AMER. ZOOL., 39:617-629 (1999)

The Origin of Bodyplans1

DOUGLAS H. ERWIN2

Department of Paleobiology, MRC-121, National Museum of Natural History, Washington, D.C. 20560

SYNOPSIS. Paleontologists have documented the progressive origination of meta-zoan bodyplans beginning about 610 million years ago (Ma) with the major periodof innovation occurring from 570 Ma to about 525 Ma. The breadth of this eventis now well documented among soft-bodied, skeletonized and trace fossils. Changesin both the phytoplankton and in geochemical markers suggest pervasive trans-formation of the environment during this interval, implicating an ecological rolein triggering this innovative burst. The extent to which developmental innovationscontributed to this evolutionary burst requires placement of the protostome-deu-terostome ancestor (PDA) in time: a PDA close to the radiation could indicate agreater role for developmental innovation. Molecular evidence points to a maxi-mum age of about 670 Ma. Uncertainties over the extent of functional homologiesamong the widely conserved developmental control genes, and gene pathways,bracket plausible dates for such an ancestor: the maximally complex ancestorcould not predate about 545 Ma; the least complex alternative could date to 575Ma or even earlier. The nested hierarchical structure of developmental controlgenes and bodyplan originations suggests certain temporal inhomogeneities to theevolutionary process: as certain developmental patterns are established they limitsubsequent evolutionary trajectories.

INTRODUCTION

George Gaylord Simpson began Tempoand Mode in Evolution, his magnificentcontribution to evolution's modern synthe-sis, with the following words: "How fast,as a matter of fact, do animals evolve innature? That is the fundamental observa-tional problem that the geneticist asks thepaleontologist" (Simpson, 1944 p. 3). Re-placing geneticists with developmental bi-ologists, we can paraphrase Simpson byasking: How fast, as a matter of fact, dobodyplans evolve in nature? Although it isno doubt true, as Sean Carroll was recentlyquoted as remarking, that the search for theprotostome/deuterostome ancestor is "Do-ing paleontology without fossils." (Di-Silvestro, 1997 p. 729), the current func-tional role of shared developmental controlgenes is not an unambiguous guide to then-function in the last common ancestor (Miill -er and Wagner, 1996). Moreover, the fossil

1 From the Symposium Developmental and Evolu-tionary Perspectives on Major Transformations inBody Organization presented at the Annual Meetingof the Society for Integrative and Comparative Biolo-gy, 3-7 January 1998, at Boston, Massachusetts.

2 E-mail: Erwin.Doug@NMNH.SI.EDU

record provides the only available con-straints on the rates and timing of evolu-tionary innovations (which was Carroll'sactual point; Carroll, personal communica-tion 1998). The first appearance of a cladewith a particular biological innovation setsonly a minimum estimate on the time oforigin of the clade. The actual time of di-vergence of the group may be considerablyearlier, and the point of origin of particularmorphological or developmental innova-tions is not necessarily congruent with lin-eage divergence.

The fossil record provides constraints onthe timing of morphological, and by exten-sion, developmental, innovations recog-nized as bodyplans. For those innovationswhere the first appearance in the fossil re-cord can be established to coincide closelywith the time of origin (i.e., where the na-ture of the innovation necessarily will ap-pear in the fossil record relatively rapidly),first appearances may also provide impor-tant information on the environmental con-text in which these innovations occur. Thisallows testing of alternative models for theassociation of innovation with environmen-tal change, ecological context and devel-

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opmental novelties. Are evolutionary radi-ations driven by new ecological opportu-nities, as suggested by many models ofadaptive radiations (e.g., Schluter, 1996)?By changes in the physical environmentwhich create ecological opportunities? Ordo morphological innovations derive fromthe possibilities created by new develop-mental programs? Our ultimate goal in con-sidering the origin of bodyplans must be toconsider not only the developmental eventswhich permit, or even encourage morpho-logical innovation, but also the perplexingquestion of why such innovation is clus-tered in the history of life.

Consider dinosaurs. The discovery ofHerrarsaurus and other early dinosaursfrom the Ischigalasto sequence in Argentinaand a subsequent phylogenetic analysis ledSereno (1997) to argue that the primary lin-eages of dinosaurs were established by theCarnian Stage of the Late Triassic, and ev-idently contemporaneous with the origin ofthe clade as a whole. Now as any five yearold could show us, later dinosaurs discov-ered a host of architectural modifications,but the point is that early dinosaurs quicklyestablished the major architectural groupswhich were to define the group for the suc-ceeding 135 million years. Yet all of thishappened before dinosaurs become ecolog-ically significant components of terrestrialfaunas: the morphologic radiation which es-tablished the major dinosaur bodyplans ap-pears to have been essentially decoupledfrom the later, Early Jurassic, ecological ra-diation of the dinosaurs.

The dinosaur radiation is just one ofmany in the fossil record which suggest thatmajor morphological innovations may oc-cur independently of significant open eco-logical space, seemingly contradicting oneof the central postulates of many views ofthe origin of bodyplans. In this contributionI wil l first address alternative models for theorigin of bodyplans during the "Cambrian"explosion and then turn to the geologicalcontext of the event and the extent to whichit can constrain both the timing and the na-ture of bodyplan innovation, in particularthe age of the last "urbilateria" or the lastcommon ancestor of the protostomes anddeuterostomes.

METAZOAN DIVERGENCE: EARLY OR LATE?

A literal reading of the fossil record sug-gests that virtually all metazoan bodyplansappear rapidly during the late Neoprotero-zoic and Early Cambrian, between about600 million years ago (Ma) and about 520Ma (e.g., Valentine, 1986; Valentine andErwin, 1987; Valentine et al., 1991), pos-sibly with more concentrated bursts withinthis interval. Many authors, beginning withCharles Darwin, have been unwilling to ac-cept such rapid rates of evolutionarychange, arguing either that vagaries of thefossil record had simply failed to preservethe gradual unfoldings of new morpholo-gies, or that such transitions had somehowbeen hidden from the fossil record.

There are three possible explanations ofthis pattern. First, the fossil record could bea reasonably faithful record of both the di-vergence of the major metazoan lineagesand the acquisition of their distinctive bod-yplans. Alternatively, metazoan divergenc-es may be effectively decoupled from theacquisition of bodyplans, with the diver-gences of the lineage greatly preceding the'Cambrian' radiation (for recent restate-ments of this view see Fortey et al., 1997,1996). This view has a lengthy pedigree,and embraces those who view the Cambrianradiation as primarily associated with thedevelopment of skeletons and durable hardparts, to others who argue for a lengthy pe-riod of Proterozoic divergence, perhaps as-sociated with a planktonic life style (e.g.,Cohen and Massey, 1983; Boaden, 1989;Davidson, et al. 1995).

Since the Cambrian metazoan radiationaffects a large number of lineages, this viewdemands a change in the external environ-ment as a trigger for the evolutionarychanges. A third alternative invokes an ex-ponential diversification of lineages (Sep-koski, 1979), with lineages during the pre-expansion phase simply too uncommon tobe preserved. Thus the apparent explosivephase of the Cambrian may reflect an in-crease in the probability of preservation dueto increased abundance, rather than a bio-logical event.

The advent of the molecular clock ap-peared to present a means to test the depth

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of lineage divergence independent of thefossil record (Runnegar, 1982, but see Er-win, 1989). More recently Wray et al.(1996) conducted a thorough analysis basedon seven genes with a variety of differentfunctions. Their results indicate a prolongedradiation of animal phyla, with suggesteddivergence times of 1,200 Ma for the pro-tostome-deuterostome split, and 1,000 Mafor the echinoderm-chordate split. If accu-rate, these divergence times would requirethat the lineage divergences leading tomodern bodyplans were far more ancientthan the acquisition of the distinctive mor-phologies.

Although these results are already takingon the status of orthodoxy {e.g., Arthur,1997) the Wray et al. results remain contro-versial. Wray et al. elected to not recalibratethe sequence data, likely compounding theapparent rates of substitution {e.g., Van derPeer et al., 1993). Additionally, the diver-gence points of interest are extrapolated farbeyond the vertebrate calibration dates,rather than interpolated between calibrationdates, rendering relative rate tests particu-larly important. Nikoh et al., (1997) criti-cized the suitability of the mitochondrial se-quences and recalculated the cytochromeoxidase subunit I protostome-deuterostomedivergence to 900 Ma rather than 1,300 Ma.Their analysis of aldolase and triose phos-phate isomerase molecular clocks dated thesponge-eumetazoan split to about 940 Ma,and the amphioxis-vertebrate split to about700 Ma (Nikoh et al, 1997). Wray et al.also dismiss the alternative possibility, aburst of greatly increased substitution rates,arguing that this would require far greatersequence divergences than have been iden-tified. In merely the latest documentation ofincreased substitution rates, Friedich andTautz (1997) documented a 20-fold increasein 18S rDNA associated with the founda-tion of the Dipteran insect clade; such aburst during the late Neoproterozoic wouldaccommodate the Wray et al. data within aradiation of 40 million years or so, consis-tent with the fossil record. Other data alsosuggest a burst of increased substitutionrates early in metazoan history {e.g., Cav-alier-Smith et al., 1996).

A variety of methodological problems

with the Wray et al. study have been iden-tified by Ayala et al. (1998), particularly inthe calibration of the clock using slowlyevolving vertebrate sequences to infer sub-stitution rates among more rapidly evolvinginvertebrate clades. These authors concludethere is littl e support for either the methodsor results of the Wray et al. study. Theiranalysis of 18 protein coding genes pro-duced an estimated divergence time ofabout 670 million years ago for the proto-stome-deuterostome ancestor and about 600million years ago for the divergence ofechinoderms and chordates, dramaticallyreducing the apparent discrepancies be-tween the molecular clock and fossil esti-mates of divergence times.

The molecular clock clearly does notprovide a straightforward view of diver-gence times. The Ayala argument permits(although does not require) a maximum"missing" record of perhaps 130 millionyears at most—a considerable length oftime, but far less than claimed by Wray etal. (1996). Thus any decoupling of lineagedivergence from bodyplan formation wouldhave been far more limited than many au-thors have suggested. The argument thatmuch of the early phase of the metazoanradiation simply occurred below the thresh-old for fossilization is possible, but neglectsa variety of other evidence supporting thereality of this explosive burst of diversifi-cation during the late Neoproterozoic andEarly Cambrian. Thus, at present, we can-not rule out the possibility of divergencewell before 600 Ma, but the fossil recordappears to be a faithful record of the ac-quisition of major bodyplans.

THE NEOPROTEROZOIC-CAMBRIANTRANSITION

Calculating evolutionary rates requires areliable temporal framework, and this isavailable only through precise determina-tion of radiometric dates for the interval ofinterest, combined with reliable correlationbetween different regions. Fortuitously, twoof the regions with better records of lateNeoproterozoic-Early Cambrian fossils, Si-beria and Namibia, also contain abundantvolcanic ash beds interbedded with fossilsand suitable for radiometric dating. The

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base of the Cambrian is now confidentlydated at 543 million years ago (Ma) and thebase of the Tommotian Stage, associatedwith the "explosive" burst of the Cambrianradiation, occurs at 530 Ma (Bowring et al,1993). New dates indicate the Early Cam-brian ended about 509 Ma. (Landing et al,1998). Volcanic ash beds associated withsoft-bodied Ediacaran fossils in the lateNeoproterozoic sequence of Namibia, inconjunction with stratigraphic correlationsto other Ediacaran localities, has revealedthat the diverse Ediacaran assemblage isyounger than 549 Ma, with the less diverseassemblages extending back to about 570Ma (Grotzinger et al., 1995). This is a star-tling change from the view only a few yearsago that the Ediacaran fossils dated to 650Ma or so, and were separated from the ear-liest Cambrian fossils by a non-fossiliferousgap of at least 30 million years. This tem-poral framework allows us to establish thesequence of biological and physical eventsduring this interval with a far higher degreeof precision than previously (Fig. 1).

Geological patternsThe late Neoproterozoic was a dynamic

geological interval. The period began withat least four continental glaciations, each ofwhich are associated with pronounced shiftsin the carbon and sulfur cycles of the at-mosphere and oceans (Kaufman et al,1997) and a probable increase in atmo-spheric oxygen (Canfield and Teske, 1996).(Claims for a rapid reorganization of con-tinents [Kirschvink et al., 1997] rely on in-adequate radiometric dates, and, in anyevent, postdate the late Manykaian onset ofthe Cambrian phase of the radiation).

Biological patterns: The LateNeoproterozoic

Three semi-independent lines of evi-dence illuminate the diversification of ani-mals (or animal-like groups) during the lateNeoproterozoic: the fossils of soft-bodiedorganisms known as the Ediacaran Fauna,trace fossils, the burrows and trails preserv-ing the behavior of unknown animals, and,most recently, direct evidence of metazoanlarvae. One critical question about thesefossils is whether they harbor evidence of

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Atdabanian •Tommntian ^

Manykaian

Ediacaran —2Faunas ^

•̂t Burgess Shale Faunat

.^A Chengjiang Fauna- ^ ( First Trilobites

.^0 Onset of Cambrian^ explosion

1 Assemblage III

M Assemblage

% Precisely dated volcanic ash beds

FIG. 1. Chronology of the late Neoproterozoic-EarlyCambrian interval showing the major biological eventsand divisions of geological time. The soft-bodied Edi-acaran faunas are divided into three assemblages. As-semblage I dates to 610-600 Ma and is known onlyfrom the MacKenzie Mountains of western Canada.The other two assemblages have progressively morediverse and complex organisms (Narbonne et al.,1994). Radiometric dates are from Bowring et al.,1993, Grotzinger et al, 1995 and Landing et al., 1998.

either protostomes or deuterostomes, andthus whether the common ancestor lies be-fore or after this interval. Regrettably, con-clusive evidence is frustratingly sparse.

The Neoproterozoic sequence in theMackenzie Mountains of northwestern Can-ada contains three distinctive assemblagesof Ediacaran elements (Narbonne et al.,1994). The oldest, dating to about 610 to600 Ma, are simple centimeter scale discsand are found below the youngest Neopro-terozoic glacial sediments. The second as-semblage dates from about 575 Ma to 549Ma, is found world-wide and includes atleast nine genera of discoidal fossils. As-semblage III extends from 549 Ma to 543Ma and includes the full diversity of discs,fronds and seemingly segmented forms.

Three approaches are available for deter-mining the phylogenetic position of these

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fossils. The first is through gross morpho-logic similarity with living groups. In thisapproach the apparently segmented organ-ism Dickinsonia is allied with the annelidworms, the fronds Charnia and Charnod-iscus are allied with pennatulacean octocor-als and so forth {e.g., Glaessner, 1984;Gehling, 1991; Jenkins, 1992). Gross mor-phologic similarity is frequently misleadinghowever, and this approach provides fewsafeguards against convergence, particular-ly when dealing with such enigmatic forms.More recently, Waggoner (1996) has pio-neered the use of discrete character statesto assess phylogenetic relationships amongthe Ediacaran fossils. His results place sev-eral forms with an apparent cephalic shieldand segmentation (e.g., Spriggina and Par-vancorina) within the Arthropoda. Such an-alyses depend critically on the presumedhomologies identified through the characteranalyses and many of the character assign-ments are open to dispute. The third alter-native involves assessing the evidence pre-sented by the fossils to interpret the natureof the original morphology. This approachled Seilacher (1989) to propose that manyof the Ediacaran forms constituted a cladeof multicellular organisms independent ofthe metazoa, although he later modified thisview (Buss and Seilacher, 1994; see alsoRunnegar, 1995). A similar approach to therecently redescribed Kimberella (Fedonkinand Waggoner, 1997) suggests that it is atriploblastic, benthic organism with a broad,well-muscled foot and a broad visceral cav-ity. Such an organism would have requiredat least a hemaeocoel. No appendages arepresent (as is true of all Ediacaran forms)nor is a mouth apparent. Although this isnot clearly a mollusc (Fedonkin and Wag-goner's preferred interpretation) or even aprotostome, it is more complex than a cni-darian.

The first two approaches have led a va-riety of investigators to suggest that arthro-pods, annelids, echinoderms and other pro-tostomes are found in the Ediacaran fauna,and thus that the protostome-deuterostomeancestor (PDA) predated about 570 Ma.The presence of Kimberella certainly sup-ports the presence of triploblastic animalslate in the Neoproterozoic, and if the origin

of the bilateria coincides with the origin oftriploblastic animals, then this view of theearly origin of the PDA is correct. How-ever, triploblastic bilateria must predate thelast common ancestor of extant protostomesand deuterostomes (PDA), perhaps by aconsiderable amount. Those who would as-sign Ediacaran fossils to protostomes anddeuterostomes have generally failed toidentify any diagnostic characters whichunambiguously support such assignments.At present then, claims of a higher meta-zoan affinity must be regarded as unproven.The first body fossils with mineralized skel-etons appear late in the Neoproterozoic(Grotzinger et al., 1995). All are minuteshells: three are conical, with at least onebeing closed at the apex. The conical formscould be cnidarians (Knoll et al., 1995) or"pseudocoelomate" bilaterians, thoughconical skeletons are not known in such an-imals.

The trails and burrows of the late Neo-proterozoic provide another line of evi-dence into the metazoan complexity of thetime. Although often considered as unrelat-ed to the Ediacaran body fossils, Gehling(1991) argues that smaller, bilateral Edi-acaran elements may have produced someof these trace fossils. The architecturalcomplexity of trace fossils increasesthrough the late Neoproterozoic, particular-ly during Assemblage III . Crimes (1994)has described a progressive increase incomplexity, and while quantitative confir-mation of this pattern has failed (Matt Kos-nick, personal communication 1997) it cap-tures in broad outline the changes seen dur-ing this interval. Critically, no substantialpenetrating burrows (indicating a coelom)nor evidence of locomotory appendageshave been observed before the ManykaianStage of the Early Cambrian. Thus neitherbody fossils nor trace fossils provide com-pelling evidence of a PDA older than 544Ma.

The final, and most recent line of evi-dence began with the discovery of fossil-ized metazoan embryos from the earliestCambrian of China and Siberia, including ascyphozoan and a segmented worm (Bengt-son and Zhao, 1997). Xiao et al. (1998)have reported similar material from the

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Doushantou Formation in southern China,including probable bilaterians. Althoughconfirmation of the assumed phylogeneticaffinity of this material wil l require furtherwork, these exciting discoveries have intro-duced a new line of evidence. The infor-mation presented in Xiao et al. suggeststhat bilaterians, and possibly protostomes,were present near 570 Ma. This would pre-date the fossil evidence for these groups byat least 10 million years. Perhaps of greatestsignificance, this work establishes a newline of evidence in the search for the originof metazoa.

Biological patterns: The Early CambrianAlthough a few conical tubes of uncer-

tain affinities are found in the latest Neo-proterozoic, the true development of skel-etonized animals began late in the first stageof the Lower Cambrian. But an overempha-sis on skeletonization misses the larger eco-logical story, for the fossil record docu-ments increased diversity and complexityamong the plankton, trace fossils andthrough windows into rarely preservedmetazoans as well.

A variety of conical, tubular and spicularfossils, known collectively as the smallshelly fauna gradually during the last 3 to6 million years of the Manykaian Stage inboth Siberia (Kaufman et al., 1996) andMongolia (Brasier et al., 1996) and becomevery diverse and widespread during theoverlying Tommotian stage. Earlier studiessuggested the small shelly fossils appearabruptly at the base of the TommotianStage, but intensive field work has demon-strated that this was an artifact, and ap-pearances of the small shelly fossils arespread across perhaps ten million years,with the appearance of molluscs, brachio-pods, echinoderms and other major groupsextending from the late Manykaian Stageinto the Atdabanian Stage, an interval of atleast 15 million years.

As in the underlying late Neoproterozoic,trace fossils provide important informationon the diversity of body plans present. Al-though the first arthropod body fossils ap-pear at the base of the Atdabanian Stage,the discovery of the arthropod trace fossilRusophycus avalonensis from Manykaian

age-equivalents in Australia (Mcllroy et al.,1997) and probable late Manykaian rocksfrom Mongolia (Goldring and Jensen,1996) indicates that members of the Ecdy-sozoa with appendages had become estab-lished by this time.

Microfossils reveal an equally complexhistory during the late Neoproterozoic andEarly Cambrian. The organic-walled micro-fossils known as acritarchs are a diverse as-semblage, probably including unicellularprokaryotes, phytoplankton, and other taxa.They experienced several cycles of diver-sification and extinction during the lateNeoproterozoic, with a notable drop closeto the Neoproterozoic-Cambrian boundary.During the Early Cambrian spiny acritarchsunderwent a remarkable radiation in diver-sity. Butterfield (1997) argues that this di-versification primarily, or perhaps entirely,involves the phytoplankton, a relatively in-significant component prior to the Cambri-an. Small planktic metazoans that grazedupon phytoplankton appear and diversify atthe same time. Indeed, Butterfield (1997)suggests that the establishment of the me-sozooplankton may have triggered the ex-plosive radiation of Early Cambrian phy-toplankton, and through them, caused thechanges which led to the Cambrian radia-tion.

In summary, the fossil record indicatesthe presence of simple, diploblastic-gradeorganisms by 610 Ma, followed by bilater-ian, triploblastic animals near 570 Ma.There is no evidence for lineages unambig-uously assigned to either protostome ordeuterostome lineages prior to the earliestCambrian, near 535 Ma. An important fo-cus of future work in the terminal Neopro-terozoic will be to determine whether un-ambiguous protostomes or deuterostomesare present in rocks of this age.

The small shelly fossils, the centimeter-sized soft-bodied animals which producedburrows and trails, the growth of phyto-plankton and the planktic metazoans whichfed upon them, the wild profusion of ani-mals, particularly arthropods, in the Che-ngjiang and later Burgess Shale faunas,and, most obviously, the rapid diversifica-tion of skeletonized animals—all demon-strate the phylogenetic breadth of lineages

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involved in the Early Cambrian phase of theradiation. The radiation of so many diverselineages implicates a change in the physicalenvironment (Erwin, 1992). What remainsunclear, but perhaps the most intriguing is-sue of all is the extent to which the Cam-brian radiation was driven solely by eco-logical and environmental factors? In otherwords, is the Cambrian radiation simply anecological release resulting from a changein the environment, or were there other crit-ical innovations during the radiation itselfwhich were necessary for the outcome? Theanswer to this question lies in the detail ofmetazoan phylogeny and the evolution ofthe developmental process.

THE SEARCH FOR THE COMMON ANCESTOR

Metazoan phylogeny

Ten years ago the publication of the first18S rRNA analysis of metazoan phylogenybegan a continuing revolution (Field et al.,1988). Prior to 1988, invertebrate zoologistshad achieved a consensus that reflected ex-haustion over the intractability of the mor-phological data as much as it did a reliableunderstanding of patterns of descent. Agrowing body of sequences, coupled withincreasingly powerful analytical techniqueshave produced an entirely new view ofmetazoan phylogenetic relationships. Al-though 18S rRNA has now been joined byother sources of molecular data, many un-certainties persist, in part because severallines of evidence suggest caution in relyingupon the results of 18S rRNA analyses(Marshall, 1997; Maley and Marshall,1998). Despite these continuing difficulties,certain results appear to be moderately ro-bust, and of considerable significance in in-terpreting the evolution of bodyplans.

Does the last common ancestor of theprotostomes and deuterostomes also markthe origin of the bilateria, or is there a dis-tinctive clade of bilaterian animals lying be-tween cnidarians and the PDA? Several re-cent molecular studies suggest the aschel-minthes do not form a monophyletic assem-blage branching before the PDA, but are apolyphyletic assemblage of degenerate pro-tostomes {e.g., Winnepenninckx et al.,1995). Some uncertainties persist, particu-

larly over the position of nematodes {e.g.,Winnepenninckx et al., 1995 vs. Aguinaldoet al., 1997). Platyhelminthes may be poly-phyletic (Carranza et al., 1997) but at leastsome appear to lie within the protostomes(Balavoine, 1997; Carranza et al., 1997).These results suggest that the origin of ex-tant bilaterian clades may correspond withthe PDA, but this does not mean that nowextinct bilaterian, but pre-PDA, lineages didnot exist during the Neoproterozoic andCambrian (Valentine, 1994). Above thePDA, there is reasonable agreement on theaffinities of the major deuterostome groups,and on the division of an arthropod clade,or ecdysozoa, and a separate clade of eu-coelomate protostomes known as the lopho-trochozoa (Aguinaldo et al., 1997; Halan-ych et al., 1995).

The Protostome-Deuterostome ancestorDespite the magnitude of the develop-

mental, morphologic and phylogenetic di-vide between protostomes and deutero-stomes, extensive conservation of regula-tory sequences has been revealed betweenthe two groups. Many of the regulatorygenes shared among distantly related ani-mals (see Table 1) have been used to infernot only the genetics of the PDA, but itsmorphology as well. For example, the pres-ence of Pax-6 and its homologs has beentaken to imply the presence of eyes in theircommon ancestor (Haider et al, 1995a, b).By similar logic, the role of tinman/Nkx2-5as a mediator of heart development in fliesand mammals (Bodmer, 1993; Harvey,1996) implies the presence of a heart intheir common ancestor. Similar argumentshave been developed for cephalization(Finkerstein and Boncinelli, 1994; Manakand Scott, 1994), limb formation (mediatedby the hedgehog/sonic hedgehog path-way)(De Robertis and Sasai, 1996) and seg-mentation (based on homologies in en-grailed, hairy; Holland et al., 1997; Mulleret al, 1996; De Robertis, 1997).

Combining these inferences yields amodel for a relatively complex ancestralbody plan: an elongate bilaterian animalwith a differentiated head, eyes, a subder-mal longitudinal central nervous system,blood-vascular system with a heart, proxi-

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TABLE 1. Genes conserved between protostomes and deuterostomes that have a role in the regulation ofdevelopment.

Gene

Pzx-oVeyelesssine occulus/Six3? unidentifiedtinman/Nkx 2.5-DMEF2Otxl, Otx2/Otd, Emxl, Emx2/emsforkheadsog/chordin, dpp/Bmp-4spalt/Xsal-1

delta/x-delta-1Hox complex

Polycomb Group

engrailedhairyDistall-tess/DLX

Fringe/radical fringe

apoptosis

lin-12/Notch

achaete-scute Group

Function

anterior CNS/eye regulationanterior CNS/eye pattern formationcGMP cascade in photoreceptionheart/blood vascular systemanterior patterning, cephalizationterminal differentiationDorso-ventral patterning, neurogenesishead specification/anterior CNS devel-

opment in Xenopus, function differsin Drosophila

primary neurogenesisanterio-posterior patterning

controls Hox expression/cell differenti-ation

segmentation

appendage formation (P/D axis)

formation of limb margin (apical ecto-dermal ridge in vertebrates)

programmed cell death

cell-fate specification

cell-fate specification

Distribution

Drosophila, vertebrates

Drosophila, vertebratesDrosophila, mouseDrosophila, vertebratesDrosophila, vertebratesDrosophila, XenopusDrosophila, Xenopus

Drosophila, Xenopuswidespread among meta-

zoansDrosophila, vertebrates

Drosophila, AmphioxisDrosophila, zebrafishnumerous phyla; proto-

stomes and deutero-stomes

Drosophila, chicken

C. elegans, Drosophila,vertebrates

C. elegans, Drosophila,vertebrates

cnidarians, Drosophila,vertebrates

* The functions are those which have been shown to be conserved between the clades in the right column;many genes may have other functions as well. In each case sequence similarity and functional similarity havebeen demonstrated, but in many cases whether the functional similarity is due to homology or convergenceis unclear. References: Bodmer (1993); De Robertis (1997); De Robertis and Sasi (1996); Ferguson (1996);Gellon and McGinnis (1998); Haider et al. (1995a, b); Harvey (1996); Holland et al. (1997); Laufer et al.(1994); Manak and Scott (1994); Muller et al. (1996); Panganiban et al. (1997); and Schierwater and Kuhn(1998).

modistal differentiation of bodywall struc-tures, a considerable degree of anteropos-terior and dorsoventral differentiation, andpossibly segmentation and appendages (DeRobertis and Sasi, 1996; Ferguson, 1996;Ohno, 1996).

Reconstructing the animal in this fashion,however, requires that genomic homologiesnecessarily imply morphogenetic ones (Gil-bert et al, 1996; Muller and Wagner, 1996).The critical information comes not simplyfrom conservation of these developmentalcontrol genes, but the retention of entireregulatory pathways within a functionallyconstrained role. Sequence similarity neednot imply functional homology, and appar-ent functional homology combines bothfunctional conservation (true functional ho-

mology) and functional convergence. Limbformation in arthropods and vertebrates,clearly non-homologous at a morphologicallevel, nonetheless involves deep similaritiesat a developmental level, including the ac-tivity of: hedgehog, patched, and decapen-taplegic in Drosophila imaginal disks andtheir vertebrate homologs Sonic hedgehog,Patched, and bone morphogenic protein-2(Laufer et al., 1994) and distalless and itsvertebrate orthologs, (Panganiban et al.,1997; Shubin et al, 1997). The apparenthomology of the blood vascular system,controlled by tinman/Nkx2-5 poses a similarproblem. The blood vascular system in deu-terostomes and haemocoel in protostomesare both fluid-filled spaces whose morpho-logic homology has not been demonstrated.

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ORIGIN OF BODYPLANS 625

Deuterostomia

Ecdysozoa

I Lophotrochozoa

Chord ataUrochordataHemichordataEchmodermata

PnapulidaKinorynchiaArthropod aTardigradaOnycophoraNematodaNematamorpha

BryozoaBrachiopodaPhoronidaPlatyhelminthesMolluscaSipunculidaPogonophoraAnnelidaEchiuraNemertinaEntoprocta

Cnidana

Ponfera

FIG. 2. Metazoan phylogeny based on 18S rDNA,based largely on Aguinaldo et al., 1997 and Halanychet al., 1995, and references therein.

Just as coeloms have arisen independentlythe blood vascular system may also be aconvergent feature.

Examining the fossil record in light ofmetazoan phylogeny provides an indepen-dent framework for evaluating the molecu-lar developmental data. One of the moststriking features of the phylogeny depictedin Figure 2 is the position of priapulans andnematodes within the protostomes, ratherthan as members of the now-dispersedpseudocoelomate group that lay outside theprotostome-deuterostome clade. If this to-pology is correct, it permits the assembly ofan exceedingly simple PDA, at about thesame morphological grade as a primitiveflatworm, lacking even a haemal system.This minimalist portrait is consistent withthe molecular phylogeny and sets a lowerbound on the complexity of the PDA, withthe upper bound set by an assumption thatshared sequence similarity in regulatorygenes implies shared morphological func-tions. The actual position of the ancestorlies within this range of possibilities.

Because we do not know the architectur-al grade of the PDA, we cannot place it inthe sequence of tracks and burrows of in-creasing complexity known from the late

Neoproterozoic fossil record. But those dis-tinctive traces do allow us to characterizethe timing of appearance of morphologicalgrades through the metazoan radiation. Edi-acaran Assemblage I contains only cnidar-ian resting traces. The earliest late Neopro-terozoic traces (e.g., Geyer and Uchman,1995) dating to about 565 Ma require abody plan with a fluid skeleton antagonizedby muscles, and thus an architectural gradegreater than cnidarians or flatworms. Kim-berella is a similar age and supports thisconclusion (although Kimberella could alsorepresent a stem-group bilarerian before thePDA). If the PDA was simple, then all trac-es younger than 565 Ma represent eitherprotostomes or deuterostomes; however, ifthe PDA was complex, late Neoproterozoicfossils are likely pre-PDA bilaterians. Sig-nificantly, recent arthropod phylogenies(Will s et al, 1995; Budd, 1996) includebasal arthropods groups (e.g., anomalocar-ids, opabinids) that may have disturbed thesediment only slightly and so may not haveleft a trace fossil record. Arthropods could,therefore, pre-date the first undoubted ar-thropod trace fossils in the late Manykaian.(This does not effect suggestions above forthe earliest appearance of bilaterians, how-ever).

EVOLUTIONARY UNIFORMITARIANISM

The scope of evolutionary biology hasgreatly enlarged in the past few decades aspaleontologists have exhaustively docu-mented a much richer variety of evolution-ary rates and patterns than previously ac-cepted by most evolutionary biologists. Asthey fulfilled the vision first articulated bySimpson in Tempo and Mode in Evolution,paleontologists have confirmed that evolu-tionary rates are both more rapid, and,slower, than previously accepted. Investi-gations of mass extinctions and other eventsdemonstrate that microevolutionary pro-cesses are often effectively decoupled fromlong-term patterns in the history of lif e(much to the evident dismay of at least oneOxford biologist). More recently, develop-mental biology has similarly reclaimed amore prominent role in evolutionary biol-ogy (Gilbert et al, 1996).

There are clear temporal vectors in the

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626 DOUGLAS H. ERWIN

patterns of the history of life, of which therestriction of the origin of new bodyplansto the lower Paleozoic is among the moreprominent (Erwin et al., 1987). If ecologyand changing environmental context wasthe primary factor influencing the establish-ment of new metazoan bodyplans duringthe late Neoproterozoic-Cambrian, thereshould be littl e reason why, given similarsituations, new bodyplans could not origi-nate now, or at any point in the past 500million years. But the simple, empirical factis that the establishment of new bodyplansis not a frequent event.

Why not? Two possibilities present them-selves. First, and most obviously, the eco-logical and evolutionary conditions whichtriggered the Cambrian radiation (most sig-nificantly available ecospace) have simplynever recurred. The best test of this is theelimination of perhaps 90% of all marineanimal species during the Permian mass ex-tinction. Yet the subsequent biotic recoverydisplays no burst of innovation even vague-ly reminiscent of the Cambrian (Erwin etal., 1987). Yet as deep as this mass extinc-tion was, it may have been insufficient toreset the evolutionary clock to the late Neo-proterozoic (Bottjer et al., 1996).

The second explanation for the reducedpost-Cambrian origination of bodyplans lieswith the structuring of developmental con-trol systems. There is now littl e doubt thatpervasive modifications of regulatory path-ways continue to occur (for two recent ex-amples see Lowe and Wray, 1997 and Av-erof and Patel, 1997). Yet these are modi-fications to a pre-existing developmentalsystem, while the Cambrian radiation ap-pears to be fundamentally associated withthe establishment of that system. As devel-opmental biologists expand their knowl-edge of the breadth of similarities betweenprotostomes and deuterostomes an impor-tant avenue for future research wil l be theextent to which developmental innovationsestablished a framework which constrainedfurther innovation.

Modern physics operates under the Cos-mological Principle, which roughly statesthat the Universe is the same in every placeand in every direction. Evolutionary biol-ogists have long implicitly operated under

a similar principle, which roughly statesthat the nature of the evolutionary processis the same at all times and places. Pale-ontologists have broadened the range ofprocesses, and attendant tempos, encom-passed by this principle but the principleitself has rarely been questioned. But thevery uniqueness of the developmental ho-mologies underlying all complex animals isa powerful argument against such evolu-tionary uniformitarianism. There is everyindication that the range of morphologicalinnovation possible in the early Cambrianis simply not possible today—that the cre-ation of the developmental hierarchieswhich are now so pervasive itself con-strained subsequent architectural repattern-ing. If this is so, an important agenda forevolutionary biology must be to understandthese temporal vectors to the evolutionaryprocess and how they have structured thehistory of life.

ACKNOWLEDGEMENTS

I greatfully acknowledge research sup-port from the Charles and Mary WalcottFund of the Smithsonian Institution and theExobiology Program of NASA. The ideaspresented in this paper were stimulated bydiscussions with Sam Bowring, David Ja-blonski, Charles Marshall and Jim Valen-tine, all of whom wil l doubtless be delight-ed by my acknowledgment that they bearno responsibility for any statements herein.I also thank Francisco Ayala for permissionto cite his work prior to publication and twoanonymous reviewers for comments.

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Corresponding Editor: Gregory A. Wray

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