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A Jurassic ceratosaur from China helps clarify avian digital homologies

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A Jurassic ceratosaur from China helps clarify avian digital homologies
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  ARTICLES A Jurassic ceratosaur from China helpsclarify avian digital homologies Xing Xu 1 , James M. Clark 2 , Jinyou Mo 3,4 , Jonah Choiniere 2 , Catherine A. Forster 2 , Gregory M. Erickson 5 ,DavidW.E.Hone 1 ,CorwinSullivan 1 ,DavidA.Eberth 6 ,SterlingNesbitt 7 ,QiZhao 1 ,ReneHernandez 8 ,Cheng-kaiJia 9 ,Feng-lu Han 1,10 & Yu Guo 1,10 Theropods have traditionally been assumed to have lost manual digits from the lateral side inward, which differs from thebilateral reduction pattern seen in other tetrapod groups. This unusual reduction pattern is clearly present in basaltheropods,andhasalsobeeninferredinnon-aviantetanuransbasedonidentificationoftheirthreedigitsasthemedialonesof the hand (I-II-III). This contradicts the many developmental studies indicating II-III-IV identities for the three manualdigitsoftheonlyextanttetanurans,thebirds.HerewereportanewbasalceratosaurfromtheOxfordianstageoftheJurassicperiod of China (156 – 161 million years ago), representing the first known Asian ceratosaur and the only known beaked,herbivorous Jurassic theropod. Most significantly, this taxon possesses a strongly reduced manual digit I, documenting acomplexpatternofdigitalreductionwithintheTheropoda.ComparisonsamongtheropodhandsshowthatthethreemanualdigitsofbasaltetanuransaresimilarinmanymetacarpalfeaturestodigitsII-III-IV,butinphalangealfeaturestodigitsI-II-III,ofmorebasaltheropods.GivenII-III-IVidentitiesinavians,thesimplestinterpretationisthattheseidentitiesweresharedbyall tetanurans. The transition to tetanurans involved complex changes in the hand including a shift in digit identities, withceratosaurs displaying an intermediate condition. Ceratosaursaresuggestedbymanyrecentstudiestobecloselyrelatedto Tetanurae 1,2 , within which birds are nested, and they are mainly known from the Cretaceous southern hemisphere 3–6 . Our recentexcavations in the Middle–Late Jurassic Shishugou Formation inthe Junggar Basin of western China recovered a new ceratosaur,which is one of the earliest known ceratosaurs. This find sheds new light on the morphological evolution in Ceratosauria and inTheropoda as a whole and particularly the digital reduction patternof theropods.Theropoda Marsh, 1881Ceratosauria Marsh, 1884 Limusaurus inextricabilis   gen. et sp. nov. Etymology.  Limus  , Latin for mud or mire;  saurus  , Latinization of Greek for lizard;  inextricabilis  , Latin for impossible to extricate. Thisname is in reference to the specimens’ inferred death in a mire. Holotype.  Institute of Vertebrate Paleontology and Paleoan-thropology (IVPP) V 15923 is an articulated, nearly complete skel-eton (Fig. 1a, b). Referred material. IVPPV15924isasemi-articulatedskeletonmiss-ing the skull; it is 15% larger than the holotype. Locality and horizon.  Wucaiwan area, Junggar Basin, Xinjiang;Oxfordian upper part of the Shishugou Formation 7 . Diagnosis.  Small ceratosaur with the following autapomorphies:short skull (half as long as the femur); skull and mandible toothless;nasal with a lateral shelf; premaxilla with a convex buccal edge; shortand wide nasal less than one-third of skull roof length and only twice as long as wide; ventral process of lacrimal strongly inclinedanteriorly; slender jugal with rod-like sub-orbital and sub-temporalrami; large external mandibular fenestra about 40% of mandibularlength; flange on anterior margin of scapular blade; radius tightly adhering to ulna, and longer than the latter bone; olecranon processabsent; metacarpal II much more robust than other metacarpals;metacarpal III with sub-triangular proximal articular surface andnon-ginglymoidal distal end; metacarpal I highly reduced and car-rying no phalanges; phalanx II-1 with distinct lateral process prox-imodorsally; pubis with laterally ridged, prominent posterior boot;metatarsusformingastrongtransversearch;robustventralprocessatmedialmarginofproximalendofmetatarsalIII;metatarsalIVnearly straight, appressed against lateral surface of metatarsal III for nearly its whole length; and pedal digit I small, only 17% as long asmetatarsal III. Morphological description and comparison Osteologicalandhistologicalfeaturesindicatethatbothspecimensof  Limusaurus inextricabilis   are young adults, probably between theexponential and stationary phases of growth (Fig. 1c; Supplemen-tary Information). It shares some cranial features with both coelo-physids and other ceratosaurs and also possess some uniquefeatures.  Limusaurus   has a fully developed rhamphotheca. Amongnon-avian theropods, this condition has been previously reportedonly in some Cretaceous coelurosaurs 8 , so this new find extendsthedistributionofrhamphothecaewithintheropodsbothtemporally and phylogenetically.Postcranially,  Limusaurus   displays a single, fused sternal plate.Unquestionable ossified sternal elements have been previously  1 Institute of Vertebrate Paleontology and Paleoanthropology, Beijing 100044, China.  2 Department of Biological Sciences, George Washington University, Washington DC 20052,USA.  3 Natural History Museum of Guangxi, Nanning, Guangxi 530012, China.  4 Faculty of Earth Sciences, China University of Geosciences, Wuhan, Hubei 430074, China. 5 Department of Biological Science, Florida State University, Tallahassee, Florida 32306, USA.  6 Royal Tyrrell Museum, Drumheller, Alberta T0J 0Y0, Canada.  7 American Museum ofNatural History, Central Park West at 79th Street, New York, New York 10024, USA.  8 Instituto de Geologia, Universidad Nacional Auto´noma de Me´xico, Ciudad Universitaria, Del.Coyocan,Me´xicoDF04510,Mexico. 9 ResearchInstituteofExplorationandDevelopment,XinjiangOilfieldCompany,Karamay,Xinjiang834000,China. 10 GraduateSchoolofChineseAcademy of Sciences, Beijing 100039, China. Vol 459 | 18 June 2009 | doi:10.1038/nature08124 940   Macmillan Publishers Limited. All rights reserved ©2009  reported only in relatively derived coelurosaurs among theropods 9 .A widely arched furcula is present, a feature first reported amongceratosaurs 3 .  Limusaurus   has an abbreviated forelimb as in otherceratosaurs. Metacarpal I is extremely reduced and lacks phalanges,and metacarpal IV is very slender with an unknown number of pha-langes (Fig. 2a, b). The elongate hind limbs have a femur 1 tibiotar-sus 1 metatarsal III/trunk length ratio of 1.80. The tibiotarsus andpes measure about 120% and 130% of the length of the femur,respectively. Similar proportions are seen in derived coelurosaurs 10 ,and their appearance in  Limusaurus   indicates that strong cursorialcapability emerged independently at an early stage of theropodevolution (see Supplementary Information for more morphologicaldescription). Implications for neotheropod evolution Our phylogenetic analysis places  Limusaurus   in a very basal positionwithin Ceratosauria (Supplementary Information). Some character-istics of   Limusaurus  , such as the hypertrophied scapulocoracoid andhighly abbreviated forelimbs with very short hands, were previously considered to diagnose lower-level or even species-level ceratosaur-ian taxa 3,11,12 . In our analysis, they are optimized as synapomorphiesof much more inclusive ceratosaurian groups. Even more significantis thepresence in  Limusaurus   of many features also seen in coelophy-sids and/or tetanurans 9 , further reducing the morphologicalgaps among the three major theropod groups. Features shared withcoelophysids are mostly plesiomorphic, but those shared withtetanurans are derived, thus providing further support for a closerelationship between Ceratosauria and Tetanurae 3 .Biogeographically,  Limusaurus   is the first definitive ceratosaurknownfromEastAsia 4 ,toourknowledge,suggestingacosmopolitandistribution for the group. In combination with other recent discov-eries 13 , this new ceratosaur makes the Asian dinosaurian fauna lessendemic during the Middle–Late Jurassic, suggesting a faunal con-nectionbetweenAsiaandothercontinentsduringthattimeperiodinspite of the presence of the Turgai Sea 14 . Convergent evolution of herbivory Limusaurus  , ornithomimosaurs and shuvosaurid suchians such as Effigia   are distantly related phylogenetically and also significantly separated temporally  15,16 , but they are remarkably similar in many gross skeletal features. They all have a small head with large orbits,toothless upper and lower jaws, a long neck and elongated hindlimbs 15 .  Limusaurus   and shuvosaurids also share an extremely largemandibular fenestra and reduced forelimbs. Furthermore, both spe-cimensof  Limusaurus  preservegastrolithsthataresimilarinquantity,size and shape (Fig. 1d) to those found in some ornithomimid speci-mens 17 . Another basal ceratosaur,  Elaphrosaurus  , was once actually placedwithintheOrnithomimosauria 18 .Togetherwiththediscovery of   Limusaurus  , this represents an extraordinary case of convergenceamong three higher archosaurian groups.Someanatomicalfeatures of  Limusaurus  (smalltoothlessheadandlong neck), and particularly the presence of a gastric mill, indicate aherbivorous diet. Secondary herbivory has previously been docu-mented only in some relatively derived Cretaceous taxa amongnon-avian theropods 17,19 . As a basal ceratosaur from the Oxfordian, Limusaurus   represents the earliest and most basal theropod inferred abcd 50 μ m Figure 1  |  Limusaurus inextricabilis  (IVPP V 15923).  Photograph ( a ) andlinedrawing( b )ofIVPPV15923.Arrowsin a pointtoanearlycompleteandfully articulated basal crocodyliform skeleton preserved next to IVPP V15923 (scale bar, 5 cm).  c , Histological section from the fibular shaft of  Limusaurus inextricabilis  (IVPP V 15924) under polarized light. Arrowsdenote growth lines used to age the specimen; HC refers to round haversiancanals and EB to layers of endosteal bone. The specimen is inferred torepresent a five-year-old individual and to be at a young adult ontogeneticstage, based on a combination of histological features including narroweroutermost zones, dense haversian bone, extensive and multiple endostealbone depositional events and absence of an external fundamental system. d , Close up of the gastroliths (scale bar, 2cm). Abbreviations: cav, caudal vertebrae; cv, cervical vertebrae; dr, dorsal ribs; ga, gastroliths; lf, left femur;lfl, left forelimb; li, left ilium; lis, left ischium; lp, left pes; lpu, left pubis; lsc,left scapulocoracoid; lt, left tibiotarsus; md, mandible; rfl, right forelimb; ri,right ilium; rp, right pes; sk, skull. NATURE | Vol 459 | 18 June 2009  ARTICLES 941   Macmillan Publishers Limited. All rights reserved ©2009  tohavebeenherbivorous, significantly expanding theknowntrophicdiversity of Jurassic theropods. Manualdigitreductionoftheropodsandaviandigitalhomologies Theropods have long been assumed to display a pattern of lateraldigit reduction (LDR), in which the digits have been progressively reduced from the lateral (that is, ulnar) side of the manus 20–23 . Incontrast, bilateral digit reduction (BDR) is characteristic of mostother tetrapod groups 23 . However, the reduction of digit I in Limusaurus   constitutes strong new evidence for BDR in ceratosaurs,particularly because other ceratosaurs also possess a somewhatreduced digit I 24,25 .The occurrence of BDR in Ceratosauria, the sister group of Tetanurae,invitesareconsiderationofdigitalevolution intheropodsas a whole, and particularly of the complex issue of tetanuran digitalhomologies 21–23 . On the basis of morphological evidence from fossiltaxa, the three digits retained by tetanurans have traditionally beeninterpreted as homologues of digits I–III of the primitive theropodmanus, exemplifying LDR  20,21 . However, the discovery of BDR in Limusaurus   and its close relatives introduces the possibility that thispattern might be more broadly distributed among non-avian thero-pods and indicates that the three digits of extinct tetanuran thero-pods could be II–IV, an alternative hypothesis previously littleconsidered in palaeontological literature 26 .Positional relationships have been widely accepted as the mainoperationalcriterionforprimaryhomology  27 ,althoughcasesofposi-tional shifts have been documented 28 or experimentally induced 29 . Inthe present case, the conservative pentadactyl pattern seen in theembryos of extant birds and crocodilians, and by inference allcrown-group archosaurs including theropods, provides a reliablereference system for topologically assessing the primary homologiesoftetanurandigits.RecentdevelopmentalstudiesfavourtheII-III-IVhypothesis by showing that the three digits of the only living tetanur-ans,thebirds,originatedevelopmentallyfromthemiddlethreeofthefive digital primordia 23,30–33 . Ontogenetic research on expression pat-terns of posterior  Hoxd   genes shows that digits that develop frompositions II-III-IV in birds acquire a I-II-III identity later in onto-geny  34,35 , resolving the apparent conflict between palaeontologicaland developmental data. Despite the strength of this evidence, devel-opmental data from extant taxa cannot indicate the point at whichdigital identities shifted during the evolution of the Theropoda, norreveal the tempo of that shift. The fossil record remains the only source of information on these aspects of the transition.Furthermore, in fossil tetanurans early embryonic stages cannot beobserved, so only morphological criteria are available to infer digitidentities.Comparing thedigitsoftetanurans tothoseoftheirclosestrelatives, Ceratosauria and  Dilophosaurus  , is particularly helpful inelucidating digital primary homologies.The main morphological features cited in support of the tra-ditional I-II-III hypothesis include the topographic relationship of the ‘semilunate’ carpal to the metacarpus, the short and distally asymmetrical medial metacarpal, and the apparently conservedphalangealformulaof2-3-4(refs20–22,36).Thephalangealformulais particularly striking because it characterizes digits I-II-III acrossa wide range of disparate tetrapod groups 21 . However, contrary evid-ence can be adduced against each of these points. Theropod carpalhomologies are complicated by anomalies such as the presence of arelatively small, separate medial distal carpal in non-maniraptorantetanurans and the absence of a large distal carpal in  Dilophosaurus  37 .Metacarpal II is distally asymmetric in  Limusaurus  ,  Dilophosaurus  38 and some specimens of the coelophysid  Coelophysis  39 , so theasymmetry of metacarpal I is not a unique feature. Finally, digitsI–III do not display a 2-3-4 phalangeal formula in any knownceratosaur, demonstrating that the conservatism of this formula isnot absolute.New information from  Limusaurus   and various other theropodsreveals a number of morphological features that support the alterna-tive II-III-IV hypothesis (Fig. 2). In basal theropods the proximalends of metacarpals I and II are mutually appressed without overlapwhereas the dorsolateral corner of the proximal end of metacarpal IIforms a flange that slightly overlaps the dorsal surface of metacarpalIII. In  Limusaurus   and tetanurans, a similar flange extends distally toform a large, oblique contact between metacarpals II and III in Limusaurus   and between the medial and middle metacarpals of teta-nurans. This indicates that the medial and middle metacarpals of tetanurans correspond to metacarpals II and III. Similarly, the prox-imal end of metacarpal IV is appressed to the ventrolateral face of metacarpal III innon-tetanuran theropods. The lateralmetacarpal of tetanurans contacts the ventrolateral face of the middle metacarpalin the same way, reinforcing the II-III-IV interpretation. The medialmetacarpal of basal tetanurans is the most robust in the manus,like metacarpal II in more basal theropods including ceratosaurs, Dilophosaurus  38 and coelophysids 3 . The elongate proximal phalanx of the medial digit of tetanurans is similar to phalanx I-1 in somecoelophysids but unlike the relatively short phalanx I-1 seen in a bc d e 222I II III IVI II III IV1  V 11I II IIIIV1 Figure 2  |  Theropod manual morphologies as represented by several non-avian theropods. a ,  b , Ceratosaur  Limusaurus  (IVPP V 15923 and 15924); c , basal theropod  Dilophosaurus  (UCMP 37302);  d , tyrannosauroid Guanlong   (IVPP V14531);  e , dromaeosaurid  Deinonychus  (YPM 5206). 1,dorsolateralprocess;2,metacarpalIVlocatedventraltometacarpalIII.Notethat the three metacarpals of   Guanlong   and  Deinonychus  display many similarities to metacarpals II–IV of   Limusaurus  and  Dilophosaurus .Interestingly, many metacarpal features, such as the contacts among thethree metacarpals and the morphology of the lateral metacarpal, werepreviously considered to be tetanuran synapomorphies, but in fact can bebetter interpreted as retained unchanged from the condition in non-tetanuran theropods if the three metacarpals of tetanurans are identified asII-III-IV. ARTICLES  NATURE | Vol 459 | 18 June 2009 942   Macmillan Publishers Limited. All rights reserved ©2009  ceratosaurs 3 ,  Dilophosaurus  38 and  Herrerasaurus  40 . The middlemetacarpal is longer than the others in tetanurans, like metacarpalIII in  Limusaurus  ,  Dilophosaurus  38 , at least some coelophysids, Herrerasaurus  40 and most other archosaurs 26 . The four-fingeredornithischian  Psittacosaurus   displays LDR, and its metacarpal III isalso the longest in the manus 41 . A dorsolateral process is present onthe proximal end of the middle metacarpal of basal tetanurans, and asimilar process characterizes metacarpal III of   Limusaurus  , Dilophosaurus   and  Herrerasaurus  . Finally, the lateral metacarpal isshort, slender and proximally sub-triangular in outline in basal teta-nurans, like metacarpal IV in non-tetanuran theropods 3 . It is note-worthy that most of these similarities are more evident between basaltetanurans and their close outgroups,  Dilophosaurus   and the cerato-saurs, than between derived tetanurans and coelophysids.We conducted a quantitative analysis of digital homologies to testthe alternative I-II-III and II-III-IV hypotheses in tetanurans(Supplementary Information). When birds are coded as II-III-IV,coding all Tetanurae as II-III-IV(-V) is a minimum of ten stepsshorter than a shift from I-II-III to II-III-IV anywhere within theTetanurae, and four steps shorter than a shift at the base of theAverostra. Coding all Tetanurae as having II-III-IV is the same intree length as (characters unordered) or six steps longer than (char-acters ordered) an alternative scheme in which all Tetanurae, includ-ing birds, are interpreted as having I-II-III, a hypothesis that clearly contradicts developmental data fromextant birds. Weconclude that,if birds possess digits II-III-IV as most developmental studies indi-cate, the data strongly support the interpretation that all tetanuranshave digits II-III-IV(-V), as outlined above. If extant birds are ulti-mately found to possess digits I-II-III, of course, then no conflictbetween neontological and traditional palaeontological data exists.This implies the reduction of digit I before the divergence of theCeratosauria and the Tetanurae, the appearance of some pollex-likefeatures in digit II and the acquisition of a novel phalangeal formula(X-2-3-4-X) early in tetanuran evolution. Both modifications arepartially indicated by the manual morphologies of ceratosaurs andmore basal theropods. Also, they are indirectly supported by obser-vations in living animals that a digit will display features normally associated with the neighbouring medial digit if the latter fails tochondrify in early development 21 , that phalangeal counts can vary even within species 29,42 and that secondarily cartilaginous elementscan regain their ability to ossify  43 .The frameshift hypothesis of digital evolution in theropods holdsthateachdigit,positionallydefined, assumedmorphological featuresthat primitively characterized the next most medial digit due tohomeotic transformations 21 . Recent studies indeed confirm that ahomeotic change has affected the development of the avian digits:in extant birds, condensation II receives a Hox signal (absence of posterior Hoxd  expression)appropriatefordigitI 34,35 .Theframeshiftwas, however, not necessarily a sudden, discrete event, and its re-patterning of the digits was not complete, because the metacarpals of basal tetanurans in general retained key features indicating theirsrcinal identities. The uneven modification of the tetanuran manusmay reflect the fact that tetrapod digits develop from proximal todistal 44 , each metacarpal appearing before its associated phalanges.The manus may have been repatterned by a late-acting devel-opmental signal that influenced the phalanges to a greater degreethan the metacarpals.In conclusion, both the I-II-III and II-III-IV hypotheses can draw some supporting morphological evidence from the hands of extincttetanurans, but largely from different manual regions (Fig. 3). If extant tetanurans have retained the middle three digits, as many developmental studies suggest 23,30–33 , it is more parsimonious toidentify the three digits of extinct tetanurans as digits II–IV. Thisnew evidence from  Limusaurus   and other basal theropods suggeststhat a gradual homeotic shift in digit identity characterized early stages of theropod evolution, that an intermediate stage of this shiftispreservedintheCeratosauriaandthattheshiftwascompletebythetime of the diversification of the earliest tetanurans. Received 24 January; accepted 29 April 2009. 1. Rauhut, O. W. M.  The Interrelationships and Evolution of Basal Theropod Dinosaurs (Palaeontological Association, 2003).2. Carrano, M. T., Sampson, S. D. & Forster, C. A. The osteology of  Masiakasaurusknopfleri , a small abelisauroid (Dinosauria: Theropoda) from the Late Cretaceousof Madagascar.  J. Vertebr. Paleontol.  22,  510 – 534 (2002). Neornithes  Archaeopteryx Deinonychus  AllosauroideaCeratosauriaTetanurae Averostra Dilophosaurus CoelophysidaeSauropodomorphaOrnithischia  Alligator  Figure 3  |  Manual digital evolution in theropod dinosaurs.  Manual digitalevolution involves both BDR and LDR in theropod dinosaurs. The shift toBDR in ceratosaurs is coincident with features indicating a reduction in thegrasping function of the manus. In ceratosaurs, the manus is small, themanual phalanges are abbreviated and the claws are non-raptorial. Thissupportsthehypothesisthata graspingfunctionconstrainedthehand toLDR in non-tetanuran theropods 21 . If BDR applies to the more inclusive Averostra,as the II-III-IV hypothesis suggests, early stages of tetanuran evolution musthave involved lossofthe already highlyreduced metacarpal I, reduction inthelength of metacarpal II and the reappearance of additional phalanges onmetacarpal IV. 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Developmental morphology of limb reduction in  Hemiergis (Squamata: Scincidae): chondrogenesis, osteogenesis, and heterochrony.  J.Morphol.  254,  211 – 231 (2002). Supplementary Information  is linked to the online version of the paper atwww.nature.com/nature. Acknowledgements  The authors thank H.-J. Wang for organizing the fieldwork,R. S. Li for illustrations, L.-S. Xiang and X.-Q. Ding for preparing the specimens,X.-Q. Ding for editing the illustrations, M. Kundra´t and J. Gauthier for criticalcomments, O.Rauhut,P.Makovicky andD.Chure forsometheropod images,R.-S.Tykoski for references, and members of the Sino-American expedition team forcollecting thefossil.The fieldwork was supported by the National Natural ScienceFoundationofChina,theNationalScienceFoundationDivisionofEarthSciencesofthe USA, the Chinese Academy of Sciences, the National Geographic Society, theJurassicFoundation,theHilmarSalleebequestandGeorgeWashingtonUniversity.Study of the specimens was supported by the Chinese Academy of Sciences, theNationalScienceFoundationDivisionofEarthSciencesoftheUSAandtheNationalNatural Science Foundation of China. Author Contributions  X.X. and J.M.C. designed the project. X.X., J.M.C., J.C.,G.M.E.,S.N.andJ.-Y.M.performedtheresearch. X.X.,J.M.C., G.M.E.,J.C.,C.S.andD.W.E.H.wrotethemanuscript.X.X.,J.M.C.,J.-Y.M.,J.C.,C.A.F.,D.A.E.,Q.Z.,R.H.,C.-K. J., F.-L.H. and Y.G. excavated the specimens. Author Information  Reprints and permissions information is available atwww.nature.com/reprints. Correspondence and requests for materials should beaddressed to X.X. (xingxu@vip.sina.com). ARTICLES  NATURE | Vol 459 | 18 June 2009 944   Macmillan Publishers Limited. All rights reserved ©2009
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