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Perspective

The ‘‘explosion’’: Slow-fuse or megatonnage?

Simon Conway Morris*

Department of Sciences, University of Cambridge, Cambridge CB2 3EQ, United

Clearly, the record from the Cambrian period is an invaluable tool for deciphering . Less clear, however, is how to integrate the paleontological information with molecular phylogeny and developmental data. Equally challenging is answering why the Cambrian period provided such a rich interval for the redeployment of genes that led to more complex bodyplans. illiam Buckland knew about it, The First Metazoans. assem- 1). The overall framework of early - WCharles Darwin characteristically blages (2, 5) are presumably integral to zoan evolution comes from molecular agonized over it, and still we do not fully understanding the roots of the Cambrian data, but they cannot provide insights into understand it. ‘‘It,’’ of course, is the seem- ‘‘explosion,’’ and this approach assumes the anatomical changes and associated ingly abrupt appearance of in the that the fossil record is historically valid. It changes in ecology that accompanied the Cambrian ‘‘explosion.’’ The crux of this is markedly at odds, however, with an emergence of bodyplans during the Cam- evolutionary problem can be posed as a alternative view, based on molecular data. brian explosion. The fossil record of interrelated questions. Is it a real These posit metazoan divergences hun- provides, therefore, a unique historical event or simply an artifact of changing dreds of millions of earlier (6, 7). As perspective. fossilization potential? If the former, how such, the origination of animals would be Only those aspects of the Ediacaran rapidly did it happen and what are its more or less coincident with the postu- record relevant to the Cambrian diversi- consequences for understanding evolu- lated ‘‘Big Bang’’ of diversifi- fication are noted here. , antho- Ϸ tionary processes? The Cambrian explo- cation 1,000 Myr ago (8). The existence zoan cnidarians, and stem-group triplo- sion addresses problems of biology as di- of some sort of pre-Ediacaran metazoan blasts can all be identified with reasonable verse as the origin of metazoan bodyplans, history is a reasonable assumption (9), but confidence. Anthozoans, which are per- the role of developmental genetics, the such animals must have been minute be- haps best known from such animals as sea validity of molecular clocks, and the in- cause anything larger than about one mil- anemones, are represented by frond-like fluence of extrinsic factors such as ocean limeter would leave a sedimentary imprint . These types persisted into the chemistry and atmospheric . as a . The literature is littered Cambrian (Fig. 2e) (13, 14) and are similar with claims for pre-Ediacaran traces, but to the living sea-pens (pennatulaceans). The Framework. Stratigraphic sections the history of research has been one of Despite the widespread onset of biomin- spanning the Vendian-Cambrian bound- continuous rebuttal. Will the most recent eralization, it is curious that an authenti- ary show a broadly similar pattern candidates avoid the same fate? If such cated record of Cambrian cnidarians is examples as the Ϸ1,000-Myr-old struc- whereby the key events are bracketed by relatively sparse but does include some tures from are genuine (10), it is the Ϸ600-million- (Myr)-old Neopro- primitive . , which belong to strange that there was not a rapid and terozoic glacial deposits (tillites) and in the scyphozoans, are virtually unknown. A global colonization of marine sediments. the succeeding Cambrian diverse meta- benthic scyphozoan shows, however, an A failed adventure in metazoan history? zoan assemblages, typified by abundant astonishingly complete ontogenetic se- Motility and hence the potential for sed- skeletons, diverse trace fossils, and Bur- quence that can be traced from the early iment disturbance are not, moreover, au- (15). Remarkably, given their very gess Shale-type (Fig. 1). One key tomatically a prerogative of the metazo- development is a series of accurate radio- delicate and gelatinous construction, rep- ans. Conceivably, simple traces could be resentatives of the sea gooseberries metric determinations (1). The Vendian- Ϸ produced by strolling protistan ‘‘,’’ (ctenophores) are also known (Fig. 2b). Cambrian boundary is now placed at 543 analogous to slime-mold Dictyostelium. Myr, and the duration (Ϸ45 Myr) of the Lophotrochozoans. The ancestral lophotro- Cambrian is substantially shorter than The Way Forward. The key element in de- chozoan may have looked -like, creep- once thought. The preceding Ediacaran ciphering the (11) is ing across the seafloor on a muscular foot. faunas have an approximate range of to integrate the expanding insights of mo- The Ediacaran may be an early 565–545 Myr. Accordingly, the overall lecular phylogeny (12) and developmental representative (16), and the armored time-scale for discussion is a relatively biology with the totality of paleontological (Fig. 2c) from the Lower Cam- protracted 65 Myr, although the principal evidence, including the Ediacaran assem- brian are possibly a subsequent develop- events of evolutionary interest are proba- blages. Somewhere, and this is the tricky ment (17). A surprising discovery is fossil bly more tightly bracketed (550–530 Myr) point, in the Ediacaran assemblages are (Fig. 2d), from the Lower Cam- between the diverse Ediacaran faunas of animals that may throw particular light on brian of , that are reasonably at- latest age (2) and the key transitions. Of these, the most signif- tributed to the halkieriids (18). From a -type faunas (3). icant are those between sponges and dip- -like stock, it may be possible to Correlations are also assisted by emerging loblasts, cnidarians and triploblasts, as derive not only the molluscs, but more schemes of chemostratigraphy (2, 4), no- well as the early evolution of the three tably with reference to strontium (␦87Sr) superclades of triploblast (, and (␦13C). ecdysozoans, and lophotrochozoans) (Fig. *E-mail: [email protected].

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Fig. 1. Principal events across the Vendian-Cambrian boundary, spanning an interval of approximately 60 Myr (570–510 Myr), in the context of the early evolution of metazoans. On the left are denoted a series of important fossil assemblages, e.g., Burgess Shale, and various other significant events, e.g., cessation of . To the right is the carbon isotope curve (redrawn from ref. 4), which provides an independent tool for correlation by chemostratigraphy and may also

indicate substantial changes in ocean state with possible implications for evolutionary diversification. The evolutionary framework is largely based on molecular SPECIAL FEATURE data (12, 19, 20), but the available fossil record not only gives a temporal perspective but also indicates major anatomical transitions that mark the emergence of distinct bodyplans. The sister-group of the Metazoa are the Fungi (35), and a possible time of divergence was Ϸ650 Myr ago. No fossil evidence for this event is yet available, and the early history of animals (Ϸ650–570 Myr) is also cryptic. This is presumably because the earliest metazoans were microscopic and too fragile to fossilize readily. The most primitive animals in the fossil record may be represented by the vendobionts (36). Metazoans are otherwise divided into various major groupings, of which the most significant depends on the number of germ layers: respectively, two in the diploblasts and three in the triploblasts. The Ediacaran faunas postdate episodes of major glaciation and, with the exception of a few mineralized taxa (e.g., Cloudina), lack hard-parts. These Vendian-age assemblages comprise the problematic vendobionts, various coelenterates, and stem-group representatives of the three main groups of triploblast, referred to, respectively, as the ecdysozoans, lophotrochozoans, and deuterostomes. The process of molting, known as ecdysis, is a characteristic of the ecdysozoans. The most important group is the , and, possibly, they derive from a priapulid-like worm. Lophotrochozoans derive their name from a tentacular feeding organ () found in some groups and the most widespread occurrence of a type of ciliated larva known as the trochophore. Lophotrochozoans are a diverse group encompassing the molluscs, , and . The ancestral form was probably rather slug-like. The deuterostomes are notably disparate and include the and .

surprisingly two more bodyplans, specifi- status for the platyhelminthes (free-living record. In contrast, the notion of the ec- cally in the form of the brachiopods and and various parasitic groups) dysozoans (20) is much more revolutionary. annelids (17) (Fig. 1). (12). Classically regarded as primitive trip- Its principal phyla are the arthropods, nem- Although molecular data define the lo- loblasts, the flatworms appear now to be atodes and priapulids, all of which molt (or photrochozoans, with some exceptions anatomically degenerate, dispensing with ecdyse) their cuticle (or exoskeleton) at such features as an anus. (19) internal resolution of the phylogeny is some point in their cycle. The unusual limited. This makes the Cambrian fossil Ecdysozoans. If the concept of the Lophotro- bodyplan, based on a hydrostatic record of potentially key importance. Nev- chozoa overthrows some long-cherished be- ‘‘skeleton,’’ and the reduced complement of ertheless, several phyla remain ‘‘floating,’’ liefs, it remains consistent with some earlier Hox genes (12) suggest these worms, of arising from unresolved polychotomies. lines of evolutionary thinking and is at least central importance in molecular science in Most surprising, perhaps, is a changed partly congruent with the Cambrian fossil the form of Caenorhabditis elegans, are

Conway Morris PNAS ͉ April 25, 2000 ͉ vol. 97 ͉ no. 9 ͉ 4427 Downloaded by guest on September 24, 2021 highly derived. Nematode origins, however, remain unresolved, although possible con- nections between some Cambrian priapu- lid-like fossils and the group of ‘‘nemathel- minthes’’ (which includes the ) have been made (21). The priapulids (Fig. 2h) are a diverse and prominent group in the Cambrian (11). As a group newly recruited to the ecdysozoans, can we find a link with the arthropods? One interesting proposal (22) looks to a distinctive group of priapulids with an armored cuticle, known as the palaeoscolecidans, as potential precur- sors. The key step is to affect a functional transition from the peristaltic burrowing action of priapulids to a walking cycle based on the leg-like lobopods (Fig. 2f) that are found in the first arthropods. Functional interpretations of the subse- quent evolution of early arthropods can be put in a context of changing ecology, linked to defense and shifts in feeding style. In this scenario (23), a number of hitherto enigmatic taxa, notably Kerygma- chela (24, Fig. 2g) and the large and active predator , are seen as key staging posts leading from the primitive lobopodians (Fig. 2f) to the somewhat more familiar of advanced arthro- pods (CCT ϭ -chelicerate- ). Morphometric and phyloge- netic studies (25) have shown that the supposedly ‘‘bizarre’’ Burgess Shale-type arthropods fall into a phylogenetic scheme that gives no support to the idea that they are outliers in morphospace awaiting the grim reaper of contingent extinction.

Deuterostomes. Although there seems to be some congruence between the fossil record and molecular phylogenies with respect to the ecdysozoans and lophotro- chozoans, in the case of the deuteros- tomes, matters are less clear-cut. One difficulty is the extreme morphological distinction of the component phyla, so that plausible functional intermediates be- tween echinoderms, , and chordates remain effectively ad hoc con- Fig. 2. Representative Cambrian animals from Burgess Shale-type deposits (all except d) and an example of structions (26). Molecular data are cer- early phosphatization (d). (a) The agnathan fengjiao from the Lower Cambrian tainly yielding important insights, most (lower Botomian) Chengjiang lagersta¨tte, at Haikou near Kunming, , . The photograph is notably in terms of amphioxus (27) and courtesy of D. Shu (North-West University, Xilan, People’s Republic of China). (b) The holotype and only known the developmental biology of ascidians specimen (part and counterpart) of the ctenophore vesanus from the Middle Cambrian Burgess Shale lagersta¨tte, at Field in British Columbia, . (c) The halkieriid Halkieria evangelista from the Lower (28). With the addition of the fossil Cambrian (upper Atdabanian) lagersta¨tte in Peary Land, North . (d) Phosphatized record, there may now be the glimmerings embryos, possibly of a halkieriid, and referred to as Markuelia secunda from the Pestrotsvet Formation of a resolution (Fig. 1). (Tommotian) of south-east Siberia. The figures show views of two embryos that are wrapped around the Arguably the basal body- surface. The photograph is courtesy of S. Bengtson (Swedish Museum of Natural History, Stockholm). [Re- plan is best conceived as basically consist- printed (abstracted͞excerpted) with permission from ref. 37. Copyright 1997, American Association for the ing of two sections: a head with pharyn- Advancement of Science.] (e) The Ediacaran survivor and presumed anthozoan () geal perforations (gill-slits) and, to the walcotti from the Middle Cambrian Burgess Shale lagersta¨tte, at Field in British Columbia, Canada. (f) The posterior, a segmented unit. The most lobopodian Hadranax augustus from the Lower Cambrian (upper Atdabanian) Sirius Passet lagersta¨tte in primitive of living deuterostomes are Peary Land, North Greenland. The photograph is courtesy of G. Budd (Uppsala University, Uppsala). (g) The primitive kierkegaardi from the Lower Cambrian (upper Atdabanian) Sirius Passet taken to be the hemichordates, although lagersta¨tte in Peary Land, North Greenland. The photograph is courtesy of G. Budd. (h) The posterior trunk of living representatives, such as the acorn- the priapulid worm prolifica from the Middle Cambrian Burgess Shale lagersta¨tte, at Field in British worms, are evidently derived. Chengjiang Columbia, Canada. The specimen shows the intestine and three hyoliths, interpreted as ingested prey. (a, ϫ2.0; fossils, such as (29) and the b, ϫ0.3; c, ϫ0.8; d, ϫ55; e, ϫ0.3; f, ϫ0.8; g, 0.9; h, ϫ1.9.) almost identical (30), possess a

4428 ͉ www.pnas.org Conway Morris Downloaded by guest on September 24, 2021 segmented body, with incomplete cuticu- is synonymous with Yun- tionary context (34). It is evident that at lar rings, and an anterior section with nanozoon verges on the whimsical. The least some components of a given body- prominent gill slits. Although interpreted more famous , from the Burgess plan are assembled by virtue of a genetic as advanced chordates, in the artist’s Shale (11), remains more of a conundrum. ‘‘toolbox.’’ This, in turn, has provoked reconstruction (30) of Haikouella, the It has myotomes and a , but a extensive discussions on definitions of ho- supposed myotomes show a subtle peculiar bilobed head. Neither Cathay- mology, but perhaps deflects the interest- ‘‘enhancement’’ of a sigmoidal profile myrus nor Pikaia are particularly similar to ing question of how such toolboxes are when compared with the illustrated fos- the living amphioxus, suggesting that, al- recruited. This is no trivial point because sils. The supposed notochord is also in a though genomically primitive (27), this there is increasing evidence for extensive biomechanically peculiar position, incon- living representative is anatomically co-option and redeployment of genes. Not only that, but there are intriguing mis- sistent with its role as an antagonist to the derived. matches between genomic architecture purported myotomes. These strange- and bodyplan complexity. To complicate looking taxa from Chengjiang may be our What Triggered the Cambrian Explosion? Iso- matters further, a substantial proportion best glimpse of the first deuterostomes. topic and chemical indicators (2, 4), no- of the metazoan genome was probably ␦13 ␦32 ␦87 The first definite echinoderms do not tably C (Fig. 1), S, Sr, and phos- available well before the Cambrian explo- appear until the Lower Cambrian. The phogenesis, suggest substantial changes in sion. Genes make bodies and bodyplans riot of ensuing forms has proved difficult and circulation on vari- require a corresponding genetic architec- to place in a coherent phylogeny. Never- ous time-scales. Despite repeated specu- ture, but we are still far from understand- theless, the classic five-fold symmetry is lation, the extent to which these changes in ing either their interconnections or apparently a derived feature and as such is the oceans influenced, let alone stimu- evolution. consistent with marked redeployment of a lated, the Cambrian explosion is obscure. To conclude: The Cambrian explosion number of developmental genes (31). The motor of the Cambrian explosion was is real and its consequences set in motion What then did the first echinoderms look largely ecological, notably with the rise of a sea-change in evolutionary history. Al- like? The concept of a basic deuterostome macroscopic (and defense) and though the pattern of evolution is clearer, bipartite bodyplan of head with gill slits effective filter-feeding on the seafloor and the underlying processes still remain sur- and tail could reinvigorate the status of in the pelagic zone. Skeletal hard-parts, prisingly elusive. the otherwise highly controversial fossils the most tangible expression of this event, known as the ‘‘calcichordates’’ (32), which seem to have been largely protective, even I thank Sandra Last for typing numerous ver- sions of this manuscript, Sharon Capon and show a puzzling combination of echino- though the proportion of animals with Dudley Simons for technical assistance, and derm and chordate characters. robust hard-parts in the original commu- Stefan Bengtson and for gener- The fossil record of the earliest chor- nities was small (11). ously providing photographs (Fig. 2d and Fig. 2 dates remains sporadic, but new fossil There is also continued interest in the f and g, respectively). Critical remarks by Nick discoveries are beginning to fill in the role of genomic change, especially with Butterfield and an anonymous referee are ap- picture. From Chengjiang, these include respect to the homeotic genes. Although preciated. My work is supported by the Natural Environment Research Council, Leverhulme the Cathaymyrus and, they are clearly of central importance in Trust, Royal Society, and St. John’s College PERSPECTIVE more sensationally, two types of agnathan the definition of bodyplan architecture, (Cambridge, U.K.). This is Cambridge Earth (33) (Fig. 2a). The proposal (3) that there is a risk of losing the overall evolu- Sciences Publication 5933.

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