An exceptional fossil skull from South America and the origins of the archosauriform radiation

Birds, dinosaurs, crocodilians, pterosaurs and their close relatives form the highly diverse clade Archosauriformes. Archosauriforms have a deep evolutionary history, originating in the late Permian, prior to the end-Permian mass extinction, and radiating in the Triassic to dominate Mesozoic ecosystems. However, the origins of this clade and its extraordinarily successful body plan remain obscure. Here, we describe an exceptionally preserved fossil skull from the Lower Triassic of Brazil, representing a new species, Teyujagua paradoxa, transitional in morphology between archosauriforms and more primitive reptiles. This skull reveals for the first time the mosaic assembly of key features of the archosauriform skull, including the antorbital and mandibular fenestrae, serrated teeth, and closed lower temporal bar. Phylogenetic analysis recovers Teyujagua as the sister taxon to Archosauriformes, and is congruent with a two-phase model of early archosauriform evolution, in response to two mass extinctions occurring at the end of the Guadalupian and the Permian.

Type locality and age. Exposure of the Sanga do Cabral Formation 13 , Paraná Basin, São Francisco de Assis municipality, Rio Grande do Sul State, Southern Brazil (29°36ʹ 56″ S, 55°03ʹ 10″ W) (Fig. 1). An Induan to early Olenekian age (Lower Triassic) is inferred for the Sanga do Cabral Formation based on the presence of the parareptile Procolophon trigoniceps, and comparisons with the coeval Lystrosaurus Assemblage Zone of the South African Karoo [13][14][15] . Teyujagua was found in close association with archosauromorph vertebrae, cranial and postcranial remains of P. trigoniceps, temnospondyl amphibians and as-yet-unidentified tetrapod bones.

Diagnosis.
Archosauromorph with the following unique character combination: confluent, dorsally positioned external nares; maxilla participating in orbital margin; antorbital fenestra absent; trapezoidal infratemporal fenestra with incomplete lower temporal bar; teeth serrated on distal margins; surangular bearing a lateral shelf; external mandibular fenestrae present and positioned beneath the orbits when the lower jaw is in occlusion (autapomorphic for Teyujagua).
Description. The 115 mm long skull is well preserved and almost complete, and is associated with four cervical vertebrae (Figs 2 and 3; Supplementary Fig. 1). The occipital and palatal regions and parts of the left side of the skull are still covered by the enclosing matrix, but were partially examined using computed tomography (CT) ( Supplementary Fig. 2).
The snout is relatively broad and flattened, with dorsally positioned, confluent external nares. Dorsal confluent nares are an unusual condition that is often linked to aquatic or semi-aquatic habits, being present in many crocodyliforms, although they also occur in the terrestrial rhynchosaurs 16 , which are near relatives of early archosauriforms. The nasals contribute substantially to the skull table, followed by short and broad frontals, and parietals that bear a small pineal foramen. Although the loss of the pineal foramen has been identified as a synapomorphy of archosauriforms 8 , this structure is variably absent or present in the early archosauriform Proterosuchus fergusi 12 and the close archosauriform relative Prolacerta broomi 17 . The prefrontals and sculptured postfrontals almost exclude the frontals from the dorsal orbital margin, whereas the maxilla participates in the anteroventral orbital margin. The orbits face anterolaterally, and were probably capable of at least limited binocular vision. The slender supratemporals are visible in dorsal view.
The premaxillae have well-developed, slender posterodorsal processes but lack anterodorsal processes, as a result of the confluent nares. An antorbital fossa/fenestra is absent from the maxillae (Fig. 3C). The jugals are triradiate, with main bodies ornamented with longitudinal ridges. The posterior jugal process tapers distally and does not reach the quadratojugal (Fig. 3B). The trapezoidal infratemporal openings were ventrally bordered by incomplete lower temporal bars, similar to the condition in non-archosauriform archosauromorphs such as Prolacerta, Protorosaurus and Mesosuchus 16,17 . By contrast, the lower temporal bar is complete in nearly all archosauriforms, although this character is variable in Proterosuchus fergusi 12 .
On the lower jaw, the surangulars bear lateral shelves that match closely with the ventral margins of the posterior processes of the jugals. The external mandibular fenestra is present, unusually anteriorly positioned, and ventrally bordered by a slender ascending process of the angular. The posterior contacts of the dentaries with  30 ; stratigraphic profile modified from Da Rosa, et al. 13 .
the post-dentary bones cannot be identified. However, CT scans reveal that the dentary tooth row ends slightly anterior to the maxillary one ( Supplementary Fig. 2). Abbreviations: an, angular; dt, dentary; emf, external mandibular fenestra; fr, frontal; ju, jugal; la, lacrimal; mx, maxilla; na, nasal; pa, parietal; pmx, premaxilla; po, postorbital; pofr, postfrontal; prf, prefrontal; q, quadrate; q j, quadratojugal; rap, retroarticular process; sa, surangular; sq, squamosal; st, supratemporal. Artwork by J. Anderson. Each premaxilla possesses four teeth and the maxilla had a maximum of 15. The teeth bear serrations on their distal margins only, as in proterosuchid archosauriforms, but differing from the condition in more derived archosauriforms in which serrations are usually present on both mesial and distal margins 18 (Fig. 3A). Pronounced heterodonty is evident, with small premaxillary teeth followed by considerably larger anterior maxillary teeth. The teeth are labiolingually compressed, held in well-defined sockets, and not firmly associated with surrounding alveolar bone. Implementation therefore appears to be thecodont, rather than ankylothecodont as in many of the earliest archosaurifoms 19 . Phylogeny. Our novel cladistic analysis recovered two most parsimonious trees with 872 steps ( Supplementary Fig. 3). The strict consensus of these topologies (Fig. 4) positions Teyujagua as the sister taxon of Archosauriformes, a position previously occupied by the Lower Triassic Prolacerta 8,11,17 . The clade Teyujagua plus Archosauriformes is supported by five synapomorphies: (i) Serrations on tooth crowns; (ii) trapezoidal shape of the infratemporal fenestrae; (iii) frontal-parietal suture at right angle to parasagittal plane; (iv) mandible bearing an external fenestra; (v) lateral shelf on surangular.
Archosauriformes includes the traditional basal groups, such as Proterosuchidae and Erythrosuchidae, together with the crown group Archosauria. Proterosuchidae consists of Proterosuchus, Archosaurus and Sarmatosuchus, although the relationships within this clade are unresolved. Fugusuchus, Koilamasuchus and the clade Erythrosuchus + Archosauria also have unresolved positions relative to one another. The clade Chanaresuchus + (Doswellia + Vancleavea) is recovered as the sister group of Archosauria, and Euparkeriidae is the sister group of this less inclusive clade. As such, four recognised groups compose non-archosaurian Archosauriformes: Proterosuchidae, Erythrosuchidae, Euparkeriidae and the clade including Chanaresuchus + (Doswellia + Vancleavea).
Another analysis was performed including the poorly known Eorasaurus, which may be the oldest known archosauriform. The analysis recovered 14 most parsimonious trees with 873 steps. Most of the recovered topologies are similar to those recovered in the first phylogenetic analysis. The consensus tree differs in positioning Eorasaurus in an unresolved polytomy together with Koilamasuchus, Fugusuchus, erythrosuchid taxa, and a clade composed of Euparkeriidae + Proterochampsia + Archosauria (Supplementary Fig. 5). This provides additional support for the archosauriform affinities of Eorasaurus, and the existence of archosauriform ghost lineages extending into at least the middle Wuchiapingian 11 .

Discussion
Teyujagua presents an unexpected combination of basal archosauromorph and typical archosauriform features. For example, Teyujagua resembles basal archosauromorphs in lacking an antorbital fenestra and retaining open lower temporal bars 1,8,11,20 . However, Teyujagua possesses external mandibular fenestrae and serrated teeth, features previously considered unique to Archosauriformes 8,11 . Comparisons between Prolacerta, Teyujagua and early archosauriforms demonstrate for the first time that these key anatomical features of Archosauriformes were acquired in a mosaic fashion (Fig. 4). Serrated teeth and external mandibular fenestrae, important features underpinning the evolution of large, powerful hypercarnivores, were acquired before a closed lower temporal bar and the antorbital opening. Thus, key dietary adaptations emerged in the early history of the Archosauriformes before the onset of the major skull pneumatisation that played an important role in the group's later evolutionary history 21 .
The oldest known unambiguous archosauriform is Archosaurus rossicus, from the uppermost Permian of Russia 11,19 . However, the late Guadalupian to early Lopingian age of the possible archosauriform Eorasaurus 11 suggests that the clade had a substantial evolutionary history before the end-Permian mass extinction. Although hampered by the scarcity of Permian archosauromorph remains, the results of our phylogenetic analysis are congruent with two major pulses of opportunistic radiation experienced by early archosauriforms and close relatives such as Teyujagua. The first of these would be a phylogenetic diversification during the Lopingian, coincident with the recovery from the end-Guadalupian mass extinction 22,23 (Fig. 5), perhaps as disaster taxa filling empty niches of small piscivores and predators. The rarity of archosauriform body fossils in Permian strata suggests that the clade formed a minor component in latest Palaeozoic faunas, when terrestrial trophic chains had therapsids as the main higher-level predators 7,22,24 .The end-Permian extinction disrupted these food chains, and during the faunal recovery the Archosauriformes underwent a major increase in abundance, size and species richness 7,19,22,24 , becoming the main terrestrial predators 7,22,24 , and later expanding to also dominate large herbivorous niches 8,9 . The ichnological record provides additional support for this two-phase radiation 25 . The discovery of Teyujagua thus helps to clarify early archosauriform evolution, allowing a better understanding of how this clade rose to dominate Mesozoic faunas and shape the modern biota.

Methods
Type horizon and locality. The type locality of Teyujagua paradoxa is a known fossil site that has been thoroughly described by Da Rosa et al. 13 . The locality is informally known as Bica São Tomé and is situated about 10 km east of São Francisco de Assis municipality, Rio Grande do Sul State, Southern Brazil. Teyujagua was found in one of the five outcrops that compose the Bica São Tomé (outcrop 5 of Da Rosa et al. 13 ). The outcrop consists of a 15 m thick section with a predominance of fine reddish sandstones, intercalated with coarse sandstones and intraformational conglomerates, this being a typical lithology of the Sanga do Cabral Formation 13 . The Teyujagua holotype was found in a layer rich in calcareous concretions, about 5 m from the baseline of the outcrop. The fossil assemblage so far reported for the Bica São Tomé site is dominated by procolophonoid cranial and postcranial material, some of which is referable to Procolophon trigoniceps. Less commonly, the site has produced temnospondyl cranial and postcranial fragments, incomplete long bones attributable to Cynodontia and incomplete archosauromorph vertebrae. Sanga do Cabral Formation fossils are typically found in association with the intraformational conglomerates and, as a result, show signs of intense reworking and fragmentation. The holotype of Teyujagua paradoxa is the most complete vertebrate specimen collected in this sedimentary unit to date. An Induan to early Olenekian (Lower Triassic) age is inferred for the Sanga do Cabral Formation based on the presence of Procolophon trigoniceps, which is restricted to the upper Katberg Formation (Lystrosaurus Assemblage Zone) in the Karoo Basin of South Africa [13][14][15] . Procolophon trigoniceps is the only taxon from the Sanga do Cabral Phylogenetic analysis. In order to test the phylogenetic position of Teyujagua, a novel data matrix was assembled including taxa and morphological characters from two previous studies that aimed to address the phylogeny of Archosauromorpha and that of basal archosauriforms outside Archosauria 11,26 . In total, the dataset included 44 operational taxonomic units (OTUs) and 252 morphological characters (see the supplementary material for full details).