The Precambrian to Cambrian Fossil Record and Transitional Forms
Keith B. Miller*
Department of Geology
Kansas State University
Manhattan, KS 66502
There is much confusion in the popularized literature about the evidence for macroevolutionary change in the fossil record. Unfortunately, the discussion of evolution within the Christian community has been greatly influenced by inaccurate presentations of the fossil data and of the methods of classification. Widely read critiques of evolution, such as Evolution: A Theory in Crisis by Denton,1 and Darwin on Trial by Johnson,2 contain serious misrepresentations of the available fossil evidence for macroevolutionary transitions and of the science of evolutionary paleontology. In "On the Origin of Stasis by Means of Natural Processes," Battson similarly does not accurately communicate the rapidly growing body of evidence relevant to the Precambrian/Cambrian transition.3
The implication of much of the evangelical Christian commentary on macroevolution is that the major taxonomic groups of living things remain clearly distinct entities throughout their history, and were as morphologically distinct from each other at their first appearance as they are today. There is a clear interest in showing the history of life as discontinuous, and any suggestion of transition in the fossil record is met with great skepticism. The purpose of this short communication is to dispel some of these misconceptions about the nature and interpretation of the fossil record.
Taxonomy and Transitional Forms
The recognition of transitional forms is as much a question of taxonomy as it is a statement about the nature of the fossil record. Taxonomy, the process of classifying living and fossil organisms, produces its own patterns which order the diversity of life. It is thus important to recognize that names do much more than describe nature. They also interpret it. There is considerable ferment now within the field of taxonomy because of conflicting philosophies of classification, and different perceptions of which patterns in the history of life should be reflected in the taxonomic hierarchy.4 Higher taxa can be either groupings of species with similar morphologies, or "natural" groups sharing derived characteristics inherited from a common ancestor. Thus, the taxonomic assignment of organisms cannot be used uncritically in the reconstruction of the history of life as though taxonomic names were raw data.
The Linnean classification system was originally based on a typological concept of species. All individuals were compared to an ideal "archetype" that defined the species, and all observed variation was understood as variation from that type. Typology thus excluded transitions by definition. Denton appeals to this typological model as a basis for arguing that it represents an objectively accurate picture of biologic reality. He fails to see that typology imposes its own order on the natural variation of the biological world and is not objectively descriptive of it. To use an illustration given by Denton, triangles and quadrilaterals have clear typological definitions and are easily separated into two classes of geometric shapes. Now, if one side of the quadrilateral were reduced in length by infinitesimal amounts until it was only two geometric points wide, it would still be a quadrilateral by definition although absolutely indistinguishable from a triangle. The most conceivably gradual transition has been made, yet typologically there were no intermediates! For Denton to apply this typology to living organisms and the fossil record, and then claim the absence of intermediates is meaningless.5 Such arguments hinge on our human constructions and categories, not on the reality of variation in the biologic world.
The Linnean classification system is also hierarchical, with species grouped into genera, genera into families, families into orders, etc. This system reflects the discontinuity and hierarchy that are commonly, but not always, observed among living organisms. However, "this system leads to the impression that species in different categories differ from one another in proportion to differences in taxonomic rank.6 This impression is false. Higher taxa are relatively distinct and easily recognizable groups only when we ignore the time dimension of the history of life. Taxonomic categories are blurred during times representing the branching points of the tree of life. Once a lineage is split, its branches continue to evolve and diverge such that their morphological (and genetic) distance increases and they become more readily distinguished taxonomic entities.
Since taxonomy is superimposed on a branching tree of life, a higher level in the taxonomic hierarchy does not imply a greater degree of morphologic distance. For example, two species which belong to different classes are not necessarily more different from each other than two species belonging to different genera. When using the fossil record to look backward through time, it is found that representatives of different higher-level taxa become more "primitive," that is, have fewer derived characters, and appear more like the primitive members of other closely related taxa.7 The more complete the fossil record of the origin and early radiation of higher taxa the more similar the transitional species, and the more difficult it is to determine their taxonomic assignments. Species placed into two different higher taxa may thus have very similar morphologies. Were it not for the subsequent evolutionary history of the lineages, species spanning the transitions between families, orders, classes, or phyla would be placed in the same lower taxon.8 This is completely consistent with the paradigm of common descent, and with the origin of higher taxa through evolutionary processes at the population and species level.
Based on the above discussion, a transitional form is simply a fossil species that possesses a morphology intermediate between those of two others belonging to different higher taxa. Such transitional forms commonly possess a mixture of traits considered characteristic of these different higher taxa. They may also possess particular characters that are themselves in an intermediate state. During the time of origin of a new higher taxon, there are often many described species with transitional morphologies representing many independent lineages. It is usually very difficult if not impossible to determine which, if any, of the known transitional forms actually lay on the lineage directly ancestral to the new taxon. For this reason, taxonomists commonly have difficulty defining higher taxa, and assigning transitional fossil species to one or another taxo9 But, although the details may elude us, the patterns of evolutionary change are in many cases well recorded in the fossil record.
Battson emphasizes the pattern of appearance of higher taxa in which phylum-level diversity reaches its peak in the fossil record before class-level diversity, and class-level diversity before that of orders, etc.10 Battson and other critics of macroevolution interpret this apparent "top-down" pattern as contrary to expectations from evolutionary theory. However, this pattern is generated by the way in which species are assigned to higher taxa. When a hierarchical classification is applied retrospectively to a diversifying evolutionary tree, a "top-down" pattern will of necessity result. Consider, for example, species belonging to a single evolving lineage given genus-level status. This genus is then grouped with other closely related lineages into a family. The common ancestors of these genera are by definition included within that family. Those ancestors must logically be older than any of the other species within the family. Thus the family level taxon would appear in the fossil record before most of the genera and species included within it. The "top-down" pattern of taxa appearance is therefore entirely consistent with a branching tree of life.
The origin of any new higher taxon, including phyla, must ultimately have occurred through the origin of a single new speciesCthat is, by a speciation event. The diversifying descendants of this founding species are then included within that new higher taxon. If common descent is accepted as a working hypothesis, this must be the case. This is recognized by all evolutionary paleobiologists, even those who stress the uniqueness of the origins of phyla and classes. As stated by Valentine:
A phylum has had to originate as a founding species by definition, and thus via microevolutionary processes. The microevolutionary questions concern how and why such a speciation occurred: what genetic, ecologic, or other features in the population biology of the lineage conspired to produce the new species. There are macroevolutionary questions as well; they concern how and why a particular new species founded a higher taxon, such as an entire phylum, rather than being just another species within an extant taxon.11
The Cambrian "Explosion" and the Origin of Invertebrate Phyla
The presentation by Battson seriously misrepresents our present knowledge of the Latest Precambrian and Early Cambrian fossil record.12 There has been a flood of major fossil discoveries within the last decade or so that has shed great light, and overturned many established views on the origin and early diversification of the metazoans. Our understanding of the early history of life is presently in an exciting stage of rapid change and revision.
The Late Precambrian and Early Cambrian fossil record of the metazoan phyla shows the same pattern as that of class- and order-level taxa in the Phanerozoic. Near the origin of these higher-level taxonomic categories, the boundaries between the taxa become blurred and fossils become difficult to classify. Moving back in time toward their presumed point of diversion from a common ancestor, organisms belonging to separate phyla converge in morphology. Several Early Cambrian organisms possess morphologies that bear similarities to more than one phylum, making their placement in existing phyla a matter of dispute. This classification problem is resolved either by erecting new phyla or by broadening definitions to include the new forms.
Some Late Precambrian Ediacaran fossils (~580-560 My) bear strong resemblances to colonial coelenterates called pennatulids, or sea pens.13 Others appear to have been solitary coelenterate medusoids attached to the sea floor.14 Some of these medusoid fossils show clear impressions of tentacles around their margins. There are also sack-shaped organisms interpreted as sea anemones.15 Although Seilacher has questioned the placement of many Ediacaran fossil forms in living phyla,16 he also recognizes the presence of a group of sand-filled cnidarian coelenterates he has called the Psammocorallia.17 The fossil record thus indicates that the Late Precambrian was dominated by solitary and colonial coelenterates that may have included all four living cnidarian classes.18 Recently spicules from sponges of the class Hexactinellida have been identified in Ediacaran age rocks.19 There is also evidence for the presence of arthropods as well as echinoderms before the beginning of the Cambrian.20
The other major component of the ancient Ediacaran communities was burrowing and trail-making worms of unknown affinity. These trace fossils increase in abundance and diversity throughout the Latest Precambrian indicating both an increase in the diversity of organisms, and in the variety of feeding and locomotory behaviors.21 Annelid worms may be represented by the mineralized tubes of Cloudina and by multi-segmented forms such as Dickinsonia.22 Casts interpreted as echiurid worms have also been described from the Ediacaran.23 Nearly half of all living phyla are worms, and only a few phyla have a significant fossil record, so that it is clear that the phylum-level diversity of the Late Precambrian may have been much greater than I have indicated. Certainly some modern phyla appeared before the end of the Precambrian.
The Cambrian, particularly the Early Cambrian, was a time of amazing diversification among the metazoans. Two aspects of the Early Cambrian fossil record will be emphasized here. First, with important new fossil discoveries and the redescription of previously known forms, the many peculiar Cambrian taxa are now being grouped into coherent phyla. These phyla include living phyla and groups interpreted as ancestral to living phyla. Secondly, many Early Cambrian taxa have morphologies that bear similarities with more than one living phylum, that is, their morphologies are mosaics of phylum-level characters.
Probably the most bizarre Burgess Shale fossil is Hallucigenia. This fossil has been completely reinterpreted since the description presented by Gould24 This reinterpretation has resulted both from more detailed study of existing fossil specimens and the discovery of exceptionally well-preserved fossils of similar organisms in China.25 Hallucigenia is now recognized as a member of a diverse and widespread group of Cambrian organisms called lobopods. They are very similar to, and may belong to, an obscure living phylum called the Onychophora. These caterpillar-like organisms walked on fleshy legs and bore plate-like or spine-like mineralized structures on their dorsal sides. Although these small plates and spines were previously recognized as part of the Early Cambrian "small shelly fauna," their biological affinities were unknown until these recent discoveries.
The Cambrian lobopods occupy a transitional morphological position between several living phyla. The oldest known lobopod from the Early Cambrian is Xenusion. This organism bears similarities to both palaeoscolecid worms and to living onychophorans and tardigrads.26 Furthermore, lobo-pods also have morphological features in common with the arthropods, particularly with peculiar Cambrian forms such as Opabinia and Anomalocaris.27 Recent redescription of Opabinia has also disclosed the presence of lobopod limbs strongly suggesting a lobopod to arthropod transition.28 The discovery of a Cambrian gill-bearing lobopod reinforces this conclusion.29 These forms fall nicely into a transitional position between extant phyla.
Another very important group of Early Cambrian fossils is represented by a wide variety of tiny cap-shaped and scalelike skeletal elements. It is now known that many of these belonged to slug-like animals that bore these hollow mineralized structures like a dermal armor. Two well-known, and well-preserved, examples of this group of organisms are Wiwaxia and Halkieria. Called the Machaeridia or the Coelosceritophora, these organisms are mosaics of phylum-level characteristics, and their taxonomic affinity is a matter of present debate. A strong case can be made for the assignment of at least some of these taxa to the Mollusca.30 However, a relationship to the polychaete annelid worms is also strongly suggested by some workers, as with Wiwaxia.31 The taxonomic confusion associated with these scale-bearing slug-like animals, and with the lobopods, is consistent with their stratigraphic position at the base of the Cambrian metazoan radiation.
The above discussion shows that the presentation of the Precambrian to Cambrian fossil record given by Battson does not reflect our present understanding of the history of life.32 Many metazoan groups appeared before the Cambrian, including representatives of several living phyla. Furthermore, the many small scale, plate, and spine-bearing organisms of the earliest Cambrian, while sharing characteristics with several living phyla, are also similar enough to each other to be classified by some workers into a single phylum.33 Even when the metazoan fossil record for the entire Cambrian is considered, the morphological disparity cannot be equated with that of living organisms, unless the subsequent appearance of all vertebrate and insect life be ignored. In addition, many living phyla, including most worm phyla, are unknown from the fossil record until well into the Phanerozoic.34 Thus, to claim the near simultaneous appearance of virtually all living phlya in the Cambrian is not an objective statement of the fossil evidence but a highly speculative, and I believe unsupported, interpretation of it35
Finally, there is a question of whether the rapid diversification of metazoans in the Late Precambrian and Early Cambrian reflects an equally rapid increase in complexity. An interesting study by Valentine and others uses the number of cell types as a useful measure of morphological complexity. They plot the estimated times of origin of major body plans against their cell type numbers. The resulting plot shows that the upper bound of complexity has increased steadily and nearly linearly from the origin of the metazoa to the present. Furthermore, they conclude that "...the metazoan `explosion' near the Precambrian/Cambrian transition was not associated with any important increase in complexity of body plans...36 This suggests that the appearance of new higher taxa in the Cambrian did not involve the sudden appearance of major new levels of complexity.
1M. Denton, Evolution: A Theory in Crisis (Bethesda, MD: Adler & Adler, 1985).
2.P. E. Johnson, Darwin on Trial (Downers Grove, IL: InterVarsity Press, 1991).
3A. L. Battson, III, "On the Origin of Stasis by Means of Natural Processes," Perspectives in Science and Christian Faith 46 (1994): 230-241.
4N. Eldredge and J. Cracraft, Phylogenetic Patterns and the Evolutionary Process (New York: Columbia University Press, 1980), and R. M. Schoch, Phylogeny Reconstruction in Paleontology (New York: Van Nostrand Reinhold Company, 1986).
5M.Denton, Evolution: A Theory in Crisis, p. 96.
6R.L. Carroll, Vertebrate Paleontology and Evolution (New York: W. H. Freeman & Co., 1988), 578.
7For example, D.R. Prothero and R.M. Schoch, "Origin and Evolution of the Perissodactyla: Summary and Synthesis," in The Evolution of the Perissodactyls, eds. D. R. Prothero and R. M. Schoch (New York: Oxford University Press, 1989), 504-29 and L.B. Radinsky, "The Early Evolution of the Perissodactyla," Evolution 23 (1979): 308-28.
8A.S. Romer, Vertebrate Paleontology (Chicago: University of Chicago Press, 1966), 232.
9For example, M. Desui, "On the Origins of Mammals," in Origins of the Higher Groups of Tetrapods: Controversy and Consensus, eds. H.-P. Schultze and L. Trueb (Ithaca, NY: Comstock Publishing Associates, 1991), 570-97 and J.A. Hopson, "Systematics of the Nonmammalian Synapsida and Implications for Patterns of Evolution in Synapsids," ibid., 635-93.
10A.L. Battson, III, "On the Origin of Stasis by Means of Natural Processes."
11J.W. Valentine, "The Macroevolution of Phyla," in Origin and Early Evolution of the Metazoa, eds. J.H. Lipps and P.W. Signor (New York, Plenum Press, 1992), 525-6.
12A.L. Battson, III, "On the Origin of Stasis by Means of Natural Processes."
13R.J.F. Jenkins, "The Enigmatic Ediacaran (Late Precambrian) Genus Rangea and Related Forms," Paleobiology 11 (1985): 336-55; CCC, "Functional and Ecological Aspects of Ediacaran Assemblages," in Origin and Early Evolution of the Metazoa, eds. J.H. Lipps and P.W. Signor (New York: Plenum Press, 1992), 131-76; and S. Conway Morris, "Ediacaran-Like Fossils in Cambrian Burgess Shale-Type Faunas of North America," Palaeontology 36 (1993): 593-635.
14J. G. Gehling, "The Case for Ediacaran Fossil Roots to the Metazoan Tree," in The World of Martin F. Glaessner: Memoir No. 20, ed. B.P. Radhakrishna (Bangalore: Geological Society of India, 1991), 181-223; and R.J.F. Jenkins, "Functional and Ecological Aspects of Ediacaran Assemblages," in Origin and Early Evolution of the Metazoa, eds. J.H. Lipps and P.W. Signor.
15J.G. Gehling, "A Cnidarian of Actinian-Grade from the Ediacaran Pound Subgroup, South Australia," Alcheringa 12 (1988): 299-314.
16A. Seilacher, "Late Precambrian and Early Cambrian Metazoa: Preservational or Real Extinctions?" in Patterns of Changes in Earth Evolution, eds. H.D. Holland and A.F. Trendall (Heidelberg: Springer-Verlag, 1984), 159-68; and A. Seilacher, "Vendozoa: Organismic Construction in the Proterozoic Biosphere," Lethaia 22 (1989): 229-39.
17A. Seilacher, "Vendobionta and Psammocorallia: Lost Constructions of Precambrian Evolution," Journal of the Geological Society, London 149 (1992): 607-13; and L.W. Buss and A. Seilacher, "The Phylum Vendobionta: A Sister Group of the Eumetazoa?" Paleobiology 20 (1994): 1-4.
18S. Conway Morris, "The Fossil Record and the Early Evolution of the Metazoa," Nature 361 (1993): 219-25.
19M. Brasier, O. Green, and G. Shields, "Ediacaran Sponge Spicule Clusters from Mongolia and the Origins of the Cambrian Fauna," Geology 25 (1997): 303-6.
20J.G. Gehling, "Earliest Known EchinodermCa New Ediacaran Fossil from the Pound Subgroup of South Australia," Alcheringa 11 (1987): 337-45; and J.G. Gehling, "The Case for Ediacaran Fossil Roots to the Metazoan Tree," in The World of Martin F. Glaessner: Memoir No. 20, ed. B.P. Radhakrishna.
21T.P. Crimes, "Changes in the Trace Fossil Biota Across the Proterozoic-Phanerozoic Boundary," Journal of the Geological Society 149 (1992): 637-46; and CCC, "The Record of Trace Fossils Across the Proterozoic-Cambrian Boundary," in Origin and Early Evolution of the Metazoa, eds. J.H. Lipps and P.W. Signor (New York: Plenum Press, 1992), 177-202.
22M.F. Glaessner, "Early Phanerozoic Annelid Worms and Their Geological and Biological Significance," Journal of the Geological Society, London 132 (1976): 259-75; J. G. Gehling, "The Case for Ediacaran Fossil Roots to the Metazoan Tree;" and R.J.F. Jenkins, "Functional and Ecological Aspects of Ediacaran Assemblages."
23M.F. Glaessner, "An Echiurid Worm from the Late Precambrian," Lethaia 12 (1979): 121-4.
24S.J. Gould, Wonderful Life: The Burgess Shale and the Nature of History (New York: W.W. Norton & Co., 1989), 347.
25L. Ramsk?ld, and H. Xianguang, "New Early Cambrian Animal and Onychophoran Affinities of Enigmatic Metazoans," Nature 351 (1991): 225-8; Jun-yuan Chen and B-D. Erdtmann, "Lower Cambrian Fossil Lagerstatte from Chengjiang, Yunnan, China: Insights for Reconstructing Early Metazoan Life," in The Early Evolution of Metazoa and the Significance of Problematic Taxa, eds. A.M. Simonetta and S. Conway Morris (Cambridge: Cambridge University Press, 1991), 57-76; L. Ramsk?ld, "Homologies in Cambrian Onychophora," Lethaia 25 (1992): 443-60; andCCC, "The Second Leg Row of Hallucigenia Discovered," Lethaia 25 (1992): 221-4.
26J. Dzik and G. Krumbiegel, "The Oldest `Onychophoran' Xenusion: A Link Connecting Phyla?" Lethaia 22 (1989): 169-81.
27Ibid.; J. Dzik, "Early Metazoan Evolution and the Meaning of its Fossil Record," in Evolutionary Biology 27, eds. M.K. Hecht, et al. (1993): 339-86; and Jun-yuan Chen, L. Ramsk?ld, and Gui-ging Zhou, "Evidence for Monophyly and Arthropod Affinity of Cambrian Giant Predators," Nature 264 (1994): 1304-8.
28G. E. Budd, "The Morphology of Opabinia Regalis and the Reconstruction of the Arthropod Stem-Group," Lethaia 29 (1996): 1-14.
29G. Budd, "A Cambrian Gilled Lobopod from Greenland," Nature 364 (1993): 709-11.
30S. Bengston, "The Cap-Shaped Cambrian Fossil Maikhanella and the Relationship Between Coeloscleritophorans and the Molluscs," Lethaia 25 (1992): 401-20; and J. Dzik, "Early Metazoan Evolution and the Meaning of its Fossil Record."
31N. J. Butterfield, "A Reassessment of the Enigmatic Burgess Shale Fossil Wiwaxia Corrugata (Matthew) and its Relationship to the Polychaete Canadia Spinosa Walcott," Paleobiology 16 (1990): 287-303.
32A. L. Battson, III, "On the Origin of Stasis by Means of Natural Processes."
33J. Bergstr?m, "The Origin of Animal Phyla and the New Phylum Procoelomata, Lethaia 22 (1989): 259-69.
34M. J. Benton, The Fossil Record 2 (London: Chapman & Hall, 1993), 841.
35A. L. Battson, III, "On the Origin of Stasis by Means of Natural Processes," 232.
36J. W. Valentine, A. G. Collins, and C. P. Meyer, "Morphological Complexity Increase in Metazoans," Paleobiology 20 (1994): 131.