RESEARCH PALEONTOLOGY Galeaspida JAWLESS Osteostraci Marginal dentition and Brindabellaspis multiple dermal jawbones Romundina as the ancestral condition Radotina of jawed vertebrates Kosoraspis Valéria Vaškaninová1,2*, Donglei Chen1, Paul Tafforeau3, Zerina Johanson4, Boris Ekrt5, Henning Blom1, Per Erik Ahlberg1* Tlamaspis ´ACANTHOTHORACI´ STEM GROUP The dentitions of extant fishes and land vertebrates vary in both pattern and type of tooth CPW.9 replacement. It has been argued that the common ancestral condition likely resembles the Antiarchi nonmarginal, radially arranged tooth files of arthrodires, an early group of armoured fishes. Macropetalichthys Downloaded from We used synchrotron microtomography to Kujdanowiaspis describe the fossil dentitions of so-called acanthothoracids, the most phylogenetically basal jawed vertebrates with teeth, belonging to the Buchanosteus ARTHRODIRA JAWED Radotina Kosoraspis Tlamaspis genera , ,and (from Gemuendina the Early Devonian of the Czech Republic). Their Entelognathus dentitions differ fundamentally from those of http://science.sciencemag.org/ arthrodires; they are marginal, carried by a Janusiscus cheekbone or a series of short dermal bones along the jaw edges, and teeth are added lingually as is the case in many chondrichthyans (cartilaginous Lophosteus fishes) and osteichthyans (bony fishes and tetrapods). We propose these characteristics as ancestral for all jawed vertebrates. palatoquadrate external dermal bone Moythomasia OSTEICHTYES he origin of teeth was one of the key events dermal odontode in the evolutionary transition from jawless on July 13, 2020 bone of outer dental arcade CROWN to jawed vertebrates. Stem osteichthyans GROUP (1, 2) and most chondrichthyans (3)have bone of inner dental arcade T Ptomacanthus transversely arranged whorl-like tooth entopterygoid files with lingual addition, whereas crown osteichthyans have longitudinal tooth rows tooth (Fig. 1). In arthrodires, a clade of jawed stem youngest tooth position gnathostomes, teeth are added in diverg- Squalus site-specific resorption ing files from a progenitor tooth or region; CHONDRICHTYES the number of files is highly variable, and shedding additioncanbelabialaswellaslingualor longitudinal (4–9). The recent discovery of Fig. 1. Distribution of dentition types among gnathostomes. The images represent schematic transverse osteichthyan-like marginal dermal jawbones sections of palatoquadrate complexes, except for that of CPW.9, which represents the prenasal region. combined with an arthrodire-like body plan Genera with these schematic images are noted in bold. For strict consensus phylogeny, see fig. S1. The in Entelognathus and Qilinyu (10, 11)has arthrodire and stem osteichthyan reconstructions are based on (2, 9, 27). The division between stem resulted in a proposed evolutionary succes- and crown is based on (2, 9, 27, 28), which resolve Lophosteus as a stem osteichthyan and Entelognathus sion (11) in which these genera form a bridge and Janusiscus as stem gnathostomes. between an arthrodire-like condition (assumed to be primitive for jawed vertebrates) and the In this work, we present dentitions of the specimen CPW.9 from the Canadian Arctic osteichthyan condition (assumed to be prim- Early Devonian acanthothoracid stem gnatho- (mistakenly assigned to Romundina by some itive for crown gnathostomes). However, the stomes Radotina, Kosoraspis,andTlamaspis authors) (7, 12). Acanthothoracids, antiarchs, dentitions of Entelognathus and Qilinyu are from the Czech Republic, and we reexamine and Brindabellaspis (13)aretheonlyjawed poorly understood. the only described acanthothoracid dentition, vertebrates with an anteriorly projecting 1Department of Organismal Biology, Uppsala University, Norbyvägen 18A, SE-752 36, Uppsala, Sweden. 2Institute of Geology and Palaeontology, Faculty of Science, Charles University, Albertov 6, Prague, 12843, Czech Republic. 3European Synchrotron Radiation Facility, 71 avenue des Martyrs, 38043 Grenoble, France. 4Department of Earth Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK. 5Department of Palaeontology, National Museum, Václavské náměstí 68, Prague, 11579, Czech Republic. *Corresponding author. Email: [email protected] (V.V.); [email protected] (P.E.A.) Vaškaninová et al., Science 369, 211–216 (2020) 10 July 2020 1of5 RESEARCH | REPORT Downloaded from http://science.sciencemag.org/ on July 13, 2020 Fig. 2. Palatoquadrate complex and dentition of Radotina tesselata. (A to shown in (E) and (F) have a voxel size of 0.72 mm. In (A) to (D), green denotes C) Palatoquadrate in internal (A), external (B), and ventral (C) views. (D) Dentition in external dermal bone, cream indicates natural mold of external dermal bone, blue mesoventral (top) and medial (bottom) views. (E) Detailed image of teeth in indicates endoskeleton, and yellow indicates teeth and/or tooth-bearing dermal ventral view, with the relationship to (C) indicated with gray lines. (F)Blockmodelof bone.In(E)and(F),redtopurpletonesdenote different tooth rows, gold indicates dentition in transverse view, showing the region indicated by the yellow box in a replacement tooth, green indicates pulp cavities, and blue indicates vasculature. (E).Thescansshownin(A)to(D)haveavoxelsizeof13.49mm, and the scans Scale bars, 10 mm [(A) to (C)]; 1 mm (D); 0.1 mm [(E) and (F)]. precerebral trabecular region (14). This dis- (not previously analyzed) genera discussed The tooth addition in the dentition of CPW.9, tinctive facial geometry resembles that of jaw- herein are included in the analysis (fig. S1). which comprises a pair of supragnathal plates less stem gnathostomes, especially galeaspids The jaws and dentition of Brindabellaspis are on a snout (fig. S2) (12), has been described as (15). Recent phylogenetic analyses have recov- unknown, whereas antiarchs lack teeth (17). concentric (7, 18). As a result, a detached dermal ered antiarchs, Brindabellaspis, and acantho- Thus, the teeth of acanthothoracids have the tessera with concentrically arranged odontodes thoracids as basal to other jawed vertebrates unique potential to illuminate the origin of from the same formation was misinterpreted (11, 14, 16), a position they retain when the vertebrate dentition. as an acanthothoracid supragnathal (18–20). Vaškaninová et al., Science 369, 211–216 (2020) 10 July 2020 2of5 RESEARCH | REPORT Downloaded from http://science.sciencemag.org/ on July 13, 2020 Fig. 3. Palatoquadrate complex, ethmoid, and dentition of Kosoraspis articulated premedian plate, two articulated supragnathals, and disarticulated peckai. (A and B) Národní Muzeum (NM) specimen Lc 552 palatoquadrate dental elements. (F) Dental element (c) (supragnathals) in occlusal (top) and complex in external (A) and internal (B) views, with associated tooth-bearing basal (bottom) views. (G) Dental element (d) in occlusal (left) and oblique (right) elements. Lowercase letters refer to detailed views of dental elements, as views. See fig. S9 for further details. Voxel size of (A) to (D) is 24.59 mm and specified. (C) Dental element (a) in external (top), internal (bottom), and oblique that of (E) to (G) is 11.35 mm. The color coding used for (A) to (F) is the same as anteroventrolateral (left) views. (D) Dental element (b) in occlusal (left) and that in Fig. 2, A to D. Scale bars, 10 mm [(A), (B), and (E)]; 1 mm [(C), (D), basal (right) views. (E) NM Lc 16 ethmoid-trabecular region in ventral view with (F), and (G)]. Reanalyzing the micro–computed tomogra- labial tooth addition (fig. S3). Instead, the Using propagation phase contrast syn- phy (micro-CT) scans of CPW.9 reveals that the oldest small teeth in the founder region be- chrotron microtomography, we have discov- supragnathals suture labially with the dermal come overgrown by larger dermal odontodes ered the previously unknown dentitions of premedian plate. In fact, tooth addition is radial as has been observed in the stem osteichthyan Radotina, Kosoraspis,andTlamaspis (21). from a labial founder region, and there is no Andreolepis (2). All differ substantially from that of CPW.9. Vaškaninová et al., Science 369, 211–216 (2020) 10 July 2020 3of5 RESEARCH | REPORT Downloaded from http://science.sciencemag.org/ on July 13, 2020 Fig. 4. Dentition of Tlamaspis inopinatus. (A) Photo of specimen NM Lc 166, other bones of the specimen are not shown. The tooth-bearing bones cluster in the a partly disarticulated head compressed in oblique left dorsolateral view, anterior to anterior part of the head. Labeled bones are shown in (C). (C) Four tooth-bearing the left. (B) Scan model of assembled block Lc 166 plus 167 rendered semitrans- bones, each shown in labial (top left), end-on (top right), lingual (middle), and occlusal parent; Lc 166 is outlined in blue. Tooth-bearing bones are denoted in yellow, and (bottom) views. Voxel size, 24.59 mm. Scale bars, 10 mm [(A) and (B)]; 5 mm (C). The dentition of Radotina (Fig. 2) comprises that of marginal dermal ornament odontodes lingualmost row has been repaired with a new four rows of teeth carried on the ventral face onthetesseraeofthecheek(fig.S6E).How- crown inserted into the break (fig. S5, E and F). of a large dermal cheekbone sutured to the ever, unlike those odontodes, the teeth are Kosoraspis (24)andTlamaspis (21)have external surface of the palatoquadrate. This fused into rows by a distinct basal attachment multiple short tooth–bearing dermal jawbones. ventral face forms a longitudinal trough, with tissue (fig. S7D). The arms of the stellate teeth, They vary in