(6.4.2)--古生物学.pdf

Letterhttps:/doi.org/10.1038/s41586-018-0419-1A Triassic stem turtle with an edentulous beakChun Li1,2*,Nicholas C.Fraser3,Olivier rieppel4&Xiao-Chun Wu5*The early evolution of turtles continues to be a contentious issue in vertebrate palaeontology.Recent reports have suggested that they are diapsids16,but the position of turtles within Diapsida is controversial712 and the sequence of acquisition of turtle synapomorphies remains unclear13.Here we describe a Triassic turtle from China that has a mixture of derived characters and plesiomorphic features.To our knowledge,it represents the earliest known stem turtle with an edentulous beak and a rigid puboischiadic plate.The discovery of this new form reveals a complex early history of turtles.The turtle is represented by a nearly complete skeleton from the lower Carnian(about 228 million years ago)of the Guanling District,Guizhou Province,southwestern China(Fig.1a);it was collected from sediments approximately 7.5m below the horizon that contained the stem turtle Odontochelys13(Extended Data Fig.1).The most notable features of the newly described taxon are the edentulous beak formed by the anterior parts of the upper and lower jaws,the closure of the supratemporal fenestra by the contact of the parietal with the postor-bital and postfrontal,the reduced number of the dorsal vertebrae with the transversely broadened ribs,and the formation of a rigid pubois-chiadic plate,whereas a carapace and plastron are absent.Reptilia Laurenti,1768Pantestudines Joyce,Parham and Gauthier,200414Eorhynchochelys sinensis gen.et sp.nov.Etymology.Eo-(dawn),rhyncho-(beak),chelys(turtle):the earliest turtle with a beak;sinensis,from China.Holotype.Sanya Museum of Marine Paleontology(SMMP)000016 in Hainan Province,China,an articulated specimen displaying the post-cranium in dorsal view,and the skull in ventral view(the skull and pelvis were prepared from both sides).Locality.Heshangjing of Baiyuncun,Xinpuxiang,Guanling District,Guizhou Province,southwestern China.Horizon.The upper unit of the lower part of the Wayao Member of the Falang Formation,approximately 8.5m above the top of the Zhuganpo Member;Late Triassic(Carnian age).Diagnosis.A stem pantestudine of large size;proportionately small skull broadly triangular in outline;supratemporal fenestra closed;infratemporal fenestra partially open;edentulous beak;pleurodont tooth implantation;teeth on parabasisphenoid;12 dorsal vertebrae;neural spines with disc-like dorsal tables in cervical vertebra 8 to caudal 5;dorsal ribs 1 through 10 horizontally(anteroposteriorly)broadened,T-shaped in cross-section;rigid puboischiadic plate with median ven-tral keel;and ischium with posterior elongation.The edentulous premaxillae and the anterior parts of the dentaries show a noticeably rugose surface with small pits and fine grooves,indi-cating the presence of a keratinous beak in Eorhynchochelys(Fig.2a,c,e,f and Extended Data Fig.2ad).The exposed anterior teeth of the right maxilla are conical,but the exposed posterior teeth of the left max-illa are pleurodont,column-like and have a blunt tip(Extended Data Fig.2a,e).The supratemporal fenestra is closed and the supratemporal bone is absent(Fig.2a,c and Extended Data Fig.3).The pterygoid exhibits a distinct transverse flange and numerous conical teeth scattered across its entire ventral surface.The prominent parabasisphenoid has well-developed basipterygoid processes,and anteriorly extends into a broad-based,dentigerous cultriform process(Fig.2b,d).The large basioccipital displays robust basal tubera.The sutures remain unfused in the exoccipitalopisthotic complex,which extends into a robust paroccipital process.The disarticulated supraoc-cipital shows a concave inner(ventral)surface.There are 9 cervical,12 dorsal,2 sacral and 56 caudal vertebrae,all of which are non-notochordal and amphicoelous.The vertebral column is characterized by mid-dorsals that bear elongate prezygapophyses with a small,concave articular facet and short postzygapophyses and by neural spines that have broadened dorsal tables in posterior cervi-cal vertebrae through anterior caudal vertebrae(Figs.1ac,3a,b and Extended Data Fig.4).Cervical ribs 7 to 9 are complete and lack an anterior process(Fig.1b,c).Cervical rib 9 has a much more elongate distal shaft of uniform diameter,a sharp transition that occurs at the eighth vertebra in Proganochelys15.Dorsal ribs 1 to 10 are dichocephalous and approx-imately T-shaped in cross-section as they expand to form prominent anterior and posterior horizontal flanges.These ribs extend later-ally with minimal ventral curvature and together form a flattened carapace-like shield(Fig.1a).There is,however,no contact or overlap of successive ribs.Dorsal ribs 11 and 12 are shorter and much less expanded than the more anterior ones.The sacral ribs are stout and fused to the sacral vertebrae(Fig.3a,b and Extended Data Fig.5).The scapular blade is long and narrow with a slight distal expansion.There is a very weak development of an acromion(Fig.1b,c).The clavicle is broad and stout anteromedially along its articulation with the rather narrow lateral process of the dorsoventrally expanded inter-clavicle;posterolaterally the scapular process of the clavicle becomes more slender.With a pronounced postacetabular process,the ilium is similar to that of Pappochelys and Odontochelys(Fig.3a,b).As preserved,the puboischiadic plate was broken,the right portion partially obscuring the left portion in ventral view.The rounded anterior edge of the pubis shows no evidence of an epipubic process;however,an incipient lateral process is present(Fig.3ce).A deep incision in the posterior margin of the pubis,closed posteriorly by the ischium,marks the obturator fora-men.A second foramen piercing the ischium lies immediately behind the latter.In ventral view the ischium is practically indistinguishable from that of Odontochelys(Fig.3cg),exhibiting a prominent lateral tubercle behind the acetabulum.Posteromedial to the lateral tubercle,the ischium narrows to form an elongate process.The pubes and ischia meet in a broad suture along the ventral midline,thus forming a robust and solid puboischiadic plate with a distinct medioventral keel,as is also the case in Odontochelys(Fig.3cg).The posterior elongation of the ischium terminates in a blunt tip,similar to Odontochelys;how-ever,Eorhynchochelys lacks a separate hypoischium that is present in Odontochelys and Proganochelys(Extended Data Fig.6).The arrangement of the gastralia remains unclear.Some rod-like gastral elements are loosely scattered below the dorsal ribs(Fig.3a,b),1Key Laboratory of Vertebrate Evolution and Human Origins,Institute of Vertebrate Paleontology and Paleoanthropology(IVPP),Chinese Academy of Sciences,Beijing,China.2Center for Excellence in Life and Paleoenvironment,Chinese Academy of Sciences,Beijing,China.3National Museums Scotland,Edinburgh,UK.4Field Museum of Natural History,Chicago,IL,USA.5Canadian Museum of Nature,Ottawa,Ontario,Canada.*e-mail:;xcwunature.ca4 7 6|N A t U r e|V O L 5 6 0|2 3 A U G U S t 2 0 1 8 2018 Springer Nature Limited.All rights reserved.Letter reSeArCHhowever,it was not possible to determine whether there was any fusion of some of the gastral ribs,similar to Pappochelys.The fore-and hindlimbs are approximately equal in length and generally very robust.Both the humerus and femur have well-developed proximal and distal heads.The humerus exhibits a shallow S-shaped flexure and a prominent ectepicondylar groove(Fig.1b,c).The femur has a distinct internal trochanter and the proximal head is offset from the shaft.The carpals and tarsals are well-ossified,but unlike in Odontochelys,the astragalus and calcaneum,both of irregular contours,remain separate.Each digit terminates in an ungual that is always longer than the penultimate phalanx(Fig.1d,e).Eorhynchochelys exhibits a mosaic of characters,some of which are shared with Pappochelys and others with Odontochelys and more derived turtles.Eorhynchochelys and Pappochelys have double-headed and expanded dorsal ribs with gently tapering distal ends,whereas in Odontochelys,the single-headed dorsal ribs have blunter distal ter-minations and in Eunotosaurus9 the weakly double-headed dorsal ribs show a strongly curved shaft with narrowed distal portions.In Eorhynchochelys,the trunk is noticeably broader in the mid-dorsal region,whereas in Pappochelys the trunk is approximately parallel sided.As in Odontochelys,Proganochelys,and all crown-group tur-tles,the supratemporal fenestra is closed in Eorhynchochelys,but the infratemporal fenestra would seem to have been partially open ven-trally.The acromion is slightly more prominent than in Pappochelys,but not as pronounced as in Odontochelys.In the absence of a plastron,the ventrolateral process of the pubis is only minimally developed and,unlike in Pappochelys and Odontochelys,there is no trace of an ossified epipubic process in Eorhynchochelys.The presence of a lateral tubercle and a posterior elongation in the ischium are features that are shared with Odontochelys;the rigid puboischiadic plate is a feature that is shared with Odontochelys and more derived turtles.There is no trace of a separately ossified hypoischium in either Eorhynchochelys or Pappochelys.hulraol3 cmscschdr1dr5dr2coclabc5 cmcr9cr7iclacectnstd3 cmascafti10 cmeFig.1|The holotype of E.sinensis(SMMP 000016).a,Complete articulated skeleton,as preserved.b,c,Photograph and interpretative drawing of anterior axial skeleton,pectoral girdle and right zeugopodium in dorsal view with elongate and narrow scapula blade and enlarged,circular neural spine tables that are deeply concave.d,Right autopodium of forelimb in posteroventral view.e,Right autopodium of hindlimb in posterior view.Eorhynchochelys is only known from a single specimen,reaching almost 2.3m in total length including the conspicuously long tail,and is much larger than Odontochelys in size.The relatively small,broad and triangular skull,approximately 9.0cm long,was separated from the neck by about two centimetres,and is exposed in ventral view,whereas most of the postcranial skeleton is articulated and exposed in dorsal view.The fusion of the neural arches to their centra and well-ossified ends of all long bones suggest that the specimen represents a fully grown adult.ac,acromion;as,astragalus;ca,calcaneum;cl,clavicle;co,coracoid;cr9,cervical rib 9;dr1,dr2,dr5,dorsal ribs 1,2,5;ect,ectepicondylar groove;fi,fibula;h,humerus;icl,interclavicle;nst,neural spine table;ol,olecranon;ra,radius;sc,scapula;ti,tibia;ul,ulna.andspsppofqsqpoppopbobspspmsytrpqrpprqppfpposqq?mprqtrpanrapdbpbthysopthyqrppopeoeoecparcbd1 cmpopoffprfljnmpmddsaanqqjpprapsadhqpop?sqana?ar?prqa1 cm1 cmefmnnpmdpmdlFig.2|Skull of E.sinensis(SMMP 000016).ad,Photographs and interpretative line drawings of the skull in dorsal and ventralviews.e,f,The snout in dorsal and slightly lateral view.As shown in ad,the maxilla meets the premaxilla in a broad suture and the posterior region of the skull has been crushed so that the squamosals,parietals and associated occipital region have been pushed underneath the back end of the skull;nevertheless,it is clear that the much-enlarged postorbital,postfrontal and parietal broadly contact each other,indicating the absence of a supratemporal fenestra;the large quadrate and associated quadratojugal have been displaced anteriorly and crushed,leaving the extent of the lower temporal fenestra equivocal;and the jugal has a distinct posterior process but there is no indication that it established a sutural contact with the quadratojugal.an,angular;ana,atlantal neural arch;ar,articular;bo,basioccipital;bp,basipterygoid process;bs,basisphenoid;bt,basal tubera;d,dentary;dhq,dorsal head of quadrate;ec,ectopterygoid;eo,exoccipital;f,frontal;fp,articular facet of parietal;hy,hyoid;j,jugal;l,lachrymal;m,maxilla;n,nasal;p,parietal;pm,premaxilla;po,postorbital;pof,postfrontal;pop,paroccipital process;prf,prefrontal;pt,pterygoid;q,quadrate;qj,quadratojugal;qrp,quadrate ramus of pterygoid;rap,retroarticular process;rapsa,retroarticular process of surangular;sa,surangular;so,supraoccipital;sp,splenial;sq,squamosal;trp,transverse process of pterygoid;?,an undetermined bone.Zigzag lines denote broken surfaces.2 3 A U G U S t 2 0 1 8|V O L 5 6 0|N A t U r e|4 7 7 2018 Springer Nature Limited.All rights reserved.LetterreSeArCHA phylogenetic analysis using TNT v.1.016 based on a data matrix derived from the reduced,previously published dataset4(Supplementary Information)recovered a phylogeny in which Pantestudines,including a ClaudiosaurusAcerosodontosaurus clade,appears as the sister group of a clade including Archosauromorpha,Lepidosauria,Kuehneosauridae and aquatic groups(Fig.4;see Extended Data Fig.7,in which Pantestudines is less inclusive based on the large data matrix derived from the previously published datasets3,4).Within Pantestudines,the phylogenetic position of Eorhynchochelys is more derived than that of Pappochelys,whereas Eunotosaurus retains its position more basal than that of the latter24.With a Bremer support value of 11,the monophyly of an ingroup formed by Eunotosaurus and more derived turtles is strongly supported.The sister-group relation-ship of Eorhynchochelys with the OdontochelysProganochelys clade in the group is supported by the following unequivocal synapomor-phies:absence of supratemporal fenestra,presence of bony symphy-sis(sutured)of pubes and ischia,and rigid puboischiadic plate with a medioventral keel in adult.Turtles,including Odontochelys,typically have a reduced count of 9 dorsal vertebrae with 9 pairs of expanded ribs.The same count was also given for Pappochelys2,4 and Eunotosaurus9,although we note that it is difficult to provide a definitive vertebral count for Pappochelys based on disarticulated and sometimes disassociated material.The count of 12 dorsal vertebrae in Eorhynchochelys represents an evolutionary reversal and so does the toothed premaxilla of Odontochelys.The development of broadened ribs in stem turtles has recently been associated with digging habits1719.For Eorhynchochelys,digging activ-ity is further supported by the stout limbs,prominent condyles on the humerus and femur,moderately developed olecranon of the ulna and the enlarged claws.Taken together,these characters seem to indicate predominantly terrestrial habits.It has been argued that the oldest tur-tles with a fully developed shell were terrestrial17,20.The occurrence of Eorhynchochelys in marine sediments and the failure of the astragalus and calcaneum to fuse in an adult are features consistent with aquatic habits.However,although found in marine black shaly marlstones,this may not reflect a local biocoenosis(Supplementary Information).The new form may have been an inhabitant of coastal waters foraging on land as well as in the water,searching the mud along the shore using its powerful limbs in a way that many living pond turtles also do(Fi