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The origin of conodonts and of vertebrate mineralized skeletons

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Abstract

Conodonts are an extinct group of jawless vertebrates whose tooth-like elements are the earliest instance of a mineralized skeleton in the vertebrate lineage1,2, inspiring the ‘inside-out’ hypothesis that teeth evolved independently of the vertebrate dermal skeleton and before the origin of jaws3,4,5,6. However, these propositions have been based on evidence from derived euconodonts. Here we test hypotheses of a paraconodont ancestry of euconodonts7,8,9,10,11 using synchrotron radiation X-ray tomographic microscopy to characterize and compare the microstructure of morphologically similar euconodont and paraconodont elements. Paraconodonts exhibit a range of grades of structural differentiation, including tissues and a pattern of growth common to euconodont basal bodies. The different grades of structural differentiation exhibited by paraconodonts demonstrate the stepwise acquisition of euconodont characters, resolving debate over the relationship between these two groups. By implication, the putative homology of euconodont crown tissue and vertebrate enamel must be rejected as these tissues have evolved independently and convergently. Thus, the precise ontogenetic, structural and topological similarities between conodont elements and vertebrate odontodes appear to be a remarkable instance of convergence. The last common ancestor of conodonts and jawed vertebrates probably lacked mineralized skeletal tissues. The hypothesis that teeth evolved before jaws and the inside-out hypothesis of dental evolution must be rejected; teeth seem to have evolved through the extension of odontogenic competence from the external dermis to internal epithelium soon after the origin of jaws.

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Figure 1: Element growth and microstructure of the paraconodont Furnishina, Threadgill Creek section, Wilberns Formation, central Texas, 1,115 feet above base of Cambrian strata.
Figure 2: Element growth and microstructure of the paraconodont Problematoconites, Windfall Formation, Tremadocian, Ordovician, Eureka County, Nevada, USA.
Figure 3: Element growth of the euconodont Proconodontus posterocostatus, Gros Ventre Formation, Late Cambrian, Bighorn Mountains, Wyoming, USA.
Figure 4: Proposed phylogenetic hypothesis for the relationship between paraconodonts and euconodonts, and the evolution of conodont skeletal characters.

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Acknowledgements

The SRXTM experiments were performed on the TOMCAT beamline at the Swiss Light Source, Paul Scherrer Institut (Villigen, Switzerland), funded through a project awarded to P.C.J.D. and S. Bengtson (Stockholm). NERC grant NE/G016623/1 to P.C.J.D., a studentship to DJEM funded by NERC and the Paul Scherrer Institut, and NSFC Project 41372015 to X.-P.D. Thanks to R. Stamm (USGS) for reviewing a draft of this manuscript; and thanks to J. E. Cunningham, D. O. Jones and M. Rücklin for assistance at the beamline. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Authors and Affiliations

Authors

Contributions

D.J.E.M. and P.C.J.D. conceived and designed the research; D.J.E.M., F.M. and M.S. collected the SRXTM data; J.E.R. and X.-P.D. provided material and taxonomic information; D.J.E.M. analysed the data, prepared the figures and wrote the paper with substantive edits from P.C.J.D. and minor edits from the remaining authors.

Corresponding author

Correspondence to Philip C. J. Donoghue.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Growth of the paraconodont elements Prooneotodus, Windfall Formation, Tremadocian, Ordovician, Eureka County, Nevada, USA.

a, d, e, Initial two growth stages highlighted using SRXTM rendering. b, c, Longitudinal sections through the element showing successive lines of cessation of growth. Note the protoelement is not engulfed by subsequent growth lamellae and basal cavity begins to develop in the second set of lamellae. Scale bar represents 75 μm (a, b); 50 μm (ce).

Extended Data Figure 2 Comparison of the internal structure of the elements of the paraconodont Rotundoconus tricarinatus and the euconodont Granatodontus sp.

a, R. tricarinatus from the Cordylodus intermedius Zone, Furongian (upper Cambrian), Panjiazui Formation, Wa’ergang section, Wa’ergangvillage, Taoyuan County, Hunan Province, China Steptoe South section. b, Granatodontus sp. from the Whipple Cave Formation, uppermost Cambrian, northern Egan Range, White Pine County, Nevada, USA. Longitudinal and orthogonal sections generated from SRXTM data. In elements of R. tricarinatus, wall consists of three layers, the outermost tapering rings that do not extend fully over outer surface nor are continuous over basal surface. In elements of Granatodontus, a thin crown extends over the outer surface of the element, basal body consists of a lamellar layer with sub-parallel lamellae surrounding a poorly defined porous tissue layer. Scale bar represents 50 μm (a); 30 μm (b).

Extended Data Figure 3 Proconodontus serratus, Windfall Formation, Tremadocian, Ordovician, Eureka County, Nevada, USA.

a, b, SRXTM rendering of external morphology (a) and lateral aspect of internal structure (b) of an element of the euconodont Proconodontus serratus. Note distinction of tissues into crown and basal body. Scale bar represents 100 μm.

Extended Data Figure 4 Descriptive terminology of paraconodont and euconodont elements.

Labels are superimposed over the proposed phylogenetic hypothesis for the relationship between paraconodonts and euconodonts, and the evolution of conodont skeletal characters. Euconodonts are derived from a paraphyletic assemblage of paraconodonts that exhibit increasing basal body complexity, but are differentiated by the acquisition of the crown. Thus, the euconodont crown cannot be a homologue of vertebrate enamel.

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Murdock, D., Dong, XP., Repetski, J. et al. The origin of conodonts and of vertebrate mineralized skeletons. Nature 502, 546–549 (2013). https://doi.org/10.1038/nature12645

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