The visceral skeleton of jawed vertebrates consists of a series of jointed arches including the jaws, hyoid arch and gill arches. This fundamental arrangement is shared by all chondrichthyans (sharks, rays and chimaeroids) and osteichthyans (bony fishes and their limbed relatives), as well as the extinct ‘placoderm’ and ‘acanthodian’ fishes. It thus represents a highly conserved feature of gnathostomes. Important differences in arch structure between modern chondrichthyans and osteichthyans5,9,21,22 could reflect their long independent evolutionary history (over 420 Myr). The modern osteichthyan arrangement is already recognizable in early actinopterygian (‘ray-finned’) and sarcopterygian (‘lobe-finned’) osteichthyans (for example, Pteronisculus8, Mimipiscis9, Eusthenopteron12) and is commonly assumed to be derived, whereas the modern shark pattern is viewed as primitive3,20. Crucially, little was known about visceral arches in Palaeozoic chondrichthyans11,13,14,15,17 (Supplementary Notes), precluding a detailed comparison with other early jawed vertebrates.

Articulated, three-dimensionally preserved specimens of a small symmoriiform shark (stem chondrichthyan23) from the Lower Carboniferous period of Arkansas, United States, were investigated by propagation phase contrast X-ray synchrotron microtomography, which revealed the complete series of visceral arches on both sides (Fig. 1 and Supplementary Video 1). Although several specimens were examined, the most complete example (American Museum of Natural History (AMNH) FF20544) is used here to illustrate our findings (Fig. 1 and Extended Data Fig. 1). The specimens possess tessellated calcified cartilage, which is considered to be the hallmark character of ‘conventionally defined’ chondrichthyans19, a group that we informally name ‘euchondrichthyans’.

Figure 1: Three-dimensional reconstructions of Ozarcus mapesae AMNH FF20544. a, Concretion in right lateral view. b, Braincase and associated visceral skeleton in right lateral view. c, Branchial skeleton in right lateral view (mandibular and hyoid arches removed). d, Concretion in left lateral view. e, Braincase and associated visceral skeleton in left lateral view. f, Braincase and the right elements of the visceral skeleton in medial aspect, left lateral view. Colour coding of the skeletal elements: yellow, epi-; blue, cerato-; green, hypo-; orange, infrapharyngo-; turquoise, suprapharyngo-; purple, accessory elements; red, basi-; peachy pink, braincase. The colours of the mandibular elements are lightened and those of the hyoid are darkened. The white circle indicates the space between the mandibular and hyoid arches. ac1–4, accessory elements of branchial arches 1–4; bb2–3, basibranchials 2–3; br, braincase; cb1–5, ceratobranchials 1–5; cp, copula of posterior basibranchials; eb1–5, epibranchials 1–5; eh, epihyal; hb1–3, hypobranchials 1–3; hh, hypohyal; ib1–4, infrapharyngobranchials 1–5; mc, Meckel’s cartilage/lower jaw; postp, postorbital process; pq, palatoquadrate/upper jaw; sb1–4, suprapharyngobranchials 1–4. Scale bar, 10 mm. Full size image Download PowerPoint slide

Class Chondrichthyes Huxley, 1880

Order Symmoriiformes Zangerl, 1981

Family Falcatidae Zangerl, 1990

Ozarcus mapesae gen. et sp. nov.

Etymology. The generic name derives from Ozark (a highland region of Arkansas where the specimens were found) and ultimately from arcus (Latin for arch). The species is named after G. K. Mapes in recognition of her work collecting and describing fossils from Palaeozoic strata in the United States for more than 40 years, and who found the holotype specimen.

Holotype. AMNH FF20544 (Fig. 1 and Extended Data Fig. 1).

Referred material. Articulated heads: AMNH FF20525, 20528 and 20542.

Locality and horizon. Fayetteville Formation (lower shale member), Chesterian, Upper Mississippian, from the ARC-07 locality24 (section (sec.) 22, township (T.) 14 N, range (R.) 15 W) near Leslie, Searcy County, Arkansas, United States.

Diagnosis. Falcatidae possessing small cladodont, pentacuspid and symmetrical teeth; ten upper and lower tooth families; palatoquadrate lacks a continuous posterior quadrate margin; no dermal denticles covering the top of the head; no ‘spine–brush’ complex; no laterally extended supraorbital shelf; laterally extended antorbital process that overlies a suborbital process possessing a series of four ridges and grooves for the articulation with the palatoquadrate (Supplementary Notes and Extended Data Fig. 2).

The visceral skeleton of Ozarcus has the same basic organization as in most other piscine jawed vertebrates, with a series of paired, jointed arches including a mandibular arch (jaw), hyoid arch (behind the jaw) and five branchial arches (Fig. 1). The palatoquadrate articulates with the postorbital process of the braincase (Fig. 1b) as in many other Palaeozoic sharks. No traces of labial cartilages were identified.

The hyoid arch of Ozarcus includes paired epihyals and ceratohyals, but neither pharyngohyals nor interhyals. Unlike in modern chondrichthyans22, anteriorly directed, osteichthyan-like21 paired hypohyals are present instead of a median basihyal (Figs 1f, 2 and Extended Data Fig. 3). Some other Palaeozoic euchondrichthyans also possess hypohyals, but the distribution of basihyals and hypohyals among most early gnathostomes is poorly resolved (Supplementary Notes).

Figure 2: Reconstructions of the branchial skeleton of O. mapesae. a, Right elements of the branchial skeleton (mandibular arch removed) in lateral aspect, right lateral view. b, Branchial skeleton reconstructed as horizontally spread, viewed dorsally and with anterior above (mandibular arch removed). Same colours and abbreviations as in Fig. 1. Not to scale. Full size image Download PowerPoint slide

The epi- and ceratohyals are morphologically similar to the corresponding branchial elements (Figs 1b, e, 2a), as in modern chimaeroids but unlike in elasmobranchs, where the hyoid arch is specialized towards jaw suspension5. The epihyal extends forward to just behind the orbit, but both the epihyal and the braincase lack any articular processes or recesses, suggesting that the epihyal was weakly connected to the braincase (Extended Data Fig. 3b, c). The epihyal meets the ceratohyal well posterior to the jaw joint, leaving a space between the mandibular and hyoid arches that, even allowing for compaction of the fossil, is far wider than those between the branchial arches (Fig. 1b and Extended Data Fig. 3a); a similar space has been inferred in the symmoriiform Cobelodus15. Its conjunction with the recessed palatoquadrate margin in Ozarcus may indicate the presence of a larger version of the non-respiratory, pseudobranch-bearing spiracular pouch seen in modern jawed vertebrates5, or perhaps even a fully respiratory hyomandibular gill pouch1,3,16,25 (Supplementary Notes and Extended Data Fig. 4).

The branchial arches include the basi-, hypo-, cerato-, epi- and pharyngobranchials (Figs 1, 2), arranged in a way not previously observed in a euchondrichthyan. Instead of a single pharyngobranchial as in modern chondrichthyans, arches 1–4 each have two pharyngobranchials (Figs 1c, 2). We regard these as homologues of the infra- and suprapharyngobranchials in osteichthyans6,21 (Supplementary Notes). The single pharyngobranchial in modern chondrichthyans is topographically homologous with osteichthyan infrapharyngobranchials6,10, not with the suprapharyngobranchials26, because both chondrichthyan pharyngobranchials and osteichthyan infrapharyngobranchials6 support the roof of the pharynx. Unlike in modern chondrichthyans, the infrapharyngobranchials of Ozarcus are directed anteriorly, as in osteichthyans.

A separate, fifth epibranchial element is present in Ozarcus (Figs 1b, c, e, 2), as well as in Debeerius13, some extinct hybodont sharks (for example, Tribodus27) and Acanthodes28. By contrast, epibranchial element 5 is fused with pharyngobranchial 4 in modern chondrichthyans and is absent in crown osteichthyans20.

The last ceratobranchial in Ozarcus is not broadened laterally, a feature shared with xenacanths, Debeerius13 and chimaeroids. By contrast, in many modern sharks and the Carboniferous shark Tristychius17, the last ceratobranchial is much wider than those farther anteriorly.

Ventrally, arches 3–5 meet the lateral margins of the basibranchial copula, as in osteichthyans (Figs 1f, 2), whereas only the last ceratobranchial is attached to the copula in modern chondrichthyans. All the hypobranchials are directed anteriorly in Ozarcus (Figs 1c, f, 2), an arrangement shared with osteichthyans5, Acanthodes10, modern chimaeroids7 and Debeerius13. By contrast, only hypobranchial 1 is anteriorly directed in some modern elasmobranchs (for example, Scyliorhinus canicula; Fig. 3).

Figure 3: Evolution of the branchial skeleton in the crown gnathostomes, mapped onto a tree compiled from the most recent phylogenetic analyses19,23,28. Only the right and median parts of the branchial skeletons of Scyliorhinus, Callorhinchus, Ozarcus, Acanthodes10,28, Pteronisculus8 and Eusthenopteron12 are shown, as viewed dorsally and with anterior above. Diagrammatic right views of one branchial arch are shown at the crown gnathostome, chondrichthyan and osteichthyan nodes of the tree. To maximize clarity, the branchial skeletons are reconstructed as horizontally spread and the opercular cartilage of Callorhinchus is not shown. Some elements of Acanthodes, Pteronisculus and Eusthenopteron are outlined in dashes or are uncoloured, because of their uncertain existence or uncertain homologies (Supplementary Notes). hb ant., hypobranchials anteriorly directed; hb post., hypobranchials posteriorly directed; ib ant., infrapharyngobranchial anteriorly directed; ib post., infrapharyngobranchial posteriorly directed. Light orange, compound infrapharyngobranchial 4, 5 (Scyliorhinus) or 3, 4, 5 (Callorhinchus) plus epihyal 5 (Scyliorhinus) or 4, 5 (Callorhinchus). Other colours and abbreviations are the same as in Fig. 1. Shared derived characters of each clade are listed at the corresponding nodes. The layout is not intended to reflect strict chronological history. Not to scale. Daggers indicate fossil taxa. Full size image Download PowerPoint slide

Small ‘accessory cartilages’ are present between the ceratobranchial and epibranchial on each of the first four gill arches (Figs 1c, e, 2). These were previously unknown in chondrichthyans, but similar elements are present in modern basal actinopterygians (Polypteriformes, Lepisosteiformes, possibly Acipenseriformes)20 and in the Triassic actinopterygian Pteronisculus8. It has been suggested that these accessory cartilages are serially homologous with the symplectic or the interhyal of the hyoid arch8,20. Their occurrence in a stem chondrichthyan considerably expands their distribution, suggesting that they are a gnathostome symplesiomorphy. No traces of extrabranchial cartilages3 were found in Ozarcus.

Ozarcus considerably broadens our understanding of visceral arch morphology in jawed vertebrates. Several features can now be reinterpreted as primitive for crown gnathostomes (Fig. 3 and Supplementary Notes), including: presence of supra- and infrapharyngobranchials, anteriorly directed infrapharyngobranchials, chevron arrangement of branchial arches along the basibranchial copula, all hypobranchials directed anteriorly, accessory cartilages between the cerato- and epibranchials, and paired hypohyals. Additionally, several features are reformulated here as potential synapomorphies of crown chondrichthyans, including a single (infra)pharyngobranchial element per arch, infrapharyngobranchials directed posteriorly, hypobranchials of the branchial arches concentrated at the anterior part of the basibranchial copula, absence of accessory cartilages, and absence of paired hypohyals anterior to the ceratohyals. The presence of a basihyal and fusion of epibranchial 5 with pharyngobranchial 4 may be apomorphic for, or within, crown chondrichthyans (Supplementary Notes). Having most of the hypobranchials directed posteriorly is interpreted as a synapomorphy of living elasmobranchs and extinct hybodont sharks (collectively known as euselachians29), not shared with modern chimaeroids.

Ozarcus challenges a widely held opinion that the ancestral state of the gnathostome branchial arch resembled the Σ-shape arches of modern sharks, which have posteriorly directed pharyngo- and hypobranchial elements. Instead, the <-shaped arrangement of the bony fishes, with anteriorly directed pharyngo- and hypobranchial elements, is likely to be primitive (Fig. 3). Ozarcus thus shows a novel combination of chondrichthyan and osteichthyan characters, thereby demonstrating that the most recent common ancestor of crown gnathostomes possessed an osteichthyan-like branchial apparatus. Our findings cast doubt on the traditional view of visceral arch evolution that modern chondrichthyans mirror the ancestral morphotype of jawed vertebrates. Bony fishes and stem chondrichthyans may have more to tell us about our first jawed ancestors than do living sharks.