Evolutionary Exploitation of Design Options by the First Animals with Hard Skeletons Author(s): R. D. K. Thomas, Rebecca M. Shearman, Graham W. Stewart Source: Science, New Series, Vol. 288, No. 5469 (May 19, 2000), pp. 1239-1242 Published by: American Association for the Advancement of Science Stable URL: http://www.jstor.org/stable/3075264 Accessed: 22/09/2008 16:28

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http://www.jstor.org REPORTS that do not come directly from the epicenter. The generation process of such a surface EvolutionaryExploitation of wave is reproduced here from the real records, and its physical mechanism is inter- Design Options by the First preted as refraction to compensate for a wavefront discontinuity. Animals with Hard Skeletons To confirm the interpretation of the ground motion pattern, we performed ray R. D. K. Thomas,* Rebecca M. Shearman,t Graham W. Stewartt tracing for Love waves in models of the structure in the Kanto basin (9, 10). The The set of viable design elements available for animals to use in building S-wave velocities in the basement and sed- skeletons has been fully exploited. Analysis of animal skeletons in relation to imentary layers are estimated from P-wave the multivariate,theoretical "SkeletonSpace" has shown that a large proportion data because they are not well constrained of these options are used in each phylum. Here, we show that structural from the previous studies. The model for elements deployed in the skeletons of BurgessShale animals (MiddleCambrian) ray tracing uses the local-mode approxima- incorporate 146 of 182 character pairs defined in this morphospace. Within 15 tion (11), employing a 100 x 100 grid with million years of the appearance of crown groups of phyla with substantial hard a spacing of 2.00 km (E/W) and 1.75 km parts, at least 80 percent of skeletal design elements recognized among living (N/S). A horizontally layered structure is and extinct marine metazoans were exploited. retrieved from the three-dimensional (3D) structural model at each point, and the Fundamentallydifferent strategies for construct- skeletal designs of these early metazoans? phase velocity of the fundamental mode of ing hardskeletons emerged in the evolutionof To what extent were changes in the genetic the Love wave is then calculated for each each animalsubkingdom (1) now recognizedon basis of pattern formation, the expansion of grid point at a period of 8 s. We carried out the basis of ribosomalRNA sequences (2, 3) taxonomic diversity, and the exploitation of ray tracing in this phase velocity distribu- and patters of early embryonicdevelopment design options concurrent? tion with the shooting method (12). The (4). The Ecdysozoa(2) consist largely of ani- Our theoretical morphospaceis based on calculated rays were traced to 40 s after the mals that molt their skeletonsperiodically, as seven general propertiesof animal skeletons origin time of the earthquake (Fig. 2C). the name implies. The Lophotrochozoa(3, 5) or their components. Each has two, three, or Because rays are defined as normal to a includeprotostomes with externalskeletons that four broadly defined states, illustrated here wavefront, the tips of the rays indicate the typically grow by accretion.Internal skeletons schematically and by examples drawn from theoretical wavefronts at 40 s, which agree that can be remodeled,especially in more de- animalsof the Burgess Shale, of early Middle well with the observed wavefronts. rived taxa, are characteristicof the Deuterosto- Cambrianage, in British Columbia (Fig. 1): mia. The SkeletonSpace (6, 7) is a theoretical 1) A skeleton may be internal, as in the References and Notes morphospacethat providesa framework,inde- elephant, or external, as in the lobster. 1. T. H. F. D. M. W. Heaton, J. Hall, J. Wald, Hailing, pendentof time and the charactersof The skeleton be of Science 267, 206 (1995). any given 2) may composed rigid 2. S. Kinoshita,Seismol. Res. Lett. 69, 309 (1998). groupof organisms(8), in which to assess rates material like vertebratebone, or it may be 3. Japan Meteorological Agency, On Seismic Intensity and patters of exploitationof morphospaceby flexible like the notochord of the lancet. (Gyosei, Tokyo, 1996). these animals. We use it here to analyze the 3) A skeleton may consist of one element, 4. S. Zama, Proceedings of the 10th WorldConference on Engineering, 19 to 24 July 1992, Madrid, Spain initial,early Cambrianemergence of hardparts as in most snails; two, like the bivalved shells (A. A. Balkema, Rotterdam, Netherlands, 1992). that complemented,and to varyingdegrees re- of animals evolved independentlyin several Surface waves induced from S body waves at a skeletonsof metazoansthat different classes and or ele- basin are known as another kind of seismic placed,hydrostatic phyla; multiple edge evolved to sizes. phenomenon related to a sedimentary basin [E. D. larger ments, as in crinoids and crabs. Field, Bull. Seismol. Soc. Am. 86, 991 (1996)]. Such A spanof 40 millionyears (9) embracesthe 4) In shape,the partsof skeletonsare essen- waves are expected to have been generated for this appearanceof the first small, simple shells that rods, or solids. Rods define and but would be buried in the well-devel- tially plates, earthquake, have been secreted metazoansand the like the oped Love wave coming from the source region. may by supportspatial frameworks, scaffolding 5. K. Yomogida and J. T. Etgen, Bull. Seismol. Soc. Am. subsequentexuberant diversity of Chengjiang formedby sponge spicules,or they are used as 83, 1325 (1993). (10) andthe BurgessShale (11-14). This is not levers, like vertebratelimb bones. 6. K. B. R. R. Interlocking Olsen, J. Archuleta, J. Matarese, Science so shorta time for an like those of tortoise shells and sand 270, 1628 (1995). evolutionary"explosion." plates, 7. T. Sato, R. W. Graves, P. G. Somerville,Bull. Seismol. However,the proliferationof animalswith the dollars,enclose space.A cone is a foldedplate; Soc. Am. 89, 579 (1999). well-differentiatedhard parts characteristicof we set these apartbecause they are so widely 8. S. H. T. T. Kinoshita, Fujiwara, Mikoshiba, Hoshino,J. specificmetazoan was restrictedto used as exteral skeletons.Three-dimensional Phys. Earth40, 99 (1992). phyla largely 9. K. Koketsuand S. Higashi,Bull. Seismol. Soc. Am. 82, the last 15 millionyears of this interval(15). We solids are typically machine parts, like ankle 2328 (1992). addressthree issues: How rapidlywere the op- bones, vertebrae,and teeth. 10. H. Suzuki,Rep. Nat. Res. Inst. EarthSci. Disast. Prev. of skeletal taken in Growthof a skeleton 77 portunities morphospace up 5) that must function 56, (1996). this 11. J. H. Woodhouse, Geophys.J. R. Astron. Soc. 37, 461 evolutionary radiation? What patterns continuously as it develops can be accom- (1974). of change over time are expressed in the plished by accretion, as in molluscan shells; 12. V. I. A. I. in Cerveny, Molotkov, Psencik,Ray Method by molting and replacement;by the addition Seismology (Charles University, Prague, 1977). of units to a modular as in colonial 13. We thank the Japan Meteorological Agency; the Department of Geosciences, Franklin& Marshall Col- structure, National Research Institute of Earth Science and lege, Lancaster, PA 17604, USA. organisms;or by the sort of remodeling that Disaster Prevention; the Tokyo Metropolitan Gov- makes ball-and-socket in the Fire the *To whom correspondenceshould be addressed.E- joints possible ernment; Tokyo Department; Prefec- mammals. ture Governments of Kanagawa, Saitama and mail:[email protected] Chiba; and the City Governments of Yokohama, tPresent address:Department of OrganismalBiology 6) Most skeletal parts grow in place, and of Kawasaki, and Sagamihara for providing strong Anatomy,University Chicago,1027 East 57 where they function, but some are motion records. Monbusho Street, IL60637, USA. prefabri- ground Supported by Chicago, cated and then moved into (grant 10490010). :Presentaddress: Rose Center for Earthand Space, working position, AmericanMuseum of Natural History,200 Central such as shark's teeth. 11 January2000; accepted 20 March2000 ParkWest, New York,NY 10024, USA. 7) Multiple components are integratedin

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fourbasic ways. They may stiffensoft material, ACWGNXQ.It consists of multiple, internal, binationsare unrecognizedamong living and without direct contactwith one another.They rigid, jointed rods that are remodeledas they extinct animals.To determinehow rapidlythis may be linked by joints, which provide flexi- growinplace. Given2 x 2 x 3 x 4 x 4 x 2 X exploitation of available morphospace took bility and mechanicaladvantage. They may be 4 combinations of characters,the Skeleton place, we soughtto establisha benchmarkearly suturedor fused together,like the bones of the Spaceembraces 1536 possibledesigns. To sim- in metazoanevolution. We electedto assess the human skull. They may overlap, providing a plify the analysisof this largenumber of cases, occurrenceof design options among animals sliding articulationlike that between tergites, we compare the skeletons used by different found in the Burgess Shale. The fossils are which allows a woodlouseor trilobiteto roll up. groupsof organismsin a matrixof all possible exceptionallywell preserved,detailed descrip- The SkeletonSpace constitutesa system of pairsof characterstates. tions of most taxa are available,and this marine theoreticaldesigns against which the skeletal Thomasand Reif (7) have shownthat more faunahas long been regardedas the epitomeof parts of living and extinct organismscan be than half of these characterpairings are abun- earlymetazoan life (12, 14). compared.Each structureis characterizedby a dantly used, generally by animals in several We determinedthe design formulafor each seven-letterformula that defines its form. The phyla;two-thirds of thesepairings are common. kind of skeletal element present in 104 well- skeleton of the human finger has the formula Only logicallyor functionallyimplausible com- documentedBurgess Shale genera with hard

Fig. 1. The SkeletonSpace (6, 7). The rangeof potentialforms of animal bly: X, growth in place;Y, prefabrication.Interplay of elements: P, no skeletons or their subunitsis defined in terms of seven essential prop- contact;Q, jointed;R, sutured or fused;S, imbricate.Examples: a, Pikaia, erties, each with two to four possible states, yielding a total of 21 notochord;b, Elrathia,exoskeleton; c, Marrella,paired spines; d, Burges- variables.Graphics characterizing parameters of the skeletal morpho- sochaeta,setae; t, Scenella,shell or velum;v, Isoxys,bivalved carapace; w, space are shown on the left. Examplesof skeletal elements from the Emeraldella,thoracic tergites; g, Burgessia,telson; h, Branchiocaris,car- BurgessShale fauna representingeach descriptorare illustratedon the apace;j, Haplophrentis,shell; k, Odontogriphus, teeth; I,Paterina, shell; m, right. Situation: A, internal;B, external.Material: C, rigid;D, flexible. Chaunograptus,thecae; z, Elrathia,exoskeleton; n, Pikaia,notochord; x, Number:T, one element;V, two elements;W, more than two elements. Gogia,plates; y, Wiwaxia,sclerites or paleae;p, Diagoniella,spicules; q, Shape: G, rods;H, plates;J, cones; K,solids. Growth: L,accretionary; M, Leanchoilia,great appendages;r, Saratrocercus,fused spines;s, Anoma- serialunits + branching;Z, replacement/molting;N, remodeling.Assem- locaris,lateral lobes.

1240 19 MAY2000 VOL288 SCIENCE www.sciencemag.org REPORTS parts. These formulasare listed in a database becausedifferent parts of an organismmay have A large proportionof the design options thatincludes comments and quotations from the charactersin common. To comparethese data available for making animal skeletons is rep- primaryliterature, documenting our assessment with a compilationfor all living and extinct resented in the Burgess Shale fauna. Within of each skeletalstructure and any uncertainties marineorganisms (7), we arbitrarilyconsider a 15 million years of the appearanceof meta- thatmay be associatedwith ourinterpretation of characterpairing to be abundantif it is repre- zoans sufficiently large and well-differentiat- its characteristics(16). Frequenciesof the pairs sentedin >50 and commonif it occursin >10 ed to appearin the fossil record (17), at least of characterstates represented among these de- skeletalelements of the BurgessShale animals. 146 of 182 of the options presented by the sign formulaswere tabulated(Fig. 2A). Some Differencesbetween the two data sets are rep- Skeleton Space had been exploited (Table 1). frequenciesgreatly exceed the numberof taxa resentedgraphically (Fig. 2B). Put another way, >80% of characterpairs represented among the design elements ob- served in skeletons of all living and extinct 0e animals were used within the first 6% of the c 0 I. time of metazoan evolution. A i span ~~~~~~~0 0 E The most strikingfeatures of this initialra- 0 0 0 0 z L 3 diationinto skeletal are uJa a h O) s morphospace the high c of u ai iE U _ & frequencies single-elementrods and multi- element, metameric exoskeletons. Rigid 37 301 broadly These reflectthe abundanceof Flexible 9 27 sponges,arthro- and taxa of One element 2 95 88 8 pods, arthropod-like uncertainaffin- The skeletal structuresof these taxa are Two elements 0 74 67 6 ity. linked to the for > two elements 44 161 183 22 simplest possible strategies size. sessile struc- Rods 35 122 141 15 16 31 110 increasingbody They support tureswith limitedcellular in Plates 9 181 169 20 76 37 77 integration spong- es, and house modularanimals with Cones 0 12 11 1 5 6 1 they vary- of differentiation Solids 2 14 16 0 0 0 16 ing degrees anterior-posterior in the arthropod-likeforms. In contrast,three- Accretionary 11 37 44 4 14 11 23 16 17 12 3 dimensionalsolids and structureswhose growth Unit/serial 0 4 4 0 F 0 4 2 2 0 0 involvescontinuous remodeling are F 264 245 17 78 58 128 100 151 0 12 underrepre- Replace/molt sented, the limited diversificationat 0 reflecting Remodeling 1 0 1 1 0 0 1 0 0 0 this time of animalswith internalskeletons. 46 328 In place 336 36 97 74 203 157 188 12 16 48 3 264 1 The small numberof cones in this faunais Prefabrication 0 1 1 0 0 0 1 0 1 0 0 0 1 0 F an artifactof facies and preservation.The Bur- No contact 21 26 32 15 7 2 38 34 9 3 1 16 1 7 1 47 0 gess Shaleaccumulated on a muddysea floor at Imbricate 1 52 53 0 9 7 37 0 49 4 F 6 2 43 0 52 1 the foot of a steep carbonateramp (18). Con- Jointed 3 129 128 4 49 29 54 52 74 2 3 6 0 122 0 132 0 temporaneousand earlier small shelly faunas sutured 21 119 124 Fused, 15 29 36 75 71 54 3 12 20 1 91 0 140 0 favoredshallow platformenvironments, as did archaeocyathidreefs of the Lower Cambrian. B Preliminarydata for the Tommotian stage Rigid o (-530 million years ago), based on faunas of Flexible O o the LenaRiver region in Siberia(19), show that One element o at least 89 characterpairs were alreadyused by Two elements this time. The low frequencyof structuresthat > two elements o grow by serial additionof elementsor individ- Rods ? ? ? ? ? uals reflectsthe absenceof colonial cnidarians Plates 0 o * with hard parts from faunas of this age. This Cones o o O00 may reflect a diversity of zooplankton, on Solids o o o o which cnidariansfeed, that was still limited at Accretionary o o o o o o o o o o this time [(20), but see (21)]. Unit/serial 0 0 00 O0 0 0 o These results lead to the following Replace/molt o * 0 o conclusions: Remodeling O O O o o O O o 1) A large proportion of the available In place o o o o 0 0 morphospace was exploited very rapidly, Prefabrication o o o o o O o o o O No contact* * * o0 0o * * o o Table1. Comparativeexploitation of the Skeleton Space. Imbricate o o * Jointed 0 0 o 0 00 0 o Group Designs used Fused, sutured o * * ? o 0 o 0 Tommotianmetazoans 89 Fig. 2. Exploitationof the SkeletonSpace by animalsof the BurgessShale. (A) Numbersof skeletal Shalemetazoans 146 elements in 104 with hard that exhibiteach of characteristics. Differencesin Burgess genera parts pair (B) Cnidaria(living and extinct) 89 frequenciesof characterpairs between the BurgessShale and latermarine faunas. Among skeletons of Mollusca and 122 all and extinct marine the of each character was scoredas (living extinct) living animals, frequency pair absent (0), Arthropoda and 90 common or abundant Thomasand Reif a character is considered (living extinct) present(1), (2), (3) by (7). Here, pair Vertebrata(living and extinct) 133 to be abundantif its frequencyis 250, andcommon if it is representedin 10 skeletalelements of the All marinemetazoans 178 Shaleanimals. Differences in scoresbetween the two datasets areshown Burgess graphically:bold open All livingand extinctanimals 180 circles,-3; open circles,-2; smallopen circles,-1; smallsolid circles,+1; largesolid circles, +2.

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once animals with skeletons appearedon the distinctive types of skeletal development re- 10. J. Chen, Y. Cheng, H. V. Iten, Eds., The Cambrian and the Fossil Record Nat. Mus. Nat. evolutionarystage. This is consistentwith the flect prescriptive patterns of embryogenesis Explosion [Bull. Sci. Taiwan 10 (1997)]. later rapid exploitation of more narrowlyde- that appearto have evolved long before hard 11. H. B. Whittington, The Burgess Shale (Yale Univ. fined morphospaces,documented for crinoids skeletons emerged (29). Convergentpatterns Press, New Haven, CT, 1985). and other in the Ordovician of diversification in the two 12. S. J. Gould,Wonderful Life (Norton, New York,1989). taxa, (22). evolutionary 13. D. E. G. D. H. Erwin,F. The Fossils clades with the most varied modes Briggs, J. Collier, of 2) Predominanceof serialsegmentation and metazoan the Burgess Shale (Smithsonian Institution Press, design elementsbroadly comparable with those of life reflect common geometric constraints Washington, DC, 1994). of indicates selection of and mechanical function 14. S. Conway Morris, The Crucible of Creation: The arthropods strong, early growth process Shale and the Rise Animals Univ. and on skeletons with different Burgess of (Oxford for rapidduplication subsequentspecializa- radically origins. Press, New York,1998). tion of structuralsubunits (7, 23). Viable design options are fixed point at- 15. A. H. Knoll and S. B. Carroll, Science 284, 2129 The of skeletal elements tractorsthat actual skeletons must approach, (1999). 3) disparatetypes 16. Database availableat that occur in some to the em- www.fandm.edu/Departments/ together organisms (14) leading evolutionaryconvergence Geosciences/faculty/r_thomas.html suggest a low level of morphologicalintegra- phasized by Conway Morris (14). Real ani- 17. A. B. Smith, Evol. Dev. 1, 138 (1999). tion that would later be streamlinedby more mals evolve as strange attractors,far-from- 18. W. D. Stewart, O. A. Dixon, B. R. Rust, Geology 21, even with combinations of 687 (1993). precise gene regulation(24). However, equilibrium systems 19. P. D. Kruse,Yu. Zhuravlev,N. P. James, Palaios 10, the most seemingly bizarre taxa, such as properties that are unpredictable in detail. 291 (1995). Anomalocaris (25, 26), do not have more Rapid exploitation of the Skeleton Space by 20. P. W. Signor and G. J. Vermeij,Paleobiology 20, 297 distinct of skeletal elements than con- early Cambriananimals confirms that evolu- (1994). types 21. N. J. Butterfield,Paleobiology 23, 247 (1994). temporaryarthropods assigned to the Crusta- tion follows rational and consequently pre- 22. M. Foote, Annu. Rev. Ecol. Syst. 28, 129 (1997). cea. Some Burgess Shale crustaceansalready dictablepatterns, as Niklas (32) and McGhee 23. D. K. Jacobs, Proc. Natl. Acad. Sci. U.S.A. 87, 4406 had skeletons as structurallyspecialized as (8) have shown for land plants and a variety (1990). 24. G. E. Budd,Bioessays 21, 326 (1999). those of their close living relatives (27). of animals in the context of analogous theo- 25. H. B. Whittington and D. E.G. Briggs,Philos. Trans.R. 4) Skeletons of terminal Proterozoicand retical morphospaces. Soc. LondonSer. B 309, 569 (1985). earliest Cambriananimals consisted of 26. D. Collins,J. Paleontol. 70, 280 (1996). (28) 27. M. A. D. E. G. R. A. mineralized Wills, Briggs, Fortey,Paleobiology scales and spicules,weakly shells, Referencesand Notes 20, 93 (1994). 1. J. W. Valentine, D. D. H. Erwin, and structuresbuilt with Jablonski, Develop- 28. S. Bengtson, in EarlyLife on Earth, S. Bengtson, Ed. largely radiatingag- ment 851 of The late Cam- 126, (1999). (Columbia Univ. Press, New York, 1994), pp. 412- gregates crystals. rapid, Early 2. A. M. A. Aguinaldoet al., Nature 387, 489 (1997). 425. brianexploitation of opportunitiespresented by 3. K. M. Halanychet al., Science 267, 1641 (1995). 29. J. W. Valentine, D. H. Erwin,D. Jablonski,Dev. Biol. 4. J. W. Proc. Natl. Acad. Sci. U.S.A. 8001 the SkeletonSpace was facilitatedby the par- Valentine, 94, 173, 373 (1996). (1997). 30. P. W. H. Holland,J. Garcia-Fernandez,N. A. Williams, allel evolutionof complex,biologically tailored 5. R. Rosa et al., Nature 772 399, (1999). A. Sidow, Development (suppl.), 124 (1994). constructedfrom a vari- 6. R. D. K. Thomas and W. E. in Constructional multilayercomposites Reif, 31. D.-G. Shu et al., Nature 402, 42 (1999). and N. Schmidt-Kittlerand K. ety of organicand inorganicmaterials. Recur- Morphology Evolution, 32. K.J. Niklas, The EvolutionaryBiology of Plants (Univ. Eds. 283- structuralmaterials Vogel, (Springer-Verlag,Berlin, 1991), pp. of Chicago Press, Chicago, 1997). ring featuresof these sug- 294. 33. We thank D. E.G. Briggs,S. Conway Morris,M. Foote, that their is controlled a _ 341 gest development by 7. , Evolution 47, (1993). E. L.Yochelson, and three reviewers for helpful com- 8. G. R. Theoretical The common regulatorynetwork of genes that was McGhee, Morphology: Concept ments on the manuscript.This work was supported and Its Univ. Press,New York, alreadyestablished in ancestralstem-group bi- Applications(Columbia by the HackmanScholars program, Franklin& Mar- 1999). shall College. laterians(29). 9. S. A. Bowringand D. H. Erwin,GSA Today 8 (no. 9), 1 5) Internalskeletons and growthby remod- (1998). 10 January2000; accepted 15 March2000 eling are uncommonamong the Burgess Shale animals.These optionshave since been exten- sively exploitedby vertebrates,after two dupli- Distinct Classes of Yeast cationsof the Hox gene cluster(30). No causal relation between regulatoryfunctions of Hox genes and the emergenceof internalskeletons Promoters Revealed by has yet been established.However, the duplica- tion of high-levelregulatory genes would have Differential TAF Recruitment made it possible to bypass constraintsset by establishedlower-level linkages, opening the Xiao-Yong Li,* Sukesh R. Bhaumik,* Michael R. Greent way for the establishmentof a novel Bauplan with more independentcontrols over the devel- The transcriptionfactor TFIIDcontains the TATAbox binding protein (TBP)and opmentof local structuralunits. Basal agnathan multiple TBP-associatedfactors (TAFs).Here, the association of TFIIDcompo- chordatesare now knownfrom the LowerCam- nents with promoters that either are dependent on multiple TAFs(TAFdep) or brianof Chenjiang(31), so the fossil recordis have no apparent TAF requirement (TAF,nd)is analyzed in yeast. At TAFdep consistentwith two phases of vertebrateHox promoters, TAFsare present at levels comparable to that of TBP,whereas at duplication,one precedingthe early Cambrian TAFindpromoters, TAFsare present at levels that approximate background.After radiationand the other that could come much inactivation of several general transcriptionfactors, includingTBP, TAFs are still later,in the Ordovician,if it was associatedwith recruited by activators to TAFdeppromoters. The results reveal two classes of the developmentof bony endoskeletons. promoters: at TAFindpromoters, TBP is recruited in the apparent absence of After the divergence of protostomes and TAFs,whereas at TAFdeppromoters, TAFsare co-recruited with TBPin a manner deuterostomes, a major clade within each consistent with direct activator-TAFinteractions. group went in for active locomotion, evolv- ing strong anterior-posteriordifferentiation TFIID is a general Pol II transcriptionfactor the mechanismof action of certainpromoter- and jointed-lever skeletons. In arthropods, (GTF) that initiatestranscription complex as- specific activator proteins (activators) (1). these emerged as exoskeletons; in verte- semblyby bindingto the TATAbox throughits Whereas TBP is a general factor, TAFs are brates,they are predominantlyinternal. These TBP subunit.TFIID has also been implicatedin highly promoter selective, which raises the

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