than their reptilian ancestors. A group like the reptiles, which does not contain an ancestor and all its descendants, but which appears to demarcate a level of evolutionary significance, is known as a grade. As Gee notes, grades are valid categories for evolutionary systematists because "grades reveal much about presumed adaptive transitions in evolution."134 For an evolutionary systematist, then, a grade, even if not holophyletic, is a biologically real group.

Cladists, however, recognize only clades as valid groups, not grades. In cladistics, a group cannot be delineated solely on the basis of shared primitive characters, or a shared mode of life (unless that shared mode of life is expressed in the form of synapomorphies).

For a cladist, Reptilia is an artificial group because it is made up only of those species who have not gone on to become other things (mammals and birds), not those that are most closely related to each other. The cladists' insistence on the use of holophyletic groups is not a mere methodological convention, but reflects their own commitment to biological reality.

For cladists, only holophyletic groups truly carve nature at the joints, therefore they are the only groups that provide meaningful information for any analyses that rely on systematic data. As Joel Cracraft wrote, "In any comparison of this type [=the study of diversity patterns in the fossil record], one underlying assumption is that the taxa employed are all strictly monophyletic [= holophyletic], i.e., the groups... must be real units of nature."135

Cracraft's own underlying assumption is that the way one defines units of nature is through monophyly. As a cladist, Cracraft privileges recency of common ancestry over

134 Gee, 146. 135 Joel Cracraft, "Pattern and process in paleobiology: the role of cladistic analysis in systematic paleontology," Paleobiology vol. 7, no. 4 (Autumn 1981),461. 83

morphological or ecological similarity. Fish systematist E.O. Wiley recognized that cladists

and evolutionary systematists had different definitions of natural groups; he defined these in

his 1981 Phylogenetics textbook. "Phenetic naturalness," the kind recognized by

evolutionary systematists, involves groups "composed of members that resemble each other

(are similar) more than they resemble any nongroup member. In other words, all of the members are more similar to each other than to anything outside the group." Cladists, by

contrast, employ "phylogenetic naturalness," where group members "share a common

ancestor not ancestral to any other group."136 The phylogenetically natural group is unified

by descent alone, not overall similarity.

Cladists further argue that the fossil record does not provide enough information,

even in principle, to speculate about the adaptive significance of particular features - features that an evolutionary systematist might use to justify recognizing a grade as a group of real biological significance. Gee boldly asserts: "To speculate about adaptation in extinct

creatures is at best pointless, at worst recklessly misleading."137 Richard Fortey, while he uses cladistics in his own paleontological work, acknowledges that, particularly with

examples like the Reptilia, "it's awfully hard to be a pure cladist; on the other hand, the logic of working out how to classify things using cladistics is irreproachable." This example highlights the tension many paleontologists experienced between wanting to have a rigorous methodology of systematics to follow, and wanting to retain the cherished groups of pre- cladistic paleontology.

136 E.O. Wiley, Phylogenetics: The Theory and Practice of Phylogenetic Systematics (New York: John Wiley & Sons, Inc., 1981), 71. 137 Gee, 88. 138 Richard A. Fortey, Interview by author, 1 August 2007 (London, England, MP3 recording). This destruction of so many cherished groups was a major stumbling block to the acceptance of cladistics. As Ashlock explained, "It is in the use of his concept of monophyly in a purely cladistic classification [i.e., in requiring holophyly and rendering paraphyletic groups unacceptable] that Hennig's admirable logic leads to conclusions so disastrous that some taxonomists reject all of his ideas."139 Paleontologists David B. Lazarus and Donald R.

Prothero would agree; as they wrote in 1984: It is no accident that cladistic procedures were first formulated by an entomologist and now find their most outspoken advocates among scientists who work with insects and other rarely fossilized invertebrates, fish, lower tetrapods, birds, and early mammals, all with relatively poor stratigraphic records.140

Ernst Mayr explained the evolutionary systematist's point of view in a 1981 Science article:

A paraphyletic taxon is a holophyletic group from which certain strikingly divergent members have been removed.... [Tjhe traditional class Reptilia is monophyletic, because it consists exclusively of descendants from the common ancestor, even though it excludes birds and mammals owing to the high number of autapomorphies of these classes.141

It is clear, then, that evolutionary systematists and cladists have a fundamental disagreement over the importance of autaporphies in the recognition of natural groups.

Bringing Cladistics to the Burgess Shale

In the second phase of Burgess Shale studies, exemplified by Whittington's phylogenetic lawn diagram, Burgess organisms with unusual features were seen as members of previously unknown phyla because of those unusual features. Branchiocaris and Opabinia

139 Ashlock, 64. 140 David B. Lazarus and Donald R. Prothero, "The role of stratigraphic and morphologic data in phytogeny,' Journal of Paleontology, vol. 58, no. 1 (January 1984), 164. 141 Ernst Mayr, "Biological classification," 514. 85 were excluded from the branchiopod crustaceans by their unusual head appendages (and, in

Opabinia's case, possession of five eyes); Marrella was removed from the trilobites because of its unusual arrangement of appendages and bizarre paired head spines; and Hallucigenia and Anomalocaris were so unusual in almost every aspect that they could not even be reconstructed correctly, initially.

This method of classification according to unique characters acted to emphasize the strangeness of each Burgess genus, widening the phylogenetic gulf between it and other genera, and was a hallmark of pre-cladistic taxonomic methods. Briggs, as early as 1979, expressed dissatisfaction with the phylogenetic lawn or grass that resulted from an evolutionary systematics view of the Burgess Shale. In his unpublished notes for a talk given at a Geological Society of America meeting in San Diego, Briggs wrote:

We might consider these few forms [of Burgess arthropods] which are related to the later established taxa as phylogenetic bushes (rather than trees). What about the remaining arthropods? - the grass or lawn surrounding these bushes - to use the analogy that Stermer and Manton preferred - and indeed Whittington currently advocates. I dislike the implications, because the gardeners are reluctant to take a spade to the hard soil to examine the roots beneath. The obvious approach is to apply the rigorous tenets of a cladistic analysis, but this can't be done yet as most of the grass has yet to be described - only 9 of the 30 non-trilobite genera have been published following a rigorous study by the Burgess Shale group.142

Briggs did not have to wait long for sufficient descriptions to be published on which to base a cladistic analysis; by 1980 he deemed there was sufficient material on the Burgess arthropods, at least, to attempt a cladistic analysis of their relationships.

Briggs cannot recall precisely when he first encountered cladistics, but knows it was not during his Ph.D. studies. It may have been through Richard Fortey, another former

Briggs, Unpublished notes for "A short course on arthropods," Briggs Notes, 7-8. student of Whittington's, who had finished his Ph.D. the year before Briggs started bis.

Though Fortey, an expert on trilobites, had never worked on the Burgess Shale directly, he was an excellent choice as a partner for cladistic analysis, having published several cladistic analyses of other groups, as well as at least one paper on the methodology of cladistics

(written with Richard Jefferies).144 Fortey and Briggs went on to write several papers together, including some of the first cladistic analyses of the Burgess Shale. Fortey worked at the British Museum of Natural History, where his coworkers included some of the strongest advocates for cladistics in the UK, Colin Patterson and Richard Jefferies.145 For his part, Fortey recalls that sometime in the early 1980s, Conway Morris gave a talk at the

Museum of Natural History on his Burgess Shale work, and he remembered that "at that meeting, people [were] saying 'well, why doesn't he do a cladistic analysis of the Burgess

Shale?' That was one of the things that might have sparked off my [Fortey's] interest" in doing such a cladistic analysis himself.146

The first talk on cladistics that Briggs can remember attending - though he thinks it likely he had at least heard of cladistics before this - was a presentation Jefferies gave at a

1978 meeting of the Systematics Association at the University of Hull. In this presentation

(and the subsequent paper, published in a volume of conference proceedings in 1979 - the same volume containing Whittington's phylogenetic lawn diagram), Jefferies presented an outline of Hennig's cladistic method, along with his (Jefferies's) own related stem, crown

Derek E.G. Briggs, Interview by author, 29 March 2007 (New Haven, Connecticut, MP3 recording). 144 Richard A. Fortey, Life-An Unauthorised Biography: A Natural History of the First Four Thousand Million Years of Life on Earth (Glasgow: Harper Collins Publishers, 1997), 181. The methodological paper is Richard A. Fortey and Richard P.S. Jefferies, "Fossils and phytogeny: a compromise approach,'' in Problems of Phylogenetic Reconstruction, K.A. Joysey and A.E. Friday, eds. 197-234. (London: The Systematics Association Special Volume No. 21,1982). 145 We will encounter Jefferies again later in this chapter, when we discuss his stem group concept 146 Fortey, Interview 1 August 2007. 87 and total group definitions, and used the outlined methodology to propose a re-classification of the echinoderms and chordates.

Jefferies's talk was, as best Briggs can recall, his first exposure to the stem and crown group concept, and one of the first times he took explicit notice of cladistic methodologies.147

This knowledge came just at a time when, Briggs believed, the Burgess Shale arthropods were finally understood well enough to be amenable to an analysis involving a comparison of numerous morphological characters.148 His first paper attempting such an analysis had two parts, a principal components analysis and a cladistic analysis. The goal of the former was to give an idea of the distribution of the analyzed arthropods in a theoretical morphospace; the goal of the latter was to attempt to sort out their phylogenetic relationships. These analyses were applied to nineteen genera of Burgess arthropods with fossilized appendages, as well as

"the only other two Cambrian forms in which appendages are known," Aglaspis and

Phosphatocopina (an informal group comprising two genera).149 The presence of appendages in the chosen taxa, and the availability of detailed descriptions of them, was the key factor in the feasibility of the analysis, since a large number of characters are needed for numerical study, and since so many diagnostic features of arthropods center on the number, type and placement of appendages. This circumstance also explains why so many of the debates over the morphology, diversity, and relationships of Burgess and other Cambrian organisms have centered so heavily on the arthropods: the arthropods are the most numerous and best preserved of the Cambrian fossils, and are also those with the highest number of discrete,

147 Briggs, Interview 29 March 2007. 148 Derek E.G. Briggs, Unpublished notes for a talk given at the Second International Symposium on the Cambrian System, Golden, Colorado (9-13 August, 1981), Briggs Notes, 2. 149 Derek E.G. Briggs, and Harry B. Whittington, "Relationships of arthropods fromth e Burgess Shale and other Cambrian sequences," in Short Papers for the Second International Symposium on the Cambrian System. Michael E. Taylor, ed., 38-41. (U.S. Department of the Interior, Geological Survey Open-File Report 81-743, 1981), 38. 88 easily identifiable, and readily fossilized morphological characters. For all of these reasons, arthropods are highly suitable for analyses which involve the identification and discrimination of a large number of characters - analyses like the construction of cladograms, and principal components analysis.

The analysis was carried out in late 1980 and early 1981, and eventually became a paper by Briggs and Whittington for the Second International Symposium on the Cambrian

System (the conference was held in Golden, Colorado, 9-13 August 1981, and the papers were published by the United States Geological Survey in time for the volume to be referenced by conference participants at the meeting). Though Briggs and Whittington were not pleased with the stability of the groups suggested by their cladogram, and confessed that they were not yet able to "draw a cladogram that we consider an acceptable representation of possible relationships between the arthropods," this paper nevertheless represents an important first step.150 Also, as their correspondence during the writing of the paper indicates, Whittington was skeptical about the usefulness of Briggs's proposed analyses.

Briggs wrote to Whittington on 29 January 1981:

I appreciate that you may be skeptical about how useful this [principal components analysis] will be. However, the table itself will be indispensable for any sort of careful consideration of possible relationships. It indicates which characters occur in common and, therefore, which may be important. I have more faith in an approach involving weighting the attributes [as he planned to do with the cladistic analysis] but I feel this numerical study will be a useful pointer, and much of the work is a necessary pre-requisite for other analyses anyway.151

This passage demonstrates not only Whittington's reluctance to apply numerical methods to the Cambrian arthropods, but also Briggs's willingness to tailor the new taxonomic methods to suit his own research needs. He intended to employ methods of both

150 Briggs, and Whittington, "Relationships of arthropods from the Burgess Shale," 40. 151 Letter from Briggs to Whittington, 29 January 1981, Briggs Correspondence. numerical phenetics and cladistics, and also intended to modify the cladistic study by weighting the characters. This modification of the new systematic methods to suit the particular needs and goals of paleontologists was typical in the gradual incorporation of cladistics (and aspects of numerical phenetics) into paleontological classification. As Briggs noted, prior to attempting cladistic analysis, "we couldn't make any sense of what these things were; ...traditional taxonomic methods just did not work."152 Cladistics seemed to be worth a try.

Thus Briggs, first with Whittington and later with Fortey, attempted several cladistic analyses of the Burgess arthropods through the 1980s. Briggs's 1983 paper included an updated version of his 1981 cladogram, whereas the paper he co-wrote with Fortey presented an entirely new analysis. Briggs and Fortey felt much more confident about their 1989 cladogram, to the point of concluding that their results might have important implications for the reclassification of living groups of arthropods.153 In this work, they discovered that cladistics, with its focus on shared derived characters and its de-emphasis of the bizarre, unique features of some Burgess creatures, could make taxonomic sense of these strange creatures after all. As Briggs and Fortey expressed in their 1989 Science paper:

The view of the Cambrian arthropods originating as a multiplicity of separate lineages reflected the differences between them. It was influenced, at least in part, by some of the more bizarre attributes of the Burgess Shale genera: the two massive spinose projections from the head shield of Marrella, for example. It led to a perception of the Cambrian radiation as resulting in a much greater morphological as well as taxonomic diversity of arthropods than is displayed by the living representatives. The cladistic approach, on the other hand, focuses on shared characters. Unique attributes, autapomorphies, are of no use in assessing relationship and are consequently accorded little significance.154

Derek E.G. Briggs, Interview by author, 27 March 2007 (New Haven, Connecticut, MP3 recording). 153 Derek E.G. Briggs, and Richard A. Fortey, "The early radiation and relationships of the major arthropod groups," Science vol. 246, no. 4927 (13 October 1989), 243. 154 Briggs and Fortey, "The early radiation and relationships of the major arthropod groups," 242. 90

Cladistics, then, gives no weight to unique characters in determining relationships, seeking

instead the shared derived characters that indicate common descent. With this new

methodology, bizarre and unique attributes like Marrella,s head spines and Opabinia's five

eyes were not just given less emphasis as indicators of evolutionary relationship; they ceased to function in phylogenetic analysis at all (except to define terminal taxa). As

autapomorphies, or derived characters not shared with other groups, the bizarre features were now perceived as useless for phylogeny reconstruction.

Briggs and Fortey followed proper cladistic methodology in using only shared

derived characters for their cladistic analysis, and they succeeded in proposing a phylogeny

of the arthropods under study. This was a major step forward in assessing the relationships

among Burgess arthropods. But were they correct in thinking, as they suggested above, that previous methods had overestimated the morphological disparity of the Burgess fossils? It is true that the autapomorphies of the Burgess arthropods were not useful for cladistic analysis, but this does not prove they are not useful for anything. Cladistic analysis does not make unique characters disappear, it simply does not employ them. Briggs and Fortey did not

show that Gould and others were wrong about the great morphological disparity of the

Burgess Shale fauna; they just left this disparity out of their analysis. The implications of this aspect of cladistic methodology will be discussed below.

Though new fossil discoveries were made, and some errors155 were revealed, a large

amount of the shift in understanding of the Burgess fauna in the 1980s came simply from this

shift in systematic methodology. Because of its new emphasis on shared characters and its

dismissal of unique characters, no matter how bizarre, the cladistic method brought the

155 Such as the incorrect orientation of Hallucigenia, which will be discussed in Chapter 3. 91

Burgess oddballs closer together. A corollary of cladistics, the stem group concept, further served to place the Burgess creatures within a taxonomic scheme that included modern groups.

The Stem vs. Crown Group Concept

Another concept, related to cladistics, also played a key role in the new (Phase 3) understanding of Burgess Shale taxonomy. This is the stem versus crown group concept.

Hennig, in a 1969 article, defined what he called the w group as the latest common ancestor of a monophyletic group of extant organisms plus all descendants of this ancestor, whether living or extinct.156 Richard Jefferies - the same Jefferies whose 1979 talk is the first exposure to cladistics that Briggs can now recall - renamed this group the crown group, and added some further definitions in a 1979 paper which proved to be highly influential in paleontological taxonomy in general, and in the classification of Burgess Shale and other

Cambrian organisms in particular. In fact, I believe that this new understanding of the relationship between Jefferies's crown and stem groups, applied to the increasing quantity of

Cambrian fossils discovered in the Burgess Shale and its sister faunas, has been a major cause of the profound change in the perception of the evolutionary relationships of the

Burgess organisms beginning in the 1980s (i.e., the shift from Phase 2 to Phase 3).

Though Briggs, Graham Budd, and others are currently engaged in a debate over how exactly to define a phylum relative to the stem and crown groups, 5 they all agree that the identification of the stem group has played an important role in helping paleontologists

156 Jefferies, 449. 157 See for example Graham E. Budd and S. Jensen, "A critical reappraisal of the fossil recordo f the bilaterian phyla," Biological Reviews of the Cambridge Philosophical Society vol. 75, no. 2 (2000): 253-295, and Briggs and Fortey, "Wonderful strife." Also, this debate will be discussed in more detail in Chapter 5. 92 classify extremely ancient and decidedly unmodern-looking creatures, particularly those of the Burgess Shale. In a 2005 article written as a contribution to Paleobiology's collection of essays commemorating the work of Stephen Jay Gould, Briggs and Fortey noted that "Since

1989 cladistic analyses have accommodated most of the problematic Cambrian taxa as stem groups of living taxa," and also asserted that:

[T]he great majority of Cambrian taxa can be accommodated with their modern counterparts in a plausible hypothesis of relationships - by building a phylogeny from the bottom up rather than trying to place fossils into higher taxa defined exclusively on the basis of living organisms. This approach shifted the emphasis from - the much-bruited 'weirdness' - to synapomorphy, the characters shared between one animal and another.158

This statement recognizes cladism's focus on synapomporphies, and also recognizes the bottom-up approach facilitated by the recognition of stem groups. (But again, ignoring weirdness does not make it go away.)

What exactly was the stem group concept that Jefferies introduced? In his 1979 paper, Jefferies offered the following diagram (Figure 17) to explain his stem and crown group concepts, which proved so crucial in the shift to Phase 3. (Interestingly, this article first appeared in the same book which contained Whittington's phylogenetic lawn diagram, so exemplary of Phase 2.

Jefferies gave an example of "two monophyletic groups (1 and 2) of extant organisms, each being the sister group of the other... [I]f we take account of extinct relatives also, there will be two obvious delimitations, wide or narrow, of each of these two groups." The narrow delimitation is the newly-renamed crown group, fitting Hennig's definition of the *T group above, and united by possession of a particular suite of synapomorphies. "The wide

Briggs and Fortey, "Wonderful strife," 96. 93 delimitation of group 1," Jefferies continued, "would include the daughter species ultimately ancestral to the living members of 1, plus all descendants of that daughter, both living and extinct" - including those who do not possess the requisite synapomorphies to admit them to the crown group, but still lie between it and its most recent shared ancestor with group 2.

This wider group just defined Jefferies calls the total group. His third group, the stem group,

Figure 17. The Stem Group Concept Modified from Jefferies, 450. is "a residue of extinct forms" left over when you subtract the crown group from the total group. Jefferies goes on to say that "stem groups are extinct by definition and will be paraphyletic in that some members will be more closely related to the crown group than others are," because "not all synapomorphies connecting members of a crown group together, and distinguishing it from its sister crown group, will have been acquired at once. Instead they will have been acquired successively within the two stem groups."159

These definitions seem simple, even perhaps to be stating explicitly what seems merely common sense, but they have caused a profound change in how paleontologists think of and attempt to classify the so-called weird wonders of the Burgess Shale. The key factor here is the realization that the modern animal phyla (those that were recognized before the

Burgess Shale was studied) are crown groups, defined based on extant organisms and excluding their extinct ancestors and related forms (the stem groups) which went extinct.

The suite of characters that unites each of these crown groups may be diagnostic only because other representatives of the total group, which shared some but not all of these characteristics, went extinct. These diagnostic characters are no longer of primary importance, defining the distinctive body plan of the group, but instead are less crucial, defining only that portion of the group with modern descendants. We are able to recognize the modern phyla as discrete, well-defined groups only because those species which possessed body plans intermediate between them (i.e., the weird wonders of the Burgess

Shale) have gone extinct.

Jefferies, 449. 95

The Contribution ofCladistics and the Stem Group Concept

Even as Stephen Jay Gould was writing the book which would bring the weird wonders of the Burgess Shale to the attention of scientists and interested laypeople worldwide, Derek Briggs and Richard Fortey were using cladistic analysis to show that the

Burgess creatures were not so weird after all. A diagrammatic representation of the different classifications typical of each phase of perception of the Burgess Shale might prove useful here, in illustrating the insights provided by both cladistics and its subsidiary stem group concept. Let us consider three of the strangest Burgess genera, Hallucigenia, Anomalocaris, and Opabinia. (Figure 18)

ONYCHOPHO&A ARTHROPODA s t \ misSHNT ""ST "7 V

H A O MIDDLE CAMBRIAN

H = Hallucigenia A AnomakHxnis O - Opabinia

Figure 18. Classification of Three Burgess Genera Three unusual genera are discovered in the Middle Cambrian Burgess Shale. They possess unique combinations of characters not seen in known groups of animals, such as the arthropods and onychophorans. How should they be classified?

Recall that many Burgess oddballs frustrated paleontologists by their possession of some, but not all, features diagnostic of a particular phylum. In Phase 1, these difficulties 96 were ignored, and Burgess species were shoehorned into modern phyla. So Walcott's classification, superimposed on this diagram, would look like this (Figure 19):

11'I I, iPIII 'KA W:NFT in.-, ARTHROPODA I \ PRESENT V V

H A O MIDDLE CAMBRIAN

H - Maiimigeftf®

Figure 19. Classification of Three Burgess Genera - Phase 1 Walcott included Burgess genera within already established modern phyla: he placed Hallucigenia (then known as Canadia sparsa) among the annelid worms, and placed Anomalocaris and Opabinia with the crustacean arthropods.

It would have been inconceivable in Walcott's day to erect new phyla based solely on extinct organisms.160 With no other options available to him, Walcott had no choice but to force the

Burgess organisms into those existing phyla with which they shared at least some characters.

In the case of Hallucigenia (known to Walcott as Canadia sparsa), these were the annelid worms; Anomalocaris and Opabinia were classified as crustaceans within the arthropods.

In Phase 2, the arthropods were no longer seen as a monophyletic group, and the emphasis in taxonomic methodology at the time was on the possession of diagnostic features.

This will be discussed more fully in Chapter 5. 97

The Burgess species that lacked the features diagnostic of known phyla and possessed unique attributes of their own were placed in their own, separate phyla (Figure 20):

ONfCHOPHOEA ARTHROPQDA r i / " \ IESEHT V V

MH)fM.K CAMBRIAN www

t II = HaUucigenia •J A - Anomatouaris i O = Opahinia

mmmmcEfmu vmsmms AUCISTOE

Figure 20. Classification of Three Burgess Genera - Phase 2 Each unusual Burgess genus appears to require its own phylum, and seems to have evolved independently of other Burgess and modern phyla from separate ancestors.

In Phase 3, with the advent of cladistics and its corollary stem group concept, came the realization that those Burgess species which possessed some, but not all, features diagnostic of modern phyla might be stem group lineages basal to the modern phyla, not unique phyla of their own. The classification of HaUucigenia, Anomalocaris, and Opabinia would now appear like this (Figure 21): ONYCHOPHORA BPAJKTHROPODA

PRESENT

H A mtmM -p- CAMBRIAN

11 » Baltmigenia if A ^Anmmfoeatis 0<*'Ops8»!>jta * *r

V

mmmmcEvwm mBmMmmmsmm,

Figure 21. Classification ofThree Burgess Genera - Phase 3 The three unusual Burgess creatures can now be classified with modern groups^—Hallucigenia on the stem leading to crown-group onychophorans, and Anomalocaris and Opabinia on the stem leading to the true arthropods.

Hallucigenia is now considered a stem-group onychophoran, while Anomalocaris and

Opabinia are stem-group arthropods.

An example of a Phase 3 classification of the arthropods can be seen in a 2003 paper by Graham Budd. In this diagram, the onychophorans, including Hallucigenia, are shown as the sister group to the true arthropods. The onychophorans are now grouped with other former Burgess oddballs Opabinia and Anomalocaris, on the stem leading to the crown group comprised of the modern phylum Arthropoda.161 In this article, Budd presented a diagram which illustrates the culmination of the phylogeny of the third phase of Burgess

Shale studies (Figure 22):

161 Graham E. Budd, "The Cambrian fossil record and the origin of the phyla," Integrative and Comparative Biology vol. 43, no. 1 (2003), 160. mmmmmm. wmmmtm - HaUudgeniB JR; 4*

mmmmmmt

Ammalocaris wmmomtmrnT Etarthropoda

•««*««»«•(»« MM men*

Figure 22. Stem-Group Arthropods fromth e Burgess Shale If this diagram were redrawn to fitJefferies' s stem and crown group model, the genera Aysheaia through Anomalocaris would comprise the stem group, and the Euathropoda would be the crown group. While the adoption of cladistics and the stem and crown group model alleviates the problem of me Burgess weird wonders, a new classification problem arises: stem groups are extinct by definition, yet there are living representatives of the onychophorans and tardigrades. These and other issues are the subject of current debate, and will be discussed in Chapter 5. Modified from Budd, "The Cambrian fossil record and the origin of the phyla," 160.

This new classification recognizes that the Burgess oddballs, such as (in the above example) Hallucigenia, Opabinia, and Anomalocaris, possess some but not all features possessed by true (crown group) arthropods. Whereas in Phase 2 these differences were thought to warrant new phyla for the Burgess misfits, the new insights afforded by cladistics and the stem and crown group concept allow paleontologists to place these species within the stem lineage leading to the arthropods. The weird wonders of the Burgess Shale now have a place within our established classification: on the stem group lineages leading up to, and filling the gaps between, the modern phyla.

Briggs and Fortey clearly recognized the importance of the stem and crown group concept and cladistics in the new understanding of the Burgess Shale. In their 2005 paper, they wrote: Wills et al (1994) demonstrated that the great majority of Cambrian taxa can be accommodated with their modern counterparts in a plausible hypothesis of relationships - by building a phytogeny from the bottom up rather than trying to place fossils into higher taxa defined exclusively on the basis of living organisms. This approach shifted the emphasis from autapomorphy - the much-bruited 'weirdness' - to synapomorphy, the characters shared between one animal and another.162

In his 2000 popular science book, Trilobite: Eyewitness to Evolution, Fortey further drove home the difference between the phylogenetic lawn of Phase 2 and the cladistic approach of

Phase 3:

It is a measure of how misleading Gould's theory would have been if taken at face value: these animals which were once touted as designs of uncommon originality would have been simply labelled 'failed experiments' and there's an end to it. As it now is, they have been recognized as important steps in our understanding of the subsequent history of life. The lesson of cladistics is that it is what animals share that is important in identifying their relatives, not our subjective judgements about oddity.163

The influential paleobiologist James Valentine, too, agreed with the improved Burgess Shale taxonomy afforded by cladistics:

By the logic that permits classification by monophyletic taxa that are arranged hierarchically and ranked by morphological disparity - Linnean taxonomy - these extinct forms [i.e., the unusual Burgess Shale arthropods] should be subphyla or classes. By the logic of cladistic classification, not recognizing

162 Briggs and Fortey, "Wonderful strife," 96. Wills et al is a paper written by Wills, Briggs, and Fortey, so the authors are here referring to their own earlier work. 163 Richard A. Fortey, Trilobite: Eyewitness to Evolution (London: Harper Collins Publishers, 2000), 131. 101

higher and lower taxa but rather earlier and later ones, these forms should be positioned according to their ancestral branching patterns.164

Briggs and Fortey expressed a similar view in their 1989 paper, and also recognized that "the treatment of these arthropods goes beyond the question of how to classify them - it affects our understanding of the nature of the Cambrian radiation."165 They reiterated this view in their 1992 paper, writing: "The taxonomic treatment is not merely a question of pigeon­ holing the taxa; it colors our perception of the nature of this early radiation and what can be deduced on the basis of early fossils belonging to a major group."166

Briggs and Fortey are right that the method of systematics one chooses to use has consequences beyond merely "pigeon-holing the taxa." While the adoption of cladistic methods allowed paleontologists to finally include both Burgess and modern taxa in the same classification, did it have any negative consequences? Did they have to sacrifice anything in making this shift to cladistic methodology?

Cladistics: Better Answers, or Just Different Questions?

Supporters of cladistics argued that their method was superior to the old systematics because they had a method. Cladistics had a concrete, explicitly articulated methodology, which when applied yielded a cladogram which stated a precise hypothesis of a sequence of evolutionary events. Different cladistic hypotheses could be compared and tested against one another. A particular cladogram might turn out to be wrong, but it was constructed with a rigor and a transparency that made it scientific and testable. In contrast with the rigorous and

164 James W. Valentine, On the Origin of Phyla (Chicago and London: The University of Chicago Press, 2004), 36. 165 Briggs and Fortey, "The early radiation and relationships of the major arthropod groups," 241. 166 Briggs and Fortey, "The early Cambrian radiation of arthropods," 350. explicit methodology of cladistics, evolutionary systematica, with no universal procedure to follow and relying on the intuition and accumulated wisdom of individual taxonomists, looked very unscientific by comparison. Cladistics won the day primarily by making evolutionary systematics look methodologically unsupportable and therefore unscientific.

What is usually not appreciated, however - and what only comes to light in a debate like the one over the Burgess Shale - is that cladistics and evolutionary systematics are not merely different methods of accomplishing the same goals, but that they are systems of taxonomic thought that pursue distinctly different goals. Adopting the methodology of cladistics also entails, whether overtly or tacitly, accepting the objectives of cladistics - and these are not the same as the objectives of evolutionary systematics. The goal of evolutionary systematics is the reconstruction of ancestor-descendant relationships, for the purpose of classifying organisms in natural groups, where "natural" includes not just recency of common ancestry, but also some notion of biological similarity or congruence. This latter notion is not a basis for valid grouping in cladistics, to the great consternation of some

(Gould, for example, announced: "I refuse to abandon the useful notion offish' because coelacanths are closer cladistic relatives of humans than of trout").167 The evolutionary systematic further hopes to use the resulting natural groups to investigate important biological questions, such as whether and how morphological disparity has changed over time. The goal of cladistics, by contrast, is to reconstruct a sequence of evolutionary events.

For a cladist, systematics can only show the sequence in which synapomorphies arose, and thereby yield a nested series of sister groups. But a cladogram, by itself, cannot answer questions about morphological disparity. A cladogram tells us the branching order of

167 Stephen J. Gould, "The promise of paleobiology as a nomothetic, evolutionary discipline," Paleobiology vol. 6,no. 1 (Winter 1980), 112. evolutionary events, but not whether some of these events are more significant, in a morphological or ecological sense, than others.

For Gould, who used the disparity of body plans in the Burgess Shale as crucial evidence for his contingent and punctuated view of evolution, cladistics was unacceptable because it simply ignores what he saw as the most important questions to ask about the significance of the Burgess Shale. As Gee noted, "Cladistics is concerned with the pattern produced by the evolutionary process; it is not concerned with the process that created the pattern, or the swiftness or slowness with which that process acted."168 As is obvious from

Gould's punctuated equilibrium and diversification and decimation models, he was particularly interested in posing questions about the tempo and mode of evolution, and thus could not even in principle have had much use for a systematics that denied paleontologists' ability to answer these questions. Likewise, Conway Morris seeks to answer questions about the tempo and mode of evolution, and though he disagrees with Gould on what the answers to these questions are, they both agree that these answers are not to be found in the results of a cladistic analysis.

Conway Morris lists several flaws of cladistics, one being the difficulty of choosing characters for cladistic analysis. This can be problematic because only homologous characters - those that are truly shared acquisitions from a common ancestor - are useful in elucidating phylogenetic relationships. But it can be very difficult to determine if what looks like the same feature in the different groups you are classifying is actually the same homologous character - it might only look similar but actually represent a convergence on the same design by groups with unrelated ancestors. If you believe, as Conway Morris does, that "convergence [is] rampant" in the history of life, it becomes more and more likely that many seemingly homologous characters are actually convergences, and are therefore useless ascladisticdata.169

The difficulty of choosing characters is only one challenge of cladistics. According to Conway Morris, an even worse problem is that cladistics focuses on character identification and classification at the expense of more important evolutionary questions. If, as Conway Morris suggests, cladistics just "treats taxa as basically sort of exploded particles of character states," then "this sort of atomistic approach to organisms is completely abiological. Organisms simply don't work that way." Instead, like Gould, Conway Morris wants to take a view that is not just taxonomic, but evolutionary. For him, the more important questions involve determining the origins and relationships of the major animal phyla, and are questions that cladistics is not equipped to answer:

By and large I don't find that cladists are really terribly interested in evolution. They'd be horrified to be told that, but I don't think they really are. They're not actually interested in transformation; they're interested in stamp collecting. Of a very high order, but it's still stamp collecting.170

Conway Morris hastens to add that cladistics can be a useful tool, if you recognize its limitations:

Obviously cladistics has immense virtues because it does define things, and it's rigorous inasmuch as it has to describe things, even if it is atomistic. And correspondingly it does at least present you with a tree which then has predictive value. It will at least say, 'did you know these two groups are more closely related than we realized?' Because the mind is not very good at collapsing a data matrix. And that, in certain cases, can be very valuable. But does it really talk about transformation, the process of evolution, no. I don't think it's particularly interested in doing that at all.171

Conway Morris, The Crucible of Creation, 179. Conway Morris, Interview 10 January 2007. Simon Conway Morris, Interview by author, 31 July 2007 (Cambridge, England, MP3 recording). For Conway Morris as for Gould, the most important questions to ask about the fossils of the Burgess Shale are questions about the origin and evolution of body plans and phyla, and both men agree that these are questions cladistics cannot answer. Cladistics can take the fossil groups in question and tell you which ones are most closely related to each other, but it cannot tell you how large or significant an evolutionary leap is needed to move from one group to the other. An examination more rooted in traditional evolutionary systematics, which evaluates not just the number of shared characters but their biological and evolutionary significance, is needed to answer questions about evolution. Conway Morris and Gould both asked these non-cladistic questions, and got very different answers.

In the particular case of the Burgess Shale - which has become the field upon which battles over the tempo and mode of early animal evolution are fought - the differing objectives of cladistics versus evolutionary systematics suddenly gain crucial importance.

Where some people, like Briggs, saw cladistics as the best tool for answering their questions about the Burgess Shale organisms, others, like Gould, argued that cladistics changed the very questions one could ask, leaving the most important ones untouched. What were the questions that Gould wanted to ask, and how did the adoption of cladistics change or obviate these questions?

A Question Cladistics Cannot Answer: Morphological Disparity Then and Now

Gould and Conway Morris agreed that cladistics could not answer their questions about evolution. While Conway Morris's central question involved the origin of the known phyla and the step-by-step assembly of their characteristic body plans,172 Gould's central question concerned the overall morphological disparity displayed by organisms through the

172 Of which more will be said in Chapters 3 and 5. history of life. Cladistics ignores the weirdness of the Burgess Shale fossils because it is of little apparent use in phylogenetic reconstruction. But for Gould, the weirdness of the

Burgess Shale is the object of study - you cannot simply ignore it. Gould argued vehemently, in Wonderful Life and especially in a series of papers published in the 1990s, that the adoption of cladistic methods left this most important question raised by the Burgess

Shale unanswered. Gould argued that the Burgess Shale contained, in addition to representatives of the four known arthropod classes and approximately thirty-five known animal phyla, twenty novel arthropod classes and fifteen to twenty completely new phyla.

Gould's reason for claiming these new phyla and classes was purely on the grounds of morphological difference: he argued that the Burgess oddballs are so morphologically unlike modern animals that they deserve to be ranked as separate from and taxonomically equivalent to them.173

Biologists have often talked of the diversity of life increasing over time. Gould pointed out that this term can be defined two ways: we may mean to say that the number of species (or genera, or families, etc.) is increasing over time; or we may mean to say that the morphological difference among organisms is increasing over time. (Another way of expressing this second sense is to say that organisms have occupied an increasingly large volume of morphospace through time.) These two definitions of diversity (taxonomic and phenetic) have often been conflated because in a sense they are coupled: if we are distinguishing taxonomic groups by their differing morphologies, then at any given time we can expect a rough equivalence between the number of such different groups and the amount of morphological difference among organisms.

Gould, Wonderful Life, 100. Only in the case of organisms like those of the Burgess Shale do we encounter a situation where it becomes crucial to disentangle these two definitions: paleontologists hesitate to erect higher taxa like classes and phyla on the basis of only one or a few genera, yet according to Gould at least, if we were to group these genera in a way which truly reflects their biological uniqueness, they should be in their own classes and phyla. If we do not establish new classes and phyla for groups which deserve them by virtue of anatomical uniqueness, then in this case an artificially reduced taxonomic diversity will mask what should be revealed as a much higher morphological diversity.

In preparing to argue his case for the uniqueness of the Burgess creatures, Gould first set out to decouple these two definitions of diversity. Following Runnegar (1987), Gould renamed diversity in the second, phenetic, sense "disparity."174 His reason for doing so was to allow the argument that disparity has not been increasing over time, even if, as is commonly assumed, diversity has.

As mentioned above, it has been a common belief among biologists and paleontologists that diversity has increased with time. Biologists Krebs and Dawkins refer to this widely held belief as "the commonsense feeling that there is temporal polarity in evolution, an arrow pointing in the direction of increasing complexity and even improved adaptedness." And, they point out, there must be some sense, some very coarse scale, on which this belief is unassailable: "Directionalist common sense surely wins on the very long time scale : once there was only blue-green slime and now there are sharp-eyed metazoa."175

If we have progressed fromblue-gree n slime to millions of different species of arthropods

174 Bruce N. Runnegar, "Rates and modes of evolution in the Mollusca," in Rates of Evolution, K.S.W. Campbell, and M.F. Day, eds„ 39-60 (London: Allen & Unwin, 1987). 175 and J. R. Krebs, "Arms races between and within species," Proceedings of the Royal Society of London. Series B, Biological Sciences, vol. 205, no. 1161 (1979), 508. alone, then surely taxonomic diversity has increased over time. But has morphological disparity increased along with it?

If Gould was right, then at the time of the Burgess Shale 505 million years ago, there were approximately fifty-five animal phyla, and within the Phylum Arthropoda, twenty-four arthropod classes. If this is correct, then disparity must have decreased over time, because even if taxonomic diversity has increased in surviving lineages, the fact remains that we now have only (approximately) thirty-five animal phyla, including only three living arthropod classes, today. As Gould wrote, "The later history of life proceeded by elimination, not expansion. The current earth may hold more species than ever before, but most are iterations upon a few basic anatomical designs."176 This is Gould's key argument in Wonderful Life - that his diversification and decimation model of evolution, which inverts the traditional cone of increasing diversity, is the more accurate model of how evolution works, and as I have said before, it depends crucially on the anatomical uniqueness of the Burgess oddballs.

So, what effect has the adoption of cladistics had on the perception of the Burgess

Shale? According to Gould, cladistics has absolutely nothing to say about disparity. For many others, however, the fact that cladistics and its associated stem and crown group concept have allowed the classification of Burgess organisms within (or as stem lineages of) modern phyla has been taken as evidence that disparity was not as high in the Cambrian as

Gould claimed. This disagreement is not so much over the fossils themselves, as over systematic methodology.

As Gould argued convincingly in his 1991 paper "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis: why we must strive to quantify morphospace," cladistics by definition does not and cannot answer questions about the

176 Gould, Wonderful Life, 47. relative disparity of groups of organisms, such as the Burgess versus the Recent arthropods.177 Cladograms trace sequences of evolutionary events, and taxa are grouped on cladograms according only to their shared derived characters. The cladogram gives no indication of the morphological weight or significance of one character compared to another, and there is no place on a cladogram for unique characters possessed only by one taxon

(autapomorphies). How then can one judge the biological and evolutionary significance of the range of morphological designs seen in the Burgess Shale? Remember, if we are cladists and care only about recency of common ancestry, then we would classify things like humans and coelacanths in the same group, at the expense of putting coelacanths and trout together in a different group called "fish." Our feeling (admittedly subjective, but perhaps justified nonetheless?) that we are very different things from both coelacanths and trout, while they are in more ways alike, would count for nothing, in cladistics. Cladists might point out, if thus accused of making nonsensical groups, that they are only making claims about sister- group relationships, not about ecological roles or biological significance - but then they admit to not being equipped to deal with precisely those questions which Gould wants to answer.

The most highly contested ground in the debate over Cambrian versus Recent disparity is the Phylum Arthropoda. According to Gould, one can distinguish twenty-four different arthropod body plans in the Burgess Shale, compared to the three arthropod body plans that Gould said survive today (represented by three extant arthropod classes Crustacea,

Uniramia, and Chelicerata).178 While it is true, Gould acknowledges, that many different

177 Gould, "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis," 411-423. 178 Arthropod classification is a very active field, and much has changed even in the twenty years since Gould published Wonderful Life. Most arthropod systematists working now no longer recognize the Uniramia as a valid group, and instead distinguish four extant arthropod classes or subphyla (the ranking too is in flux),no t 110 morphological variations exist within each of the three modern groups, all members of each group are nevertheless instantly identifiable by their shared patterns of tagmosis and number, type, and position of appendages. Lobsters, crabs, and barnacles look very different from each other, but they are all crustaceans, and therefore all have two pairs of pre-oral antennae

(the first uniramous and the second biramous), and three pairs of post-oral feeding appendages. Similarly, though spiders, , and horseshoe crabs look very different at first glance, they all share the key features that unite the chelicerates, including a precise and unique pattern of tagmosis and segmentation, and the possession of a uniquely specialized pair of feeding appendages, known as chelicerae.

Among the Burgess Shale organisms, however, one can distinguish twenty unique patterns of tagmosis and appendages distinct from those found in the three living groups and in the trilobites, another group of arthropods which were discovered long before the Burgess

Shale, and which became extinct approximately 250 million years ago. Regardless of whether one formally recognizes each of the twenty unique Burgess designs as new arthropod classes, wrote Gould, these patterns of tagmosis and appendage distribution clearly show a much higher disparity of arthropod design in the Cambrian Burgess fauna than in the three designs remaining today.

In a 1990 review of Wonderful Life, zoologist Mark Ridley suggested that in making this disparity claim, Gould had succumbed to an error in judgment, created by a reliance on three: the Crustacea, Chelicerata, Myriopoda, and Hexapoda. The myriopods and hexapods were formerly united to comprise the uniramians, but recent work, especially molecular phytogeny, suggests mat the hexapods are more closely related to the crustaceans than the myriapods, thus making the Uniramia a paraphyletic (and therefore unacceptable) group. (For a recent general overview of arthropods, including their classification, see Ward C. Wheeler, Gonzalo Giribet, and Gregory D. Edgecombe, "Arthropods," in Encyclopedia of Evolution, vol. 1. Mark Pagel, ed., 74-77 (Oxford: Oxford University Press, 2002).) These changes do not negate Gould's argument - as he noted in Wonderful Life, questions of actual morphological disparity should still stand regardless of the particular classification imposed on the organisms in question - but the changes to arthropod classification do serve to show that opinions of arthropod relationships and body plans are most definitely in a state of flux. Ill our modern-centric taxonomy. As Ridley noted, "an increasing diversity at higher taxonomic levels will arise automatically if you take the modern definitions of higher categories and apply them retrospectively."179 What Ridley meant by this "retrospective fallacy," as Gould later named it (in denying that he had succumbed to it), was that if you insist on rigidly classifying ancient, extinct organisms according to modern groups, the number of higher categories you need will be artificially inflated. Today, as Ridley pointed out, we distinguish crustaceans from other arthropods because (among other things) they possess two pairs of antennae. But, said Ridley, it is merely an accident of history that all crustaceans alive today happen to have two pairs of antennae. There might have been crustaceans in the past that had one pair or even three pairs. Likewise, in the future a species of crustacean might arise that has one or three pairs of antennae. It is only because such a species hasn't done so yet that we attach any importance to the possession of two pairs of antennae. Gould, according to

Ridley's analogy, is seeing things like crustaceans with one or three pairs of antennae in the

Burgess Shale, failing to recognize them as crustaceans because he is clinging too hard to a present-biased classification, and thus mistakenly thinking they represent entirely new (and equivalent, in taxonomic rank) body plans.

In a 1991 response to both Ridley's review and Briggs and Fortey's cladistic analysis,

Gould continued to argue for his weird wonders interpretation of the Burgess fauna. He insisted that the higher disparity he saw in the Burgess Shale is not dependent on the formal classification (i.e., on assigning high taxonomic rank to Burgess oddballs), and denied committing the retrospective fallacy. Gould agreed that the retrospective fallacy is a genuine pitfall that must be avoided:

179 Mark Ridley, "Dreadful beasts", Review of Wonderful Life by Gould, London Review of Books, vol. 12 (28 June 1990), 12. 112

Tagmosis and pattern of appendages may be characters that define classes today, but a Cambrian paleontologist would not have known this later history. He [sic] would have peered into the Burgess sea, found a bunch of arthropod species, each with differing numbers and arrangements of segments and appendages, and concluded mat such distinctions are superficial, easily made, and worthy only of defining, say, genera within families. Thus, Burgess arthropods were not so disparate in their own terms, but only by the invalid criterion of what happened to separate large groups later on.180

Nevertheless, Gould argued, it remains true that disparity was much greater in the Cambrian.

It may be true that we cannot use tagmosis and appendage patterning as the basis of classification in the Burgess Shale because these characters had not yet stabilized into their modern arrangements, but, Gould noted, there were no stable characters yet among Burgess arthropods. It is, Gould argued, the fact that these characters became stabilized or entrenched

- to the extent that they came to define all future arthropods to the level of classes (or subphyla in some classifications) - that both demonstrates a loss of morphological disparity, and raises questions about evolution that cladistics simply cannot answer. Gould's claim that disparity was demonstrably maximal in the Cambrian even without committing the restrospective fallacy is problematic, for it continues to rest on the importance he assigns to the characters which define the modern groups - not because we happen to have chosen them as the basis of our classification, but because they have proven themselves to be somehow more biologically important than other characters. The reason they are important is because they have stabilized over time. These particular combinations of tagmosis and appendage patterns have become developmentally entrenched, and therefore, on Gould's system,

"count" for more than more variable characters.

Gould responded to Ridley's example of crustaceans with one, two, or three pairs of antennae by pointing out that all crustaceans from the Burgess Shale down through 500

180 Gould, "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis," 413-414. 113 million years of evolution to the present have had precisely two pairs of antennae, even while other aspects of crustacean morphology have proven highly variable, capable of evolving into "forms as disparate as barnacles and lobsters." Gould continued,

I think it fair to assume that this and other features of the crustacean developmental Bauplan represent active stabilizations. The fact that tagmosis was so labile in Burgess times, and that only four patterns both survived and congealed, points to marked reduction in disparity for characters of special interest by virtue of their powers to constitute active archetypes.181

If readers share Gould's faith in the increased value of stabilized over non-stabilized characters, then perhaps they will agree with him. If they don't, then it seems Gould is indeed committing the retrospective fallacy -just not for reasons of retrospection. He agreed that we should not expect to be able to apply a taxonomy based on modern animals to creatures which lived 500 million years earlier and assume they will fall neatly and precisely within the modern categories, but he also argued that because the suites of characters we use as the basis of our modern classification have mysteriously become entrenched, then any differing suites of characters we find 500 million years ago must represent alternate body plans that went extinct for no good reason and might otherwise have themselves gotten stabilized. A lot of tacit categories and claims are packed into this assertion, including the idea of developmental entrenchment or stabilization, and the definition of a body plan, based on a suite of what Gould describes as characters of fundamental architectural depth.182 These tacit claims will be explored in Chapter 5.

It is the existence and rigorous scientific examination of such woolly things as the architectural depth of one character compared to another that the Burgess Shale is best suited to provide answers to, and yet the new methodology of cladistics is not. Cladistics only

181 Gould, "The disparity of die Burgess Shale arthropod fauna and the limits of cladistic analysis," 418. 182 Gould, "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis," 418. 114 reconstructs a sequence of evolutionary events; it does not measure the biological importance of these events. The great tragedy in the shift from Phase 2 to Phase 3 was not that Gould was proven wrong about the morphological disparity of the Burgess Shale, but that this disparity became, in some senses, a non-question. For many scientists, the fact that the

Burgess oddballs can now be slotted into a cladogram with modern animals seems to have put the disparity question to rest. But as Gould pointed out, "temporal branching order and morphological disparity are separate issues."183 The former is the province of cladistics; the latter is the domain of phenetics,184 and neither method can solve the problems of the other.

Gould particularly lamented the cladistic practice of disregarding autapomorphies on the basis that they do not reveal anything about branching order. This is true as far as it goes, and is therefore a sound practice when one is trying to reconstruct a sequence of branching events. But it does not follow that because autapomorphies are irrelevant for temporal branching order, that they are also irrelevant to answering other important questions. As

Gould vehemently argued, "autapomorphies lie at the heart of arguments about disparity."185

As Gould noted, a cladogram showing a sequence of key morphological (or molecular) innovations does not tell you anything about the tempo or mode of evolution. It does not tell you how much time has passed between the acquisition of one character and another, nor can it show the adaptive significance of the transition between one nested group and another. These points, especially the latter, are the reasons Gould cited for being unsatisfied with the application of cladistics to the Burgess Shale:

Gould, "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis," 415. 184 From the context, I believe that Gould here and elsewhere intends phenetics to mean the analysis and comparison of morphological characters, and is not referring specifically to the school of numerical taxonomy, which is sometimes called numerical phenetics. 185 Gould, "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis," 415. 115

How can anyone make a claim about Burgess versus modern disparity with a chart [i.e., a cladogram] that has eliminated all the unique tagmoses of the Burgess taxa and does not acknowledge the spiny carapace of Marrella, the three-pronged tail fluke of Odaraia, and the remarkable (and different) frontal appendages of Leanchoilia and Yohoia7m

Briggs, Fortey, and Wills on Morphological Disparity: A Response to Gould

Even as Gould was writing his first impassioned plea for greater disparity in the

Cambrian (i.e., Wonderful Life), Briggs and Fortey, along with Matthew Wills, a Ph.D. student under their joint supervision, were looking for ways to address this question.187 From a more cladistics-oriented perspective, which Briggs and Fortey gradually acquired as the

1970s became the 1980s, the claims about enormous morphological disparity in the Burgess

Shale (which came originally from the Cambridge team's own preliminary work) looked especially unlikely. Briggs noted that "certainly before Wonderful Life came out, Richard

[Fortey] and I had started worrying about the whole issue of disparity, and definitely thought that it was probably hugely exaggerated by Steve's approach."188 The question was, how could morphological disparity be properly measured, and compared between different groups?

Briggs and Fortey encouraged Wills to do his dissertation on this specific question.

The results of Wills's studies (1990-1994) were a thesis and a series of articles co-authored with Briggs and Fortey, in which they used both principal components analysis and cladistic

Gould, "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis," 415. 187 In feet, Briggs and Fortey set out to find a Ph J>. student who would, as his or her dissertation research, find ways to quantity and compare Cambrian and recent disparity. When they found Matthew Wills, this became his project. See for example Wills, The Cambrian Radiation and the Recognition of Higher Taxa, Briggs, Fortey, and Wills, "Morphological disparity in the Cambrian," and Wills, Briggs, and Fortey, "Disparity as an evolutionary index." 188 Briggs, Interview 27 March 2007. 116 analysis to estimate and compare Cambrian versus Recent morphological disparity.189 The cladistic analysis was evaluated in terms of the distance (i.e., number of branching events) separating Recent versus Cambrian taxa from the basal node of the cladogram, while the principal components analysis mapped the Recent versus Cambrian taxa on a multidimensional morphospace - taxa were mapped on 134 different character axes, and the average distances (deviations) from the centres (most prevalent character states) were compared between Cambrian and modern taxa. The results of both methods indicated to

Briggs, Fortey, and Wills that morphological disparity seemed to peak rapidly in the

Cambrian explosion and that it has remained steady or increased slightly since then - not declined as Gould's diversification and decimation model proposed.

Gould and his co-author, Mike Foote, a paleontologist at the University of Michigan, challenged these results on the grounds that the sample of Recent taxa chosen by Briggs and his co-authors was not random, and was selected in a way that artificially maximized Recent disparity.190 They also argued that their colleagues' results, in showing little or no increase in disparity through the Phanerozoic, supported Gould's inverted cone model and not the traditional cone of increasing disparity. Briggs, Fortey, and Wills agreed that their sample was not random, but retorted that the Cambrian sample is not random either, but is "biased in favor of benthic muddy substrate dwellers" - the kinds of organisms most likely to have been trapped in the Burgess Shale when it was created.191

Briggs, Fortey, and Wills, "Morphological disparity in the Cambrian," 1670. 190 See Mike Foote, Stephen J. Gould, Michael S.E. Lee, Derek E.G. Briggs, Richard A. Fortey, and Matthew A. Wills. "Cambrian and Recent morphological disparity," Science vol. 258, no. 5089 (11 December 1992), 1816, and Mike Foote, "The evolution of morphological diversity," Annual Review of Ecology and Systematics vol. 28 (1997): 129-152. 191 Foote et al., "Cambrian and Recent morphological disparity," 1817. 117

Though the debate is still open, most scientists now seem to agree that Recent disparity is at least equal to, if not greater than, that of the Cambrian, though Gould continued to hold out for his inverted cone model until his death in 2002. However, even if

Gould was wrong after all about the question of morphological disparity, the important thing to note is the raising of this particular question. The debate over disparity is an excellent example of the way the questions one can ask, and usefully answer, change according to the theoretical and methodological framework within which one is practicing. The question of morphological disparity is the crucial element of the pre-cladistic Phase 2, and yet is not even a relevant question within the cladistic framework of Phase 3. It required a deviation from the new cladistic framework and a return to numerical phenetic methods to examine this question - and still, in many ways this issue has been rendered a non-question, or at least has had much of the wind knocked out of its sails.

For all Gould's later claims that his arguments for greater Cambrian disparity did not depend on actually assigning the weird wonders of the Burgess Shale to their own higher taxonomic categories, the fact that cladistic analysis does not support the weird wonders view seems to have settled the disparity issue in the cladists' favour, in most paleontologists' minds. The fact that cladistic analysis (and its corollary stem group concept) has shown how to integrate Burgess and modern animals in the same classification, and the further fact that cladistics tends to downplay the significance of autapomorphies, have tamped down the burning question of the remarkable morphological disparity of the Burgess weird wonders.

Instead of believing, as Gould did, that "the autapomorphies exhibited by some of the early arthropod stem groups are... 'worth' a high-level taxon," a recent article by Briggs and Fortey argued instead that "many of them constitute plesions [i.e., stem groups] on the tree leading 118

to the crown group." Fortey and Briggs further asserted that Gould's "claims about the

numbers of Cambrian body plans are not taken seriously today."192 The adoption of

cladistics has radically changed the way the Burgess Shale animals are perceived.

Conclusion: Shifting Methods and Shifting Perceptions

The shift in understanding of the Burgess Shale creatures between Phase 2 and Phase

3 occurred largely because of factors outside of the fossils themselves. The adoption of

cladistic methodology and its corollary stem group concept provided an entirely new

taxonomic framework within which to situate these bizarre and seemingly unique forms. In a

sense, then, this phase shift can be seen as a methodological artifact, a new understanding

forged not by new data but by the reinterpretation of the systematic significance of

autapomorphies. This interpretation does not imply that this shift was not real, however, nor

that it was not extremely useful. As both Conway Morris and Briggs have pointed out, the phylogenetic lawn or weird wonders view characteristic of the second phase was not actually

a useful tool for understanding the diversity of Cambrian animals and their relationship to

modern phyla, since it drew very few connections between Burgess and modern forms, pushing their divergence from common ancestors back into the unknown Precambrian.193

While cladistics has its limitations, at the least it enables its practitioners to construct clearly

stated hypotheses about the relationships among the organisms under examination. But do these clearly stated hypotheses come at the expense of other, equally important questions for

paleontology - namely, the investigation of the tempo and mode of evolution?

192 Briggs and Fortey, "Wonderful strife," 97,94-95. 193 Conway Morris, The Crucible of Creation, 176-183, and Briggs and Fortey, "The early Cambrian radiation of arthropods," 350. 119

Briggs, Conway Morris, Budd, and other paleontologists studying the Burgess Shale have recognized its value not only in cataloguing the animal life of 500 or so million years ago, but in giving us crucial information about the origin and early evolution of the animals, and the nature of the evolutionary process itself. Cladistics has proven indispensable in accomplishing the former, yet cannot be used to judge the latter. Thus, the tension between these two goals of Burgess Shale research is highlighted by the adoption of cladistic methodology, exemplified by the work of Briggs, Fortey, and Wills, which has been the focus of this chapter. The focus of the next chapter is on the work of Simon Conway Morris, and the reasons behind his shift from Phase 2 to Phase 3. Chapter 3 Conway Morris's Reclassifications: "Fishing in the Cambrian Sea"194

Simon Conway Morris, like Derek Briggs, came to disagree with the Phase 2 or weird wonders view of the Burgess Shale, eventually adopting what I have characterized as a Phase

3 view, in which the Burgess creatures were seen as less strange, and as stem group relatives of modern organisms. Conway Morris, however, did not change his mind because of the adoption of cladistic methods; in fact, Conway Morris, like Gould, does not believe that cladistics is an especially useful tool, particularly as applied to the Burgess Shale. If it was not the new cladistic classification that converted Conway Morris, what was the cause of his shift in perception? According to Conway Morris, there were three main causes of his conversion to Phase 3. The first was the reclassification of Hallucigenia by Ramskdld and

Hou in 1991, and the discovery of related creatures in the Lower Cambrian Chengjiang fauna of China. The reorientation of this enigmatic organism from Conway Morris's original reconstruction allowed a better understanding of Hallucigenia's true nature - and this, combined with the discovery of related organisms such as Microdictyon and in the Chengjiang fauna, made it much easier to sort out the affinities of these strange creatures with already-known animal groups. The second factor was the discovery and description of the and halwaxiids, best known from another Burgess Shale-type fauna, the Sirius Passet fauna of Greenland. These were a group of armoured slug-like animals, which Conway Morris came to believe helped to bridge the gap between several different modern phyla, thus illustrating the step-by-step evolution of their respective body plans. The third factor was the reclassification of Anomalocaris, an animal so unusual that

194 Conway Morris, Interview 10 January 2007.

120 121

different parts of its body were at various times classified in five different known phyla (and

one previously unknown one), and then - when the entire animal was finally assembled - it

was placed in a unique phylum of its own. More recent work showed, however, that

Anomalocaris was actually a stem group relative of a modern phylum, the Arthropoda. It is

apparent that Conway Morris's three causes are actually three aspects of the same cause: an

increased understanding of the fossils themselves, based on the examination of new fossil

material as well as the re-examination of existing material, leading to a new appreciation of

their morphologies and similarities. This new appreciation gave Conway Morris a

completely new perspective of the Burgess Shale, one very different from the view on which

Gould based his weird wonders interpretation.

In this chapter I will explore these changes and their implications for the

understanding of the Burgess Shale. First, I will present evidence of Conway Morris's initial

(Phase 2) interpretation of the Burgess Shale, which was not only largely consistent with, but was actually the inspiration for, Gould's weird wonders view. Next, I will document the shift

in Conway Morris's thinking, by discussing in detail the three examples which led him to a new classification and thus a new understanding of the Burgess Shale. Of these three

examples, first we will detail the classification and reclassification of Hallucigenia sparsa;

second, we will examine the re-study of Wiwaxia corrugata and the discovery of its relatives among three modern animal phyla, and third, we will explore the unusual taxonomic history

of Anomalocaris. These explorations will allow us to fully tease out the very different route by which Conway Morris (as opposed to Briggs) arrived at a new understanding of the

Burgess Shale. "That's easy: I changed my mind."

One interesting circumstance of Burgess Shale history that has been remarked upon by several authors is the fact that, although Conway Morris came to hold a position opposite to Gould's, his initial view of the Burgess Shale was not only very similar to Gould's but actually served as the inspiration for Gould's interpretation. In Wonderful Life, Gould acknowledges Conway Morris's 1985 redescription of Wiwaxia as "the original source of

[his] interest in writing about the Burgess Shale."195 In this monograph, Conway Morris acknowledged some similarities between Wiwaxia and the molluscs, but concluded

"Nevertheless, Wiwaxia has a distinctive bodyplan and as such cannot be accommodated in any known phylum."196 Conway Morris also speculated that the Cambrian explosion might have been a time of many '"experiments' in metazoan design," during which "diversification

[was] simply a reflection of the availability of an almost empty ecospace with low levels of competition permitting the evolution of a wide variety of bodyplans, only some of which survived in the increasingly competitive environments through geological time." He also mused that the molluscs might not necessarily have been adaptively superior to the somewhat similar wiwaxiids, which would suggest that "if the clock was turned back so metazoan diversification was allowed to re-run across the Precambrian-Cambrian boundary, it seems possible that the successful bodyplans emerging from this initial burst of evolution may have included wiwaxiids rather than molluscs."197 The image of turning back the clock, and the suggestion of contingently different outcomes, both appear in much more detail in Gould's

193 Gould, Wonderful Life, 189. 196 Simon Conway Morris, "The Middle Cambrian metazoan Wiwaxia comigata (Matthew) fromth e Burgess Shale and Ogygopsis Shale, British Columbia, Canada," Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 307, no. 1134 (30 January 1985), 508. 197 Conway Morris, "The Middle Cambrian metazoan Wiwaxia corrugatar 570,572. 123

Wonderful Life, in which he argues that a replay of the tape from the time of the Burgess

Shale would yield a vastly different history of life.

Gradually, however, through the mid 1980s, Conway Morris changed his mind about the classification and interpretation of the Burgess Shale fossils. As he examined more fossil evidence, both from the Burgess Shale and from its sister faunas in China and Greenland, he slowly began to puzzle out the relationships of the Burgess animals to each other, and to modern groups. Conway Morris wrote two books presenting his new understanding: The

Crucible of Creation (1998), about the discovery and significance of the Burgess Shale, and

Life's Solution (2003), about the role and implications of convergence in evolution. Both of these books can be seen as direct responses to Wonderful Life. Two chapters in The Crucible of Creation, and the entire text ofLife's Solution, are devoted to presenting a view of evolution that is diametrically and explicitly opposed to that presented by Gould in

Wonderful Life.

Several reviewers of Conway Morris's books have commented on Conway Morris's failure to mention that he once held views very similar to Gould's - views which he opposes in these books. For example, Desmond Collins noted in his 1999 review of The Crucible of

Creation that "the surprising aspect of Conway Morris's account is that he gives no indication that Gould's 1989 contingency theory is strikingly similar to his own views at that time."198 Conway Morris may not have written much about having changed his mind, but he is perfectly willing to own up to it in conversation. The first thing I ever said to Conway

198 Collins, 'To be or not to be," 26. See also Andrew Berry, "Wonderful crucible," Review of The Crucible of Creation: The Burgess Shale and the Rise of Animals by Simon Conway Morris (Oxford: Oxford University Press, 1998) Evolution vol. 52, no. 5 (October 1998), 1529, Nigel CHughes, "Heat and light in the 'Crucible of Creation'," Review of The Crucible of Creation: The Burgess Shale and the Rise of Animals by Simon Conway Morris (Oxford: Oxford University Press, 1998) Paleobiology vol. 24, no. 4 (Autumn 1998), 536, and Jeffrey Levinton, "Who owns the Cambrian explosion?" Review of The Crucible of Creation: The Burgess Shale and the Rise of Animals by Simon Conway Morris (Oxford: Oxford University Press, 1998) The Quarterly Review of Biology vol. 74, no. 2 (June 1999), 202. Morns was to ask him, during the question period following a public lecture he gave at the

University of Toronto, how he explained the fact that he now disagreed with Gould's

interpretation of the Burgess Shale as containing many unique animal classes and phyla, and

demonstrating the importance of contingency in evolution, when he had at one time shared

these views and even served as Gould's inspiration in taking them up. Conway Morris

answered immediately, matter-of-factly, and with some amusement: "That's easy: I changed

my mind."199 Also, in addition to the Wiwaxia monograph referred to by Gould as his

inspiration, Conway Morris wrote another article, in 1987, which expressed his former views

even more explicitly. Conway Morris directed my attention to this article during our first

interview: "In fact, there was another paper which I reprint part of in a chapter I wrote in a

book called Cambridge Minds, and that was by far the most explicit thing about, you know,

if the world had really been radically different. And it's curious, I'll put it in a very English

way, that Gould didn't refer to that paper even though he was given a xerox of it."200

In this paper, originally published in Geology Today, Conway Morris speculated that

"hypothetical time travellers" visiting the Burgess Shale organisms when they were alive

"would have no means of predicting which groups would be destined to success, and which

to failure by extinction. Therefore, out of the vast diversity of forms, each with its own

peculiar body-plan, only a small proportion survived to populate ultimately the entire planet

with their evolutionary progeny."201 When he wrote this article, therefore, Conway Morris

seemed to hold a view of evolution similar to that espoused by Gould in Wonderful Life.

Simon Conway Morris, "What evolution tells us about extraterrestrials," (Public Lecture, Ecology and Evolutionary Biology Seminar Series, University of Toronto, Toronto, Ontario, 24 October 2006). 200 Conway Morris, Interview 10 January 2007. 201 Simon Conway Morris, "Cambrian enigmas," Geology Today vol. 3 (May-June 1987): 88-92. Why does it seem so important that Conway Morris has since changed his mind? As discussed briefly in Chapter 1, there was a time when Briggs, Conway Morris, and

Whittington all made statements endorsing what seemed to be a Phase 2 view of the Burgess

Shale. Specifically, they each remarked on the fact that the Burgess Shale contains representatives of what seem to be several unique animal phyla. Conway Morris wrote in

1979 that "About 16% of the [Burgess Shale] fauna cannot be placed in known phyla."202

Briggs wrote in 1983: "A huge number of metazoans have been described from the Burgess

Shale which do not belong to any living phyla."203 And Whittington wrote in 1985: "Far more remarkable in the Burgess Shale, however, is the large number of miscellaneous animals that do not fit into any phylum or class of animal known today."204 Thus each of these men once thought that the Burgess Shale contained representatives of many new phyla as well as representatives of modern phyla.

Gould's interpretation of the Burgess Shale did not stop at postulating many new phyla, however, but also used them to argue that contingency has played a huge role in the history of life, to the point that this history would never be repeated, in any replay of the tape of life. As we have already seen, Conway Morris presented a similar metaphor in his monograph on Wiwaxia. Perhaps it is the failure to admit to this change of heart for which

Conway Morris should be singled out. But what has not been appreciated is that Briggs seems to have briefly held this view as well. In a 1983 article on the "Affinities and early evolution of the Crustacea," Briggs indicated his hopes that cladistic analysis would help elucidate the relationships of the Burgess fossils, but also wrote:

Conway Morris, "The Burgess Shale (Middle Cambrian) fauna," 343. Briggs, "Affinities and early evolution of the Crustacea," 2. Whittington, The Burgess Shale, 128. The identification of living arthropods to phylum or superclass level is rarely a problem, as the effect of evolution through the Phanerozoic has been to eliminate all but three major morphologically distinct groups (Crustacea, Chelicerata and Uniramia)... There is also ample evidence that arthropod taxa in addition to the three major living groups, and the trilobites, were present in the Palaeozoic. While the Burgess Shale may bias the record it appears that the number of such additional taxa was greatest in the Cambrian and decreased through geological time as extinct forms were replaced by diversification at lower levels in the taxonomic hierarchy.2 5

The views presented in this quotation sound very much like those of Gould, in which a burst producing maximum morphological disparity in the Cambrian Period was followed by the extinction of many of these unique body plans, and the subsequent diversification of species within the body plans that remained. Yet, in a series of articles published through the late

1980s and 1990s, Briggs (along with colleague Richard Fortey and their student Matthew

Wills), explicitly opposed this view, using cladistics and morphospace analyses to argue that morphological disparity has not decreased since the Cambrian. In a 2005 article (perhaps ironically, part of a special volume intended to pay tribute to Gould), Briggs and Fortey wrote that "early claims about the numbers of Cambrian body plans are not taken seriously today," and that "this view of evolution came under scrutiny [by themselves and Wills] almost from the outset."206

My purpose in making this comparison is not to argue that Briggs should be criticized for changing his interpretation of the Burgess Shale - changing one's mind is a frequent and necessary component of science - but rather to contrast this case with that of Conway Morris.

Why has everyone noticed that Conway Morris changed his mind, but no one seems to have noticed that Briggs did as well? There seem to be two reasons. One difference seems to be the vehemence with which Conway Morris - and not Briggs - has attacked Gould's

205 Briggs, "Affinities and early evolution of the Crustacea," 2. Emphasis added. 206 Briggs and Fortey, "Wonderful strife," 94-95. 127 interpretation of the Burgess Shale. Another difference, of course, is that Gould credited

Conway Morris - and not Briggs - as the source of his interpretation of the Burgess Shale.

Dennett noted in Darwin's Dangerous Idea that while the early Burgess Shale publications of Whittington, Briggs, and Conway Morris bemoaned the fact that these bizarre creatures were difficult to assign to known phyla, and wondered if it would be necessary to erect new phyla to accommodate them, they never took this view to the extremes that Gould did, and "their caution has proven to be prophetic; subsequent analyses have tempered some of their most radical reclassificatory claims after all... If it weren't for the pedestal Gould had placed his heroes on, they wouldn't now seem to have fallen so far - the first step was a doozy, and they didn't even get to take the step for themselves."207

The pedestal Dennett mentions must have been an awkward one to stand on. On the one hand, Gould's book made the Cambridge team famous. As Budd explained, "Simon was very well-known before Wonderful Life came out... He had a very good reputation. But after

Gould's book came out, he became stratospherically famous... In that sense it was a big deal for Simon and to that extent for Derek Briggs as well."208 In a sense, then, Gould did

Conway Morris and Briggs a favour, by bringing them and their work on the Burgess Shale to the attention of millions of readers, scientists and laypeople alike, who might not otherwise have heard of them. But Gould wrote his book based on the Cambridge team's preliminary interpretations of the Burgess fossils, and as Gould himself noted (in the case of Walcott, and with some derision), preliminary interpretations are often wrong. Conway Morris freely admits that his initial descriptions and attempted classifications of several Burgess fossils

Dennett, 301. Graham E. Budd, Interview by author, 12 May 2006 (Toronto, Ontario, MP3 recording). were not correct, and that these mistakes led to incorrect interpretations of the fossils. As Conway Morris explained:

it [working on the Burgess Shale] was a bit like having a time machine which happened to have fishing equipment on it and having twenty minutes to go fishing in the Cambrian Sea. So, you know, one had the first cut through the diversity there. And...had I been slightly smarter and slightly more intelligent, then I would have seen things slightly more easily. But, you know, we didn't, so we made plenty of mistakes.

Gould's accolades in Wonderful Life, then, are for interpretations with which their originators no longer agree. This situation would be awkward enough, but these accolades came at an even higher price, because Gould did not just praise the Cambridge team's work; he appropriated it to serve his own theory of evolution, which is the real focus of the book.

Anyone who reads Wonderful Life does not just learn about the discoveries made by Briggs,

Conway Morris and the others; he or she also learns that these discoveries led to a view of evolution as a highly contingent process in which outcomes are not counterfactually robust, and morphological disparity reached a maximum in the Cambrian and has declined ever since. And furthermore, he or she learns that this view of evolution originated with Simon

Conway Morris. Gould is not just praising Conway Morris and the others, then; he is tarring them with his own evolutionary brush, and subsuming their interpretations within his own theories. Gould might be called presumptuous just for having written the book at all: he did no work on the Burgess fossils himself, and Conway Morris (and the other members of the

Cambridge team) might have preferred to tell their own story, rather than having an outsider tell it for them. As marine ecologist and paleobiologist Jeffrey Levinton observed, "One can't help but notice that Gould skipped the hard work of analysing characters and relationships among fossil groups, and instead substituted the 'Oh my! Ain't they weird!'

Conway Morris, Interview 10 January 2007. 129 approach."210 As Levinton hinted, not only did Gould "scoop" the Cambridge team in telling their story, he also firmly appended his own interpretations and conclusions to their work.

Conway Morris noted,

you could say, from one perspective, he [Gould] was just hijacking a set of scientific observations and using them for his metaphysics. But everyone has metaphysics, so that's okay. I can't complain about that. I think his metaphysics is completely wrong, about as wrong as you can be, but that's another story.211

This other story, about Conway Morris's own "metaphysics" and his own theory of evolution, is told in the two books I mentioned above, The Crucible of Creation and Life's

Solution.

Conway Morris did indeed make some preliminary speculations about contingency, in the 1985 Wiwaxia monograph and in one other paper, but it seems that when he realized where these ideas could lead - to a theory of evolution like that presented in Wonderful Life - he changed his mind. But his initial "mistake" is forever preserved, not just in print, but in one of the best-selling popular science books of all time. This is surely an uncomfortable position to be in, and surely the reason why Conway Morris has tried all the harder to make his own theory of evolution - one almost diametrically opposite to Gould's - heard and understood.

These two theories of evolution, Gould's and Conway Morris's, will be explored and contrasted in Chapters 4 and 5. Now let us turn to the reason for Conway Morris's changing interpretations of the Burgess Shale fossils. After further opportunities to "fish in the

Cambrian sea," Conway Morris realized that several Burgess creatures were not as they had initially appeared to be. His new understanding allowed him to begin to sort out the affinities

210 Levinton, 203. 211 Conway Morris, Interview 10 January 2007. of these organisms to each other, and to modern groups - not with cladistics, as in Briggs's case, but simply through an increased appreciation of morphology. We begin with

Hallucigenia.

The inversion of Hallucigenia

Hallucigenia sparsa was first discovered by Walcott, who named it Canadia sparsa and classified it among the polychaete annelids (bristle worms). When Conway Morris began his examination of Hallucigenia, he saw immediately that it was very different from

Walcott's other Burgess polychaetes, such as Canadia spinosa, and in fact, resembled nothing Conway Morris had ever seen. His "dissections" of various specimens showed that the creature then known as Canadia sparsa had no immediately identifiable head, a row of paired spikes on one side of the body, and a single row of tentacle-like structures on the other, with bifid, hardened tips, resembling little beaks. (See Figure 9, p. 29.) Conway

Morris surmised that the creature had walked on the paired spikes and fed with the beaked tentacles, each of which probably therefore led independently to the gut, and he (in collaboration with a friend, trilobite paleontologist Ken McNamara) renamed the unusual

91*? creature Hallucigenia "as a tribute to its dream-like appearance." Hallucigenia was, at the time, one of the most obviously unique Burgess creatures, and Conway Morris concluded his

1977 paper with the observation that "i£ sparsa cannot be compared to any living or fossil animal."213 Like many other Burgess genera, Hallucigenia was initially given "Phylum

Uncertain" status.

Conway Morris, "A new metazoan fromth e Cambrian Burgess Shale," 624. Conway Morris, "A new metazoan fromth e Cambrian Burgess Shale," 638. 131

Hallucigenia featured prominently in Gould's cast of weird wonders, strange

creatures of the Burgess Shale of such unique anatomical design as to deserve taxonomic

recognition in their own phyla. Gould wrote in Wonderful Life: "If one creature must be

selected to bear the message of the Burgess Shale - the stunning disparity and uniqueness of

anatomy generated so early and so quickly in the history of modern multicellular life - the

overwhelming choice among aficionados would surely be Hallucigenia,,"214 Others agreed;

Richard Fortey described Hallucigenia as the "oddest of the oddities" of the Burgess

Shale, and Conway Morris himself noted that "The apparent weirdness of Hallucigenia

began to be taken as the exemplar of the Burgess Shale." Harvard evolutionary biologist

Andrew Berry referred to it as "the pinup of Burgess weirdness."217 In the early 1990s,

however, a dentist-turned-paleontologist set out to discover if Hallucigenia was really as bizarre as it seemed. Lars Ramskold, like a few other critics of Conway Morris's

Hallucigenia reconstruction, pointed out that no known animals walked on hard spikes as

Conway Morris's Hallucigenia seemed to. It would make much more sense to turn the

creature upside down: if the tentacle-like extensions on the other side of the animal were its

legs, then the inflexible spines (now on the creature's back) could serve as a sharp deterrent to predators. The only problem was, Conway Morris's work on the thirty known specimens

of Hallucigenia had only revealed one row of tentacles - and it would be even harder to walk

on a single row of legs than to walk on paired spikes.

214 Gould, Wonderful Life, 153. Gould immediately qualified this statement by adding in parentheses, "though I might hold out for Opabinia or Anomalocaris." Like Hallucigenia, these too are now considered to be much less weird than was thought at the height of Phase 2. 215 Richard A. Fortey, "Shock lobsters," Review of The Crucible of Creation by Simon Conway Morris, London Review of Books vol. 20 (October 1,1998), 24. 216 Conway Morris, The Crucible of Creation, 54. 217 Berry, 1531. 132

But was there really only a single row of tentacles? Ramskold obtained permission to carefully "dissect" through the top layer of rock and fossilized tentacles on the type specimen of Hallucigenia, to see if another row of tentacles could be found beneath. In this Ramskold was successful: the row of tentacles turned out to be paired after all, making it functionally possible to suppose that these "tentacles" were actually soft, flexible legs on which

Hallucigenia walked, and that the paired spines were not locomotory appendages but protective dorsal armor.218 (Figure 23)

Figure 23. Hallucigenia sparsa (Ramsk6ld, 1992) Modified from Ramskeld, 224.

In this new orientation, Hallucigenia no longer seemed like a solitary oddball, but instead found some relatives among Cambrian as well as modern groups. In the mid 1980s, a

Lars RamskSld, and Xianguang Hou, "New early Cambrian animal and onychophoran affinities of enigmatic metazoans," Nature vol. 351, no. 6323 (16 May 1991): 225-228, and Lars RamskSld, "The second leg row of Hallucigenia discovered," Lethaiavol 25 (15 April 1992): 221-224. 133

fossil locality similar to the Burgess Shale in its preservation of soft body parts, but several

million years older, was discovered in the Province of China. This Chengjiang fauna

yielded several fossils of armored, worm-like creatures, including Microdictyon. (Figure 24)

With Hallucigenia turned right side up, the resemblance between it and Microdictyon was

clear. The resemblance between Microdictyon and the Burgess Shale genus Aysheaia was

also readily apparent, and it had already been noted by several scientists (as far back as

Walcott's day) that Aysheaia bore a remarkable resemblance to the modern velvet worms or

onychophorans, a terrestrial group of soft-bodied invertebrates, worm-like but with lobopods

Figure 24. Microdictyon sinicum Modified from Bergstrom and Hou, 239. Originally drawn by Polyanna von Knorring. 134

or squishy, tentacle-like legs. (Figure 25) No longer the "wondrous beast" embodying "the

stunning disparity and uniqueness of anatomy" of the Phase 2 Burgess Shale, Hallucigenia is

now one of several genera placed firmly on the stem leading to the onychophorans, primitive

relatives of the Arthropoda.219 And far from being an experimental body plan which

perished forever in Gould's great lottery of life, the onychophoran body plan lives on in the

form of several modern genera, including the velvet worm Peripetias. This realization was

Figure 25. Aysheaia pedunculata Modified from Gould, Wonderful Life, 169. Originally drawn by Marianne Collins.

Gould, Wonderful Life, 153-157. very important in altering Conway Morris's perception of the Burgess creatures. As he explained,

I couldn't put my finger on when it [my perception of the Burgess organisms] began to shift, but clearly Ramskold's reinterpretation of Hallucigenia and recognition of similar Chengjiang onychophorans was instrumental in making one realize that some of these things were not as strange as they appeared to be.220

Gould's example, on the other hand, shows that perhaps things are just as strange as one wants them to be. In 1992 he wrote an article (one of his regular Natural History Magazine columns) about the reclassification of Hallucigenia, and in it concluded that nothing had really changed - yes, perhaps Hallucigenia is an onychophoran instead of its own weird phylum, but that just proves that the onychophorans are themselves weird wonders! In the article, Gould argued for his own philosophy of classification, as against the "traditional" shoehorn (Phase 1) and straightening rod (Phase 3), and then concluded: "The Onychophora, under this view [i.e. his own weird wonders view], might represent a separate group, endowed with sufficient anatomical uniqueness to constitute its own major division of the animal kingdom, despite the low diversity of living representatives." As noted above, most paleontologists and biologists regard the Onychophora as a stem group or sister group of the Arthropoda, and though they are given phylum status by some scientists, they still have living members and have been formally recognized since 1853, so they should not be suddenly surprising anyone with their bizarre and unique morphology.

Conway Morris, Interview 10 January 2007. 221 Gould, "The reversal ofHallucigenia" 344. This is a reprint of the original article which was published in Natural History Magazine in January of 1992. 136

The Affinities of Wiwaxia

A similar transformation occurred in another species that Conway Morris originally designated "Phylum Uncertain" - Wiwaxia corrugata. (See Figure 10, p. 30.) Wiwaxia corrugata was originally discovered and named in 1899 by G. F. Matthew, based on disarticulated hard parts. Matthew found an isolated spine of Wiwaxia in the Ogygopsis

Shale, a set of fossil beds now considered to be part of the Burgess Shale, and named for the most abundant trilobite species found within it. Walcott found more spines and body fossils of Wiwaxia in the Ogygopsis Shale and in his own Walcott Quarry, and he classified it among the polychaete annelids. Conway Morris undertook an extensive redescription of

Wiwaxia, using both old and new specimens, the results of which were published in the

Philosophical Transactions of the Royal Society of London in 1985. In this monograph,

Conway Morris removed Wiwaxia from the annelids and suggested instead a possible relationship with the Phylum Mollusca. He also proposed, as had others before him, that the similarity of Wiwaxia'$ sclerites to other isolated sclerites, named Halkieria, found in older

(Tommotian) rocks as well as the Burgess-type Sirius Passet fauna of Greenland, suggested that they were from the same kind of animal.

Wiwaxia, measuring approximately five centimetres at adult length, was a somewhat oblate, compact creature, densely covered in overlapping sclerites, and with additional spines sticking up from its back, presumably as protection from predators. Walcott had speculated that these sclerites and spines were modified chaetae, his reason for classifying them among

222 See for example Stefan Bengtson and V.V. Missarzhevsky, "Coeloscleritophora - a major group of enigmatic Cambrian metazoans," in Short Papers for the Second International Symposium on the Cambrian System. Michael E. Taylor, ed., 19-21 (U.S. Department of the Interior, Geological Survey Open-File Report 81-743,1981), and P.A. Jell, "Thambetolepis delicata gen. et sp. nov., an enigmatic fossil from the early Cambrian of South ," Alcheringa vol. 5 (1981): 85-93. the polychaetes. Conway Morris pointed out, however, that the sclerites and spines of

Wiwaxia were not distributed across the body in the same way as the comparable structures of polychaete annelids, nor did they seem to attach to the body in the same way.

On the other hand, as Conway Morris noted, Wiwaxia's ventral surface (the underside) was not covered in sclerites and bore a feeding apparatus that seemed to have a significant resemblance to the molluscan radula. On the basis of this similarity, Conway

Morris suggested that Wiwaxia and the molluscs might share a distant ancestor, but acknowledged also that they are sufficiently different that they probably could not be accommodated within the same phylum. He opted to tentatively adopt a classification proposed by James Valentine in 1973, in which the wiwaxiids, molluscs, and hyolithids (a group of extinct, bivalved, conical animals) are united in the Superphylum Molluscata.223

Over the next few years, further studies by Conway Morris and by others seemed to strengthen the links between Wiwaxia and both the polychaete annelids and the molluscs.

Nicholas Butterfield, a Canadian paleontologist, used hydrochloric acid to dissolve the shale surrounding several disarticulated wiwaxiid sclerites, allowing him to study the sclerites with a transmission light microscope and a scanning electron microscope for the first time.

Butterfield's examination revealed that Walcott had in fact been right in thinking that

Wiwaxia's sclerites resembled comparable structures of polychaete annelids, both compositionally and structurally. Like polychaete setae, the sclerites of Wiwaxia are broad, flattened, hollow structures ornamented with microscopic knobs and denticles.224 Molecular

22 James W. Valentine, "Coelomate superphyla," Systematic Zoology vol. 22, no. 2 (June 1973): 97-102. 224 Nicholas J. Butterfield, "A reassessment of the enigmatic Burgess Shale fossil Wiwaxia corrugata (Matthew) and its relationship to the polychaete Canadia spinosa. Walcott," Paleobiology vol. 16, no. 3 (Summer 1990): 287-303. phylogenies of living animals, as early as the late 1980s, also began to suggest a close link between molluscs and annelids.225

At the same time, the sclerites and body fossils found abundantly in the

Sinus Passet fauna of Greenland suggested an equally close link between halkieriids,

Wiwaxia, and molluscs. Sirius Passet is a fossil locality in Peary Land, Greenland, with similar fossils to the Burgess Shale, but about ten million years older (Lower Cambrian, as opposed to the Middle Cambrian Burgess Shale). Sirius Passet was discovered in 1984 by A.

Higgins, a geologist with the Geological Survey of Greenland. Expeditions to the locality in

1989,1991, and 1994, led by British geologist John Peel and including Conway Morris, have yielded a collection of approximately 10,000 specimens.226 In terms of fossil quality, the

Sirius Passet fauna is preserved in slightly coarser shale than that of the Burgess, yielding less exquisite (but still visible) preservation of anatomical detail, especially of soft tissues.

Among the many fossil creatures represented in the Sirius Passet fauna was a group known as the halkieriids. Halkieriids {Halkieria and related genera), armoured slug-like creatures, were already known from other (Tommotian) fossil locales primarily as disarticulated sclerites, similar to those of Wiwaxia in size, shape and apparent composition.

The discovery of some articulated sclerites and - crucially - body fossils of halkieriids at

Sirus Passet yielded an unexpected outcome: in addition to the Wiwaxia-like sclerites covering most of their dorsal surface, the halkieriids also possessed shells on their anterior and posterior ends - shells that looked remarkably like those of the brachiopods, a separate

225 See for example Katharine G. Field et al, "Molecular phytogeny of the animal kingdom," Science vol. 239, no. 4841 (12 February 1988): 748-753, Simon Conway Morris, "The fossil record and the early evolution of the Metazoa," Nature vol. 361, no. 6409 (21 January 1993), 219, and Wheeler et al. 226 Graham E. Budd, "Stem group arthropods fromth e Lower Cambrian Sirius Passet fauna of North Greenland," in Arthropod Relationships, Systematics Association Special Series 55, Richard A. Fortey and R.H. Thomas, eds., 125-138 (London: Chapman & Hall, 1998), 125. 139 phylum of bivalved, clam-like invertebrates. (Figure 26) At the same time that Wiwaxia was proving to be closely linked with the annelids and the molluscs, then, its very close relatives, the halkieriids, were demonstrating their affinities with the brachiopods.

Figure 26. Halkieria evangelista Modified from Conway Morris and Peel, 337.

In addition to the influx of new Cambrian specimens from the Chengjiang and Sirius

Passet faunas, new fossils from the Burgess Shale gradually came to light, fromne w collections undertaken in the late 1970s and 1980s. Expeditions from Canada's Royal

Ontario Museum (ROM), led by two successive Curators of Invertebrate Paleontology,

Desmond Collins and Jean-Bemard Caron, yielded many exciting new specimens, including

Orthrozanclus reburrus, a fossil bearing both wiwaxiid sclerites and halkieriid shells. This new "halwaxiid," as Conway Morris and Caron dubbed it in a 2007 paper, cemented the evolutionary ties between the halkieriids and wiwaxiids. Conway Morris and Caron included a phylogeny diagram indicating two possible positions for Wiwaxia and other halwaxiids on the family tree connecting the major lophotrochozoan (lophophore-bearing) phyla: the Mollusca, Annelida, and Brachiopoda. (Figure 27) Though the precise location of the halwaxiids relative to the molluscs is uncertain, this discovery has already had the important effect of reducing the disparity of Cambrian animal groups. On the Phase 2 interpretation,

Wiwaxia and Halkieria would each have been classified in their own phylum. Here, in Phase

3, they are classified together on the stem leading to the molluscs, annelids, and brachiopods, which are themselves united in the Superphylum Lophotrochozoa.228 Thus the disparity of

Burgess taxa is reduced, while at the same time relationships between modern phyla are being elucidated.

Anomalocaris: Arthropod, Sea Cucumber, Worm, Jellyfish, Sponge, or Something Else?

Another factor in changing Conway Morris's perception of the diversity of the

Burgess Shale was the reclassification of Anomalocaris. Anomalocaris is such an odd creature that its remains, which are usually found in several disarticulated pieces, were initially assigned to three different higher-level taxa - the arthropods, jellyfish, and echinoderms. Later studies resulted in the reclassification of some of Anomalocaris's remains to two other phyla - the annelids and respectively. At one time or another, then, different parts of the creature now known as Anomalocaris were classified in five different known animal phyla. There was also a brief time in which it was thought that

Anomalocaris and Peytoia respectively represented two unique, unknown animal phyla.

227 Simon Conway Morris and Jean-Bernard Caron, "Halwaxiids and the early evolution of the lophotrochozoans," Science vol. 315, no. 5816 (March 2,2007), 1258. But see Jakob Vintner and Claus Nielsen, "The early Cambrian Halkieria is a mollusc," Zoologica Scripta vol. 34, no. 1 (January 2005): 81-89. Vinther and Nielsen interpret Halkieria as a crown-group mollusc, not closely related to the brachiopods or annelids at all. Mollusc crown group Annelid crown group BracMopod crown group

Mollusc crown group Annelid crown group crown group

Figure 27. Two Hypotheses of Lophotrochozoan Phytogeny A. Odontogriphus, Wiwaxia, and the halkierids are stem group molluscs. B. Wiwaxia and the halkieriids are on the stem leading to the annelids and brachiopods; Odontogriphus is on the stem leading to all three crown group lophotrochozoan phyla. Modified fromConwa y Morris and Caron, 1258. Conway Morris was responsible for the non-arthropod taxa of the Burgess Shale, so

he did the initial work on those Anomalocaris components that were thought to represent

non-arthropodan animals, even though this unusual organism was eventually placed in the

arthropods (the domain of Briggs and Whittington). The fossil originally given the name

Anomalocaris canadensis was found in 1886 on the slopes of Mount Stephen, fromon e of

the many quarries eventually comprising the as-yet-unnamed Burgess Shale, by Richard G.

McConnell, a geologist on a mapping expedition for the GSC. (Figure 28) The fossil, a

long, tapering structure with several spine-bearing segments and one broken-off end, was

prepared and named in 1892 by Joseph Whiteaves, chief paleontologist of the GSC.

Whiteaves thought the fossil was the headless body of an unknown phyllocarid crustacean (a

-like arthropod); the name he gave it means "anomalous shrimp."229

Figure 28. Anomalocaris canadensis — The Original Fossil Modified from Briggs, "Anomalocaris, the largest known Cambrian arthropod," 631.

Collins,"The 'evolution' ofAnomalocaris"280. When Walcott began collecting in the Burgess Shale, he discovered more of the broken-off

Anomalocaris "bodies" (in several different sizes, which he assigned to different species

within the genus), as well as several other unusual - and, he thought, unrelated - creatures.

One was a round, flattened disc-like animal with distinct segments and a hole through the

center of its body, making it look rather like a pineapple ring. Walcott named this creature

Peytoia nathorsti, and assigned it to the Phylum Cnidaria (jellyfish). (Figure 29) He found

broken-off pieces of other arthropods, including a carapace or outer shell without a body,

which he named Tuzoia. Walcott also named and described several sea cucumbers (Class

Holothuroidea, of the Phylum Echinodermata), including one which he called Laggania

cambria.230

Figure 29. Peytoia nathorsti Modified from Whittington and Briggs, "The largest Cambrian animal, Anomalocaris" 603.

Walcott, "Middle Cambrian holothurians and Medusae," 41-68. Most of Walcott's classifications stood until the Phase 2 reclassifications brought on by the work of the Cambridge team. One exception was a re-examination of Laggania in

1957, by a Danish paleontologist, F. Jensenius Madsen. Madsen took another look at

Laggania and decided that it was actually a polychaete annelid (a segmented worm of the

Phylum Annelida).231 This reclassification was widely accepted by the time Conway Morris and his colleagues began their re-examination of the Burgess Shale. Another change proposed between Walcott's time and Phase 2 occurred in 1928, when another Danish paleontologist, Kai Henriksen, suggested that Tuzoia and Anomalocaris might be parts of the same animal, with Tuzoia as the front half of the body, and Anomalocaris as the rear half.

The composite arthropod thus created was featured in several illustrations of Cambrian life in the 1930s and 1940s.232

Among the non-arthropodan taxa assigned to Conway Morris were the sea cucumber or polychaete annelid Laggania, and the jellyfish Peytoia. (The various species of

Anomalocaris, as well as Tuzoia, were assigned to Briggs for restudy.) In his restudy of the single known specimen of Laggania, Conway Morris discovered that the round structure at one end of the supposed sea cucumber, which Walcott had identified as its mouth, was identical to Walcott's jellyfish Peytoia, known from other, isolated specimens. Conway

Morris concluded, therefore, that the Laggania fossil actually comprised two distinct creatures: the jellyfish-like Peytoia, and the remaining bag-like structure, which he felt resembled sponges more closely than sea cucumbers or polychaetes. These conclusions were

231F. Jensenius Madsen, "On Walcott's supposed Cambrian holothurians," Journal of Paleontology vol. 31, no. 1 (January 1957): 281-282. 232 Kai L. Henriksen, "Critical notes upon some Cambrian arthropods described by Charles D. Walcott," Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening: Khobenhavn vol. 86 (1928): 1-20, qtd. in Collins "The 'evolution' ofAnomalocaris? 283. Charles Knight's famous painting of the Burgess Shale (featured on the cover of the first edition of Gould's Wonderful Life) includes such an illustration. presented m a 1978 paper in the Journal of Paleontology. Conway Morns and his co-author

Richard Robison removed Peytoia fromth e jellyfish, giving it Phylum Uncertain status, because of the un-jellyfish-like central hole which extended all the way through the "animal" from top to bottom. The remainder of the original Laggania (minus the pineapple-ring

Peytoia) was reinterpreted as a sponge.233

At the same time, Briggs was beginning his work on the arthropods, including

Anomalocaris. Though Anomalocaris did seem to be some sort of incomplete arthropod,

Briggs thought it must be a broken-off leg, rather than a broken-off abdomen and tail. The main reason for this conclusion was that if the entire specimen represented the terminal portion of an arthropod body, then the spines on each "body" segment must be individual appendages. But arthropods have jointed appendages - this is the chief diagnostic feature of the group - and the spines on each segment were continuous and inflexible, not jointed.

Another point was that the joints between each of the "body" segments were hinged, as in typical arthropod appendage joints, not made of flexible cuticle allowing movement in several directions, as in the connections between typical arthropod trunk segments. Briggs therefore concluded that each Anomalocaris specimen was the disarticulated leg of some larger arthropod, and speculated that the entire creature might resemble a very large marine centipede, with a row of Anomalocaris appendages down each side of a long body.

In the same paper, Briggs described a second appendage, similar to Anomalocaris but with fewer segments and longer and more blade-like spines, which he called (informally)

Appendage F. (Figure 30) Walcott had thought that this was a feeding appendage of the arthropod Sidneyia inexpectans, but David Bruton, in his 1981 redescription ofSidneyia,

233 Simon Conway Morris, "Laggania cambria Walcott: a composite fossil," Journal of Paleontology 52, no. 1 (January 1978): 126-131. 234 Derek E.G. Briggs, "Anomalocaris, the largest known Cambrian arthropod," Palaeontology 22 (1979), 631. 146 showed this to be incorrect.235 Briggs speculated that Appendage F was a feeding appendage used to catch prey (as opposed to the Anomalocaris appendages which he thought were walking legs), and probably belonged either to the same Anomalocaris animal, or to a very similar creature. As for Tuzoia, Briggs noted that he had never found this broken-off carapace in association with either Anomalocaris or Appendage F, and therefore concluded that Tuzoia was unrelated to the other Anomalocaris- and Appendage F-bearing arthropod.

Figure 30. Appendage F Modified from Briggs, "Anomalocaris, the largest known Cambrian arthropod," 644.

Bruton, 635. Briggs, "Anomalocaris, the largest known Cambrian arthropod," 656-657. 147

The story of Anomalocaris got even more interesting when Whittington started

"dissecting" the rock partially obscuring the fossil of a lobed, oblate animal which looked at first like a specimen of Opabinia. To his considerable surprise, as he removed the rock from around the body, Whittington discovered two Anomalocaris limbs clearly attached to one end. Other specimens he prepared next showed a pair of Appendage F limbs in a similar orientation, and between them a Peytoia "animal," affixed firmly to one end of the larger creature. Whittington (and Briggs, who joined Whittington in the analysis of this unusual animal), quickly realized that the fossil Conway Morris had interpreted four years before as a chance association of a sponge (Laggania) and an animal of unknown affinities (Peytoia) was actually another example of this mysterious new creature: Laggania was the bag-like, lobed body, and Peytoia was its mouth. The large appendages (Anomalocaris or Appendage

F) were situated on either side of the mouth and were presumably used to capture prey and force it into the oral opening.

The new creature was given the name Anomalocaris, since this was the name given to the first part of the animal to be described. Briggs and Whittington described the complete animal in a 1985 monograph, published by the Philosophical Transactions of the Royal

Society of London. (See Figure 11, p. 31.) In this monograph, Whittington and Briggs concluded that Anomalocaris represented a "hitherto unknown phylum." They further explained:

237 Other, secondary accounts of this work (e.g. Conway Morris, The Crucible of Creation, 57, and Collins, "The 'evolution' of Anomalocaris? 283) report that Whittington found both the limbs and the mouth attached to the first of these fossils that he worked on, but in Whittington's own reports, co-authored with Briggs, they clearly state that he found first a body with Anomalocaris limbs attached, and then a different body with Peytoia attached. See Harry B. Whittington, and Derek E.G. Briggs, "A new conundrum fromth e Middle Cambrian Burgess Shale," Proceedings of the Third North American Paleontological Convention vol. 2 (August 1982), 573, and Harry B. Whittington, and Derek E.G. Briggs. "The largest Cambrian animal, Anomalocaris, Burgess Shale, British Columbia." Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences vol. 309, no. 1141 (14 May 1985), 571. Although Anomalocaris bears a single pair of arthropod-like limbs, and the body is metameric, it is unlike any known arthropod, particularly in the nature of the jaw apparatus [i.e. the bizarre round mouth, formerly known as Peytoia] and the close-spaced, strongly overlapping lateral lobes [on the sides of the body].238

This sentence is an excellent illustration of two key features of Phase 2: first, it exemplifies the traditional evolutionary systematics that Whittington followed through his entire career, and which Briggs and Conway Morris also used before the advent of cladistics. In evolutionary systematics, all of an organism's characteristics are taken into account in its classification, and the possession of unusual characters (such as the Peytoia mouth and the possession of fleshy lobes in place of trunk appendages) is sufficient to exclude it from known phyla, if these unusual characters are not found in the phylum in question.239

Second, it is important to remember that at this time, Whittington and his students were following Sidnie Manton's classification of the arthropods.240 This meant that they already considered the arthropods to be a polyphyletic grade rather than a monophyletic clade, such that arthropod-like features could be acquired convergently by different groups and were not indicative of close relationship. As Whittington and Briggs wrote:

If arthropods are regarded as embracing at least three phyla (Manton 1977) then Anomalocaris must be regarded as a Cambrian representative of a new phylum of metazoan animals. The implication is that the arthropod-like pair of anterior limbs were evolved independently.241

On this system of classification, with the arthropods regarded as polyphyletic, the few similarities of Anomalocaris to arthropods are best dismissed as misleading convergences, while its many unique features require it to be given its own phylum.

Whittington and Briggs, "The largest Cambrian animal, Anomalocaris? 571,604. 239 See Chapter 2 for a full discussion of the methods and goals of evolutionary systematics, as compared to those of cladistics. 240 See Chapter 1 for a discussion of Manton's polyphyletic scheme of arthropod classification, and her influence on the Cambridge team. 241 Whittington and Briggs, "The largest Cambrian animal, Anomalocaris? 604. 149

At the height of Phase 2, Anomalocaris became yet another weird wonder, unclassifiable within existing groups and deserving of its own phylum. As more and more specimens of these unusual creatures were discovered, however, in both the Burgess Shale and in the Chengjiang fauna of China, more similarities to arthropods came to light. Several of the Chengjiang anomalocarids appeared to have trunk appendages that were lacking or not visible in the Burgess specimens, which only had the fleshy trunk lobes - and the trunk appendages of the new specimens were jointed like typical arthropod appendages (and also biramous).242 Conway Morris's former student Graham Budd, who studied the Sirius Passet arthropods as his dissertation work, named and described another new Cambrian creature from Greenland, Kerygmachela kierkegaardi, which he regards as a stem-group arthropod.243

(Figure 31) Kerygmachela shows similarities to Anomalocaris and Opabinia as well as to modern arthropods, suggesting to Budd and to Conway Morris that all three Cambrian genera are not weird representatives of extinct phyla, but rather are species very far down on the branches which led to the modern arthropods. Thus, these strange fossils do not show us wildly disparate unique phyla, but rather show the early stages of evolution of the known animal groups. On this view, then, the Burgess Shale does not show a vastly greater morphological disparity than the modern world, with a much larger number of animal phyla, but instead preserves the earliest representatives of already-known phyla.

242 Collins, "The 'evolution' of Anomalocaris," 291. 243 Graham E. Budd, "A Cambrian gilled lobopod fromGreenland, " Nature vol. 364, no. 6439 (August 19, 1993): 709-711. Figure 31. Kerygmachela kierkegaardi Modified from Budd, "The morphology and phylogenetic significance of Kerygmachela Merkegaardi? 279.

From the perspective of the new, Phase 3 understanding, Conway Morris believes he has identified a principal flaw in the Phase 2 view - especially with the reasoning behind

Manton's polyphyletic classification of arthropods, and its implications. Conway Morris observed that the phylogeny Manton constructed based on her enormously detailed body of work is in some ways "a test case" or exemplar of a common misconception in animal phylogeny in the mid^O* century.244 This misconception lies in the mistaken belief, which

Conway Morris attests that Manton and many contemporary systematists held, that in order to demonstrate a phylogenetic relationship between two modern phyla, one must be able to show how (members of) one of the phyla could be transformed into (members of) the other, through a finite series of steps, all of which are functionally viable. This belief is

Conway Morris, Interview 31 July 2007. 151 problematic because it is anachronistic: ancestors must be sought in the past, not contemporaneous with the group whose origins are in need of explanation.

An equivalent mistake would be to assert that modern humans are descended from modern chimpanzees, which is not the case. While chimpanzees are our closest living relatives, they have evolved over time just as we have, and can no more be presumed identical to our nearest common ancestor than humans can. As Conway Morris points out, to ask how one modern group might have evolved fromanothe r is getting things backwards:

And as I recall, in her great book she [Manton] was insistent that these things [= arthropods] had to be polyphyletic because it's impossible to make the transformations.... Because these things [^adaptations]... are so intricate, so finely balanced and so forth, that [you wonder] how on Earth can you break them down, and transform them into something else? Of course that's completely the wrong way to look at the question. It's completely back to front.245

In examining the evolution of primates, to continue with my example, we should not ask how one might picture a human evolving from a chimpanzee, but rather which features might characterize the common ancestor of both chimps and humans. And in the same way, it is erroneous to ask how you could possibly transform a trilobite into a chelicerate, say, or a myriapod into a crustacean - this is not the right question to ask. We should not be wondering how one modern class or phylum could evolve fromanothe r such modern group; these groups represent the end results of six hundred million years or more of animal evolution and entrenchment. The right question to ask is: could these different arthropod groups we recognize today have evolved from a common ancestor not identical to any of them, and what features might this common ancestor have possessed? Conway Morris stresses the correct questions to ask:

Conway Morris, Interview 31 July 2007. [H]ow do you get from A to B? Or, rather, how does A get to B in one direction and C in another direction? And the endpoints are just completely different from each other. And that's why I think the ongoing work on the Burgess in particular, we've been incredibly lucky, because we've had a whole set of animals turning up which really do seem to be informative about how you transform one thing into the other. Actually, as soon as you get the information it's completely trivial. It's painfully obvious. But no amount of imagination will allow us to make any headway in simply trying to suppose what the organism ought to have done.246

Graham Budd agrees with Conway Morris's assessment of pre-cladistic Cambrian phylogeny, and has made it something of a personal mission to rehabilitate this phylogeny by the introduction of the stem versus crown group distinction. Budd noted that zoologists like

Manton, whose emphasis is on modern groups, have

the idea that somehow you have to think of the adjacent position from this point [crown group one] to this point [crown group two]. But you don't have to do it like that. You don't need to convert the jaws of... a crustacean to the jaws of an or whatever because you've got a whole bunch of other stuff to look at. You've got the stem groups down here... [and] there's always evolutionary space to do this stuff [i.e., evolve crown-group sy napomorphies].247

The stem group concept is important because it forces one to take a pragmatic or nominalist view of body plans and phyla. Because classifications were originally (and understandably) based on extant organisms, we have built a present-centered bias into our biological taxonomy, which shows up in a huge way when we try to classify groups as ancient as the

Burgess creatures. From the bias of the present point of view looking back, we have already identified thirty-some modern phyla of animals, which now possess body plans completely distinct from one another, and we find it difficult to classify fossils that do not fall clearly within these modern groups. As we saw in Chapter 2, the stem group concept helps with this problem because it allows us to perceive the relationships of ancient fossils to our modern

Conway Morris, Interview 31 July 2007. Budd, Interview 12 May 2006. 153 groups, without forcing us to either shoehorn the fossils into the modern groups, or to erect higher taxa of equivalent rank to the modern groups to accommodate the unusual fossils.

Instead, fossils which possess some, but not all, of the features characteristic of a particular phylum can now be classified as stem group lineages, related to the ancestors of that phylum but not belonging within it. The research of Conway Morris in particular has also revealed some fossils, like the halwaxiids, that are stem lineages of not just a single phylum, but of several phyla simultaneously.

The realization that extremely ancient relatives of Recent groups might not look much like their modern descendants seems obvious in hindsight, but it is important to understand that this is a recent realization that has had a huge impact on taxonomy and the study of animal evolution. Thanks to the work of Simon Conway Morris, Derek Briggs, and others, paleontologists and taxonomists are learning just how much of a present-centered bias has been built into our system of taxonomic categories. Our most fundamental groups of animals

- the twenty-five or thirty phyla - were almost without exception created based on the examination and comparison of living animals. As such these phyla are very useful for classifying extant animals and recent fossils, but paleontologists have gradually realized that it is hugely problematic to attempt to classify very ancient fossils - such as those of the

Burgess Shale - according to these modern categories. They are also realizing that stem- group relatives of modern higher classes may be ancestral in some senses, but often possess unusual features of their own. 154

Conclusion: A Reduction in Morphological Diversity

As we saw in Chapter 2, the new cladistic methods adopted by Briggs allowed him to focus on the Burgess creatures' similarities to modern phyla. Briggs was able to classify

Burgess taxa within or as stem lineages of previously-known groups, leading to a reduction in taxonomic diversity of Burgess organisms, as compared to Phase 2. The continuing work on the halwaxiids, onychophorans, and anomalocarids led Conway Morris to a Phase 3 view as well, despite the fact that Conway Morris did not adopt cladistic methods. Instead,

Conway Morris's changing views of the morphology of the various groups he studied led him to perceive a reduction in morphological disparity, as he was better able to detect and appreciate the homologies between known groups and the seemingly odd Burgess creatures.

As was the case with Hallucigenia and the halwaxiids, further study on known and new specimens of anomalocarids gradually revealed connections to modern groups. The enigmatic Cambrian fossils were no longer shoehorned into modern phyla, as Walcott had done, but neither did they have to be set up in their own new phyla, as Gould argued (and as

Conway Morris himself had initially thought). Instead, they could be seen as stem group relatives of modern phyla, whose unique combinations of characters only look strange from a modern perspective - a modern classification with a 500-million-year bias built into it.

As Conway Morris explained it,

My own sense of where things changed... is that since then [i.e., since the publication of Gould's book], and especially with the advent of the Chengjiang faunas, which have filled in a number of useful gaps in the argument... and partly with Sirius Passet as well... in any of these cases... the argument I think has shifted comprehensively to the view that we are seeing the way in which the body plans are assembled. And... every body plan involves the acquisition of characters.248

Conway Morris, Interview 10 January 2007. Like Briggs, Conway Morris had come to believe that the enigmatic creatures of the

Burgess Shale did not represent a great experiment in the history of life, in which dozens of unique phyla (in addition to the thirty or so already known) arose in a great burst of morphological diversification, and then were randomly selected for extinction. For Briggs, this shift in perception was caused by his adoption of cladistics, with its emphasis on shared derived characters as indicators of common ancestry. For Conway Morris, a similar reduction in morphological disparity was achieved - but not through the adoption of cladistic methods. Instead, Conway Morris was convinced by new studies of the morphology of

Burgess taxa - both his own and those of other scientists - that the Burgess creatures were not entirely strange, but actually possessed key features identifying them as stem group relatives of modern animals. This question - the question of how body plans and phyla are gradually assembled — is for Conway Morris the most important question one can ask of the fossil record, and he predicts that more and better answers will continue to be found:

With regards to the Cambrian explosion, what the aim is, as I think has been pretty clear for about the last ten years, and the sort of things I've been trying to do, is to establish that however strange these groups might look, in point of fact they are informative about the assembly of body plans. ...And I suspect what will happen in the next ten years, I hope, with the Cambrian, is that most of the question marks which separate these apparently unrelated groups will be filled in. I'm reasonably confident. We're making progress.2 9

According to Conway Morris, then, the Burgess Shale demonstrates the step-by-step assemblage of modem body plans. According to Gould, there are dozens of unique body plans in the Burgess Shale, in addition to those representing modern groups, and each deserves taxonomic recognition as a phylum. But what are body plans, and what are phyla, and why should the one be taxonomically equivalent to the other? How do different body plans arise, and what makes one group have its own body plan, distinct from those of other

249 Conway Morris, Interview 31 July 2007. 156 groups? Conway Morris and Gould have both asked these questions, and have come up with very different answers. Their answers to these questions, and their implications for the interpretation of the Burgess Shale and the understanding of evolution, are the focus of the next two chapters.

First, in Chapter 4,1 will contrast their beliefs about the nature and occupation of morphospace, and the navigation of adaptive landscapes, to illuminate each man's commitment to two very different explanatory accounts of evolution: contingency and convergence. Then, in Chapter 5,1 will relate what we've learned from previous chapters to each man's definition of "phylum" and "body plan." The different ways that these concepts are deployed, not just by Gould and Conway Morris but also by Briggs and Budd, illustrate very different views of the history and mechanisms of evolution, and the place of the Burgess

Shale within it. Chapter 4 The Occupation and Navigation of Morphospace

"In the final analysis, we are what we are because of the process of natural selection rather than any internal specific and over-riding constraint."250

"The pool cue of natural selection may always do the actual pushing, but if internal channels - set by history, and grafted into the genetic and developmental architecture of current organisms - designate a limited set of possible pathways as conduits for selection's pushing, then these internal constraints can surely claim equal weight with natural selection in any full account of the causes of any particular evolutionary change."251

As we saw in Chapter 2, the adoption of cladistic methodology explains some reasons behind the shift from the second to the third phase of Burgess Shale studies. However, while

Derek Briggs used cladistics to forge a new understanding of the Burgess Shale, Simon

Conway Morris, who also made the transition to a Phase 3 view, is not a cladist, and disagrees with cladism's goals, methods, and results. Yet he too has come to see the Burgess fossils as much less taxonomically diverse than was thought at the height of Phase 2, though not, like Briggs, through redefining the objectives of systematics. Some of Conway Morris's motivations were explored in Chapter 3. Stephen Jay Gould, who maintained a Phase 2 view of the Burgess creatures until his death, shared Conway Morris's skepticism regarding cladistics. One might expect that this shared view of cladistics would cause them to hold similar beliefs about the Burgess Shale, but this is not correct - they disagreed completely on what the Burgess fossils are and what they mean. Why? This disagreement between

Conway Morris and Gould is fundamentally an argument about the tempo and mode of

250 Simon Conway Morris, "The Cambrian 'explosion' of metazoans and molecular biology: would Darwin be satisfied?" International Journal of Developmental Biology vol. 47 (2003), 511. 251 Stephen J. Gould, The Structure of Evolutionary Theory (Cambridge and London: The Belknap Press of Harvard University Press, 2002), 1173-1174.

157 evolution. These two men held utterly different views of the nature and operation of evolution, and it was these different beliefs that informed their differing perceptions of the

Burgess Shale. In a way, the Burgess Shale has performed as a testing ground for their radically different views about the process of evolution.

What exactly is the disagreement between Gould and Conway Morris, and what are its implications, particularly for an understanding of the Burgess Shale? In this chapter, I shall explore this disagreement. First, I will outline the major points of evolutionary theory on which Gould and Conway Morris disagree. Next, I will use the concepts of adaptive landscapes and morphospace models to illustrate the incompatible evolutionary theories of the two men. The answers to questions such as "What gives morphospace its shape?" provide an excellent tool for uncovering what exactly is at stake in this debate. And finally, having articulated the precise nature of the differences between Gould and Conway Morris, I will show how their deeply divergent views of evolution inform their radically different interpretations of the Burgess Shale and its place in the history of life.

The Contingency vs. Convergence Debate

The first point on which Gould and Conway Morris disagree - and the one on which they have been most outspoken - is the importance of contingency in evolution. Gould's

Wonderful Life (1989) is a celebration of contingency. In this book he popularized the metaphor of the "tape of life," and argued that if this tape were rewound to a time before the

Cambrian and started again, the history of life would be utterly different.252 Gould believed that small changes early in the history of life would produce radically different evolutionary

Gould, Wonderful Life, 189. histories in the long term. "Replay the tape a million times from a Burgess beginning,"

Gould asserted, "and I doubt that anything like Homo sapiens would ever evolve again."253

As Daniel C. Dennett pointed out in his 1995 book Darwin's Dangerous Idea,

Gould's argument very much depends on exactly what is meant by "anything like."254 If

Gould meant very specifically that the identical species Homo sapiens would not appear in every replay of life's tape, few would argue with him - not Dennett himself, and not even

Conway Morris. Thus, for each of these men, the origin of a particular species, arising from its one particular ancestor and bearing its own unique combination of specific characters, is seen as a highly contingent event that cannot be assumed to be inevitable. But suppose

Gould meant something much broader: what if "anything like Homo sapiens" meant some species of large-brained, tool-using, intelligent, warm-blooded, bipedal mammal? Or what if there was a large-brained, intelligent, bipedal, warm-blooded tool-user, but it wasn't a mammal? If some such species arises each time the tape of life is replayed, does it count as anything like Homo sapiens? From their various respective writings on the subject, I believe that both Gould and Conway Morris would agree that even a bipedal, intelligent, tool-using reptile would count as something like Homo sapiens, but that while Conway Morris believes the evolution of such a creature is effectively inevitable, given the origin of life itself, Gould believed the chances of any such creature evolving in any particular replay of the tape are vanishingly slim.

In this discussion of what counts as anything like a human, I have named several characteristics which seem, for Conway Morris and Dennett at least, to be shared by all creatures which can be called anything like humans. These characteristics included

Gould, Wonderful Life, 289. Dennett, 306-308. bipedahsm, and warm-bloodedness, and more importantly, large brain size and intelligence.

Dennett calls such characteristics "Good Tricks (or Good Moves) in Design Space,"255 and

Conway Morris refers to them as "biological properties." Conway Morris wrote:

[T]he number of evolutionary end-points is limited: by no means everything is possible. ...what is possible has usually been arrived at multiple times, meaning that the emergence of the various biological properties is effectively inevitable.256

The opposite of contingency is, of course, necessity: either things are necessarily the way they are, or they are contingent upon something, such that they might have been otherwise.

For Conway Morris, the history of life on Earth has not been contingent, but has instead followed a path of necessity: of all the possible forms living organisms might taken, only a relatively small number of them are viable (i.e., adaptively successful), therefore whatever organisms there are will repeatedly discover - converge upon - these few successful solutions. Thus the dichotomy can be recast as contingency versus convergence.

Dennett's answer to the replay of the tape of life is much the same as Conway

Morris's:

[W]hichever lineage happens to survive will gravitate towards the Good Moves in Design Space, and the result will be hard to tell from the winner that would have been there if some different lineage had carried on.257

Both Conway Morris and Dennett argue that it is not the evolution of specific individuals - such as the particular species Homo sapiens - which is required to make one replay of the tape the same as another, but only the repeated appearance of some individual with the relevant set of biological properties. Even at the level of something like biological properties, however, Gould sees a much greater role for contingency than for convergence:

Dennett, 306,307. Conway Morris, Life's Solution, xii, see also 283. Dennett, 306. 161

If each replay strongly resembles life's actual pathway, then we must conclude that what actually happened pretty much had to occur. But suppose that experimental versions all yield sensible results strikingly different from the actual history of life? What could we then say about the predictability of self-conscious intelligence? or of mammals? or of vertebrates? or of life on land? or simply of multicellular persistence for 600 million difficult years?258

Gould's theory of evolution is so highly contingent that even such major events as the origin of vertebrates, and the colonization of land, are unlikely to recur in his vision of the replay of life's history.

Conway Morris has been very outspoken in his opposition of Gould's contingency argument. In his book Life's Solution: Inevitable Humans in a Lonely Universe (2003),

Conway Morris argued that convergence is a much more powerful phenomenon in evolution than contingency. If there is some factor in operation which causes groups from different phylogenetic backgrounds to repeatedly converge on the same biological forms, then contingency becomes unimportant - particular paths may still be contingent, but if they all lead to the same destination, there is a sense in which they are no longer crucial. On Conway

Morris's view, re-playing the tape of life from the beginning of the Cambrian would yield a world very similar to the one we live in now. A particular Cambrian species might be wiped out in the replay that had survived in our world, but other species, faced with the same environmental challenges that our ancestors were, would eventually develop the same biological properties that would have characterized the descendants of the now-doomed lineage. The exact pedigree might be different in the alternate scenario, but the intelligent, bipedal, warm-blooded creatures would still come to be. No matter which particular lineages went extinct and which ones survived, on Conway Morris's view, those groups that did remain would navigate towards the same good design solutions that our ancestors did. Life's

Gould, Wonderful Life, 48-50. Solution is in essence a catalogue of evolutionary convergences, compiled with the aim of proving that the "emergence of various biological properties," most notably "human intelligence," is "a near-inevitability."259

This disagreement over the relative importance of contingency versus convergence is important - as the several books and articles devoted to it attest260 - but it is only the

Conway Morris, Life's Solution, xii. 260 See for example Conway Morris, The Crucible of Creation, and "Showdown on the Burgess Shale: the challenge," Natural History Magazine, vol. 107,no. 10 (December 1998-January 1999): 48-51, and Gould, Wonderful Life, "Showdown on the Burgess Shale: the reply," Natural History Magazine, vol. 107, no. 10 (December 1998-January 1999): 48,52-55, and "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis." Also, philosopher of biology John Beatty agrees with Gould's view of contingency and has expanded it into what he calls the Evolutionary Contingency Thesis (ECT). The ECT, briefly, holds that there are and can be no laws of biology, because any uniquely biological generalizations about the world (as opposed to those that can be reduced to mathematics, physics, or chemistry), "describe contingent outcomes of evolution." (John Beatty, "The Evolutionary Contingency Thesis," in Concepts, Theories and Rationality in the Biological Sciences, Gereon Wolters and James G. Lennox, eds., 45-81 (Pittsburgh: University of Pittsburgh Press, 1995) 47.) Laws cannot be contingent - by definition, they must hold universally, in all circumstances - so if biology is contingent, it does not operate according to laws of nature. Beatty cites Gould's Wonderful Life as an example and inspiration for his views on contingency, noting that his own goal is to "elaborate Gould's thesis and further defend it." (Beatty, "The Evolutionary Contingency Thesis," 46.) Other philosophers have responded to Beatty's claims, and a debate has arisen over whether there are laws of evolutionary biology, and if so, where we should look for them. Prominent figures in this debate include Martin Carrier ("Evolutionary change and lawlikeness: Beatty on biological generalizations," in Concepts, Theories and Rationality in the Biological Sciences, Gereon Wolters and James G. Lennox, eds., 83-97 (Pittsburgh: University of Pittsburgh Press, 1995)), Marc Lange, "Are there natural laws concerning particular biological species?" Journal of Philosophy vol. 92, no. 8 (August 1995): 430-451, and "Laws, counterfactuals, stability, and degrees of lawhood," Philosophy of Science vol. 66, no. 2 (June 1999): 243-267, Elliott Sober, "Two outbreaks of lawlessness in recent philosophy of biology," Philosophy of Science vol. 64, Supplement, Proceedings of the 1996 Biennial Meetings of the Philosophy of Science Association. Part II: Symposia Papers (December 1997): S458-S467, Sandra Mitchell, "Pragmatic laws," Philosophy of Science vol. 64, Supplement, Proceedings of the 1996 Biennial Meetings of the Philosophy of Science Association. Part II: Symposia Papers (December 1997): S468-S479, and "Dimensions of scientific law," Philosophy of Science vol. 67, no. 2 (June 2000): 242-265, Alex Rosenberg, "Reductionism in a historical science," Philosophy of Science vol. 68, no. 2 (June 2001): 135- 163, and Jim Woodward, "Law and explanation in biology: invariance is the kind of stability that matters," Philosophy of Science vol. 68, no. 1 (March 2001): 1-20. Conway Morris has not discussed the search for laws of evolutionary biology, and it is likely the case that this is not what he sees as the goal of his research. Gould, by contrast, did mention briefly, in Wonderful Life, the tension between "laws in the background" and "contingency in the details," and announced that he would place the boundary between these two realms "so high that almost every interesting event of life's history falls into the realm of contingency." Gould continued, "I regard the new interpretation of the Burgess Shale [i.e., the weird wonders view he advocated in this book] as nature's finest argument for placing the boundary this high." (Gould, Wonderful Life, 289.) Interestingly, this statement seems to contradict Gould's pronouncements elsewhere. For example, the emphasis Gould placed on contingency, and his declaration that paleontologists are interested in contingent historical outcomes as opposed to causal explanations, seems decidedly at odds with his explicitly stated ambition to make paleobiology into a nomothetic discipline of evolutionary biology. Perhaps Gould felt that his proposed mechanisms of macroevolutionary change, including punctuated equilibrium and the rather confusing model of diversification and decimation presented in Wonderful Life, would both suffice as laws of evolutionary biology and not suffer 163 beginning of the story. This debate points to other differences between Gould and Conway

Morris. If the history of life has been necessary, as Conway Morris believes, what in the nature of evolution, or the properties of living beings, has caused it to be this way? If the history of life has been contingent, as Gould believed, what about evolution or organisms made it so? In order to hold their respective beliefs about contingency and convergence,

Gould and Conway Morris must also hold very different views of the relative importance of natural selection and developmental constraint, and of the relationship between the organism and its environment. If convergence is as strong a factor as Conway Morris believes, then environmental pressures and selection must be the major driving forces in evolution. In other words, if species of very different phylogenetic backgrounds tend to converge repeatedly on the same form or design, this suggests that the environment is posing particular adaptive problems to which there are only a limited number of good design solutions. The fact that different species can arrive at these few good design solutions from highly disparate phylogenetic trajectories would further suggest that any internal (e.g., developmental) constraints limiting their potential form are less crucial than the natural selection directing them towards these convergent forms.

If it makes sense to describe different species as having convergently achieved the same adaptive solution to the same design problem, it must also make sense to think of the design problems posed by the environment as things that in some way exist independently of, and prior to, the organisms that must deal with them. As Lewontin pointed out, an emphasis on the importance of adaptation in evolution leads directly to such a view of the environment: "The concept of adaptation implies a preexisting world that poses a problem to unduly from the effects of contingency? See Gould, "The promise of paleobiology as a nomothetic, evolutionary discipline." which an adaptation is the solution." Though Lewontin discusses several problems with the adaptationist philosophy, including the difficulty of attempting to define niches pre- or abiotically (such an exercise, Lewontin cautions, would trap one into counting an infinite number of arbitrarily defined niches), he concludes that

Adaptation is a real phenomenon. It is no accident that fish have fins, that seals and whales have flippers and flukes, that penguins have paddles and that even sea snakes have become laterally flattened. The problem of locomotion in an aquatic environment is a real problem that has been solved by many totally unrelated evolutionary lines in much the same way.261

This is the sort of model Conway Morris seems to have in mind: a world in which the same challenges would continue to be posed no matter how many times the tape was re-played, and in which the same biological properties would arise again and again, during each repeat of the tape of life. Conway Morris gives literally hundreds of examples of such convergences in Life's Solution. One example illustrates how C4 photosynthesis, an alternative to the usual method of C3 photosynthesis which minimizes the wasteful process of photorespiration, has evolved convergently as many as forty-five times in various plant families, including two independent origins in the genus Flaveria alone.262 This convergent acquisition of C4 photosynthesis involves the evolution of particular biochemical pathways as well as specialized anatomy to support them. It also requires mutation in twenty-one amino acid-producing codons. All C4 plants have acquired these specializations, and all use the same enzyme, RuBisCO, to catalyze the key reaction that makes C4 photosynthesis possible. The ubiquity of this particular solution to such common problems as aridity and

261 Richard C. Lewontin, "Adaptation," Scientific American vol. 239, no. 3 (September 1978), 213,230. 262 Athena D. McKown, Jean-Marc Moncalvo, and Nancy G. Dengler. "Phytogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution." American Journal of Botany vol. 92, no. 11 (2005), 1911. 263 Pascal-Antoine Christin, Nicolas Salamin, Vincent Savolainen, Melvin R. Duvall, and Guillaume Besnard, "C4 photosynthesis evolved in grasses via parallel adaptive genetic changes." Current Biology, vol 17„ no. 14 (17 Jury 2007), 1241. 165 salinity strongly suggests that it might be one of what Conway Morris calls "evolutionary inevitabilities" - the only good solution to a problem that has occurred repeatedly in the history of life.264

This idea of "evolutionary inevitabilities," or universal biological properties which can be defined independently from the organisms that possess them, is a crucial component of Conway Morris's evolutionary theory. The question Conway Morris asked in response to

Gould's contingency claim was: If the groups which today possess the biological properties we observe had not themselves evolved, would these biological properties still now exist, in whatever other groups evolved instead? For Conway Morris, the answer to this question is yes, and this explains the ubiquity of convergence: if a particular group failed to evolve, another group with an analogous body plan would in all likelihood take its place. That body plan, or that collection of biological properties, would almost certainly arise at some point, because it (for Conway Morris) is the best solution to the problems posed by the environment in question.

On Gould's view of evolution, by contrast, convergence occurs, but its influence in directing the course of evolution is miniscule compared to the operation of contingency. For

Gould, selection and adaptation are important factors in evolution, but they are not the most important things going on. Before biological forms can be selected, they must exist in the first place - and Gould argued that the list of biological forms that would actually arise and survive was heavily constrained by highly contingent circumstances that obtained principally in the early history of life. What are these contingent constraints of Gould, and how are they different from the environmental constraints Conway Morris sees at work in evolution? As I will show in the next section, a useful way to explore the differences between Gould and

264 Conway Morris, Life's Solution, 293-294. 166

Conway Morris is to examine each man's use of a common heuristic in biology: a global model of actual and possible biological form.

Creating the Playing Field: Adaptive Landscapes and Theoretical Morphospaces

Both Gould and Conway Morris have used the metaphors of adaptive landscapes and theoretical morphospaces to illustrate their respective theories. A good way to tease out the precise differences in their beliefs about the tempo and mode of evolution is to examine how the two men use these visual metaphors. In this section I will define adaptive landscapes and morphospace models, and discuss how they are used and understood by Gould and Conway

Morris. Gould and Conway Morris each have a precise and very different understanding of these models, and their differences here are highly informative of their disagreement over the

Burgess Shale,

The concepts of the adaptive landscape, and later, the theoretical morphospace, were introduced and refined in the mid-twentieth century. The concept of a fitness landscape (the precursor of the adaptive landscape) was first introduced by Sewall Wright in 1932,265 providing what has been called "the most influential visual heuristic in evolutionary biology." Wright drew a "diagrammatic representation of the field of gene combinations in two dimensions instead of many thousands," in which "dotted lines represent contours with respect to adaptiveness." The peaks represent areas of increased adaptiveness, while valleys are areas of decreased adaptiveness. Thus Wright's original fitness landscape (which he called "the entire field of possible gene combinations") was a visual summary of the

265 Sewall Wright, "The roles of mutation, inbreeding, crossbreeding and selection in evolution," Proceedings of the Sixth International Congress of Genetics, vol. 1 (1932): 356-366. 266 Robert A. Skipper, Jr., "The Heuristic Role of Sewall Wright's 1932 Adaptive Landscape Diagram," Philosophy of Science vol. 71, no. 5, Proceedings of the 2002 Biennial Meeting of the Philosophy of Science Association. Part II: Symposia Papers (December 2004), 1176. 167 genetic characteristics and variability of a particular species.267 The shape of the contours, the heights of the peaks, and the very existence of the landscape itself depend on the existence and genetic makeup of the species for which the fitness landscape is a visual representation. Wright's fitness landscape does not have an independent reality, separate from its potential or actual occupation, but exists only in terms of the species it models. The landscape is created by collating and plotting the actual distributions of gene frequencies within the species in question, and the size and shape of particular peaks can be altered, if the species acquires novel genetic mutations.

The adaptive landscape, first proposed by the paleontologist George Gaylord

Simpson in his 1944 book Tempo and Mode in Evolution, is superficially similar to the fitness landscape: they both use the geometry of a contoured landscape as a visual metaphor, and in both cases the vertical dimension represents adaptiveness.268 But where the horizontal axis of Wright's model is intended to represent the fitness ratios of particular allele frequencies in a given species, the same axis on Simpson's model represents phenotypic variation within a population or species. This means that the Wrightian fitness landscape illustrates population-level properties: any point on the surface of the Wrightian landscape expresses a relation between n gene frequencies (for an n-dimensional landscape). The

Simpsonian adaptive landscape, by contrast, illustrates properties of individuals: any point on the surface of the Simpsonian landscape can be seen as an individual organism within a population, with its individual combination of phenotypic characters. As Simpson described his model: "The field of possible structural variation is pictured as a landscape with hills and valleys, and the extent and directions of variation in a population can be represented by

267 Wright, 357,358. 268 George G. Simpson, Tempo and Mode in Evolution, (New York: Columbia University Press, 1944). 168

outlining an area and a shape on the field."269 A crucial difference, then, is that a point on the surface of a Wrightian fitness landscape represents a population, whereas a point on the

surface of a Simpsonian adaptive landscape represents an individual.

Another difference is that while Wright used his model to explore adaptive and non- adaptive genetic changes within a single species, Simpson used his model to explore the creation of new higher taxa by jumping from one adaptive peak to another. This "quantum evolution," as Simpson named it, involved away fromon e adaptive peak into a valley, followed by a rapid burst of adaptive evolution propelling the new taxon onto a different peak. It is easy to see how quantum evolution might appeal to Gould, the co- founder of punctuated equilibrium. Like Gould's punctuated equilibrium, Simpson's quantum evolution is not simply a scaled-up version of the slow accumulation of adaptive genetic changes, entirely controlled by natural selection acting at the level of individuals. In quantum evolution, the initial shift away from the first peak is caused by drift, and is actually a maladaptive step; on Gould's theory, selection can occur at the species level or higher. In analysing Gould's writings about the Burgess Shale, it also becomes apparent that he has followed Simpson in equating individual adaptive peaks with different higher taxa.

The last concept, the theoretical morphospace, was introduced by invertebrate paleontologist David Raup in 1966. As Raup described his approach, "a conceptual or mathematical model is established for some aspect of morphology. The model in turn is used to formulate or describe the total spectrum of physically possible forms. This spectrum then serves as a frameworkthroug h which actually occurring forms may be interpreted."270 The most fundamental difference between a theoretical morphospace and an adaptive landscape is

269 Simpson, 89. 270 David M. Raup, "Geometric analysis of shell coiling: general problems," Journal of Paleontology vol. 40, no. 5 (September 1966), 1178. that the theoretical morphospace does not display adaptiveness on any of its axes, whereas

the vertical dimension in the adaptive landscape is an indicator of adaptiveness, as previously

discussed. This is not to say, however, that morphospace models have nothing at all to say

about adaptation. For example, since it is possible to construct a theoretical morphospace of

hypothetical as well as actual forms, one might use ideas about adaptation to analyze the

hypothetical forms and explain why they remain unrealized. Further, since both the

Simpsonian adaptive landscape and the theoretical morphospace map the distribution of

phenotypes, one could argue that an adaptive landscape model is a theoretical morphospace

with an added adaptive dimension.

As originally conceived by Simpson and Raup, both the adaptive landscape and the

theoretical morphospace are local models; in other words, the typical adaptive landscape or morphospace depicts "a particular species... viewed only in the immediate vicinity of its phenotypic mean."271 In their 2001 article "The adaptive landscape as a conceptual bridge between micro- and macroevolution," however, Arnold et al. point out that instead of this

local view, a "global view dominates popular discussions."272 One such global view is

illustrated by Daniel C. Dennett's Design Space, a "vast multidimensional space" containing

all conceivable biological form, past, present, and future; actual (extinct or extant) and merely possible.273 Dennett wrote, for example,

[F]or the last four billion years or so, the Tree of Life has been zigzagging through this Vast multidimensional space, branching and blooming with

Stevan J. Arnold, Michael E. Pfrender, and Adam G. Jones, '"Hie adaptive landscape as a conceptual bridge between micro- and macro-evolution," Genetica vol. 112-113 (2001), 23. 272 Arnold et al., "The adaptive landscape as a conceptual bridge," 23. 273 Dennett, 135-144. In feet,Dennet t intends his Design Space to contain not just all biological design, but all human design as well (e.g. architecture, music, literature), which he sees as a subset of biological design, humans being products of evolution (144). This point may be debatable, but in any case, I concern myself here only with the modeling of biological form. virtually unimaginable fecundity, but nevertheless only managing to fill a Vanishingly small portion of that space of the Possible with Actual designs.274 Another example of a global spatial model of biological form can be found in the central image of Richard Dawkins's Climbing Mount Improbable. For Dawkins, Mount

Improbable is a metaphorical mountain whose individual peaks represent biological designs of seemingly inexplicable perfection, like wings and eyes. From one side, the mountain appears impossibly steep and high, inspiring (Dawkins suggests) the incorrect assumption made by many people that the perfection at the peaks can only be attained by divine creation, since the mountain cannot be climbed. If one looks around the other side of the mountain, however, one discovers a gradual slope, which can be climbed by the slow agency of natural selection, all the way to the highest peaks.275 Mount Improbable is an example of a global morphospace model in which all biological form is represented, and evaluated (or at least distributed) according to some metric represented by the vertical dimension of the model.

Both Gould and Conway Morris have employed, at one time or another, similar global models of biological form and its adaptiveness. Gould has referred to both

"morphospace" and "adaptive landscape" in his writing, but in both instances clearly means to include in his model several animal phyla, if not all biological form, as well as an adaptive dimension. Conway Morris tends to use the terms "morphospace" or "biological hyperspace" in his discussions, but, like Gould, also extends his model to include the realm of all biological form, and (arguably) an adaptive dimension. It has become commonly accepted to use the term "morphospace" to refer to any such global model, and in general I

274 Dennett, 143. 275 Richard Dawkins, Climbing Mount Improbable (New York and London: W.W. Norton & Company, 1996), 77-107. 171 shall follow that convention here. It is my aim to prove, in the remainder of this chapter, that these two men disagree about not just the occupation and navigation of morphospace by organisms, but about the nature of morphospace itself. As I will show, this disagreement has deep implications for their respective views of the nature and significance of the Burgess

Shale fauna, and of the operation of evolution itself.

Gould vs. Conway Morris: Morphospace Modeling and Landscape Exploration

In WonderJUl Life, as an example in support of his argument that the Cambrian explosion produced an incredible burst of morphological (and therefore taxonomic) disparity which was then randomly decimated, leaving only - by chance - the ancestors of the modern crown groups, Gould presents a global adaptive landscape model. It is worth quoting at length:

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. Now we ask, How often does a large jump yield a successful outcome (a new body plan)? [Stuart] Kauffman proves that the probability of success is quite high at first, but drops precipitously and soon reaches an effective zero - just like the history of life. This pattern matches our intuitions. The first few

James Maclaurin, "The good, the bad and the impossible," Review of Theoretical Morphology: The Concept and Its Applications by George R. McGhee, Jr. (New York: Columbia University Press, 1999) Biology and Philosophy vol. 18 (2003), 465. 172

species are placed on the landscape at random. This means that on average, half the peaks are higher, half lower, than the initial homes. Therefore, the first long jump has a roughly 50 percent chance of success. But now the triumphant species stands on a higher peak - and the percentage of still loftier peaks has decreased. After a few successful jumps, not many higher peaks remain unoccupied, and the probability of being able to move at all drops precipitously. In fact, if long jumps occur fairly often, all the high peaks will be occupied pretty early in the game, and no one has anyplace to go. So the victors dig in and evolve developmental systems so tied to their peaks that they couldn't change even if the opportunity arose later. Thereafter, all they can do is hang tough on their peak or die. It's a difficult world, and many meet the latter fate, not because ecology is a Darwinian log packed tight with wedges, but because even random leave spaces now inaccessible 277

to everyone.

There are several things to note about Gould's use of this metaphor. First, he

distinguishes two kinds of jumps: small and large. These two kinds of jumps seem to be

qualitatively, not just quantitatively, different, for a large jump produces an entirely new

body plan, while a small jump does not. Second, Gould believes that "a// the high peaks will

be occupied pretty early in the game" (emphasis added). In Gould's model, then, all possible

body plans in morphospace will be achieved by real groups of organisms, and this will take

place early in the history of life. Third, while the ability of organisms to make large jumps to

higher peaks (and therefore different body plans) is hampered initially only by the finite

number of peaks and the resultant statistics embedded in the model (after only a couple of jumps from a random starting point, there are simply very few higher peaks left), there comes

a point when the inherent ability of organisms to even attempt these large jumps is lost. The

ability to make large jumps is lost as each group "evolves developmental systems so tied to

their peaks that they couldn't change even if the opportunity arose later." This means that

although all high peaks are initially occupied (at the time of maximum disparity), not all of

these peaks will remain occupied throughout the history of life; some groups will go extinct

Gould, Wonderful Life, 232. 173 and others - due to developmental entrenchment - will be unable to colonize the empty peaks. Thus extinctions "leave spaces now inaccessible to everyone." Gould argued that evolutionary trees on various scales display this initial disparity and subsequent restriction, and explained,

I like to think of it as 'early experimentation and later standardization.' Major lineages seem able to generate remarkable disparity of anatomical design at the outset of their history - early experimentation. Few of these designs survive an initial decimation, and later diversification occurs only within the restricted anatomical boundaries of these survivors - later standardization.278

If, as Gould believes, all possible body plans are realized very early in the history of life, if later evolution cannot ever again produce changes as large as these jumps to new body plans, and if there is indeed a random decimation of initially vast anatomical possibilities to an impoverished handful of restricted anatomies, then the survival of the particular body plans that would come to characterize our modern fauna would indeed be highly contingent.

If our thirty or thirty-five modern phyla are the randomly chosen survivors of an initial set of fifty phyla, then who is to say a replay of the tape of life from the fifty-phylum point wouldn't see different body plans survive, and different peaks left empty?

The developmental entrenchment which (after a certain time) prevents phyla from making large jumps to different peaks/body plans is a major linchpin in Gould's contingency argument, as is his belief that lineages can and do achieve maximum morphological disparity only very early in the history of life. The science of evo-devo was in its infancy when Gould wrote Wonderful Life, and he did not go into detail then about these restrictive developmental systems, but he greatly expanded on this idea in his grand opus The Structure of Evolutionary

Theory.119 Beginning in the 1980s, evolutionary developmental biologists have discovered a

Gould, Wonderful Life, 304. Gould, The Structure of Evolutionary Theory, 1025-1295. 174 basic genetic "toolkit," the homeobox, which is a highly conserved sequence of genes that control fundamental aspects of animal development, such as the formation of the antero­ posterior and dorso-ventral body axes, segmentation, and the formation, location, and nature of limbs. The same toolkit (with some variations) is found in all the bilaterian animal phyla, suggesting that it evolved in their common ancestor and has been retained ever since. Gould thought the highly conserved homeobox is one more example of an evolutionary contingency

(the animals in this play of life's tape share this particular developmental toolkit; maybe they would share a completely different toolkit of genes if the tape were replayed.)280 For

Conway Morris, by contrast, the homeobox is evidence in support of adaptation and large- scale convergence (animals share this toolkit because it is highly adaptive; and the reason different animal phyla can converge on the same successful designs is that they all have the right "tools" to do so).281 I shall return to the subject of evolutionary developmental biology

(evo-devo) and the homeobox in Chapter 5.

The important things to note here are that Gould believes that maximum disparity is reached early in the history of life; that this initial disparity reflects a colonization of the entirety of physically "occupiable" morphospace (remember, all peaks are occupied); that this initial period is rapidly followed by a time in the history of evolution when several body plans become extinct and new body plans cannot arise, and that all subsequent diversification must thereafter take place within the limited number body plans which remain (i.e., on existing peaks, with no further jumps to new or abandoned peaks). This idea of developmental entrenchment restricting the later evolution of different body plans is a crucial point to note, for it is a major theme in Gould's system, yet completely absent from Conway

Gould, The Structure of Evolutionary Theory, 1159. Conway Morris, Interview 31 July 2007. Morris's model. The part of Gould's evolutionary theory that is truly contingent is the vagaries of extinction. But in order for extinction to leave gaps that cannot be filled by other groups, Gould's theory requires something else: a property of organisms that prevents one body plan fromconvergin g on the form of another. This property is developmental entrenchment, or the "congealing" of body plans, in Gould's words.282 On Conway Morris's theory of evolution, extinctions may be no less contingent, but their contingency does not matter, because he believes other groups can and will occupy the peaks abandoned by extinction. Gould did not agree. This is what truly distinguishes their theories of evolution: are organisms constrained, and if so, how much, and by what? We will now turn to Conway

Morris's views.

Conway Morris also employs the metaphor of a global morphospace, but as we shall see, his is very different from Gould's. In his 1998 book The Crucible of Creation, Conway

Morris refers to "the morphological 'universe' occupied by animals," or "their morphospace." Within this animal morphospace, Conway Morris envisions several clumps or clouds. The largest clouds correspond to the different animal phyla, and within each phylum cloud there are smaller clouds of classes, and so on down the phylogenetic ladder.

Morphospace, therefore, "is decidedly clumped at a variety of scales."283 In other words, organisms are not distributed evenly throughout morphospace - as one might be led to expect from Darwin's Principle of Divergence and evolution by gradual and almost imperceptible changes. Instead, some regions of morphospace contain clumps or clusters of many animal species, whereas other regions of morphospace do not correspond to any real animal species

282 For example: "if- as I claim for me Burgess and later history of arthropods, and for life in general, Bauplane congeal and stabilize," (Gould, "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis," 419), "early congealed designs," and "all major variants... had already congealed by the end of the Cambrian explosion," (Gould, The Structure of Evolutionary Theory, 1159,1161). 283 Conway Morris, The Crucible of Creation, 169. at all. Biologists and paleontologists of the late 20 and early 21 centuries are generally agreed that the answers to why organisms are clumped in morphospace, and why some regions of morphospace are occupied versus empty, would be very important clues to understanding biological form and evolution.284 As we shall see, Conway Morris and Gould have very different answers to these questions.

For Conway Morris, the distribution of organisms in morphospace is rather like the distribution of stars in the night sky. Some of the many millions of stars are off by themselves, but the vast majority are grouped into clusters, and smaller clusters within those clusters. In biological terms, the individual dots are species, and the clusters are body plans, at various taxonomic levels - families within orders, orders within classes, and classes within the largest clusters of all: phyla. And, as in the night sky, the "stars" in morphospace are dwarfed by the vastness of the empty space which surrounds them. Conway Morris explains:

It's a very imperfect analogy, but if you think of hypothetical morphospace, which is multi-dimensional, there's a big cloud which is called arthropods. And somewhere else there's a cloud called molluscs. And if you look into that cloud [of arthropods] you'll find, actually, there are a set of smaller clouds, which would be, say, insects and crustaceans. And if you look in the insects, you'll find that even within that cloud, when you look more closely actually it's clustered. And the question of course, which is my other interest, is the extent to which, if you were to re-run the tape, the extent to which the clouds would be there at all. First of all, why are things clumped? Some people say it's phylogenetic burden, you have to carry all your history with you. I don't think there's much truth in that frankly, myself. But more particularly if you look in the arthropods, if you were to re-run the tape would you end up with an insect cloud? I think you would... My present sense is that the fact of the matter is not that most things do work, it's that almost nothing works.285

Conway Morris tends to be less explicit than Gould about discussing visual representations of adaptiveness within his morphospace model; note there is no mention of

284 See for example Gould, "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis," 422, and Maclaurin, "The good, the bad and the impossible," 470-471. 285 Conway Morris, Interview 31 July 2007. 177 peaks and valleys in Conway Morris's description of clusters in morphospace. In a sense, however, one can assume that any cluster in Conway Morris's global morphospace corresponds to an adaptive peak, because for Conway Morris, occupation of a particular region of morphospace is synonymous with possession of adaptive morphology. Occupied regions of morphospace are occupied because they represent good solutions to design problems. Those regions of morphospace that are unoccupied are empty because they do not represent good solutions. Therefore, occupied morphospace is inherently adaptive; no peak is required. Conway Morris explained:

And the argument generally, of course, as Gould was rambling on about, was that of course it's accidental that you ended up in these areas [of morphospace]. And I think that's awfully wrong. I think the evidence goes completely in the other direction now. These [occupied regions] are very stable points, and that's why they're repeatedly occupied.2

As we saw above, contingency is an extremely pervasive and powerful phenomenon in Gould's model. Gould would say that morphospace gets its shape from the organisms that inhabit it, and that as organisms evolve, morphospace changes too. As organisms develop particular features, new adaptive peaks - representing the optimization of those features - open up in morphospace. In Gould's model, organisms don't just occupy morphospace, they create it, or at least create its shape as they evolve. Peaks arise according to the evolutionary potential of groups of organisms. Of those parts of morphospace that are filled, Gould would say they are filled because of the contingencies of development. Of those parts that are not filled, Gould would say they are empty because life cannot get to them. For Gould, those regions of morphospace that are not occupied are unoccupied by chance: it is chance that the colonists of some regions of morphospace survived, while those that would have occupied other regions, now empty, perished.

286 Conway Morris, Interview 10 January 2007. Conway Morns believes the opposite: no matter which particular lineages go extinct in the Cambrian and which survive, given life, life can and will navigate repeatedly towards particular regions of morphospace - those which represent good solutions to adaptive problems. For Conway Morris, morphospace gets its shape - i.e., the topography of the peaks and valleys - from the physicochemical and biological laws and principles that were inherent in our world from its conception. The physical world has certain characteristics which impose certain constraints on any life that might arise. These constraints alone dictate the shape of morphospace - the delineation of regions that can and cannot be occupied - and the nature of the environmental problems which will challenge any and all life that arises.

For Conway Morris, the contours of morphospace are prior to and independent of the organisms that come to inhabit the space. These contours would remain the same even if the tape of life were re-played; whatever forms arise, they will have to face the same challenges proposed by the same physical laws of our universe. Those parts of morphospace that are filled are therefore those that represent good adaptive solutions to these universal problems - what Dennett calls "good tricks in Design Space."287 Those parts of morphospace that are not filled are empty because life cannot live in them; they represent poor solutions to the universal design problems - designs that would not function well and therefore do not occur in nature, either because they are immediately lethal or because they would be heavily selected against.

This disagreement highlights a crucial difference in the nature of Gould's morphospace model versus Conway Morris's: it means that the regions of morphospace that are in principle occupiable are much more restricted for Conway Morris than for Gould. In

Conway Morris's model, there are only a very few regions of morphospace that represent

287 Dennett, 307. good biological designs, and these regions will be converged upon repeatedly by groups of

varied phylogenetic relations and histories. Conway Morris explains:

The ubiquity of evolutionary convergence suggests, however, that the vast bulk (maybe > 99%) of any biological 'hyperspace' is actually 'uninhabitable' and maladaptive. It also suggests that any such 'hyperspace' is largely defined by narrow 'roads' of potentiality, and that in some sense these are embedded at very deep levels indeed. It is along these roads that life navigates towards certain inevitable solutions.288

For Gould, each adaptive peak represents a distinct body plan, always and forever tied to the phylum that possesses it. Squatters' rights are everything in the Gouldian

landscape. If that phylum succumbs to extinction, that peak remains closed - it will never be

colonized by any other group. Gould insisted that "The modern order was not guaranteed by

basic laws (natural selection, mechanical superiority in anatomical design), or even by lower-

level generalities of ecology or evolutionary theory. The modern order is largely a product of

contingency."289

Conway Morris takes a different view of peak-jumping, which allows him to give an

extremely large role to the operation of convergence in his vision of evolution. For Conway

Morris, those regions of morphospace that contain physically possible morphologies are

narrowly delimited, compared to other (and vaster) regions of morphospace that one might

conceive of in one's imagination, but that could never even in principle be occupied, because

such occupation would require the breaking of fundamental laws of nature. Within this

already-restricted region of the merely possible, according to Conway Morris, the region of

probable morphologies - in other words, those that are not just possible but are good

solutions to adaptive problems - is much narrower still. Yet there is a freedom in Conway

288 Simon Conway Morris, "The navigation of biological hyperspace," InternationalJournal ofAstrobiology vol. 2, no. 2 (2003), 152. 289 Gould, Wonderful Life, 288. Morris's narrower adaptive landscape that does not exist in Gould's vaster one, for on

Conway Morris's system, unrelated groups can navigate towards and successively occupy the same adaptive peaks. This freedom of movement is forbidden in Gould's system, after a relatively brief initial period of lability, as body plans congeal or stabilize (more on this below). Each adaptive peak represents a biological property, or set of biological properties, that constitutes a good way to live. In contrast to Gould's emphasis on the sheer size and virtually limitless possibilities of morphospace, Conway Morris pictured instead a finite number of occupied (and occupiable) morphological zones, corresponding to "points of relative stability."290 If these stable points or good design solutions are really so rare, and if selection and adaptation are as strong and constraint of form so weak as Conway Morris believes, then life will navigate toward these few arbitrary peaks over and over again, regardless of phylogeny. Dennett agreed: [W]hen you do rerun the tape of life, you find all sorts of evidence of repetition. We already knew that, of course, because is nature's own way of replaying the tape.... [E]ven if the decimation of the Burgess Shale fauna were random, whatever lineages happened to survive would, according to standard neo-Darwinian theory, proceed to grope towards the Good Tricks in Design Space.291

For Conway Morris, there is a sense in which the topography of the adaptive landscape is decoupled from the organisms which occupy and navigate it. A particular adaptive peak, P, might be occupied by Species X at time 1, but if Species X goes extinct, that same peak P may subsequently be colonized by Species Y. Thus P is not solely created nor defined by X, and its existence is not circumscribed by its association with X. An adaptive peak for Conway Morris is not primarily the location of a particular species, then

(though a species may indeed be located there), but rather the locus of a suite of adaptive

290 Conway Morris, The Crucible of Creation, 215. 291 Dennett 306-307. 181 features - a "way of life." This is similar to the relationship between me as an individual, and the address of the building in which I live. 60 Harbord Street is my address, but it is only mine because I happen to live there. I did not cause the building at this particular location in the city of Toronto to be built, and the building at 60 Harbord Street will continue to exist - and will continue to occupy the address known as 60 Harbord Street - even if I stop living there. If I move out, someone else may move in to this same building, and 60 Harbord Street will become their address instead of mine.

Paleobiologist George McGhee, in his book The Geometry of Evolution, provides a similar description of a universal adaptive landscape, and also illustrates its relationship to evolutionary convergence:

The phenomenon of convergent evolution means that there are a limited number of ways of making a living in nature, a limited number of ways of functioning well in any particular environment. We can model this reality in an adaptive landscape by specifying the location of adaptive peaks for particular ways of life: the adaptive peak for an ocean-dwelling active- swimming animal is located in the streamlined fusiform morphological region of the landscape. No matter where you begin your journey on the landscape, if you evolve to be an active-swimming oceanic animal you will wind up in the same region of the landscape; that is, you will converge on the same morphological solution, the same adaptive peak.292

From this quotation we can see why Conway Morris would - indeed must - define morphospace in this way, with individual adaptive peaks as addresses of biological properties rather than as locations of particular species: in a model of evolution as heavily dependent on convergence as Conway Morris's, any morphospace model must be able to show different groups converging on the same place. This can only be accomplished by defining adaptive peaks as places - places that can be occupied by different (indeed, multiple) groups.

292 McGhee, The Geometry of Evolution: Adaptive Landscapes and Theoretical Morphospaces (Cambridge: Cambridge University Press, 2007), 34. 182

Conway Morris sees an adaptive peak, or any particular location in morphospace, as the address of a particular set of what he calls "biological properties."

This can be contrasted with Gould's criticism of global adaptive landscapes and morphospace models, articulated most explicitly in his review of Dawkins's Climbing Mount

Improbable:

All professional evolutionists understand the fallacy in trying to understand the differential occupation of organic morphospace as an adaptive mapping to a preexisting external landscape. We can all articulate the central error of such a perspective: since organisms help to create their own environments, adaptive peaks are built by interaction and undergo complex shifts as populations move in morphospace; organisms cannot climb stable mountains of an engineer's fancyf93

For Gould, the topography of morphospace is created by organisms themselves. At first, early in the history of life, morphospace is relatively flat. Peaks become peaks because organisms evolve efficient and reliable ways of producing the phenotypes that occupy them.

Valleys occur where the developmental systems that lineages evolve prevent them from viably producing the phenotypes required to occupy those zones. Further, only organisms that have inherited the same developmental systems (i.e., only members of the same phylum) can ever truly occupy the same peak. Gould's morphospace model has interesting implications for convergence, then: different lineages (phyla or body plans) cannot converge on the same peak, and "convergence" within a lineage isn't really convergence (in the sense of independent discoveries of the same adaptive solution by different groups), it is a reflection of the use of developmental tools possessed by all members of that lineage. In

Conway Morris's world, convergence is everywhere; there is very little place for it at all in

Gould's world.

293 Stephen J. Gould, "Self-help for a hedgehog stuck on a molehill," Review of Climbing Mount Improbable by Richard Dawkins, Evolution vol. 51, no. 3 (June 1997), 1022. 183

As we have seen, this debate is underpinned by the question of exactly how (and how much) organisms occupy morphospace. Both Gould and Conway Morris might agree that morphospace itself is infinite or virtually so, but they appear to disagree on how much of this space organisms might realistically occupy. For Gould, the potential of organisms to occupy morphospace is also virtually infinite - with one caveat: while virtually any region of morphospace might in theory be occupied by some lineage of organisms, a particular lineage of organisms can only occupy a particular (and narrowly delimited) region of morphospace

(contra Conway Morris, who sees lineages traversing different regions of morphospace much more freely). For Gould, the number of lineages (phyla, or body plans) determines the amount of morphospace that will be occupied. Thus, the actual occupation of this space has been constrained by the historical accidents of random extinction acting upon initially limitless genetic possibilities. Gould seemed to envision vast areas of morphological potential that have not been realized in actual organisms, not because these areas represent morphologies that are unfit or physically unlikely, but because organisms with the potential to develop these morphologies were randomly extirpated early in life's history, and it is now too late for other groups to evolve into these areas.

For Conway Morris, by contrast, the range of morphospace organisms are seen to occupy is not much smaller or much different from the range they could ever occupy even in theory, because of all the infinite possibilities of theoretical morphospace, only a finite number will realistically occur. This is because mere are only so many physically and ecologically possible niches, and for each of these, there are only a few ways to live successfully in them. Competition and other selection pressures will ensure that organisms navigate towards these optimum solutions, often from widely disparate phylogenetic backgrounds.

As Pere Alberch asked in 1982: If we plot the distribution of organisms in morphospace, we see that they occur in clusters, where each cluster is a distinct morphotype

- perhaps a variety or species - and there is empty space between the clusters. Why is the empty space empty? He proposed two opposing explanations: "a) empty spaces represent nonadaptive forms that have been eliminated by natural selection", or "b) they are a reflection of the developmental constraints operating on the system, i.e., there are morphologies that cannot be produced by the developmental program."294 For Conway

Morris, the answer is a. A third possibility (which Alberch does not mention) is one favoured by Gould: c) empty regions of morphospace might be empty by chance. I turn now to a discussion of these opposing explanations, which will illuminate the real issues at stake in the Gould-Conway Morris debate - issues which have deep implications for the interpretation of the Burgess Shale and the understanding of evolution itself.

Internalism vs. Externalism: Different Kinds of Constraint

The above comparison shows that Gould and Conway Morris saw very different kinds of constraint at work in evolution. A constraint is any factor that limits or circumscribes the morphology or form mat organisms can take. The causes of form have not received much attention in the past 150 years, as ever since Darwin biologists have tended to think only in terms of adaptive forces acting on organisms rather than in terms of form being constrained by non-adaptive forces (by which I do not mean maladaptive forces, but merely

294 Pere Alberch, "Developmental constraints in evolutionary processes," in Evolution and Development, J. T. Bonner, ed., 313-332 (New York: Springer-Verlag, 1982), 317. 185 forces not having directly to do with adaptation). According to philosopher of biology Ron

Amundson, it is only since the rise of evolutionary developmental biology, or evo-devo, in the 1980s and especially the 1990s that the understanding of form (not design or adaptation, but form) has again been seen as an explanatory goal of evolution.295 (A more detailed discussion of evo-devo, and the investigation of form, can be found in Chapter 5.)

Several authors have attempted to categorize the different possible kinds of evolutionary constraint. For example, Amundson (1998) distinguishes between constraints

2% on adaptation ("constraintSA") and constraints on form ("constraintsF"). Traditionally, among evolutionary biologists who have recognized selection as the primary force in evolution, the word "constraint" has usually meant constraints on adaptation. That is to say, if one imagines the optimal morphology an organism should possess when faced with particular environmental challenges, any failure of the actual organism to live up to this ideal morphology has typically been explained using the notion of constraint. Some other adaptive consideration, namely the necessity of optimizing other parts of the creature's anatomy, has acted to constrain the feature in question fromrealizin g its optimal state. Bergmann's Rule provides an example: large body size is adaptive in cold climates, because larger objects have a lower surface area-to- volume ratio than smaller objects of the same proportions, thus losing heat less rapidly. One would therefore expect mammals in colder climates to be larger than their warm-weather counterparts. Other adaptive considerations might limit body size, however: island inhabitants tend to be larger than their mainland counterparts due to

295 Ron Amundson, The Changing Role of the Embryo in Evolutionary Thought: Roots ofEvo-Devo Cambridge Studies in Philosophy and Biology (Cambridge: Cambridge University Press, 2005), 108. 296 Ron Amundson, "Two concepts of constraint: adaptationism and the challenge fromdevelopmenta l biology," in The Philosophy of Biology, David L. Hull and Michael Ruse, eds., 89-116 (Oxford: Oxford University Press, 1998). 186

minimized competition.297 Therefore, despite the predictor about heat loss in warm versus

cold climates, the bears on the warm mainland might be larger than their counterparts on a

cold island. Amundson acknowledges this notion of adaptive constraint, but introduces the

distinct notion of constraint on form: the development of an organism is also constrained, not

because of adaptive selection, but because the ontogeny of an organism is necessarily a

process which has to operate according to physicochemical laws, using present materials, and yielding at every stage a functioning organism. The exigencies of the physical environment,

and the contingencies of starting materials and basic processes, constrain the form that the

organism can take, in a way that is not directly related to adaptiveness.

Though I think it is possible to apply Amundson's dichotomy to Gould and Conway

Morris, these categories do not map well onto the views of these two men. The problem is

that Amundson is not, in the end, concerned with the immediate causes of his two types of

constraint, only with the type of explanation (adaptive or formal) sought to explain the

constraint. Constraints on form might be caused by the nature of the physical environment as

well as by the phylogenetic history of the organism, for example. In contrast, Gould and

Conway Morris are deeply concerned with the causes of organic constraint, and each believes

that a different kind of constraint and its cause(s) is most important in shaping the history of

life on Earth.

In 1984, an important conference was held in Mountain Lake, Virginia, to discuss the

origin, nature, importance, and means of detection of developmental constraints and their

role in evolution. In their published summary of this conference, Maynard Smith and

colleagues defined a developmental constraint as "a bias on the production of variant

297 Mahoney et al, "Potential mechanisms of phenotypic divergence in body size between Newfoundland and mainland black bear populations," Canadian Journal of Zoology vol. 79 (2001), 1650. 187 phenotypes or a limitation on phenotypic variability caused by the structure, character, composition, or dynamics of the developmental system." They distinguished "universal" and

"local" constraints, where the former are "direct consequences of the laws of physics," operating on all organisms (indeed, on all matter) at all times, and the latter are "taxon- specific" and "arise in consequence of some particular feature of the organisms of those taxa."298 This distinction is more of a continuum than a dichotomy, for the authors point out that some local constraints are more universal than others, and that some universal constraints exist because they could not be otherwise, whereas others are only universal because they are now very difficult to alter, though things might have been different.

All of these constraints are here conceived as developmental, even those universal constraints resulting solely from the necessity of physical and chemical laws, presumably because these too, like the more local constraints, affect what can and cannot be produced in the development of an organism. Here again I do not think these definitions and distinctions are quite the right tools to bring to the Gould-Conway Morris debate, because while Gould is indeed concerned with developmental constraints, Conway Morris is concerned with something different.

I believe a more useful way to dichotomize their views is as follows: Gould is an evolutionary internalist, and Conway Morris is an evolutionary externalist. In other words,

Gould believes that the most important constraints which limit the form of organisms are those which are internal to organisms, whereas Conway Morris believes those which are external are more important. Philosopher of biology Peter Godfrey-Smith defines

298 John Maynard Smith, R. Burian, Stuart Kauffinan, Pere Alberch, J. Campbell, Brian Goodwin, R. Land, David Raup, and L. Wolpert, "Developmental constraints and evolution: a perspective fromth e Mountain Lake Conference on Development and Evolution," The Quarterly Review of Biology vol. 60, no. 3 (September 1985), 266-267. 188 externalism as "all explanations of properties of organic systems in terms of properties of their environments," while internalism uses "explanations of one set of organic properties in terms of other internal or intrinsic properties of the organic system."299 For Conway Morris, the most important factors in shaping evolution come from outside the organism: the environment constrains the evolution of life. There may be a vast number of genetic possibilities, but the pressures of the environment, both biological and physicochemical, only allow a finite set of basic solutions, and life will navigate to these solutions despite random extinctions of particular groups. As Conway Morris wrote in Life's Solution: "The

'landscape' of biological form, be it at the level of proteins, organisms, or social systems, may in principle be almost infinitely rich, but in reality the number of 'roads' through it may be much more restricted."300

For Gould, on the other hand, the most important factors in shaping evolution come from within the organism: any morphology possible within life's genetic and developmental array is initially permitted. However, once a lineage has become developmentally committed to its "chosen" body plan, large-scale changes cannot recur in that group. The reason that everyone can't keep colonizing new peaks has nothing to do with environmental pressures, on Gould's system, but is instead due to internal constraints.

A more detailed way in which one might divide these external and internal constraints is provided by McGhee. McGhee distinguishes four different kinds of evolutionary constraint: "geometric, functional, phylogenetic, and developmental. The first two constraints are extrinsic functions of the laws of physics and geometry, whereas the latter two constraints

299 Peter Godfrey-Smith, Complexity and the Function of Mind in Nature, Cambridge: Cambridge University Press, 1996), 30. 300 Conway Morris, Life's Solution, 11. 189 are intrinsic functions of the biology of specific organisms."301 An emphasis on McGhee's extrinsic constraints would overlap neatly with Conway Morris's externalist view, while a focus on McGhee's intrinsic constraints would highlight those factors that Gould believes are most important in directing the course of evolution.

McGhee's extrinsic constraints, geometric and functional, are relatively easy to grasp.

Geometric constraint divides geometrically possible from geometrically impossible forms.

An example of a geometrically impossible form would be a bivalved shell in which the two valves of the shell have overlapping whorls. (Figure 32) It is geometrically impossible to have two valves of a shell make a working hinge if the hinge surfaces are covered by bits of curled-over shell. For the hinge to work, the curled-over portions of shell would have to occupy the same space at the same time, and this is geometrically impossible.

Functional constraint is also easy to grasp intuitively: the separation of organic form into functional versus non-functional is (for McGhee) merely the separation of lethal and non-lethal biological forms. For example, the bryozoans, a group of colonial marine filter- feeding animals, are typically found in gently spiraling, helical colonies. While it is geometrically possible for bryozoans to grow in such tightly coiled spirals that the whorls of the helix are snugly nested and overlap extensively, this form is not functionally possible, because the physics of the arrangement would prevent water from flowing through the tightly overlapping layers, and the colony would be unable to extract sufficient nutrients from the water, therefore starving to death.302

McGhee, 109. McGhee, 91-93. 190

Figure 32. A Geometrically Impossible Shell It is not possible to construct a bivalved shell with a working hinge out of two valves with overlapping whorls (where one curl of the shell coils over the previous one). The overlapping means that the two halves of the hinge would have to occupy the same space at the same time, as the grey and black valves do here when put together - a geometric impossibility. Modified from McGhee, 78.

McGhee's two intrinsic constraints seem a bit harder to grasp than the extrinsic ones, or at least are harder to differentiate from each other. They have to do with different aspects of which biological forms can and cannot be achieved by organisms, beyond those constrained by geometry and the laws of physics. McGhee provides an analogy from computer programming to illustrate the difference: phylogenetic constraint has to do with whether the code (in this case, the genetic code) for running the desired program is available.

Developmental constraint, by contrast, asks if the particular "computer" (or developing organism, in this case) is capable of running the code without "crashing." In other words, phylogenetic constraints come into play when a group has lost (or never evolved) the genetic coding required to achieve a particular form, whereas in the case of developmental constraints, whether or not the genetic instructions are present in the group in question, 191 something about the particular process of its ontogeny will not let that group develop that form.

An example of developmental constraint, which is (I believe) the kind of intrinsic constraint Gould had in mind, might be illustrated by biologist Conrad Hal Waddington's concepts of canalization and the epigenetic landscape. Canalization, first proposed by

Waddington in the 1940s, "is the property of developmental pathways to produce standard phenotypes despite environmental or genetic influences that would otherwise disrupt development. It is the buffering of development against perturbations, whether of environmental or genetic origin." Waddington's epigenetic landscape is in turn a visual representation of the operation of canalization: "It represents the paths within a competent cell which allowed certain cell fates to be achieved more readily than others."303 Waddington

(1956) called it "a symbolic representation of the developmental potentialities of a genotype in terms of surface."304 Waddington's epigenetic landscape can explain both the stability and the mutability of phenotypes:3 5 a phenotype is stable because it is canalized; small perturbations, especially those farther "downstream," are channeled back into the expected outcome. But large perturbations, particularly those that occur early in development, can cause a deviation into a new and different channel. The epigenetic landscape model explains a lot of Gould's thinking: body plans become entrenched ("congealed") as developmental pathways become canalized. (Figure 33) The steep sides of the epigenetic channel represent

303 Brian K. Hall, "Waddington's legacy in development and evolution," American Zoologist, vol. 32, no. 1 (1992), 116. 304 Scott F. Gilbert, "Epigenetic landscaping: Waddington's use of cell fete bifurcation diagrams," Biology and Philosophy vol. 6 (1991), 141. 305 Denis Walsh, "Fit and diversity: explaining adaptive evolution," Philosophy of Science, vol. 70, no. 2 (April 2003), 292. Walsh credits Schwenk and Wagner, 2003, for the use of the terms 'stability' and 'mutability' in this context. (Kurt Schwenk and Gunter Wagner, "The relativism of constraints on phenotypic evolution," in Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes, Massimo Pigliucci and Katherine Preston, eds., 390-408 (Oxford: Oxford University Press, 2004).) 192

Figure 33. Waddington's Epigenetic Landscape Modified from Waddington, The Strategy of the Genes. the developmental constraints on form which Gould emphasizes. If large perturbations occur before the epigenetic channels become too deep, however, they can lead to large changes in form (jumps to new peaks in the adaptive landscape). Gould believed both that these channels were very significant features in evolution, and that a group's capacity to "cascade into a radically different channel" is great early on in its phylogenetic history, but that as developmental pathways are chosen and entrenched, the developmental channels become deeper, and detours into different channels become more and more difficult.

For Gould, then, "constraint" means developmental and phylogenetic constraint; a group is constrained by the particular developmental pathways that became canalized early in its history. Contingency is important precisely because virtually any path can be entrenched, but once a group has become entrenched in a particular developmental path, it can no longer deviate from this path. For Gould, re-playing the tape of life means going back to a time

Gould, Wonderful Life, 51. 193 before the developmental pathways of the respective major animal groups became entrenched. Before this time, major changes in morphological disparity, and the leap to new body plans, are possible. After this time, the regulatory and developmental pathways in each lineage have congealed and are no longer so extraordinarily labile. Evolutionary changes can still occur, but they will be minor variations on the entrenched theme of each lineage. If in the replay, different groups survived, different developmental pathways would become entrenched, while those that had led to our modern organisms might not get occupied, and would - on Gould's view - forever remain empty, inaccessible to those groups which did survive but became entrenched in developmental sequences of their own.

There is an important conceptual difference between intrinsic and extrinsic constraints which I believe is key in explaining Gould's and Conway Morris's different views on the proper use and definition of theoretical morphospace and adaptive landscape models. As McGhee explains,

Extrinsic constraints [=geometric and functional] exist whether any actual biological form encounters them or not. A separate class of constraint is that of intrinsic constraint, where intrinsic constraints [= phylogenetic and developmental constraints] are those imposed by the biology of a specific organism. Intrinsic constraints do not exist in the absence of an actual 307

organism.

Here again is another fundamental divide between Gould and Conway Morris: for Conway

Morris (as for McGhee), all organisms, whatever their phylogenetic heritage and historical legacy, encounter the same finite set of extrinsic constraints - these extrinsic constraints exist and are the same no matter what biological groups do or do not evolve. So if, like Conway

Morris, you believe that these extrinsic constraints are the most important in shaping evolution, you will expect a finite set of environmental problems for which evolution will

McGhee, 112. Emphasis in the original. 194 repeatedly, convergently, come up with a finite set of design solutions. But if, on the other hand, you believe with Gould that extrinsic constraints really constrain very little, and intrinsic constraints are vastly more important, then suddenly the products of five hundred million years of evolution become very contingently dependent on what did and did not evolve and survive five hundred million years before. And furthermore, on Gould's system, the complete set of external constraints would not be identical in every replay of life's tape, but would be created and shaped by the existence of particular lineages - the way niches are not merely holes that any species can be plugged into, but are created as much by their occupants as by their external environments. The reason any given evolutionary outcome is so unrepeatable is that, for Gould, the future possibilities of any group of organisms become locked in or congealed once that group has established its basic body plan. Wipe out that phylum, and the suite of future states potentially derivative from the body plan of that phylum now can never be attained. Gould wrote:

With so many Burgess possibilities of apparently equivalent anatomical promise [which did not survive] - over twenty arthropod designs later decimated to four survivors, perhaps fifteen or more unique anatomies available for recruitment as major branches, or phyla, of life's tree - our modern pattern of anatomical disparity is thrown into the lap of contingency. The modern order was not guaranteed by basic laws... or even by lower-level generalities of ecology or evolutionary theory. The modern order is largely a product of contingency.308

Conway Morris believes convergence is rampant, even between different phyla;

Gould does not believe that different phyla can converge on what is truly the same design.

And for Gould, the "discovery" of the same design by different groups within the same phylum is not convergence, even if it happens independently in the two groups; it is merely

Gould, Wonderful Life, 288. 195 both groups making use of the same parts of the deeply entrenched genetic "toolkit" that is shared by all members of that phylum (i.e., all possessors of their same body plan).

For Conway Morris, on the other hand, even leaving the question of mass extinction aside, not all things are possible, and in fact, only a very few are highly probable. Conway

Morris explained:

Rerun the tape of the history of life, as S. J. Gould would have us believe, and the end result will be an utterly different biosphere. Most notably there will be nothing like a human... Yet what we know of evolution suggest the exact reverse: convergence is ubiquitous and the constraints of life make the emergence of the various biological properties very probable, if not inevitable.309

As I hope the above discussion has shown, when Conway Morris speaks of constraint, he is concerned with the extrinsic challenges posed by the physical and ecological environment of the organism in question. On his view, organisms are constrained primarily by the design problems proposed by the world they face - and the same set of design problems would face any set of organisms, in any replay of life's tape. There are only a limited number of good solutions to these design problems, so different groups may convergently evolve towards these same good solutions. When Gould discusses constraint, by contrast, he is primarily concerned with the intrinsic phylogenetic and developmental constraints that restrict each group to a narrow range of morphological variance within the channels to which they have become committed. The environment may pose certain adaptive questions repeatedly, but for Gould, not all organisms can equally find the same solutions.

They start with different developmental tools, and each can only do so much with the tools it has been given.

Conway Morris, Life's Solution, 283-284. 196

Conclusion: Morphospace Models and the Burgess Shale

As we have seen, Gould and Conway Morris have very different ideas about the occupation, navigation, and indeed the very nature of morphospace. For Gould, evolution and development structure morphospace as they happen. For Conway Morris, morphospace is inherently structured. They also hold vastly different beliefs about the nature and significance of the Burgess Shale. What do the former tell us about the latter? Gould argued that if you wind the tape back far enough, you will get back to a place from which you could get anywhere in morphospace - and then when you go forward again, you will get to a very different anywhere this time than you did last time. Conway Morris responded that there are very few actually viable destinations in morphospace, so you (or at least somebody) will get there every time the tape is replayed. The contours of morphospace have been fixed since the beginning of the universe, when the fundamental laws of physics and chemistry were put in place, and these contours will not change no matter how many times the tape is rerun.

For Gould, the Burgess Shale represents a unique time in the history of life - "a time of unique flexibility, before definite patterns of growth from egg to adult became so locked into the embryology of complex organisms that fundamental reconstructions beeame nearly impossible." At this momentous time in history, on Gould's interpretation, the unique flexibility of early evolution had proposed many more animal body plans than have survived to today,311 In theory at least, if all these models of animal design had survived to the present day, then all the vast occupiable areas of animal morphospace might have been filled.

However, what evolution proposed, random extinction then disposed: of Gould's twenty-four arthropod classes, only four made it past the Cambrian; of his fifty-five animal phyla, only

Gould, "Showdown on the Burgess Shale: the reply," 52. 1 Gould, Wonderful Life, 232. thirty-five remain. Those regions of morphospace formerly accessible to the extinguished groups and their descendants were forever closed off: extrinsic constraints are not powerful enough in Gouldian evolution to cause any random group of survivors to converge on all the good design solutions, and intrinsic constraints would prevent many groups from converging on the same form in any case. The remaining designs then "congealed" or "stabilized," in

Gould's expressive words,312 and all subsequent evolution has been restricted to the limited possibilities available within each stabilized group. And, as Gould repeatedly reminds us with his metaphor of the tape, it might have been otherwise: different groups might have survived, different regions of morphospace would have been available, and thus the entire history of life would have been different. Gould wrote:

If life started with all its models present, and constructed a later history from just a few survivors, then we face a disturbing possibility. Suppose that only a few will prevail, but all have an equal chance.... If the human mind is a product of only one such set [of survivors], then we may not be randomly evolved in the sense of coin-flipping, but our origin is the product of massive historical contingency, and we would probably never arise again even if life's tape could be replayed a thousand times.313

For Gould, the Burgess Shale is a moment of initial maximum morphological disparity, to be followed by diversification within the restricted remnants of already- established body plans. Evolution lays all her cards on the table at the beginning of the game; she may sort them, and she may throw some away, but if she loses all the aces at the beginning, she can't just pull another ace out of her sleeve.

For Conway Morris, the Burgess Shale is really no different than any other moment in life's history, before or since; it is just harder to understand than more recent events because it is so distant from our modern world that it looks strange, and there is so little

312 See for example Gould, Wonderful Life, 209, and "The disparity of the Burgess Shale arthropod fauna and the limits of cladistic analysis," 419. 3,3 Gould, Wonderful Life, 233-234. 198 information left in the fossil record for us to interpret it with. Most of the Burgess creatures represent stem lineages of modern animal phyla, not unusual phyla of their own, and anyway it doesn't matter (in terms of the occupation of morphospace) what the precise phytogenies of the Burgess taxa are, because no matter what groups do and don't survive, the most important factors guiding evolution are the extrinsic constraints that stay the same no matter how many times the tape is replayed. The occupiable regions of animal morphospace are very limited, and life will navigate repeatedly to those few occupiable regions because they represent the best solutions to the design problems posed by the all-important extrinsic constraints. Intrinsic constraints do play a role, but it is a small one. Conway Morris wrote:

[T]he constraints of evolution [he means extrinsic constraints] and the ubiquity of convergence make the emergence of something like ourselves a near-inevitability. Contrary to received wisdom and the prevailing ethos of despair, the contingencies of biological history will make no long-term difference to the outcome.314

In this chapter I have dichotomized Conway Morris's and Gould's theories of evolution as privileging either extrinsic or intrinsic constraints. Another way to look at the same debate is to say that Conway Morris sees adaptation, or selection, as the primary force in evolution (on his theory, it is those few designs which are best adapted to extrinsic constraints which are convergently achieved and selected); whereas Gould sees structure as playing a very significant role (selection is important, but it can only select from those structures that can be created by lineages of organisms). When framed in this way, the debate between Gould and Conway Morris can be seen as only the most recent skirmish in a battle between structuralists (or formalists) and adaptationists (or functionalists) that goes back almost two hundred years, to the famous debate between and Etienne

Geoffroy St-Hilaire. This debate will be discussed in the next chapter.

314 Conway Morris, Life's Solution, 328. 199

Note also that an important claim in Gould's account, if not in Conway Morris's, regards whether the creatures of the Burgess Shale should be recognized as unique phyla or not. In fact, Gould's claim for maximal disparity in the Cambrian crucially depends on the

Burgess creatures being recognized as possessing unique body plans, and different body plans are typically differentiated taxonomically as different phyla. In Chapter 5,1 shall explore the history of the phylum and body plan concepts, the varied meanings of these terms for Conway Morris and Gould, and their implications. As we have seen in this chapter with the occupation and navigation of morphospace, disagreements over such fundamental concepts can have deep implications for the interpretation of the Burgess Shale, and the understanding of evolution itself. Chapter 5 "The Golden Age of Body Plans": Phyla in the Burgess Shale315

In Chapter 4 we observed that Gould thought intrinsic constraints were the most important factors influencing organic evolution, while Conway Morris believed extrinsic constraints were key. Another way of dichotomizing these two views of evolution is to say that Gould is a structuralist (or formalist), while Conway Morris is an adaptationist (or functionalist). It is easy to see - from our neo-Darwinian perspective - that Conway Morris fits into a tradition stretching back to Darwin (and even further, to the creationist Paley, and perhaps all the way to Aristotle), which seeks out as important those parts of organisms which appear to have been designed, and sees the task of the naturalist as explaining the function of this (apparent) design. It is somewhat less obvious, but no less true, that Gould also fits into a longstanding tradition in biology. In this structuralist tradition, scientists including Johann Wolfgang von Goethe, Etienne Geoffroy St. Hilaire and Richard Owen, have sought an understanding of organic form as a whole - not just those features of organisms which seem designed to fit them for their particular roles, but all aspects of form.

In this chapter I will situate Gould and Conway Morris within this larger, historical debate between structuralism and functionalism.

One of the oldest and most difficult questions in biology asks why different groups of organisms seem to share fundamental patterns of organization. The idea of a body plan,

Bauplan, or type has a long history, and for many biologists this body plan is expressed by or encapsulated within the notion of the phylum. In this chapter, I shall recount a brief history

315 Gregory A. Wray, "The golden age of body plans," Review of The Origin of Animal Body Plans: A Study in Evolutionary Developmental Biology by Wallace Arthur (Cambridge: Cambridge University Press, 1997) Paleobiology vol. 25, no. 1 (Winter 1999), 141.

200 201 of the phylum, type, and body plan concepts, and then examine their changing place within the debates over the Burgess Shale. In essence, there are two stances in the recent debate, which can each be broken down into a further pair. There are those (such as Briggs and

Budd) who take a cladistic approach to the Burgess Shale: they simply use "phylum" as a category of classification - it has no special biological status. Their priority is the systematics, not the biology, of the Burgess organisms - though as we will see, Briggs and

Budd do not agree on precisely how to define the phylum as a taxonomic category. Gould and Conway Morris, on the other hand, are much more concerned with the biology than the classification of the Burgess fossils. Rather than focus on the phylum as a taxonomic category, then, they both feel the real focus is on the acquisition of body plans. For them, a phylum is a group united by possession of a shared body plan. The two men do approach this question in very different ways, as we will see; and they do have very different views of the phylum. While they agree that the basic body plans which separate the major groups of animals should be designated "phyla," for Conway Morris this is mere pragmatic nominalism

(on his theory there is a body plan which corresponds with every taxonomic level, so the phylum is not anything special or different), whereas Gould wishes to use it to demarcate a real and important biological entity, a privileged biological category qualitatively very different from other categories, such as species or families. The interrelated notions of what a phylum is, what a body plan is, what categories one should use to classify living and extinct organisms, and above all, what our categories mean for the interpretation of the history of life and the nature of evolution itself- have all affected the reclassifications of the Burgess Shale fauna. 202

Phyla and Body Plans: History and Definitions

The term "phylum" was introduced by Ernst Haeckel in 1866 as a taxonomic level equivalent to Linnaeus's classes (1758) and Cuvier's embranchements (1812), which will be discussed in detail below. He devised this word fromth e Greek root "phylon," which can mean "tribe," "branch," "stem," or even "race."316 Invertebrate zoologist Benoit Dayrat argues that Haeckel's primary use was in the sense of "stem," and Haeckel's goal was to answer the following question: '7* the whole organic world of a common origin, or does it owe its origin to several acts of spontaneous generation?" The root "phylon" was employed to distinguish Haeckel's two hypotheses for the origin of life on Earth: monophyletic, in which all plants and animals share a single Moneran ancestor; and polyphyletic, in which these groups arose independently from separate Moneran ancestors.317

The phylum was the highest formal category in Haeckel's classification scheme, and the only one explicitly associated with a type. Haeckel wrote that "his phyla were mainly inherited from Cuvier's (1817) embranchements based on comparative anatomy and from

Von Baer's (1828) 'animal types' based on embryological studies," and that he was also influenced by Goethe's belief that each type represents a common anatomy from which the anatomy of all type members can be derived.318 Haeckel allowed for what cladists would call paraphyletic taxa, arguing that descendant groups which did not share the underlying body plan should be excluded fromth e phylum, despite their genealogical relationship. Thus it can be seen that Haeckel privileged morphology over genealogy, at least with respect to the definition of phyla and their accompanying body plans. In other words, like the evolutionary

316 Benoit Dayrat, "The roots of phytogeny: how did Haeckel build his trees?" Systematic Biology vol. 52, no. 4 (August 2003), 517. 317 Ernst Haeckel, qtd. in Dayrat, 517. Emphasis in the original. 318 Haeckel qtd. in Dayrat, 517. systematists discussed in Chapter 2, Haeckel grouped organisms together that were morphologically similar, even if this meant that sister taxa ended up in different groups.

Though genealogy was important to Haeckel, morphological similarity was more important in terms of drawing boundaries between groups.

According to paleontologists Olivier Rieppel and Simon Conway Morris, and developmental biologist Brian Hall, the German word Bauplan (plural Bauplane) was first used in a biological sense by embryologist and philosopher J. H. Woodger in 1945, though as we have seen, the concept of a biological plan, type, or distinctive architecture is far older.319

Cuvier's four embranchements, for example, are based on what he perceived to be the four fundamental body types of animals, or archetypes. Woodger's Bauplane (he used the anglicized plural "Bauplans") are sets of body parts that are isomorphic across a group of organisms ("lives," in his terms) related by descent. Woodger wrote: "By a taxonomic group

(in a restricted sense) we shall mean any set of lives which is determined by a Bauplan."320

Following Woodger, then, the conflation of "phylum" and "body plan" is no mere coincidence but done according to convention and definition. Woodger believed, furthermore, that body plans can be (and are) nested, such that the members of a lower taxonomic group share a more restricted body plan, which "overlaps" the more general body plan shared by higher taxa that include the lower taxonomic group. "Thus," as Woodger explained, "the determining Bauplan of the Tetrapoda overlaps the determining Bauplan of

319 Brian K. Hall, ""Bauplane, phylotypic stages, and constraint: why there are so few types of animals," Evolutionary Biology vol. 29 (1996), 223, Simon Conway Morris, "Body plans," in Encyclopedia of Evolution, vol. 1. Mark Pagel, ed., 117-120 (Oxford: Oxford University Press, 2002), 117, and Olivier Rieppel, "'Type' in morphology and phytogeny," Journal of Morphology vol. 267 (2006), 528. Some authors italicize the words "Bauplan" and "Bauplane;" others do not. For the sake of simplicity, I shall not use italics, except when directly quoting an author who does use them. 320 Joseph H. Woodger, "On biological transformations," in Essays on Growth and Form, Presented to D 'Arcy Wentworth Thompson. W.E. LeGros Clark and P.B. Medawar, eds. 95-120 (Oxford: Clarendon Press, 1945), 104. 204 the Gnathostomata and every tetrapod is a gnathostome. We can see, therefore, that given the Bauplans determining a number of taxonomic groups and their overlapping relations, the inclusion relations between the taxonomic groups are also established."321 Just as taxonomic groups are nested hierarchies, so are body plans. Woodger further explained that homology should not be mere "morphological correspondence" of parts, as it was before Darwin, but should now mean that the "lives" possessing the homologous parts "will have a common ancestor which exhibits a Bauplan which is exhibited by all three lives."322 It is this descent from a common ancestor, and inheritance of equivalent body parts, that defines homology over and above mere morphological similarity. "What did," according to

Woodger,

was to explain and thus to relate such isolated facts [i.e., that different species "exhibit a common Bauplan in spite of their differences"] by assuming that wherever there is community of Bauplan there is also community of descent accompanied by gradual modification of structure which left the Bauplan still discernible.323

Though the notion of eternal, unchanging species has been supplanted by evolution, it is still common, even customary, among biologists and especially paleontologists, to speak of body plans, and to equate body plans with phyla.324 Paleobiologist James Valentine, for example, in his magnum opus On the Origin of Phyla, refers throughout to "the body plans of the phyla," and "the body plan of each phylum," and states explicitly: "Here I will use the term body plan for an assemblage of morphological features shared among many members of a phylum-level group." Valentine also defines classes as "major architectural themes based

Woodger, "On biological transformations," 106. Woodger, "On biological transformations," 110. Woodger, "On biological transformations," 108. Conway Morris, "Body plans," 117. 205 on the phylum body plans," and orders as "modifications of class body plans."325 With these statements it is clear that the body plan refers to a particular degree, possibly even a particular kind, of morphological difference defining a group; and groups that possess morphological architectures unique enough to be distinguished biologically as different body plans are therefore also distinguished taxonomically as different phyla. Similarly, in the

Encyclopedia of Evolution, published in 2002, Doug Erwin wrote; "The Metazoa clade traditionally is divided into thirty-two to thirty-six phyla, each recognized on the basis of a common architectural framework, or body plan."326 Brian Hall wrote, in a 1996 article, "for most recent authors, the Bauplan represents the basic organizational plan common to higher taxa at the level of the phylum, order, or class," citing Gould and Conway Morris as two of several authors who use the term in this way.327 And Gould wrote in Wonderful Life: "Phyla represent the fundamental ground plans of anatomy."328

However, with the adoption of evolution (and therefore the loss of species fixity), and particularly following the vilification of essentialism by Ernst Mayr and others in the mid twentieth century (discussed in more detail below), the last fifty years or so have seen a struggle to reject those aspects of the Bauplan concept that smack of Platonic essentialism and fixity, while retaining its usefulness as a unifying morphological concept. As recently as

2003, developmental biologists Jaume Baguna and Jordi Garcia-Fernandez complained about the "excessive, almost mystical, adherence to typological concepts such as Bauplan and

Valentine, On the Origin of Phyla, see for example 8,33,199. 326 Douglas H. Erwin "Metazoans," in Encyclopedia of Evolution, vol. 1. Mark Pagel, ed., 727-731 (Oxford: Oxford University Press, 2002), 727. 327 HalL, "Bauplane, phylotypic stages, and constraint," 225. 328 Gould, Wonderful Life, 99. 206 phylum which are preformationist and pre-evolutionary."329 Conway Morris complained in

1989:

The kernel of our difficulties lies with the taxonomic hierarchy, whose deceptive utility conceals a straitjacket into which phylogenetic thinking is constrained into an essentialist mode that lacks historical perspective and loses sight of the contingent processes that haunt every step of biological diversification. Nowhere is this more evident than in the definition of a phylum. Here is the quintessence of biological essentialism, a concept that is almost inextricably linked with that of the body plan.330

The seemingly essentialist character of the body plan (and therefore the phylum) is difficult to dismiss for the simple reason that the body plan does seem to so fundamentally divide the different kinds of animals. Despite the now-pejorative nature of the word

"essentialism," some biologists do not want to dismiss it. In his grand opus published the year of his death, Gould declared that he supports a weak form of essentialism regarding the existence of "a general anatomical blueprint;" one that need not (and does not) involve

"conceptualization as a disembodied and nonmaterial archetype employed by a creator," but instead means only "an actual structure (or inherited developmental pathway) present in a flesh and blood ancestor." Or, in other words, Gould believed that organisms have essences

"in their limitation and channeling by constraints of structure and history, expressed as

Baupl&ne of higher taxa."331

What is this body plan or type, associated so firmly with the phylum? Is it a problematic metaphysical essence, or a real biological entity? And if body plans are biologically real, where did they come from, and why are there such distinctly different body plans in the animal kingdom? As we will see in the remainder of this chapter, these

329 Jaume Baguna and Jordi Garcia-Fernandez, "Evo-devo: the long and winding road," International Journal of Developmental Biology, vol. 47 (2003): 708. 330 Conway Morris, "Burgess Shale faunas and the Cambrian explosion," 345. 331 Gould The Structure of Evolutionary Theory, 10-11. 207 questions have been hotly debated for the past two hundred years, and new evidence is turning up that is vindicating some of the oldest (and seemingly silliest) ideas about body plans.

The Type Concept and Idealistic Morphology

In the same way that the Burgess Shale scientists of today seem to be divided on whether to use the phylum as a taxonomic or biological category, zoologists of the 18th and early 19th centuries sometimes used "type" as a category of classification, and sometimes as a morphological concept. Historian of biology Paul Lawrence Farber defined the morphological type concept as the recognition that "a basic plan or type" of anatomy "could be discerned at various taxonomic levels" in animals.332 This basic plan took the form of similar anatomical structures found in different animal groups. Farber also found that many naturalists, when naming and classifying several related animals, would often choose one species or genus as a type or model, to which other species or genera could be compared.

This classification-type method is still used today; if a new taxon is constructed, its creator will specify a type specimen. This method was and is a practical shorthand for classification and its use does not necessarily mean that those employing it believe in real types or essences of a Platonic nature.333 For Plato, objects in the real world reflected imperfectly the fixed, eternal essences or forms of a higher, ideal realm, and the classification of the imperfect objects of our world was made possible by our recognition of their possession or instantiation of particular ideal forms. For example, the sides of a triangle drawn by a person with a pencil can never be perfectly straight, but we can still recognize it as a triangle because we

332 Paul Lawrence Farber, "The type-concept in zoology during the first half of the nineteenth century," Journal of the History of Biology vol. 9, no. 1 (March 1976), 100. 333 Farber, 94-95. 208 retain a sort of unconscious memory of the ideal triangle. According to Ron Amundson, the traditional concept of biological essentialism involves a belief in "definitional sets of intrinsic necessary and sufficient conditions that logically determine an entity's membership" in a natural kind. He noted further that "because the definitions [of natural kinds] are timeless, the kinds are eternal and unchanging."334 For this reason, any biologist who believed that species (or other biological categories) were natural kinds defined by essences would perforce also have to believe in species fixity.

Some biologists and historians of biology have argued that pre-Darwinian biologists and systematists all believed in species as eternal, essentialist natural kinds. This position has been put forward most vehemently by Ernst Mayr, who argued that before the "population thinking" introduced by the Modern Synthesis of the early to mid^O* century, biology in general and idealistic or transcendental morphology in particular suffered from a "typological view" that prevented the true nature of species from being understood. Note that for Mayr,

"typological" was synonymous with "essentialist,"335 and referred to a belief in unchanging species, where each individual of a species is an imperfect realization of a true Platonic essence. In the past few years, the veracity of the Essentialism Story has been called into question. As historian of biology Mary P. Winsor and philosopher of biology Ron

Amundson have shown, true essentialism in biology, far from being a tradition carried forward from the ancient Greeks, did not become common until a mere century before

Darwin's publication of OK the Origin of Species, and further, essentialism was at no time

334 Amundson, The Changing Role of the Embryo in Evolutionary Thought, 18. 335 Mary P. Winsor, "The creation of the Essentialism Story: an exercise in metahistory," History and Philosophy of the Life Sciences vol. 28, no. 2 (2006), 152. necessarily tied to typology or species fixism. The great taxonomist Linnaeus and others following him did have a typological concept of species, but it was not essentialist; it was rather pragmatic and polythetic. In other words, while species were recognized by comparison to a type or suite of characters, these characters were not collectively essential, nor were the species unchanging.337

The type concept in biology, then, is (at minimum) the belief or recognition that members of a taxon share some set of common anatomical features, which can be thought of as a type or body plan. Typology may be accompanied by associated beliefs in essentialism and species fixity, as Mayr believed, but these ancillary beliefs are just that, and not components of the type concept itself, as Amundson, Winsor, and Farber have shown. On this definition, it is probably safe to say that every biologist, past and present, is a typologist, because they all recognize that organisms that belong to different species nevertheless often display anatomical similarities which cross species boundaries. Yet the concept of type seems to mark a significant divide in thinking about biological form and function: some biologists defined types as those which shared similarities caused by similar functions, whereas others, including the idealistic morphologists, sought to explain form for its own sake, without tying it necessarily to function.

The school of morphology known as idealistic or transcendental morphology began at the end of the 18th century, in , with the work of Johann Wolfgang von Goethe, and reached a pinnacle in the early to mid-19th century.338 Lynn Nyhart defines idealistic

336 See for example Mary P. Winsor, "Non-essentialist methods in pre-Darwinian taxonomy," Biology and Philosophy vol. 18 (2003): 387-400, Winsor, "The creation of the Essentialism Story," and Amundson, The Changing Role of the Embryo in Evolutionary Thought. 337 Winsor, "Non-essentialist methods in pre-Darwinian taxonomy," 392-393. 338 Georgy S. Levit and Kay Meister, "The history of essentialism vs. Ernst Mayr's 'Essentialism Story': a case study of German idealistic morphology," Theory in Biosciences vol. 124 (2006), 303. morphology as "an approach to form not yet informed by Darwinian concerns, one in which the problems of individual development, generation, and adaptation were viewed as the keys to understanding the unity and diversity exhibited by animal forms."339 Morphologists before Darwin saw their task as explaining organic form: how is it that offspring resemble their parents; why do members of a species resemble each other; and most curiously, why is it that certain larger groupings of species (higher taxa) seem to share a fundamental body plan with each other, across species? The name "idealistic morphology," and the origin of the school in Germany suggests a link to the German philosophical school of

Naturphilosophie, but the two schools of thought are very different (despite the fact that both were inspired by Goethe). Austrian zoologist Rupert Riedl has shown that the Bauplan or type in German idealistic morphology, unlike the "idea" in German Naturphilosophie, was not a Platonic essence. As Riedl noted, while German Naturphilosophie "interprets its term

'idea' not as an abstraction of the general from the particular, but as something given in advance," the opposite was true of the type concept in idealistic morphology.340 The type or body plan of idealistic morphologists was an abstraction of a generalized form from the particular forms displayed by actual organisms.341

Goethe's major contribution to the field was his proposal that "whole bodies are made up of repeated elements that serially corresponded with one another."342 Goethe suggested that all the various parts of plants could be thought of as modifications or transformations of a primordial leaf. He also noted that vertebrates contain a similar series of repeated, partially

339 Lyim K. Nyhart, Biology Takes Form: Animal Morphology and the German Universities, 1800-1900 (Chicago and London: The University of Chicago Press, 1995), 338. 340 Rupert Riedl, "The role of morphology in the theory of evolution," in Dimensions of Darwinism: Themes and Counterthemes in Twentieth-Century Evolutionary Theory Marjorie Grene, ed., 205-238 (Cambridge: Cambridge University Press, 1983), 209. 341 Nicolaas A. Rupke, "Richard Owen's vertebrate archetype," Ms vol. 84, no. 2 (June 1993), 233. 342 Amundson, The Changing Role of the Embryo in Evolutionary Thought, 55. 211 modified elements: the vertebrae. Goethe sought morphological correspondences between different species, and often found them. For example, he discovered that human fetuses and children possessed the intermaxillary bone, a structure which was known to exist in other vertebrate species but had not been found in adult humans. Goethe believed that all vertebrates shared a common form or "archetype." This unity of common form could be seen in serially repeated elements within an individual (such as the repeated backbone segments in vertebrates, or the primordial leaf as the basis of all structure in plants), as well as in the similarity between apparently equivalent body parts in different species (the limb bones of humans, whales, moles, and bats, for example). Richard Owen, one of the greatest idealist morphologists in history, referred to the former group of similarities as "serial homology," and the latter as "special homology" (special referring to species).343 A third type of similarity could be seen in ontogeny: animals of different species often seemed to pass through similar stages in embryological development, before achieving their very different adult forms.

Richard Owen was the most famous idealistic morphologist in Britain, and the concept of the "archetype" is associated with his name at least as much as with Goethe's.

Until recently, Owen was heavily tarred with Mayr's essentialist brush. Some of the blame for this is Owen's own, as in his later writing, under the influence of friends who fretted about the materialism and pantheism they were afraid they could detect in his work, he admitted that his vertebrate archetype was meant to represent a Platonic ideal. The archetype as Owen first conceived it, however, was the exact opposite: not the perfect, highest, most complete form of a vertebrate, of which all real vertebrates were but imperfect copies; rather the archetype was the most basic, undifferentiated, general vertebrate plan, of which all real

343 Amundson, The Changing Role of the Embryo in Evolutionary Thought, 56. 212 vertebrates were variations, and compared to which some - notably humans - were greatly perfected. Owen's archetype concept, especially in his later writing, seems Platonic, but as

Nicolaas Rupke has shown, this was a cloak thrown overtop of an original idea to sanitize it and protect its creator from accusations of mysticism and pantheism.344

Owen's vertebrate archetype was not a Platonic ideal, nor was it an ancestor, though

Darwin later appropriated it as such. It was rather a taxonomic type, or a sort of heuristic tool or model, against which other vertebrates could be compared and classified, according to their difference from it. Owen and other morphologists had good reason for seeking more than mere ancestors in their types. As Amundson has convincingly argued, the 19th century morphologists sought above all an explanation of biological form. This goal has been lost sight of by the neo-Darwinians; in our adaptationist framework we seek to explain adaptation

(and the agreed-upon explanation, of course, is natural selection). The explanation of form is not the same thing. As Amundson points out, adaptation may be able to tell us why the forelimbs of birds are wings while those of whales are flippers - but how do we explain the presence of those forelimbs in the first place? Why do vertebrates have forelimbs? And why do those vertebrate forelimbs always contain the same bones in the same general positions

(proximal humerus, articulating with radius and ulna, then distal digits made of carpals, metacarpals, and phalanges)? These are the questions that the idealist morphologists sought to answer.

Adaptationism vs. Structuralism: Cuvier vs. Geoffroy

The idealistic morphologists were structuralists, seeing their primary goal as the explanation of biological form. Perhaps the most famous structuralist in history was a

344 Rupke, 243,250. 213

French zoologist. In France, the science of comparative anatomy, along with the related sciences of zoology and paleontology, had its formal beginning in 1793, with the creation of the Museum National d'Histoire Naturelle. Etienne Geoffroy St. Hilaire and Georges

Cuvier, who had both worked for the Museum's predecessor, the Jardin du Roi, were appointed professorships in the new Museum, Geoffroy as the Professor of Vertebrate

Zoology, Cuvier as the Professor of Invertebrate Zoology. Though they began as friends, within a few years Cuvier and Geoffroy were bitterly divided, on opposite sides of what came to be known as the Unity of Type debate. This debate involved the interpretation of the significance of morphological resemblances between different groups of organisms, and their implications for taxonomy. These morphological resemblances were eventually dichotomized into analogies, which were accidental resemblances, or homologies, which were modified versions of the same structure. The question was, what caused these similarities? Geoffroy sided with the traditional school of idealist morphology, while Cuvier took a functionalist approach.

Cuvier sought a natural system of classification - one which reflected the real divisions of nature as God had seen fit to make them. In 1812, he proposed four embranchements, or large branches into which the animal kingdom was to be divided. These embranchements were codified to capture the four basic body plans Cuvier had identified, following others before him, among all animal species: the Vertebrata, Mollusca, Articulata, and Radiata.345 The first two groups correspond to the later Phylum Chordata and Phylum

Mollusca. The articulates comprised the modern Phylum Arthropoda and Phylum Annelida, and the Radiata was composed of taxa we now recognize as being members of the Phyla

345 Mary P. Winsor, Starfish, Jellyfish, and the Order of Life: Issues in Nineteenth-Century Science (New Haven and London: Yale University Press, 1976), 7. Echinodermata and Cnidaria. Cuvier's four embranchements are the starting point of the modern animal phyla; they are at base a type concept of organic form.

Cuvier privileged function above all other considerations in his comparative anatomy and in his classification. Each embranchement was recognized and unified primarily according to the arrangement of the nervous system common to all of its members, for

Cuvier saw the working of the nervous system as the most important and fundamental functional system of the animal body, upon which all the rest of the body's systems were built.346 On Cuvier's system, there were no links or significant resemblances across embranchements, and no way to turn one form into another form. The reason for this was

Cuvier's strong belief in the integration of function. An animal's whole body is purposely designed to suit its particular function, therefore one part cannot be changed without necessitating a change of the whole. Cuvier referred to this idea as the "Correlation of

Parts." The Correlation of Parts was a strong argument against evolution, for if the whole organization of the body works together to achieve the function for which the organism was designed, how could it evolve? It was ludicrous to imagine that the whole body could change in one step to a completely new functional organization, but to change only one part would be disastrous - it would disrupt the harmony of the whole. Famously, using this idea of the Correlation of Parts, Cuvier was said to be able to successfully infer the structure of a fossil animal's entire body from just one part, such as a tooth or leg bone. An individual organism was tailored head to toe for its particular function, then, and organisms with similar functions could be expected to look similar to each other, because they had to be similar to carry out their common functions. Each embranchement, indeed, each species, had the form

346 Toby A. Appel, The Cuvier-Geojfroy Debate: French Biology in the Decades Before Darwin (Oxford: Oxford University Press, 1987), 45. it did in response to what Cuvier called the "Conditions of Existence." Any similarities

between animals in the same embranchement thus reflected their similar function. Even

those most basic and fundamental similarities that characterize an entire embranchement -

such as the forelimb bones of the Vertebrata, which can be recognized as humerus, radius,

and ulna even in animals as diverse as the dog, the whale, and the bat - were ultimately

derived from function. For Cuvier, the general features of the Bauplan (the embranchement,

in his terms) indicate "broad function," while the more specific adaptations reflect "local

function."347 Cuvier did not recognize similarities across embranchements.

Geoffroy, by contrast, also noted morphological similarities between species, but did

not attribute them to functional causes. His doctrine was called the "Unity of Type," and was

seated firmly in the idealistic morphology tradition; he too believed that species shared deep

structural similarities, but that these did not arise from a shared function.348 As Ron

Amundson explained, both Cuvier and Geoffroy expected to find homologies between members of different species. However, Cuvier expected to find them only when they

fulfilled the same function (general or specific), because he thought that the homologies were caused by things having the same function. His emphasis was on the Conditions of Existence

- if Species X faces the same conditions as Species Y, X will have to function the same way as Y, so X will have similar structures to Y. Geoffroy, on the other hand, did not think homology was caused by similarities in function; his position was called Unity of Type because he thought "structural correspondences existed independently of functional needs."349 Geoffroy did not deny the possibility that an animal's parts might be adapted to its function, but for Geoffroy, any such adaptations were secondary additions on top of a

347 Gould, The Structure of Evolutionary Theory, 293. 348 Nyhart, Biology Takes Form, 7. 349 Amundson, The Changing Role of the Embryo in Evolutionary Thought, 56. primary, underlying structure - and he saw the true task of the biologist as discovering and explaining this fundamental structure. For example, Geoffroy discovered a bone in the pectoral girdle of fishes which he showed to be homologous to the furcula (in common parlance, the wishbone) of birds. Functionalists explained the existence of the furcula as an adaptation for the function of flight, but this explanation could not be correct if fish,whic h obviously do not share this function, have the same bone.350

The real falling out between the two men came in the 1830s, when Geoffroy began publishing work on homologies he had discovered between species in different embranchements - something that was nonsensical in Cuvier's system. Geoffroy argued, for example, that the endoskeleton of the vertebrates is homologous with the exoskeleton of the articulates. In addition to the not-inconsiderable matters of these skeletons being composed of different materials, and being located inside versus outside the body, there are other differences: in vertebrates, the nerves are found dorsally, while the circulatory system is ventral. These organs are reversed in the arthropods and annelids. In order for them to truly be homologous, the entire body organization must have gotten flipped over in one group or the other. This sort of wholesale rearrangement of parts struck Cuvier as completely impossible.

The story of the 1830 debate has typically been told as the triumph of Cuvier and his scientific functionalism over the mystical, essentialist structuralism of Geoffroy.351 This interpretation has seemed natural and correct when seen through the lens of Darwinian adaptationist biology, particularly since the "hardening" of the Modern Synthesis into a completely adaptationist framework in the late 1940s. A handful of evolutionary biologists

330 Gould, The Structure of Evolutionary Theory, 299. 351 Gould, The Structure of Evolutionary Theory, 308, and Amundson, The Changing Role of the Embryo in Evolutionary Thought, 58. 217 over the past century, including Gould, have tried to soften the stronghold of adaptationism, but it has only been with the rise of evolutionary developmental biology, or evo-devo, beginning in the 1980s, that structuralism has once again been perceived as a credible position. Why did the adoption of Darwinism banish structuralism from serious biological inquiry, and what has since allowed structuralism to return?

The New Structuralism: Gould, Evo-Devo, and the Origin of Phyla

In the earlier chapters of this thesis, we have seen how the adoption of new systematic methodologies, as well as the discovery of new fossils and the further examination of known ones, have led many paleontologists to a new (Phase 3) understanding of the Burgess Shale.

However, other recent discoveries, and the reinterpretation of old ideas, in a different sub- discipline of biology, may at the same time be strengthening the support for the old (Phase 2) interpretation of the Burgess Shale. The growing field of evo-devo and its discovery of a

"genetic toolkit" shared by most or all animal phyla may provide new corroboration for

Gould's structuralist, macroevolutionary theory of the origin of phyla. In this section we will explore the structuralist tradition of which Gould is a part, and the renaissance it, along with developmental biology, is currently experiencing.

Darwin's theory of evolution by natural selection proposed adaptation as the cause of seeming organic design. It is important to realize that in proposing this theory, Darwin did not simply provide a new answer to an old question; he also redefined which questions could be asked. Darwin's theory of descent with modification can explain why the forelimbs of bats have been modified into wings, or why those of whales are modified into flippers; the answer of course, is that they are each adapted according to the function they serve. But, as 218

Amundson points out, those wings and flippers were vertebrate forelimbs before they were modified; that homological structural identity came first, before the adaptation. It is this common identity that Darwin fails to address. Amundson has argued that Darwin's objective was not to explain organic form (the objective of the structuralists), but to explain change in organic form (the new, Darwinian, adaptationist objective).352 Where that form came from in the first place did not figure in the Origin of Species, according to Amundson.

In discussing the two great biological principles of Unity of Type (the common form shared by related organisms, such as the body plan which characterizes a phylum) and

Conditions of Existence (the integration of parts according to their function), Darwin made the former a historical consequence of the latter:

It is generally acknowledged that all organic beings have been formed on two great laws - Unity of Type, and the Conditions of Existence. By unity of type is meant that fundamental agreement in structure, which we see in organic beings of the same class, and which is quite independent of their habits of life. On my theory, unity of type is explained by unity of descent. The expression of conditions of existence, so often insisted on by the illustrious Cuvier, is fully embraced by the principle of natural selection. For natural selection acts by either now adapting the varying parts of each being to its organic and inorganic conditions of life; or by having adapted them during long-past periods of time: the adaptations being aided in some cases by use and disuse, being slightly affected by the direct action of the external conditions of life, and being in all cases subjected to the several laws of growth. Hence, in fact, the law of the Conditions of Existence is the higher law; as it includes, through the inheritance of former adaptations, that of Unity of Type.353

According to Darwin, then, the Unity of Type is not a separate phenomenon in and of itself, but merely the historical accumulation of adaptation to the Conditions of Existence. Related species appear to be of the same "type" because they have inherited their common ancestors' adaptations to the conditions they faced long ago. The Unity of Type is the consequence of

Amundson, The Changing Role of the Embryo in Evolutionary Thought, 103. Darwin, 168. 219 two things: first, that changing conditions of existence require changing adaptations, and second, that biological form seems to be inherently conservative - any character that does not have to change, in response to the Conditions of Existence, stays the same, thereby preserving in its history the "type" to which the species in question belongs. These two factors combine to preserve much of biological form over long periods of time, and this, said

Darwin, is all that is needed to explain the Unity of Type. In this respect, Unity of Type is no different, evidentially, from the fossil record.

This subordination of form to function (adaptationism), as well as the supremacy of natural selection acting upon minute genetic variations as the main force of evolution, was cemented in the modern evolutionary synthesis of the 1930s and 40s. Gould has described the modern synthesis as an attempt to "remove th[e] idea of a separate but unknown genetics for large-scale changes and to render all of evolution by known genetic mechanisms that could be studied directly in field and laboratory. It was primarily a plea for knowability and operationalism, for a usable and workable evolutionary unity."354 Gould had nothing against the desire to formulate a properly scientific, empirical, and unified theory of evolution, but thought that its architects eventually excluded too much of real biological value in their zeal to achieve these goals. The initial formulation of the evolutionary synthesis was

"pluralistic," according to Gould, in that it "admitted a range of theories about evolutionary change, Darwinian and otherwise." For example, Simpson's contribution to the Synthesis,

Tempo and Mode in Evolution (1944), allowed that species-level evolution occurred according to the slow accumulation of Mendelian genetic variation acted upon by Darwinian

Stephen J. Gould, "The hardening of the modern synthesis," in Dimensions of Darwinism: Themes and Counterthemes in Twentieth Century Evolutionary Theory. Marjorie Grene, ed. 71-93 (Cambridge: Cambridge University Press, 1983), 74. 220 natural selection, but proposed a different mechanism for the evolution of higher taxa: quantum evolution.

The pluralistic phase of the Synthesis was followed in the late 1940s by what Gould called a "hardening," in which non-adaptationist evolutionary mechanisms were cast out and biologists began to insist "to the point of dogma and ridicule that selection and adaptation were just about everything."355 Another key claim of the Synthesis was extrapolationism: that "all evolution is due to the accumulation of small genetic changes, guided by natural selection, and that transspecific [i.e., macro-] evolution is nothing but an extrapolation and magnification of the events that take place within populations and species."356 (Though genetics were unknown in Darwin's day, the extrapolationism is not new. Darwin's theory was founded upon actualism and uniformitarianism. Together these are, in Darwin's hands, simply an invitation to extend what goes on in pigeon breeding (Chapter 1 of the Origin) and community ecology (Chapter 2) to the whole of life.)

A modern-day Geoffroy surrounded by Cuviers, Gould spent much if not all of his career trying to soften this hardened commitment to adaptationism, and to carve out a prominent place in evolutionary theory for structuralism, as well as contingency, punctuationalism, and hierarchical levels of operation, to name the other major tenets of his grand theory).357 A major part of this effort is his concept (created with Richard Lewontin, in 1979) of spandrels. Spandrels are features which arise alongside adaptations, out of architectural necessity, but which are not themselves adaptations, though once they have

355 Gould, "The hardening of the modem synthesis," 75. 356 Ernst Mayr, Animal Species and Evolution (Harvard: The Belknap Press of Harvard University Press, 1963), 586. 357 Michael B. Shermer, "This view of science: Stephen Jay Gould as historian of science and scientific historian, popular scientist and scientific popularizer," Social Studies of Science vol. 32, no. 4 (August 2002), 508. 221 arisen they may be co-opted for adaptive purposes. This paper - subtitled "A critique of the adaptationist programme" - was one of Gould's many efforts to carve out a role for structuralism amidst the adaptationist hegemony. Gould stated his overall goal in 1980:

A new and general evolutionary theory will embody this notion of hierarchy [i.e., that within-population change, speciation, and macroevolution are three different levels, each with its own "modes of change"] and stress a variety of themes either ignored or explicitly rejected by the modern synthesis: punctuational change at all levels, important non-adaptive change at all levels, control of evolution not only by selection but equally by constraints of history, development, and architecture.359

This has been an uphill battle. The legacy of the hardened Synthesis was a theory of evolution in which form was entirely explained as apparent design caused by the selection and inheritance of adaptive features, and evolutionary change at all levels could be reduced to the gradual accumulation of random genetic variation acted on by selection.

Gould did, however, belong to a longstanding tradition of evolutionary biologists who did not agree that adaptationism is the only way to understand evolution; who saw other factors at work in the origin of higher taxa, especially phyla, and who saw form - especially the body plan which was possessed by all members of one phylum but not those of other phyla - as the ultimate explanandum of evolution. We have already seen that Geoffroy,

Owen, and other idealist morphologists rejected functionalism as the sole explanation of biological form. This tradition also included the early 20th-century geneticist Richard

Goldschmidt, famous for his macroevolutionary theory of hopeful monsters, and Ivan

Stephen J. Gould and Richard C. Lewontin, "The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme," Proceedings of the Royal Society of London, Series B, Biological Sciences vol. 205, no. 1161 (21 September 1979): 581-598. 359 Stephen J. Gould, "Is a new and general theory of evolution emerging?" Paleobiology vol. 6, no. 1 (Winter 1980), 119. Schmalhausen, who proposed a theory of stabilizing selection which seemed to foreshadow later notions of canalization and constraint, as proposed by Conrad Hal Waddington.360

Goldschmidt's theories of macroevolution were an important inspiration for Gould.

For example, Goldschmidt did not deny that microevolution, or change within species, happened exactly as neo-Darwinism said it did - but he did deny that microevolution had anything to do with speciation or the origin of higher taxa. According to Goldschmidt, this larger-scale change - macroevolution - could not be accomplished by point mutations in single genes, but instead might have resulted from the wholescale reorganization of all the chromosomal material. In addition to this theory of "systemic mutations," which was not well received in the evolutionary community, Goldschmidt proposed another, more plausible mechanism of speciation and other macroevolutionary change. According to Gould,

Goldschmidt suggested that small mutations which altered the timing of key events early in ontogeny might "shift development into radically different, but still viable, channels."361

Gould rejected Goldschmidt's first mechanism of macroevolution (systemic mutations reorganizing the entire chromosomal material in one step), but suggested that his second mechanism, which involved "the potential for macroevolution inherent in constraints and opportunities of developmental systems," as well as his overall approach to macroevolutionary studies, had great merit.362 Gould praised Goldschmidt for "developing] a professional sense that animals must be viewed as integrated wholes and that our organic world of divergent Bauplane cannot be rendered by models of strict, gradual continuity in

360 By naming these men specifically, together, I do not mean to suggest that they formed a coherent research group or school of thought, which they did not. Following Amundson (The Changing Role of the Embryo in Evolutionary Thought, 193-197), I merely recognize them as scientists who argued for the importance of evolutionary mechanisms other than strict selection and adaptation. 361 Stephen J. Gould, "The uses of heresy: an introduction to Richard Goldschmidt's The Material Basis of Evolution," in The Material Basis of Evolution Richard Goldschmidt. With an Introduction by Stephen Jay Gould, xiii-xlii (New Haven and London: Yale University Press, 1982 (1st ed. 1940)), xxix. 362 Gould, "The uses of heresy," xxxiv. transformation." In Goldschmidf s work, Gould saw a reflection of his own belief that macroevolution is somehow different from, or more than, microevolution carried out over a very long period of time.

Another early 20th century evolutionist who could be seen as one of Gould's intellectual forefathers was Russian biologist Ivan Ivanovich Schmalhausen (1884-1963), who proposed a concept of stabilization in 1949.364 Schmalhausen's "stabilizing selection" was an active process of ontogenetic development in which the formation of an advantageous phenotype could be entrenched and made to develop robustly. Schmalhausen proposed two types of selection: dynamic selection and stabilizing selection. Dynamic selection, also referred to as directional selection, comprises the process people normally think of when they envision the operation of natural selection. As environmental conditions fluctuate, a particular phenotype within a population becomes more adaptive than others. This phenotype is then selected for, and the phenotypic mean of the population as a whole shifts towards the favored phenotype. This shift, in the direction of the more adaptive form, is dynamic selection.365

Stabilizing selection, by contrast, is something that happens to the population after environmental conditions have settled, and the population mean has completed its dynamic shift towards the new adaptive phenotype. Later biologists and historians of science have tended to perceive Schmalhausen's stabilizing selection purely in terms of the external operation of natural selection on particular phenotypes within a population. For example,

Mark B. Adams, in a review of Schmalhausen's book, defined stabilizing selection as that

363 Gould, "The uses of heresy," xxxvii. 364 Ivan L Schmalhausen, Factors of Evolution: The Theory of Stabilizing Selection. Isadore Dordick, trans., Theodosius Dobzhansky, ed. (Chicago and London: The University of Chicago Press, 1986 (1st ed. 1949)). This book was first published in Russian in 1947. 365 Schmalhausen, 73,74. 224

"which eliminates extremes from the norm and tends to maintain the population mean." In other words, this interpretation of stabilizing selection sees it as the statistical elimination of the extreme phenotypes at the tails of the distribution around the new mean. But

Schmalhausen's stabilizing selection was in fact much more than this; as he explained in his

1949 book on the subject, stabilizing selection is a kind of "autoregulation" in which "the entire morphogenesis (i.e., the entire reaction apparatus) together with all its adaptive reactions is endowed with regulating mechanisms which protect the processes of individual development against possible disturbances by changing and accidental influences of external environment."367 Schmalhausen's stabilizing selection is not a statistical process of elimination, then, but a developmental process in which the new phenotype is more firmly entrenched in the ontogeny of individuals in the population. Schmalhausen wrote:

"Stabilizing selection produces a stable form by creating a regulating apparatus. This protects normal morphogenesis against possible disturbances by chance variations in the external environment and also against small variations in internal factors (i.e., mutations)."

Eldredge and Gould initially proposed something very much like Schmalhausen's stabilizing selection in their first paper on punctuated equilibrium (published in 1972); they wrote:

If we view a species as a set of subpopulations, all ready and able to differentiate but held in check only by the rein of gene flow, then the stability of species is a tenuous thing indeed. But if that stability is an inherent property both of individual development and the genetic structure of populations, then its power is immeasurably enhanced, for the basic property of homeostatic systems, or steady states, is that they resist change by self-regulation. That local populations do not differentiate into species, even though no external bar

366 Mark B. Adams, "A missing link in the evolutionary synthesis," Review ofFactors of Evolution: The Theory of Stabilizing Selection by Ivan I. Schmalhausen. Isadore Dordick, trans., Theodosius Dobzhansky, ed. (Chicago and London: The University of Chicago Press, 1986 (1st ed. 1949)). his vol. 79, no. 2 (June 1988), 282. 367 Schmalhausen, 10. 368 Schmalhausen, 79. 225

prevents it, stands as strong testimony to the inherent stability of species in time.369

But, as Gould explained in The Structure of Evolutionary Theory, he later changed his mind about the importance of this type of stabilizing selection acting at the species level. Gould wrote: "I now believe... that the theme of constraint, while not irrelevant to the causes of stasis in punctuated equilibrium, does not play the strong role that I initially advocated."

However, Gould did not relinquish his belief in the importance of the stabilizing influence of developmental constraints; he merely re-located it to a level above that of the species: "I now realize that my arguments for the channeling of potential direction and limitation of change apply primarily to levels above species - to aspects of the developmental Bauplane of anatomical designs that usually transcend species boundaries."370

This sort of channeling and limitation is reminiscent of a final figure who may have had an influence on Gould's theory of evolution: Conrad Hal Waddington. Waddington

(1905-1975), a British embryologist and geneticist with a strong interest in paleontology, was best known for his concept of canalization and the epigenetic landscape with which it could be visualized (discussed in some detail in Chapter 4). Waddington's canalization, much like Schmalhausen's stabilizing selection, is a mechanism by which adaptively successful phenorypes can be made developmentally robust. In other words, it is a method of stably producing a particular phenotype even in the face of genetic or environmental perturbations.

This mechanism is illustrated by the epigenetic landscape. "Epigenetic," a term coined by

Waddington in 1940, refers to phenotypic changes that are not directly caused by

369 Niles Eldredge and Stephen J. Gould, "Punctuated equilibria: an alternative to gradualism," in Models in Paleobiology. Thomas J.M. Schopf, ed. 82-115 (San Francisco: Freeman, Cooper & Company, 1972), 114-115. 370 Gould, The Structure of Evolutionary Theory, 880. 371 Hall, "Waddington's legacy in development and evolution," 113-115. corresponding genetic changes. The same genotype can produce different phenotypes if the expression of the genotype is altered by the influence of different developmental or environmental cues.373 For example, the sex of many reptiles, including many turtle species, is determined by temperature: males and females do not possess genetic determinants of sex, but instead develop differently according to the temperature at which the turtle eggs are incubated (higher temperatures produce more females, while lower temperatures produce more males). The underlying genetics are the same, but a change in environment

(temperature) produces different phenotypes; this is an example of an epigenetic phenomenon.

As discussed in Chapter 4, the epigenetic landscape can be seen as depicting the ontogeny of an organism as a ball rolling along a series of downwardly-sloping, branching channels or valleys, embedded within steep canyons. (See Figure 33, p. 187.) The branching canyons can represent the developmental and environmental conditions the embryo encounters as it develops. Even though the ball itself never changes through development, it may end up in a different place depending on how it navigates the landscape. As the ball approaches a junction, it might roll into the left branch or the right one. If the ball enters the left-hand channel, it cannot then roll back uphill and "choose" the right branch instead; it is now committed to continuing only on one of those paths accessible from the chosen branch.

Thus, development is hierarchical, and pathways chosen "upstream" constrain the choice of pathways which will be available "downstream."

Conrad Hal Waddington, Organisers and Genes (Cambridge: Cambridge University Press, 1940). 373 Eva Jablonka and M. J. Lamb, "Epigenetics," in Encyclopedia of Evolution, vol. 1. Mark Pagel, ed., 310-311 (Oxford: Oxford University Press, 2002), 310.. 227

Another important feature of Waddington's epigenetic landscape is represented by the steep canyon walls. They are the pictorial representation of Waddington's canalization. If the ball is bumped so that it rolls up the side of a canyon with shallow walls, it may be able to

"jump" out of that canyon and roll into a different path instead. If this happens, and the ball

"jumps" into a path very different from the one it was in, it may end up with a very different phenotype than the one it would otherwise have expressed. But if the canyon walls are very tall and steep, then the ball will be forced to roll back down into the same canyon. The bumps represent developmental or environmental perturbations; the process of making the canyon walls tall and steep is canalization. It can also be thought of as equivalent to

Schmalhausen's stabilizing selection, or what Gould refers to as congealing or stabilization of body plans. This process of canalization or stabilization is a sort of genetic or developmental buffering, which has the effect of reducing morphological variability, and causing the species in question to robustly develop the canalized phenotype despite environmental or developmental perturbations (by making the channels too steep to climb out of, even if the ball is bumped).

Waddington's epigenetic landscape provides a model to explain how large morphological jumps - phylum-level jumps, or the origin of new body plans - might have been possible. For if the ontogenetic ball does manage to jump right out of its canyon, it will encounter a flat, unconstrained developmental landscape, on which it might travel just about anywhere. In such a leap, then, macroevolution is possible; the ball may travel to a totally new area of morphospace, and eventually new channels of development may be forged. It would only be possible for the ball to completely escape its canyon if the canyon walls are 228 not too steep or too tall - or in other words, changes as large as phylum-level jumps may only be possible early in the history of life, before too much canalization has taken place.

This idea of canalization or stabilization increasing with time is a major premise of

Gould's theory of evolution. For Gould, it explains the different body plans possessed by different phyla; the origin of new phyla early in the history of animal life, but not much later in that history, and it also explains the clumped distribution of body plans in morphospace.

All the different animal phyla alive today, and the many others Gould believed are preserved in the Burgess Shale, can be traced back to an ancestral bilaterally symmetrical animal, which lived far back in the Precambrian seas. The developmental pathways of this creature, so close to the origin of life, were not yet canalized; a picture of its epigenetic landscape would show very shallow canyons, so that it would be very easy to push the genetic ball far out of its usual pathway. Each new body plan of each phylum that arose was created by such a large perturbation, into a completely new pathway on the epigenetic landscape. Then, as each new lineage discovered a path which led to a viable body plan, the path leading to that body plan became canalized: the canyon walls became steeper and taller, and it became more and more difficult to make the ball jump into a new but still viable pathway. This image might explain why it seemed so easy for new body plans or phyla to arise in the Precambrian, and why it has become progressively more difficult since then - but what exactly does this process of canalization entail? What are the actual genetic or developmental processes that are captured only metaphorically by the image of steepening canyon walls? The new science of evo-devo may be able to answer that question.

Historically, the study of development has been, at the same time, both a confirmation of evolution and a domain separate from it. As Darwin himself pointed out, comparing the developmental stages of different organisms can yield clues about their evolutionary relationships, because many related species look very different from each other at the adult stage, yet possess very similar embryos or larval stages.374 In his 1864 book Fiir Darwin

(translated into English as Facts and Arguments for Darwin), Fritz Muller showed, for example, that although and crabs look very different as adults, they share a larval stage called a nauplius with each other and with several other animals, thus uniting them all as crustaceans.375 There is, therefore, important information about evolution to be found in the study of development. However, many biologists agreed (again following Darwin) 76 that the developing embryo, sheltered in its egg, cocoon, or womb, with its immediate physical necessities provided for, is subject to few (or no) direct pressures of selection. The form which the developing embryo takes is therefore not directly shaped by natural selection, or as Scott Gilbert put it, "in early development one saw form unencumbered by function."377

The study of development seems to suggest, then, that much of the similarity of form can be explained quite independently of considerations of function or selective history.

As we have seen, Darwin proposed that natural selection is the cause of form, by making the Unity of Type a mere historical consequence of adaptation to the Conditions of

Existence. This explanation may have seemed satisfactory at first, and indeed - as the study of evolutionary morphology only raised more questions than it answered, leading several of its practitioners to switch careers to genetics, and causing at least one to abandon science

374 Darwin, 358. 375 Fritz Muller, Facts and Arguments for Darwin. W.S. Dallas, trans. (London: John Murray, 1869), 13-15. 376 Darwin, 358: "the structure of the embryo not being closely related to its conditions of existence, except when the embryo becomes at any period of life active and has to provide for itself." 377 Scott F. Gilbert, "The morphogenesis of evolutionary developmental biology," International Journal of Developmental Biology vol. 47 (2003), 469. altogether - it became the standard answer immediately following the Modern Synthesis, an event from which embryology was conspicuously absent.379 This field has only recently emerged as a prominent sub-discipline of evolutionary biology, with the rise of evolutionary developmental biology, or evo-devo, beginning in the 1970s and 80s. Evo-devo is relevant to the present discussion because it has started to provide some intriguing answers to questions about form. The gradual accumulation of random genetic mutations may explain variation within populations, but for many biologists - including Gould - it does not seem a satisfactory explanation of how larger changes, such as phylum-level differences, could have arisen, nor - more importantly - why these differences have been conserved, as separate body plans, for the past 600 million years or more. Many of these biologists are turning to evo-devo in search of a more satisfactory explanation.

Brian K. Hall, himself one of the foremost scientists in the field, defines evo-devo as that discipline which seeks "to identify those developmental mechanisms that bring about evolutionary changes in the phenotypes of organisms." Hall traces the origins of this discipline to three important events of the 20th century: John Tyler Bonner's work (begun in mid-century) using slime molds to seek the origins of multicellularity; the 1977 publication of Gould's Ontogeny andPhytogeny, which "reminded" biologists of the importance of heterochrony or changes in the timing of developmental processes as a mechanism of evolutionary change, and the discovery of homeobox or Hox genes in the late 1970s and

Thomas Hunt Morgan was one such scientist who, fed up with the useless metaphysics of and lack of real progress in early 20th century embryology, shifted his focus instead to the exciting new science of genetics. (Amundson, The Changing Role of the Embryo in Evolutionary Thought, 169-170.) And Morgan's friend Hans Driesch, when faced with the perplexing question of how an organism "knows" to develop properly froma n egg, even in the face of major mechanical disturbances, turned to unscientific vitalism in desperation. (Jan Sapp, Genesis: The Evolution of Biology (Oxford: Oxford University Press, 2003), 110). 379 Sean B. Carroll, Endless Forms Most Beautiful: The New Science ofEvo-Devo and the Making of the Animal Kingdom (New York and London: W.W. Norton & Company, 2005), 7. 231 early 1980s.380 The homeobox is a "toolkit" composed of Hox genes which collectively control the formation and pattern of body regions and body parts with similar functions (but very different) designs. A homeotic mutation - mutation in a homeobox gene - causes a normal-looking body part to develop in an abnormal location. For example, a mutation in the

Drosophila Hox gene antennapedia causes a pair of legs to develop on the head, where the antennae are supposed to be.381 Such mutations suggest that the Hox genes are responsible for things like determining the location and development of major body regions. Biologists discovered, to their astonishment, that variations of this toolkit are found in most members of the animal kingdom - even across morphologically diverse phyla. Additionally, the relative positions of Hox genes within the homeobox (the sequence of DNA containing these toolkit genes) correspond to the relative positions of the body regions they affect. So, for example, the Hox genes which control the formation of head structures are found anteriorly. These

Hox genes are now understood as the developmental toolkits which construct and maintain body plans.382

Ironically, Hox gene studies suggest that Geoffroy might have been right in a sense when he proposed that the basic body plans of vertebrates and arthropods are homologous, albeit reversed (dorsal heart and ventral nerves in arthropods; ventral heart and dorsal nerves in vertebrates). Evo-devo studies have shown that the toolkit genes responsible for creating these structures are homologous between arthropods and vertebrates (and, indeed, among most other animal phyla as well). This means that there is a deep conservation of structure

380 Brian K. Hall, "Evo-devo: evolutionary developmental mechanisms," International Journal of Developmental Biology vol. 47 (2003), 491. 381 Sean B. Carroll, Jennifer K. Grenier, and Scott D. Weatherbee, From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design (Maiden: Blackwell Science, Inc., 2001), 15-47. 382 Hall, "Evo-devo: evolutionary developmental mechanisms," 247. 232

("deep homology") across the animal kingdom.383 Though the various phyla of bilateral animals appear to be highly morphologically diverse, they each share a genetic toolkit for producing a set of fundamental body patterns and structures, including bilateral symmetry, differentiation into anterior and posterior ends, and segmentation. There is a Unity of Type between arthropods and vertebrates after all. The discovery of this toolkit has exciting possibilities for our understanding of evolution.

For example, in 2005, Marc W. Kirschner and John C. Gerhart proposed a theory of

"facilitated phenotypic variation" made possible by the action of "conserved core processes."

Conserved core processes are things like metabolism, cellular signaling, sexual reproduction, and the developmental role of Hox genes, which are no longer mutating themselves (they are conserved), but which can be deployed at new intensities and/or in new combinations, to create evolutionary novelty.384 Regulatory changes causing the redeployment and recombination of these core processes in response to environmental stresses creates a range of phenotypes which can then be acted upon by natural selection. (The fact that the core processes are amenable to such redeployment and recombination is what facilitates the phenotypic variation.) The selection of particular phenotypes which respond well to those stresses reinforces the development of those phenotypes in future generations; in other words selection will act to ensure that genetic and developmental pathways will robustly produce the desirable phenotype.

This is quite similar to Mary Jane West-Eberhard's theory of phenotypic plasticity.385

Phenotypic plasticity refers to the capacity of organisms to alter their phenotypes in response

383 Gould, The Structure of Evolutionary Theory, 1106-1107. 384 Marc W. Kirschner and John C. Gerhart, The Plausibility of Life: Resolving Darwin's Dilemma (New Haven and London; Yale University Press, 2005), 39. 385 Mary Jane West-Eberhard, Developmental Plasticity and Evolution (Oxford: Oxford University Press, 2003). Online < http://simplelink.library.utoronto.ca/url.cfin/50034>, Accessed 3 July 2007. to environmental changes or stresses. For example, a light-skinned human who is exposed to large amounts of sunlight will produce greater-than-normal quantities of melanin, darkening the skin to provide protection from further exposure to the sun's rays.386 A more dramatic example is the formation of queen bees versus worker bees; both originate from the same larvae, but are given different food while developing, which causes them to develop very differently.387 This kind of phenotypic variation is not directly caused by genetic variation; the pale person's genes do not change with tanning, and the bee larvae do not possess "queen genes" versus "worker genes." The potential for change - the plasticity - is in the phenotype.

In a particular environment, West-Eberhard argued, genetically similar individuals will produce a range of phenotypes, some of which will be more advantageous than others, in that environment. Further, those more adaptive phenotypes may have been produced by several different developmental pathways, some of which will be more efficient than others at reliably producing that phenotype. Then, West-Eberhard argued, genetic accommodation will follow: "If the phenotypic variation is associated with variation in reproductive success, natural selection results; and to the degree that the variants acted upon by selection are genetically variable, selection will produce genetic accommodation."388 West-Eberhard's theory represents a significant break with traditional Darwinian theory, in which genetic variation arises, producing accompanying phenotypic variation, which is then selected. On the theory of phenotypic plasticity, the opposite occurs: phenotypic variation arises and is selected, leading to genetic modification.

386 Mary Jane West-Eberhard, "Phenotypic plasticity and the origins of diversity," Annual Review of Ecology and Systematics vol. 20 (1989): 249-278. 387 Kirschner and Gerhart, 89. 388 Mary Jane West-Eberhard, "Developmental plasticity and the origin of species differences," Proceedings of the National Academy of Sciences vol. 102, Supplement no. 1 (3 May 2005), 6544. 234

These theories address population-level changes, and perhaps speciation, but what does evo-devo have to say about the evolution of higher taxa? If all bilaterian animal phyla share virtually the same set of Hox genes, how did they acquire such enormously different body plans?

Kirschner and Gerhart refer to the developmental toolkit as the "compartment map," because it dictates the formation and specialization of different body regions, or compartments.389 This compartmentalization appears to be a key factor in the evolution of different body plans, because if the body is divided into several more or less autonomous compartments, one compartment can be modified without necessarily affecting other compartments. Carroll agrees that this has been an important innovation in the history of life. This strategy avoids Cuvier's problem of the correlation of parts: one part can be changed without destroying the harmony of the whole. It also explains serial homology.

The phenomenon of compartmentalization, along with duplication and specialization, is admirably illustrated by the tagmosis and appendage specialization of the arthropods

(discussed in Chapter 1). If an ambulatory creature only has a few pairs of legs (appendages of different compartments), they will probably all be needed for walking. But if the number of these legs is increased to more than the number strictly needed for walking (by duplicating the compartments and their appendages), some of the legs are now available for recruitment to other purposes. These legs can be modified to better suit these other purposes, without harm to the animal, which still has sufficient other legs to handle walking. The lobster - with several thoracic legs for walking, and several head appendages specialized for feeding - is an excellent example of this phenomenon at work. This phenomenon - compartmentalization followed by duplication and recruitment/modification for other purposes - is controlled by

389 Kirschner and Gerhart, 194. the Hox genes: by "deploying different Hox genes in different zones along the mam body axis."390 But this is not the end of the story; evolutionary developmental biologists have discovered that this same phenomenon has occurred in the Hox genes themselves, and may explain the origin of the different animal phyla.

As Kirschner and Gerhart explain, the compartment map or genetic toolkit is not just shared within members of a single phylum, but is shared across different phyla as well. The

Urbilateria, or hypothetical ancestor of all bilaterally symmetrical animal phyla, is thought to have had a compartment map of its own, which it passed on to all of its descendant phyla.391

The compartment map of one animal phylum is not precisely identical to another; the particular identity and number of Hox genes within the compartment maps of different animal phyla can and do differ. But these maps are extraordinarily similar to one another

(for example, they contain several homologous Hox genes), and each phylum has conserved its map over several millenia. And the creation of these compartments is key to creating morphological disparity, according to Kirschner and Gerhart; each compartment is a somewhat autonomous module, which can itself be modified without greatly affecting neighbouring modules. As Kirschner and Gerhart put it, "the many compartments of the body plan... can accommodate a great range of future anatomies developed in parallel."392 In this modularity there is great capacity for change.

If Carroll, Kirschner and Gerhard, and Gould are correct, new animal body plans arose early in the history of life as variations upon the compartment map of the Urbilateria.

These variations took the form of eliminations, or duplications (followed by co-optations) of particular Hox sequences within the overall homeodomain or compartment map, and were

390 Carroll, Endless Forms Most Beautiful, 154. 391 Kirschner and Gerhart, 197. 392 Kirschner and Gerhart, 203. 236 relatively easy to produce early in the history of life, before too much developmental

"baggage" had become associated with each compartment. These changes allowed each new phylum to radically restructure the basic bilaterian body plan. But why are these changes no longer occurring? Why don't new phyla arise, from further variations upon the compartment map of any existing phylum?

Kirschner and Gerhart attribute this phenomenon to a constraint created by the directionality of history. Briefly, when the different animal phyla originally arose, they were all at the same "stage," in terms of evolutionary adaptation. In the Cambrian, these phyla began to evolve "adornments," adding things like limbs, armor, and jaws with teeth to their basic bilaterian body plan. If any new variant on the fundamental bilaterian body plan - lacking such things as appendages, a protective outer covering, and jaws - arose at that time, it would have been swiftly outcompeted by members of well-established body plans. As

Kirschner and Gerhart explained, "by the Cambrian, the locus of battle had shifted from who could make the best body plan to who could make the best jaw and appendage on an adequate body plan." This argument is even more apt today: if any new unadorned body plan were able to evolve now, it would be completely vulnerable to competition and by modern organisms. But of course, a new variant could only arise from pre­ existing variants, so it would be impossible for an unadorned from-scratch bilaterian to evolve today; instead it would inherit whatever modifications had been made by the group it evolved from. Thus, any new variant that arose now, from an already-existing phylum, would inherit the evolutionary adaptations of that phylum - its limbs, its skeleton, its feeding apparatus, and so on. And of course, if such a variant, retaining all those features, did arise,

Kirschner and Gerhart, 69. 237 we would not classify it as a new phylum; we would place it within the phylum from whence it came, and with which it shares so many diagnostic features.

Additionally, according to Gould (and borrowing from the theories of Schmalhausen,

Waddington, and West-Eberhard), once each successful body plan arose, it would have congealed or stabilized: selection would have acted to preserve those genotypes which could most reliably and robustly preserve the basic body plan. Once this canalization had taken place and the body plan had become much more specialized, routinized, or dedicated to its

"chosen" role, any large genetic or developmental perturbations would tend to be detrimental much more often than they might be beneficial, so further (successful) modifications would be on a much smaller scale - mere "iterations upon a few basic anatomical designs," in

Gould's words.394

As we have seen, recent developments in evo-devo seem to provide support for

Gould's ideas about the origin and nature of phyla and body plans, and his structuralist theory of evolution, which go hand-in-hand with his interpretation of the Burgess Shale. As I mentioned in Chapter 3, in Wonderful Life Gould did not just describe the Cambridge team's work on the Burgess Shale fossils, but used it as a platform for his own theory of the tempo and mode of evolution. The Burgess Shale was important to Gould because he saw it as a reflection, justification, and instantiation of his grand theory of evolution. According to

Gould, this unique and stunning record of exquisitely preserved species from the dawn of animal history demonstrated at once the absolute necessity of the fossil record to evolutionary biology, the punctuational nature of evolution, the development and entrenchment of the modern animal body plans (and many others as well), the significance of contingency, the pattern of morphological disparity and occupation of morphospace, and the

394 Gould, Wonderful Life, 47. 238 establishment and importance of fundamental morphological structure, as against adaptationism. This is the theory that Gould applied to, and saw as supported by, the

Burgess Shale fossils. But how have others interpreted the significance of the Burgess Shale for the origin and nature of phyla and body plans?

Gould vs. Conway Morris: The New Structuralism vs. Adaptationism Debate

As we saw in chapter 4, for Conway Morris, the most important factors in shaping evolution come from outside the organism: the environment constrains the evolution of life.

There may be a vast number of genetic possibilities, but the pressures of the environment, both biological and physicochemical, only allow a finite set of basic solutions, and life will navigate to these adaptive solutions despite random extinctions of particular groups. Thus, the occupation of morphospace should not decrease over time, but either increase or (once maximum occupation has been reached) remain more or less steady. For Gould, on the other hand, the most important factors in shaping evolution come from within the organism: any morphology possible within life's genetic and developmental array is initially permitted, therefore maximal occupation of morphospace will occur early in the history of life.

However, once a lineage has become developmentally committed to its "chosen" body plan, phylum-level changes will never recur in that group, and any extinctions will therefore reduce overall morphological disparity:

[I]f- as I claim for the Burgess and later history of arthropods, and for life in general — Bauplane congeal and stabilize, with most eventually decimated and few surviving, then the argument that early oddballs are intermediates, and that weeding has not limited the total range of morphospace (but only thinned it from within) almost surely cannot hold.... Almost surely, some peripheries will be abandoned, leaving numerous outsiders among early forms, and leading to an ultimate and marked reduction of early disparity.395

395 Gould, "The disparity of the Burgess Shale arthropod fauna," 419. 239

On Gould's theory, a phylum is a taxon defined by its body plan, and a body plan has a special biological reality, as a form or type actively maintained or stabilized by developmental canalization. Conway Morris, on the other hand, holds a much more pragmatic view of phyla and body plans. Perhaps the baldest published statement of his thoughts on phyla can be found in the glossary of his 1998 book The Crucible of Creation:

phylum: A major grouping in a scheme of biological classification, ranking next below a kingdom. Commonly included in the concept of a phylum is the notion of the body plan, with the implication that all component species are descended from a single remote ancestral form. In reality, a phylum is little more than a statement of taxonomic ignorance, and its wider relationships to other phyla is usually a matter of controversy. About 35 living phyla are recognized. They include such examples as the annelids, arthropods, brachiopods, cnidarians, and molluscs.396

For Conway Morris, a phylum is simply a collection of species. These species all share a basic architecture to be sure, but for Conway Morris it is the species which evolve first, and share a body plan solely by virtue of their evolution from a common ancestor. And this body plan, for Conway Morris, is not achieved in a single evolutionary leap and then stabilized, allowing only comparatively trivial future modification, but rather established in completely the opposite way: by starting as merely species-level differences, which then grow greater over vast amounts of time. Species evolve first and only, becoming more morphological divergent over time; and once these differences become great enough - and especially if we cannot tell what the closest relatives of these divergent groups are - we call them different phyla. But this is a taxonomic judgment we apply in retrospect, not a fundamental division imposed by nature at the moment of these groups' inception. "In the lowest Cambrian,"

Conway Morris explained, "two phyla were separated by as little as two species... "things we call phyla today were separated by a handful of species at that stage; the common

396 Conway Morris, The Crucible of Creation, xx. 240 ancestor of a brachiopod and an annelid looked nothing like a brachiopod or an annelid."397

Instead, the body plans now so fundamental to the brachiopod and annelid lineages were built up slowly, over time. Conway Morris is a true Darwinian, for whom Unity of Type is nothing more than a historical consequence of adaptation to the Conditions of Existence.

And what about the question of why most or all of the animal phyla arose rapidly (in the event known as the Cambrian explosion), and none have arisen since? If Gould is right, no new phyla have arisen since the Cambrian explosion because of a historical directionality built into the workings of evolution. He insisted that he proposed no unique mechanisms, but that "the Cambrian [was] a time of unique flexibility, before definite patterns of growth from egg to adult became so locked into the embryology of complex organisms that fundamental reconstructions became nearly impossible."398 As we have seen, the growing field of evo- devo may lend support to this hypothesis. Gould's belief in this time of unique flexibility, followed by canalization, commits him to a belief that times of radiation are qualitatively different from times of non-radiation. As one might imagine, this commitment ties in well with his theory of punctuated equilibrium, which holds that speciation occurs in geologically rapid bursts, while stasis of form is actively maintained (through stabilizing selection, or developmental entrenchment, or both) at other times.

Conway Morris's view of evolution also seems reasonable, however. For Conway

Morris, there is nothing different about radiations versus non-radiations, nor is there anything unusual about the evolution of phyla as compared to the evolution of species. It is all the same process, the only difference being that the founders of what we now call phyla separated long before we could observe them doing so, and so long ago that their descendants

Conway Morris, Interview 10 January 2007. Gould, "Showdown on the Burgess Shale: the reply," 52. 241 are now different enough from each other to be ranked as different phyla. And because the origin of phyla is really just the origin of species writ large, Conway Morris sees the same changes occurring throughout the fossil record - it is not, after all, a phenomenon confined to the Early Cambrian. It is only the present-centered bias built into our systems of classification that makes it seem so. "You can see the equivalent of phylum-level jumps after the Cambrian," Conway Morris asserted; "take for example the origin of bats. That's just as big a jump, but we don't call it a phylum-level jump just because we know where it came from. As soon as you know where it [the new body plan] came from, it's not a phylum."399

James Valentine would appear to share this pragmatic view of the nature of phyla:

One suggestion has been that the lack of new phyla after the Cambrian is entirely an artifact of the tree of life; that as the main branches have themselves branched, the many features that characterized the main branches are naturally inherited by the new branches, which we therefore simply define as classes, or as some subsidiary taxa, rather than as new phyla. There is certainly an argument to be made as to how distinctive bodyplans must be to qualify as phyla. The phyla were not recognized because they had all evolved at an early date (which wasn't known), however, but because of their morphological differences - the judgments were not made with reference to the tree of life, but with reference to bioarchitectural disparities.... When it is discovered that a group accorded phylum status has in fact evolved as a branch of an existing phylum... that group is commonly assigned a subsidiary status within the parent phylum.400

Conway Morris and Valentine, then, are classic Darwinists, for whom macroevolution is merely and entirely the long-term extrapolation of microevolution. For

Gould, however, there are macroevolutionary events that are qualitatively different from the events of microevolution, and it is these macroevolutionary events which are required to explain the origin of higher taxa. The mere extrapolation of microevolutionary events is not sufficient to explain these phenomena. There is a sense in which, for a structuralist like

Conway Morris, Interview 10 January 2007. Valentine, On the Origin of Phyla, 461. 242

Gould, there are two separate questions to ask about the diversity of organic form: 1) how does one explain the diversity of form within a single phylum, and 2) how does one explain what differentiates one phylum from another? For a functionalist like Conway Morris, the two questions have the same answer (the answer that Darwin gave in the Origin of Species): both are the result of the gradual accumulation of adaptive responses to changing environmental conditions. We recognize different phyla the same way we recognize different species; the only difference is that the phyla diverged so long ago that they have become much more different from each other than have the groups within each phylum.

For Gould, however, there are different answers to these questions, because they refer to qualitatively different levels of evolution. His theory of punctuated equilibrium explains how speciation, and differentiation within species, occurs, and the fossil record in general seems to support this theory. A different theory of evolution is required to explain the origin of phyla, and this theory, Gould believed, was illustrated by the fossils of the Burgess Shale.

Evolutionary developmental biologist Brian Hall agreed with Gould; Hall wrote:

The existence and long-term persistence ofBauplcine and constraints that favor changes in adaptive modifications beyond the level of the Bauplane lead [sic] me to the notion of two fundamental levels of change and of differing relative roles of constraint and selection of each level. The two were generation of the Bauplan and adaptive modification of form and function.401

Darwinian adaptive modification does explain the slow accumulation of change within species, and even the diversification of species within a body plan. But where does the body plan come from? On Gould's theory, the fundamental body plan of the phylum evolves first, in an evolutionary leap quantitatively if not qualitatively different from the usual evolution by natural selection (one might almost imagine a new body plan springing fully formed like Athena from Zeus's forehead), and any further change within that phylum

401 Hall, "'Bauplane, phylotypic stages, and constraint," 237. 243 consists of "generating endless variants upon a few surviving models."402 For Gould, body plans have some sort of deep physical reality, and priority - they were created first, then diversification of species followed. A phylum is a body plan, and a body plan is not just a collection or suite of characters, it's an actively stabilized blueprint: one phylum is different from another phylum not just because they ended up looking different over time, but because they actively work at staying different.

Members of different phyla each conservatively reproduce their own body plan, and they each have different developmental and genetic tools to draw on in making minor variations on that plan. Two different phyla can't converge on the same body plan because they don't have same tools for making bodies. Likewise, "convergence" within a phylum isn't actually convergence; it is merely examples of related organisms using the same tools to do the same thing. This is why Gould scoffs at global morphospace models: he doesn't believe two truly different groups can ever really get to the same place. Any groups that are in the same place can both get there because they are related (and therefore really the same group, in the way that counts for Gould - meaning the same phylum); any groups that are not related in this special way can't really both get to the same place (and Gould may be right about this; Conway Morris's 2003 book is one long list of convergences, but only one or two of his examples involve convergence by members of different phyla).403

In the early work of the Cambridge team on the Burgess Shale, Gould saw a shining example of every tenet of his own evolutionary theory. Gould wrote Wonderful Life not just to tell the story of these unusual and important fossils, but to present his theory of evolution, which for him was embodied in and exemplified by the weird wonders of the Burgess Shale.

402 Gould, Wonderful Life, 47. 403 Conway Morris, Life's Solution: one example of inter-phyletic convergence would be the camera eyes of vertebrates and molluscs, discussed on p. 151. 244

Gould was fully convinced of the importance of the Cambridge team's work and the conclusions (he believed) it supported; Gould wrote: "I regard this reinterpretation of the

Burgess Shale as the most important paleontological conclusion of my lifetime."404

But the Burgess Shale has been reinterpreted again. The new goal which defines the third phase of Burgess Shale research is not to lump Cambrian animals into modern phyla as in Phase 1, nor to create new and unrelated phyla for problematic taxa, as in Phase 2. Rather, as Conway Morris argues, it is to elucidate the steps by which these modern groups were formed: "[T]he argument, I think, has shifted comprehensively to the view that we are seeing the way in which the body plans are assembled." What the Burgess Shale does, when interpreted in this way, is inform biologists about the assembly of body plans - about the way the modern animal phyla were created, not in sudden dramatic leaps, but by the gradual acquisition of different characters among groups which began their existence as merely two different species that "parted company one day on the seafloor."405 This gradual transformation, according to the ubiquitous pressures of natural selection, is the core of

Conway Morris's theory of evolution, and his definition of a phylum. As we have seen,

Gould's theory involves the rapid, early acquisition of a body plan, which is then actively stabilized through later diversification within the phylum. How do Briggs and Budd define phyla?

Stephen J. Gould, "In touch with Walcott," in Eight Little Piggies: Reflections in Natural History. 220-237 few York: W.W. Norton & Company, 1993), 225. Conway Morris, Interview 10 January 2007. Briggs, Fortey, andBudd: Stem Groups, Phyla, and Body Plans

To put the contribution of cladistics and the stem group concept in context, I return to a topic discussed briefly in Chapter 1 - Yochelson's commentary on the use of the incertae sedis concept. Yochelson stated:

The classification of some fossil groups that are not easily assigned to a high- level hierarchical group on the basis of living organisms has gone through a three-stage evolution. First, dissatisfaction is expressed with the then-current placement, which may lead to specimens being placed as incertae sedis for some time. Finally, as additional information accumulates a new category may be proposed for the organism.406

This same commentary presents the two solutions Yochelson perceives to the problem of classifying unusual fossils. The first solution is the old unsatisfactory "shoehorn," as it was called by Gould: forcing the extinct group into a modern phylum within which it does not really fit. This solution was the only one readily available to early 20*-century paleontologists committed to a directionalist evolution. The second solution, which

Yochelson proposed in this paper, is to erect a new higher taxon for the problematic fossil

(after a suitable waiting period in the purgatory of incertae sedis). This is the solution that characterized Phase 2.

There is a third solution to this dilemma, which Yochelson and other paleontologists of his day did not recognize, and which some later paleontologists, like Gould, did not agree with. This third solution is the legacy of cladistics and the stem group concept, brought to the Burgess Shale by Briggs (working with Fortey) and Budd respectively, and it is simply this: perhaps these problematic fossil groups, possessing some similarities to modern phyla but also several bizarre and unique characters, belong neither within the modern phyla as we know them, nor within newly-erected extinct phyla, but instead represent ancient relatives of,

406 Yochelson, "Agmata, a proposed extinct phylum of early Cambrian age," 438. 246 and intermediates between, the modern phyla. This realization is revolutionary, for it requires either that our fundamental taxonomic categories be redefined, or that, in a sense, these fossil groups be regarded as outside the traditional Linnean hierarchy. Either phyla are not what we thought they were, or these fossils belong in no phylum at all. When the

Cambridge team began their work on the Burgess Shale, they saw only the dichotomy of solutions offered by Yochelson, and, in desperation, chose the second. In more recent years, cladistics and the related stem group concept have offered a third possibility.

As discussed in Chapter 2, the crown group is more or less equivalent in scope to the traditional phylum, as a group (based primarily on extant organisms, and certainly with many living representatives) sharing a body plan. On the cladistic method a phylum is now recognized as a group possessing a suite of shared derived characters, the totality of which is unique to that phylum (crown group). So far, none of this seems new - the traditional phylum has simply been renamed the crown group. But it is important to recognize that the criterion of phylum membership has changed: the old definition was morphological; the new definition is phylogenetic. As Briggs and Fortey noted in 2005, "Gould's (1989) thesis on the Cambrian radiation was based around the concept of phyla or body plans. The focus on phyla has shifted from considering them as a measure of morphological separation to attempting to understand their relationships,"407 This shift in the membership definition of the phylum has led to a radical new understanding of what does and does not belong in it.

What is also new is the realization that these modern crown group phyla cannot accommodate all life that has existed on Earth. It is this novel insight, more than anything else, which justifies the claim that a new phase of Burgess Shale studies has begun. In Phase

1, Walcott tried to force Cambrian fossils into modern crown groups. In Phase 2, Gould

407 Briggs and Fortey, "Wonderful strife," 98. 247 argued that new crown groups needed to be established to classify these problematic fossils.

Both of these solutions privilege crown groups as representing or containing the sum total of evolution and its products. Both strategies can be seen as a failure to appreciate the modern- centric bias of our classification system and the methodological difficulties resulting from that bias. The stem group concept appears to provide a solution to this problem.

The stem group concept, introduced to paleontology by Richard Jefferies (1979, based on Hennig 1966), and brought to the Burgess Shale by Graham Budd, has revolutionized the very meaning of the word "phylum" and provided a new way of understanding the relationships between fossil and extant organisms.408 (See Figure 17, p.

93.) On Budd's view, if the crown group is equated with the phylum as it is usually understood, then it is a group sharing a suite of shared derived characters, delimited by the last common ancestor of all living forms in the group. Budd's chief insight is the fact that this phylum is nothing more than the tip of the iceberg: in order for this crown group phylum to exist today, there must in the past have been a "pre-phyletic" evolutionary sequence in which these diagnostic features arose in a stepwise fashion. This evolutionary sequence is the stem group, and it is composed of extinct taxa which will probably appear very strange to modern eyes, as they will each possess some, but not all, of the features characteristic of the phylum, as well as their own unique characters not shared with their modern relatives. Budd argues that Gould's grab-bag of morphological features, the seemingly random mix of familiar and unfamiliar characters which Gould thought could not be accommodated except by the creation of entirely new phyla, is in fact exactly what we should expect to see in the

408 See especially Budd and Jensen, Graham E. Budd, "Tardigrades as 'stem-group arthropods': evidence from the Cambrian fauna," Zoologischer Anzeiger vol. 240 (2001): 265-279, and Budd "The Cambrian fossil record and the origin of the phyla." stems leading up to and connecting our now distantly separated and clearly defined modern phyla. Budd wrote:

Extant monophyletic groupings are always morphologically distinct from their extant sister-group, and that distinctness is brought about by subsequent extinction of the lineages (plus its offshoots) that led to each of them, away from their last common ancestor.... These now extinct basal taxa... would have accumulated their own autapomorphies not possessed by the extant taxa. As a result, these basal fossil taxa are bound to differ from the extant clades: they will not be diagnosable as members of those clades; and they will show a confusing mixture of some but not all features of those clades, together with a set of features absent from them."409

And this, as Budd reminds us, is exactly what the Cambridge team did find in the Burgess

Shale, and which puzzled them so mightily at first.

Briggs and Fortey disagree with Budd over the precise definition of the phylum; instead of restricting it to the extant crown group, they prefer to designate the total group

(crown plus stem) as the phylum. There are advantages and disadvantages to both definitions. Budd's method makes it easy to distinguish one phylum from the next, as his phyla are more recent crown groups, each with a fully-developed suite of autapomorphies distinct from any other, but on this definition the crown node or last common ancestor of the phylum ends up being very arbitrarily defined. If there are any "living fossils" in the group, they will pull the origin of the crown group much farther back in time than would be the case otherwise, whereas extinctions of such group will push the base of the crown group forward in time. As Briggs and Fortey point out, "There seems something very arbitrary about defining a major group on a whim of history." Also, I suspect that Gould, were he around, would object that Budd's system, because it requires that there are no extinct phyla by

Budd, "The Cambrian fossil record and the origin of the phyla," 158. Briggs and Fortey, "Wonderful strife," 99. 249 definition, artificially reduces early disparity and inflates later disparity, creating the very

"cone of increasing diversity" against which Gould spent much of Wonderful Life railing.

Briggs and Fortey's total group definition, on the other hand, avoids the problem of identifying the bases of phyla according to the vagaries of history, but encounters its own problem in distinguishing these phyla from each other, since at their bases they will be separated by only two species, likely differing from each other by only a single derived character. Though these lines can be drawn in principle, they will probably prove very hard to draw in practice. There will be no unique suite of autapomorphies which all members of one phylum, and no members of other phyla, possess. Adopting this definition would require a substantial rethinking, to say the least, of the traditional phylum concept and its equivalence to the possession of a distinct body plan. Another advantage of the total group definition, however, is that it allows one to place every species - including every fossil species - in a phylum. There are no pre-phyletic taxa, as on Budd's definition. Whichever definition of the phylum one uses - Budd's crown group or Briggs and Fortey's total group - however, both definitions recognize the Burgess fossils as stem group relatives of modern animals, and reflect the new understanding, diagnostic of Phase 3, that Cambrian animals can be classified with living ones, but that a new classification scheme has had to be constructed to accommodate the full history of life.

Both definitions also take a very pragmatic view of phyla and body plans, as suites of characters acquired piecemeal, over extended periods of time. The reason one phylum is very different morphologically from another phylum has nothing to do with some special mechanism of evolution, or historical feature of genetics, that allowed different body plans to arise rapidly, and then congeal or become entrenched; phyla only look very different from each other today because all intermediates between them are extinct. It is that extinction of stem lineages, and no special conservation of body plans, that allows the very recognition of crown groups. Conway Morris agrees:

[Phylogenetic analysis] tells me the way evolution works. It tells me about stem groups, it tells me about how you have the assembly of characters, and I think part of our misunderstanding with some of our colleagues elsewhere... ironically, I think still retain an extraordinarily essentialist view of what a phylum is. So they say 'this is an annelid' or 'this is a mollusc,' to take this particular argument we're having at the moment. Whereas, of course, you know, probably in the lowest Cambrian, the molluscs and the annelids were separated by two species which looked almost identical... But zoologists aren't, in my experience, so ready to deal with what have been thought to be these so-called problematic phyla, which I think is in part why Gould's book made the impact it did.411

Conclusion: How Many Phyla are in the Burgess Shale?

The most hotly contested question between Phase 2 and Phase 3 has been the following: "How many phyla are there in the Burgess Shale?" As we have seen in this chapter (and in the thesis as a whole), the answer to this question seems to depend on how one does the counting. After exploring the thoughts and theories of Gould, Conway Morris,

Briggs and Fortey, and Budd, it is apparent that there are three distinct phylum concepts in play in these debates. First, there is the cladistic, stem versus crown group concept, which is a strictly formal notion driven by a particular systematic theory; this view is held by Briggs and Fortey, and Budd. Second, there is the retrospective or historical definition, held by

Conway Morris, in which phyla are nothing more than the consequences of a long accumulation of gradual differences. Third, there is Gould's essentialist notion, where a phylum is a body plan and a body plan is some sort of significant unit of phenotypic control, which constrains the amount of viable variation that can occur within the body plan.

411 Conway Morris, Interview 10 January 2007. 251

For Briggs, Fortey, and Budd, a phylum is a phylogenetic lineage, defined according to strict cladistic methodology. For them, the introduction of cladistics and the stem group concept have brought the number of Burgess phyla in line with the number of modern phyla.

Any questions about the evolutionary significance of body plans are entirely decoupled from this formal phylum concept. For Conway Morris, there is a sense in which the phylum does not matter: it is not a group with any more important biological reality than any other taxon.

In that sense his definition, as well as the cladistic one, is pragmatic. What most interests

Conway Morris is the step-by-step acquisition of the biological characters which cumulatively (but not essentially) define the major animal groups. For Gould, however, the definition of the phylum is not mere pragmatism. It is rather of critical importance, because for him, a phylum is equivalent to a body plan, and the origin, number, nature, and fate of different body plans are, in Gould's opinion, the most interesting and important questions to ask about the Burgess Shale, and about evolution in general.

Perhaps, then, one reason the number of phyla in, and the significance of, the Burgess

Shale has remained such a contested topic is that coming to a consensus has not just involved a straightforward tallying of numbers, but a fundamental disagreement over what counts as a phylum, and why. Perhaps oddly, given the many other topics of dispute, all the players in this debate seem to agree that one counts morphological diversity by counting phyla. But, as we have seen, this act of counting is not so simple. The number one comes up with depends on how one defines phyla, and one's definition of phyla is deeply conditioned by one's theoretical stance on the tempo and mode of evolution, one's position in the debate between adaptationism and structuralism, and one's choice of classification methods. Depending on 252 all these factors, the answer to the seemingly simple question of how many phyla are found in the Burgess Shale turns out to be very complex. Chapter 6 Conclusion: The "Battle" for the Burgess Shale

"Fossils provide just enough data to fuel a debate but not enough to resolve it."412

"It becomes clear that there has been a battle underway to monopolize the Cambrian explosion and impose a story that fits a triumphant set of preconceived notions. So who owns the Burgess Shale now?"413

As we have seen in this thesis, the classification and interpretation of the Burgess

Shale fossils has gone through three distinct and radically different phases, since their discovery in 1909. In the first phase, they were perceived as primitive members of modern groups, and all placed within known phyla and classes of animals. This phase is represented by Charles Doolittle Walcott's discovery of and preliminary publications on this fossil fauna.

In the second phase, the same fossils were thought to be bizarre members of unique phyla and classes, representing a huge radiation of morphologies unrelated to the body plans of the modern animals. Harry Whittington, Derek Briggs, and Simon Conway Morris all held this view in the late 1970s and early 1980s, but it is most often associated with Stephen Jay

Gould, who used this interpretation of the Burgess Shale to argue for a highly contingent view of evolution in which many representatives of an initially vast pool of body plans went extinct, leaving a much smaller group of randomly-selected survivors as the players in the subsequent history of life. In the third phase, the Burgess fossils are now seen as stem lineages, each occupying an ancient branch leading to one or several of the modern phyla.

Both Conway Morris and Briggs now hold this view, as does Conway Morris's former student Graham Budd.

412 Berry, "Wonderful crucible," 1529. 413 Levinton, 204.

253 These changing classifications were triggered by corresponding changes in available fossil data, theories about arthropod relationships, and methods of biological systematics.

The work of the Cambridge team in Phase 2 was the first detailed examination of the Burgess

Shale fossils, and took place at a time when arthropods, the most abundant organisms in the fossil record and in the modern world, were thought to represent several different phyla which had each achieved arthropodization independently. This polyphyletic view, and the phylogenetic lawn it implied, generated an atmosphere conducive to receiving an interpretation of the Burgess fossils as representatives of multiple phyla, not closely related to each other or to modern animals, as discussed in Chapters 1 and 5. The shift to the third phase corresponded with (and at least partly resulted from) the demise of this polyphyletic view. Another major cause, for Conway Morris in particular, was the influx of new specimens from the Burgess Shale and from other Cambrian sites, notably the Sirius Passet and Chengjiang faunas. These events were the focus of Chapter 3. A final factor leading to the shift to the third phase was the adoption of cladistic methods of classification, and the related stem group concept. Briggs's introduction of cladistics to Burgess Shale studies, and

Budd's work on stem groups, were discussed primarily in Chapters 2 and 5.

Most importantly, however, the different interpretations of the Burgess Shale have also depended on the theoretical commitments held by the scientists in question, with the result that each scientist's understanding of the Burgess Shale has tended to reflect his prior notions about the tempo and mode of evolution. The evolutionary theories of Gould and

Conway Morris can be brought into stark contrast by comparing their different beliefs about the nature, occupation, and navigation of morphospace or adaptive landscapes, as we saw in

Chapter 4. For Gould, morphospace is shaped by organisms by the process of their own 255 evolution, as different body plans arise and then become developmentally canalized. In

Gould's theory, each phylum robustly maintains its own body plan, tied to its own adaptive peak. This means that - except during the one-time only period of extraordinary genetic and developmental lability that occurred very early in animal evolution - convergence between one phylum and another (moving from one peak to another) does not take place, and

"convergence" within phyla is not convergence at all, but the similar deployment of the same developmental resources. For Conway Morris, by contrast, morphospace takes its shape from the universal challenges created by the physical laws of the universe. There is only a limited number of successful adaptive solutions to these challenges, and in Conway Morris's scheme, organisms of very different phylogenetic histories can and must converge on these few occupiable regions of morphospace, if they are to survive.

The different morphospace models of Gould and Conway Morris point to another way to dichotomize their views. As we saw in Chapters 4 and 5, Gould was a structuralist, arguing that the origin of developmental constraints (and their active stabilization of different body plans) was the major driving force in the creation of different phyla - a macroevolutionary phenomenon qualitatively distinct from microevolution. Conway Morris is an adaptationist, and argues that all evolution, from the population to the phylum level, has consisted of the repeated, convergent discovery of a limited number of functional solutions to a universal set of adaptive problems posed by the environment.

A commitment to these different beliefs - and to very disparate concepts of the tempo and mode of evolution - has led Gould and Conway Morris to very different perceptions about the number and significance of phyla in the Burgess Shale, as we saw in Chapter 5.

For Gould, a phylum corresponds to a body plan, where a body plan is an important and 256

qualitatively distinct unit of biological reality, rapidly and actively created and then stabilized by developmental entrenchment. This concept of phyla and the origin of body plans

dovetails nicely with Gould's general theory of evolution as punctuational, in which brief and rapid radiations divide long periods of stasis (stasis created by the active stabilization of phenotypes.)

Conway Morris's definition of a phylum, on the other hand, is very similar to that originally proposed by Darwin: a phylum is a mere historical consequence of the gradual accumulation of variation over geological time. And like Darwin, Conway Morris is a phyletic gradualist, for whom the divisions between taxa are arbitrary breaks in a steady continuum of slowly changing biological form. A third perspective is seen in the work of

Briggs, Fortey, and Budd, who have adopted the phylum definition prescribed by their commitment to cladistic methodology. For these men, a phylum is a formal phylogenetic concept, in a sense decoupled from questions of morphological uniqueness. Their work has elucidated the sequence of origin of various morphological characters, and the variation in morphological disparity through time.

Gould's claim that the Burgess Shale contained representatives of twenty new arthropod classes and fifteen to twenty new phyla is "not taken seriously today," according to

Briggs and Fortey. They, along with Conway Morris, Budd, and Jean-Bernard Caron, have been instrumental in constructing a new classification "from the bottom up," which can accommodate both modern animals and Cambrian fossil taxa.414 Though Budd and Briggs disagree about where precisely to draw the line between different phyla, they agree that the former oddballs of the Burgess Shale have a place on the phylogenetic tree of modern organisms: as stem lineages leading up to the modern crown groups.

414 Briggs and Fortey, "Wonderful strife," 95,96. 257

Finally, Briggs, Fortey, Budd, and Conway Morris all share a conviction that the

Burgess Shale fossils and other Cambrian taxa demonstrate the step-by-step acquisition of

the synapomorphies that define the modern crown groups. In this conviction they oppose

Gould, for whom phyla are not put together piece by piece, species by species, but instead

originated in a rapid burst of evolution very early in the history of life, and whose body plans were then congealed through developmental entrenchment.

It seems at first glance, then, that the Phase 3 interpretation has triumphed over the

Phase 2 view. Indeed, Gould's "weird wonders" interpretation has been called not just mistaken, but scientifically sterile. In a review of Gould's Wonderful Life, Fortey wrote:

"Sorting out such complex questions [as which characters are shared by Burgess arthropods] provides more constructive insights into the classification of these arthropods than simply

saying 'Gee isn't that weird - it must be a new class!'" In Fortey's opinion, this "gee whiz"

sort of approach, unlike cladistic analysis, may be exciting but doesn't leave one with any workable hypotheses for understanding animal relationships and the history of life.415 Budd agreed, noting that if you accept Gould's Phase 2 view, "There is nothing else to say apart from 'there are all these weird groups.' It's sensational, but it's also very sterile. It doesn't lead anywhere." By contrast, the Phase 3 interpretation, according to Budd, may prove to be wrong, but at least allows scientists to formulate hypotheses about the relationships among

Burgess fossils, and between them and modern animals. Budd continues, "We might as well take this view [Phase 3] even if it's wrong in the end, because it's progressive. It allows you to ask questions and formulate hypotheses and to generally use fossils" (something that many biologists, in Budd's opinion, are sadly loath to do).416

Fortey, "The collection connection," 303. Budd, Interview 12 May 2006. 258

It is true that exciting progress in animal classification, particularly of the arthropods, has been made in Phase 3. But has this progress come at the expense of other fruitful avenues of inquiry? And does it prove Gould's theory of evolution wrong? As I have shown in this dissertation, the shift to Phase 3 - particularly the adoption of cladistic methodologies

- has changed the questions which biologists and paleontologists can ask. The new focus on shared derived characters has lessened the import of the bizarre, unique characters possessed by many Burgess taxa. But even if their role in systematics has been erased, these bizarre characters have not disappeared. They still exist and sense must be made of them.

Briggs, Fortey, and their student Matthew Wills have demonstrated that Cambrian morphological disparity was not significantly greater than that displayed by modern animals, as Gould claimed. However, their work also shows that Cambrian disparity was approximately equal to modern disparity, not significantly less, as was traditionally believed.

Gould's claims about morphological disparity thus appear to be partially vindicated. Further vindication for Gould's theory of macromutation has come from the renaissance of evolutionary embryology. Recent work in evolutionary developmental biology, particularly the discovery of a genetic toolkit or compartment map shared by all bilateral animal phyla, lends support to Gould's ideas about the origin of body plans.

But this work, like the understanding of the Burgess Shale, is open to interpretation according to different theories. Gould saw the existence of a highly conserved genetic toolkit as the ultimate evidence for contingency in evolution: if life had started with a different toolkit, the history of evolution would have been vastly different. Conway Morris, however, sees it as evidence of his own theory of adaptive convergence: members of different phyla 259

are able to converge repeatedly on the limited number of good design solutions because they

all possess the tools to do so.

As the various examples and debates explored in this thesis show, there has been a battle underway to appropriate the fossils of the Burgess Shale and assign them their place in the history of life. The evaluation of their significance has not been solely determined by the

scientific evidence in hand, but has been made according to the preconceived notions of parties with vested theoretical interests in the outcome. As evolutionary biologist Andrew

Berry aptly noted: "Fossils provide just enough data to fuel a debate but not enough to resolve it." With that in mind, it is appropriate to ask, as paleobiologist Jeffery Levinton has done, "Who owns the Burgess Shale?" An examination of the theories and motivations underlying the debate over this ownership has made a fascinating case study in the history and philosophy of science. Bibliography

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Briggs, Derek E.G. Unpublished notes for a presentation at the 1979 meeting of the Paleontological Society entitled "A short course on arthropods," part of the Geological Society of America Meeting in San Diego. Non-archived personal notes in possession of Derek Briggs, Yale University, 1979.

Briggs, Derek E.G. Unpublished notes for a talk given at the Second International Symposium on the Cambrian System, Golden, Colorado, 9-13 August, 1981. Non-archived personal notes in possession of Derek Briggs, Yale University, 1981.

Interviews (By Author) Briggs, Derek E.G. Interview by author, 27 March 2007, New Haven, Connecticut, MP3 recording.

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As of 1994, there were 171 species, in 124 genera, known fromth e Burgess Shale. Some classifications have changed since this list was firstcompiled ; for example, Anomalocaris is now assigned to the Phylum Arthropoda. This list preserves the classification of known Burgess taxa at a particular moment in time (the mid-1990s). Question marks denote uncertainty in assignation to the taxon indicated. Modified fromBriggs , Erwin, and Collier, 217-221.

Filamentous Marpolia spissa Walcott, 1919 Morania confluens Walcott, 1919 Morania elongata Walcott, 1919 Morania fragmenta Walcott, 1919 Morania? frondosa Walcott, 1919 Morania globosa Walcott, 1919 Morania parasitica W'alcott, 1919 Morania? reticulata Walcott, 1919

Algae Division Chlorophyta Margaretia dorus Walcott, 1931 Division Chlorophyta? Yuknessia simplex Walcott, 1919 Division Rhodophyta Bosworthia gyges Walcott, 1919 Bosworthia simulans Walcott, 1919 Dalyia nitens Walcott, 1919 Dalyia racemata Walcott, 1919 Sphaerocordium? cambria Walcott, 1919 Sphaerocordium? praecursor Walcott, 1919 Wahpia mimica Walcott, 1919 Wahpia virgata Walcott, 1919 Waputikia ramosa Walcott, 1919

Possible Algae Dictyophycus gracilis Ruedemann, 1931

289 KINGDOM ANIMALIA Phylum Porifera Class Demospongia Capsospongia undulata (Walcott, 1920) carteri Walcott, 1920 Choia ridleyi Walcott, 1920 Crumillospongia biporosa Rigby, 1986 Crumillospongiafrondosa (Walcott, 1920) Falospongiafalata Rigby, 1986 Fieldospongia bellilineata (Walcott, 1920) Halichondrites elissa Walcott, 1920 Hamptonia bowerbanki Walcott, 1920 Hazelia conferta Walcott, 1920 Hazelia crateria Rigby, 1986 Hazelia delicatula Walcott, 1920 Hazelia dignata (Walcott, 1920) Hazelia grandis Walcott, 1920 Hazelia luteria Rigby, 1986 Hazelia nodulifera Walcott, 1920 Hazelia obscura Walcott, 1920 Hazelia palmata Walcott, 1920 Leptomitus lineatus (Walcott, 1920) Moleculopina mammillata (Walcott, 1920) Pirania muricata Walcott, 1920 Sentinelia draco Walcott, 1920 Takakkawia lineata Walcott, 1920 Vaitxia bellula Walcott, 1920 densa Walcott, 1920 Vauxia gracilenta Walcott, 1920 Vauxia venata Walcott, 1920 Wapkia grandis Walcott, 1920 Class Hexactinellida Diagoniella hindei Walcott, 1920 Protospongia hicksi Hinde, 1887 Stephanospongia magnipora Rigby, 1986 Class Calcarea Canistrumella alternataJOigby, 1986 Eiffelia globosa Walcott, 1920

Phylum Cnidaria Class ? Thaumaptilon walcotti Conway Morris, 1993 costalis Walcott, 1911 Class ? Gelenoptron tentaculatum Conway Morris, 1993 Class Uncertain Cambrorhytiumfragilis (Walcott, 1911) Cambrorhytium major (Walcott, 1908)

Phylum Fasciculus vesanus Simonetta and Delle Cave, 1978

Superphylum Lophophorata? Odontogriphus omalus Conway Morris, 1976

Superphylum Lophophorata Phylum Brachiopoda Class Inarticulata Acroihyra gregaria Walcott, 1924 Lingulella waptaensis Walcott, 1924 Micromitra burgessensis Resser, 1938 Paterina zenobia (Walcott, 1924) Class Articulata Diraphora bellicostata (Walcott, 1924) Nisusia burgessensis Walcott, 1924 Phylum Mollusca? Class Helcionelloida amii (Matthew, 1902)

Phylum carinatus (Matthew, 1899)

Phylum Ancalagon minor (Walcott, 1911) lanceolata Walcott, 1912 Louise Ha pedunculata Walcott, 1911 (^Miskoia preciosa Walcott, 1911) prolifica Walcott, 1911 Columbia Conway Morris, 1977 (=& major Walcott, 1911) Phylum Priapulida? Lecythioscopa simplex (Walcott, 1931) Scoleofurca rara Conway Morris, 1977

Phylum Annelida Class Polychaeta Burgessochaeta setigera (Walcott, 1911) Canadia spinosa Walcott, 1911 (=C regularis Walcott, 1911 and C. grandis Walcott, 1931) Insolicorypha psygma Conway Morris, 1979 Peronochaeta dubia (Walcott, 1911) Stephenoscolex argutus Conway Morris, 1979

Phylum Onychophora Aysheaia pedunculata Walcott, 1911 Hallucigenia sparsa (Walcott, 1911)

Phylum Arthropoda Primitive Branchiocaris pretiosa (Resser, 1929) Marrella splendens Walcott, 1912 Subphylum Crustacea, and crustaceanomorphs Canadaspis avails (Walcott, 1912) Canadaspis perfecta (Walcott, 1912) (=Hymenocaris obliqua Walcott, 1912 and C. obesa Simonetta and Delle Cave, 1975) Carnarvonia venosa Walcott, 1912 Isoxys acutangulus (Walcott, 1908) Isoxys longissimus Simonetta and Delle Cave, 1975 Odaraia alata Walcott, 1912 (=Eurysaces pielus Simonetta and Delle Cave, 1975) Perspicaris dictynna (Simonetta and Delle Cave, 1975) Perspicaris recondita Briggs, 1977 Plenocaris plena (Walcott, 1912) Tuzoia burgessensis Resser, 1929 Tuzoia canadensis Resser, 1929 Tuzoia? parva (Walcott, 1912) Tuzoia praemorsa Resser, 1929 Tuzoia retifera Walcott, 1912 Waptiafieldensis Walcott, 1912 Class Ostracoda Alutcft indeterminate species Class Cirripedia? Priscansermarinus barnetti Collins and Rudkin, 1981 Subphylum Arachnomorpha Class Trilobita Chancia palliseri (Walcott, 1908) Ehmaniella burgessensis Rasetti, 1951 Ehmaniella waptaensis Rasetti, 1951 Elrathia permulta (Walcott, 1918) Elrathina cordillerae (Rominger, 1887) Hanburia gloriosa Walcott, 1916 Kootenia burgessensis Resser, 1942 Naraoia compacta Walcott, 1912 (=N. pammon Simonetta and Delle Cave, 1975 and N. halia Simonetta and Delle Cave, 1975) Naraoia spinifer Walcott, 1931 serratus (Rominger, 1887) (=Nathorstia transitans Walcott, 1912) Oryctocephalus burgessensis Resser, 1938 Oryctocephalus matthewi Rasetti, 1951 Oryctocephalus reynoldsi Reed, 1899 Oryctocephalus indeterminate species Pagetia bootes Walcott, 1916 Parkaspis decamera Rasetti, 1951 Peronopsis montis (Matthew, 1899) praecurrens (Westergaard, 1936) (=Triplagnostus burgessensis Rasetti, 1951) Spencella indeterminate species #1 (Rasetti, 1951) Spencella indeterminate species #2 (Rasetti, 1951) Tegopelte gigas Simonetta and Delle Cave, 1975 Class Chelicerata Sanctacaris uncata Briggs and Collins, 1988 Other Arthropods Actaeus armatus Simonetta, 1970 Alalcomenaeus cambricus Simonetta, 1970 Burgessia bella Walcott, 1912 (=Hymenocaris? circularis Walcott, 1912) Emeraldella brocki Walcott, 1912 (=Emeraldoides problematicus Simonetta, 1964) Habelia? brevicauda Simonetta, 1964 Habelia optata Walcott, 1912 Helmetia expansa Walcott, 1918 Houghtonites gracilis (Walcott, 1912) Leanchoilia superlata Walcott, 1912 (=Bidentia difficilis Walcott, 1912; Emeraldella micrura Walcott, 1912; Leanchoilia major Walcott, 1931; Leanchoilia amphiction Simonetta, 1970; Leanchoilia persephone Simonetta, 1970; Leanchoilia protogonia Simonetta, 1970) Molaria spinifera Walcott, 1912 Mollisonia rara Walcott, 1912 (=Parahabelia rara Simonetta, 1964) Sarotrocercus oblita Whittington, 1981 Sidney ia inexpectans Walcott, 1911 Skaniafragilis Walcott, 1931 Thelxiope palaeothallasia Simonetta and Delle Cave, 1975 Yohoia tenuis Walcott, 1912

Phylum Echinodermata Class Cystoidea Gogial radiata Sprinkle, 1973 Class Crinoidea Echmatocrinus brachiatus Sprinkle, 1973 Class Edrioasteroidea Walcottidiscus magister Bassler, 1936 Walcottidiscus typicalis Bassler, 1935 Class Holothuroidea ludwigi Walcott, 1911

Phylum Hemichordata Class Enteropneusta? Ottoia tenuis Walcott, 1911 Class Graptolithina? Chaunograptus scandens Ruedemann, 1931

Phylum Chordata Metaspriggina walcotti Simonetta and Insom, 1993 Pikaia gracilens Walcott, 1911 Animals Not Assigned to Major Groups Anomalocarids Amiella ornata Walcott, 1911 Anomalocaris canadensis Whiteaves, 1892 Anomalocaris nathorsti (Walcott, 1911) (=Laggania cambria Walcott, 1911 and Peytoia nathorsti Walcott, 1911) dentata Simonetta and Delle Cave, 1975 Hurdia triangulata Walcott, 1912 Hurdia victoria Walcott, 1912 Proboscicaris agnosta Rolfe, 1962 Proboscicaris ingens Rolfe, 1962 Proboscicaris obtusa Simonetta and Delle Cave, 1975 Others Amishvia sagittiformis Walcott, 1911 Banffia constricta Walcott, 1911 Dinomischus isolatus Conway Morris, 1977 Nectocaris ptetyx Conway Morris, 1976 Oesia disjuncta Walcott, 1911 Opabinia regalis Walcott, 1912 Platydendron ovale Simonetta and Delle Cave, 1978 Pollingeria grandis Walcott, 1911 Portalia mira Walcott, 1918 Worthenella cambria Walcott, 1911 Scleritome -Bearing Animals Chancelloria eros Walcott, 1920 Wiwaxia corrugata (Matthew, 1899)

Below is a list of those species from Sirius Passet (Greenland) and Chengjiang (China) discussed in this thesis. It is not an exhaustive list of species found in either fauna.

Sirius Passet Species KINGDOM ANIMALIA Phylum Arthropoda Class Dinocarida Kerygmachela kierkegaardi Budd, 1998

Superphylum Lophotrochozoa? Halkieria evangelista Conway Morris and Peel, 1990 Chengjiang Species KINGDOM ANIMALIA Phylum Onychophora

Microdictyon sinicum Chen et al., 1989 Onychodictyonferox Hou et al., 1991