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Synchrotron-Aided Reconstruction of the Conodont Feeding Apparatus and Implications for the Mouth of the first Vertebrates

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Synchrotron-Aided Reconstruction of the Conodont Feeding Apparatus and Implications for the Mouth of the first Vertebrates Synchrotron-aided reconstruction of the conodont feeding apparatus and implications for the mouth of the first vertebrates Nicolas Goudemanda,1, Michael J. Orchardb, Séverine Urdya, Hugo Buchera, and Paul Tafforeauc aPalaeontological Institute and Museum, University of Zurich, CH-8006 Zürich, Switzerland; bGeological Survey of Canada, Vancouver, BC, Canada V6B 5J3; and cEuropean Synchrotron Radiation Facility, 38043 Grenoble Cedex, France Edited* by A. M. Celâl Sxengör, Istanbul Technical University, Istanbul, Turkey, and approved April 14, 2011 (received for review February 1, 2011) The origin of jaws remains largely an enigma that is best addressed siderations. Despite the absence of any preserved traces of oral by studying fossil and living jawless vertebrates. Conodonts were cartilages in the rare specimens of conodonts with partly pre- eel-shaped jawless animals, whose vertebrate affinity is still dis- served soft tissue (10), we show that partial reconstruction of the puted. The geometrical analysis of exceptional three-dimensionally conodont mouth is possible through biomechanical analysis. preserved clusters of oro-pharyngeal elements of the Early Triassic Novispathodus, imaged using propagation phase-contrast X-ray Results synchrotron microtomography, suggests the presence of a pul- We recently discovered several fused clusters (rare occurrences ley-shaped lingual cartilage similar to that of extant cyclostomes of exceptional preservation where several elements of the same within the feeding apparatus of euconodonts (“true” conodonts). animal were diagenetically cemented together) of the Early This would lend strong support to their interpretation as verte- Triassic conodont Novispathodus (11). One of these specimens brates and demonstrates that the presence of such cartilage is a (Fig. 2A), found in lowermost Spathian rocks of the Tsoteng plesiomorphic condition of crown vertebrates. section (Tiandong District, Guangxi Province, China) (12, 13), consists of four “grasping” elements (S1–4 elements). apical cartilage | conodont oral skeleton | early vertebrates | homology Fused clusters partially preserve the relative 3D positions and EVOLUTION orientations of the involved elements. However, they are very ow the transition from “agnathans” to gnathostomes small, fragile, tricky to manipulate, and if more than two or three H(“jawed” vertebrates) occurred is one of the most intriguing elements are involved, very complicated to analyze. One way to problems of evolutionary biology (1). Little is known about the circumvent this is to use a nondestructive imaging method such endoskeleton of fossil jawless vertebrates [e.g., fossil cyclostomes as X-ray microtomography. In our case, the required resolution (hagfishes and lampreys) and “ostracoderms”]. Although the view and contrast could not be achieved with conventional micro- is still debated (2), euconodonts would have possessed the very tomography. Hence, we scanned this Chinese cluster, as well as GEOLOGY first vertebrate mineralized skeleton in the form of their oral a complete set of isolated elements (catalog nos. PIMUZ 39841–9) denticles (3, 4). found in the same sample and belonging to the same multielement The general architecture of the conodont oral skeleton is species, at the European Synchrotron Radiation Facility, on the a bilaterally symmetrical array of usually 15 phosphatic elements, ID19 beamline, using submicron resolution propagation phase- which generally becomes disarticulated after the decay of the contrast X-ray synchrotron microtomography (PPC-SRμCT) (14) supporting tissues. Hence most conodonts are known only as (Methods). On the basis of refs. 6, 11, and 15, we reconstructed isolated elements. From the detailed study of hundreds of ar- avirtual3DapparatusofNovispathodus. The relative sizes of the “ ” ticulated natural assemblages and photographic simulation S1–4 elements were inferred from the cluster. The other relative of their collapse, Purnell and Donoghue (5) constructed a 3D sizes (M, S0,P1,P2 relative to S1–4) were derived from the few model of the Idiognathodus apparatus [presumably a template known Neogondolella natural assemblages (Fig. 2 B–C)(15,16). for all ozarkodinid apparatuses (6)] in which one pair of Both our Novispathodus cluster and the Neogondolella natural obliquely pointed M elements are located rostrally and, behind assemblages (15, 16) show that the cusps of the S1 and S2 ele- them, one unpaired S0 (subscript number indicates distance or- ments were oriented more caudally than those of the S0 and S3, 4 dering from the symmetry axis) element lying on the axis of bi- elements, a feature that Orchard and Rieber considered to be lateral symmetry and four pairs of elements (S1–4) located on unique to the “gondolellaceans” (15, p. 480). Its recurrence in all both sides of the S0 would have grasped food and, more caudally, known Triassic assemblages (17 and 18) independently of their two pairs of pectiniform elements (P1,P2) would have processed collapse angle suggests that it is not due to a taphonomic bias – this food by crushing and/or slicing (5, 7, 8) (Fig. 1 A B) (for (postmortem rotation of elements) and indeed records a config- “ ” standard orientation of single elements, see Fig. S1). Purnell uration that differs from the Idiognathodus reconstruction (5). ’ and Donoghue s reconstruction of a generalized resting (dead) Natural assemblages of Ozarkodina, the presumed rootstock of position is very well supported and in most aspects very convincing. the Ozarkodinida (19), indicate that this caudal orientation of It is therefore adopted here as a basis upon which we build our dynamic reconstruction of the feeding apparatus at work. How could these elements actually grasp or cut prey tissues? Author contributions: N.G. designed research; N.G. and S.U. performed research; P.T. Purnell and Donoghue’s functional model (section 6 of ref. 5) contributed new reagents/analytic tools; H.B. provided biostratigraphic and paleoenvir- was based chiefly on analogies with extant agnathans. Indeed, the onmental data; N.G., M.J.O., S.U., and H.B. analyzed data; and N.G. wrote the paper. “quite simple” geometry of the Idiognathodus elements does not The authors declare no conflict of interest. provide much indication of what motions are possible or not *This Direct Submission article had a prearranged editor. [except for uncommon natural assemblages (see below)]. Thus, Data deposition: The synchrotron data presented in this manuscript is available on the hypotheses were inferred from extant putative closest relatives. open access paleontological database of the ESRF at http://paleo.esrf.eu. In our view, the more “complicated” Novispathodus apparatus 1To whom correspondence should be addressed. E-mail: [email protected]. imposes additional constraints that enable us to reconstruct the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. movement of the elements independently of phylogenetic con- 1073/pnas.1101754108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1101754108 PNAS Early Edition | 1of5 Downloaded by guest on September 25, 2021 A P1 B dorsal A B P2 sinistral rostral caudal dextral S0 S4 S1 S2 S3 M M ventral Fig. 1. Anatomical notation and orientation. (A) Dorsal view of the recon- C D structed, closed apparatus of Novispathodus. Anatomical notation after Purnell et al. (9). (B) Orientation of the apparatus within the conodont’s head. the cusp of the S1 is not restricted to the Gondolelloideans (ref. 20, reinterpreted in ref. 6, fig. 13A; 21). Fused clusters involving only the two hindeodelliform S3 and S4 elements are relatively more frequent in our collections. This suggests that they were located close and subparallel to one another (their recurrent relative position in those clusters) and Fig. 3. Geometrical correspondences between elements. (A) The S1 ele- fi had probably a common motion within the living animal. In ments match the posterior process of the S0. Per de nition, the tip of the (ab)oral view, their respective posterior processes are substraight cusp points posteriorly. ant: anterior; post: posterior. (B) Closed arrangement posteriorly and outwardly deflected behind the cusp, and their of S elements. (C) Presumed growth position of the S2 (silver) as inferred by anterior processes are laterally bowed inward, which results in an geometrical correspondences with the S3 and S4 elements (gold). (D) Pro- fi posed movement of the S0 against the M elements (silver: start and end overall sitar-like pro le. – fi positions; gold: pinching position). (A D) c: caudal; d: dextral; do: dorsal; r: The shape of the S2 ts those of the S3 and S4 in the following rostral; s: sinistral; v: ventral; blue circles: hypothetical cartilage. aspects: (i) In the “cluster position” (see above) where the cusp of the S2 is subparallel to the posterior processes of the S3 and S4 elements, the outer profile (oral view) of the S2 is similar to the If we assume that the various elements moved along trajec- fi inner pro le of the S3, and the largest denticle of its antero- tories approximately parallel to the curvature of the cusp and lateral process is aligned with the cusps of the S3 and S4 (Figs. 2A denticles (5), then the movements of the S2–4 elements must have and 3B). (ii) In a presumed “growth position” where the re- included an opening/closing pivot motion around an axis parallel spective basal cavities (initial growth centers) of the S2–4 ele- to the posterior processes of the S3 and S4. Consequently, the
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