A bird-like skull in a Triassic diapsid reptile increases heterogeneity of the morphological and phylogenetic radiation of Diapsida.

The Triassic Period saw the first appearance of numerous amniote lineages (e.g. Lepidosauria, Archosauria, Mammalia) that defined Mesozoic ecosystems following the end Permian Mass Extinction, as well as the first major morphological diversification of crown-group reptiles. Unfortunately, much of our understanding of this event comes from the record of large-bodied reptiles (total body length > 1 m). Here we present a new species of drepanosaurid (small-bodied, chameleon-like diapsids) from the Upper Triassic Chinle Formation of New Mexico. Using reconstructions of micro-computed tomography data, we reveal the three-dimensional skull osteology of this clade for the first time. The skull presents many archaic anatomical traits unknown in Triassic crown-group reptiles (e.g. absence of bony support for the external ear), whereas other traits (e.g. toothless rostrum, anteriorly directed orbits, inflated endocranium) resemble derived avian theropods. A phylogenetic analysis of Permo-Triassic diapsids supports the hypothesis that drepanosaurs are an archaic lineage that originated in the Permian, far removed from crown-group Reptilia. The phylogenetic position of drepanosaurids indicates the presence of archaic Permian clades among Triassic small reptile assemblages and that morphological convergence produced a remarkably bird-like skull nearly 100 Myr before one is known to have emerged in Theropoda.

Background

The Triassic has long been recognized as a critical interval in the history of vertebrate life, especially in terms of the diversification of important Mesozoic taxa. It saw the global recovery from the biodiversity crash of the Permo-Triassic Extinction (PTE), and the first appearances of major diapsid reptile clades that would typify Mesozoic ecosystems (e.g. Dinosauromorpha, Lepidosauria, Pseudosuchia, Pterosauria, Ichthyosauria Sauropterygia) [1-7].

However, it has recently been recognized that the morphological diversification of Diapsida in the Triassic was far broader than previously understood [8-11]. A number of bauplans long considered to be restricted to later Mesozoic diapsids are now known in unrelated Triassic lineages. These include bipedal toothless pseudosuchians closely resembling Cretaceous ornithomimosaurs [12], dome-skulled forms similar to pachycephalosaurs [13], pseudosuchian predators with high and narrow skulls similar to large neotheropods [14,15] and a number of long-snouted semiaquatic lineages similar to later neosuchian crocodylomorphs [16-18]. Thus, not only were major taxonomic categories established during the Triassic Period, but suites of morphological features—suites which would typify many Mesozoic and Cenozoic diapsid reptile clades—emerged in a variety of unrelated Triassic species.

As yet, this pattern of convergent morphologies is well established in archosaurs and their close relatives, a possible consequence of overall larger body size and higher preservational potential [19,20]. However, the Triassic Period fossil record rarely preserves small-bodied taxa and critical details of their anatomy that illuminate both their phylogenetic relationships and functional anatomy are lacking [21-23]. Among the most diverse and speciose of these small-bodied lineages are Drepanosauromorpha, a clade of superficially lizard-like diapsids that have been favourably compared with extant arboreal, swimming and burrowing tetrapods [24-28]. Some recent studies support an arboreal habitus for most drepanosauromorphs, including the eponymous Drepanosaurus [11,27,29]. Known drepanosauromorph skulls and skeletons are almost all heavily compressed, completely obscuring the three-dimensional skeletal anatomy. The few three-dimensionally preserved specimens are highly incomplete [30,31]. Hypotheses for the phylogenetic affinities of drepanosauromorphs include placement within Lepidosauromorpha [25,30,32], Archosauromorpha [27,28,33,34] and outside of the crown-group reptile clade [35,36]. These are reviewed in appendix A.

Here, we report on a nearly complete and three-dimensionally preserved skull and partial cervical series of a drepanosauromorph (figure 1) from the Upper Triassic (Late Norian to Rhaetian) Coelophysis Quarry (‘upper sandstone member’, Chinle Formation). Using micro-computed tomography (µCT) scans and three-dimensional modelling, we present a reconstruction of the skull of this new taxon, the first for any drepanosauromorph (figures 1–3; parameters for µCT scanning and reconstruction in appendix B). The quality of preservation allows us to reassess the phylogenetic affinities of Drepanosauromorpha using a data matrix focused on Permo-Triassic diapsids and early Sauria.

Figure 1.

Three-dimensional volume rendering of the in situ skull of Avicranium renestoi (AMNH FARB 30834) from µCT data in (a) dorsal view, (b) ventral view and (c) left lateral view. Abbreviations: at, atlantal neural arch; ax, axis; c3, cervical vertebra 3; c4, cervical vertebra 4; de, dentary; fr, frontal; mx, maxilla; pd, postdentary elements; pf, postfrontal; pl, palatine; pm, premaxilla; po, postorbital; pt, pterygoid; qu, quadrate; sq, squamosal; su, supratemporal.

Figure 3.

Reconstructed skull of Avicranium renestoi based on rearticulated three-dimensional surface rendering of the skull bones of AMNH FARB 30834. Callouts include (a) reconstructed endocast in dorsal view, (b) skull roof in dorsal view, (c) postorbital complex (consisting of postfrontal and postorbital) in anterior view, (d) braincase and stapes in posterior view, (e) palatal complex in ventral view, (f) left quadrate in posterior view and (g) braincase and stapes in left lateral view. All bones have been rearticulated based on the facets of the reconstructed elements. Abbreviations: fb, forebrain; mb, midbrain; pa, parietal; pf, postfrontal; pl, palatine; po, postorbital; pt, pterygoid; qu, quadrate; st, stapes; su, supratemporal.

Systematic palaeontology

Diapsida [37]; Drepanosauromorpha [27]; Drepanosauridae [38]; Avicranium renestoi, n. gen., n. sp.

Etymology

Avicranium, from aves (Latin for bird) and cranium (Latin for cranium), in reference to the suite of bird-like morphologies present in the holotype skull; renestoi, for Silvio Renesto, who described much of the drepanosauromorph fossil record from Triassic Italy.

Holotype

AMNH FARB 30834, partial skull and articulated cervical series. Additional drepanosaurid caudal vertebrae and limb fragments are preserved in the block, but are not clearly associated with the individual to which the skull and cervical vertebrae belong.

Locality

Coelophysis Quarry (‘siltstone member’, Chinle Formation). Recovered during preparation of the holotype block of the shuvosaurid pseudosuchian Effigia okeeffeae by S.J.N. [12].

Diagnosis

Specimens for anatomical comparisons are listed in appendix C. A drepanosaurid diapsid differing from Hypuronector limnaios, Megalancosaurus preonensis and Vallesaurus cenensis (the only drepanosauromorphs with skull material) in the complete absence of teeth, a dorsoventrally taller retroarticular process with a triangular shape in lateral view, and cervical neural spines with subequal anteroposterior lengths and transverse widths.

Comparative anatomy

The identification of this specimen as a drepanosaurid is based on its cervical vertebral anatomy. Drepanosaurids possess heterocoelous cervical vertebral centra with saddle-shaped articular surfaces. The prezygapophyseal facets face anteriorly and extend far anteriorly relative to the anterior margin of the centrum. The neural spines are anteroposteriorly short and strongly inclined anterodorsally. In each of these features, Av. renestoi is very similar to drepanosaurids with cervical series, specifically Drepanosaurus unguicaudatus [27,31]. The bones of the skull are loosely articulated with one another, much as in the few other known drepanosauromorph skulls. It is similar in size to the known skulls of Me. preonensis (approx. 27 mm) and substantially larger than the skull of the holotype of V. cenensis (approx. 16 mm).

Bird-like traits

The skull of Av. renestoi exhibits a number of striking similarities to avian theropods (figures 2 and 3). The rostrum is slender and acuminate, as has been noted in the Italian drepanosaurid Me. preonensis [39,40]. Avicranium renestoi combines this shape with a completely edentulous rostrum and palate (figure 3e). The construction of the orbit differs from that in most Triassic diapsids, in which the cavity is directed anterolaterally [33,41,42]. In Av. renestoi, the frontal, postfrontal and postorbital all contribute to a transversely broad postorbital septum, which directs the orbital cavity anteriorly (figure 3c). The analogous postorbital process in maniraptorans integrates processes of the frontal, squamosal and laterosphenoid [43]. In most birds, the process is formed primarily by a cartilaginous expansion of the laterosphenoid. Renesto & Dalla Vecchia [40] also suggested binocular vision for Me. preonensis, based on the tapering rostrum and broadened orbital and temporal regions.

Figure 2.

Line drawing of the restored skull of Avicranium renestoi based on the three-dimensional surface renderings of skull elements in AMNH FARB 30834.

The endocranium preserves some of the most striking departures of the Av. renestoi from other Triassic reptiles. The contribution to the braincase of the paired frontal and parietal bones is both broad transversely and tall dorsoventrally. This contribution is so prominent that the contributing portion of the frontal is domed dorsally well above the orbital margin (figure 3a). This corroborates the hypothesis by [40] that the Italian drepanosaurid Me. preonensis had an inflated, ‘bulging’ skull roof [39, p. 251]. Among diapsid reptiles, a similar shape otherwise only occurs in maniraptorans [44-47] and some pterosaurs [48,49], taxa that possess enlarged brains relative to other Mesozoic diapsid groups. The reconstructed dorsal surface of the endocast of the Av. renestoi resembles those of Pterosauria and maniraptorans in that the cerebrum is large and broad, occupying much of the anteroventral length of the frontal [49-51]. An additional large lobe is formed by the posterior portion of the parietal, likely the optic lobes (based on comparisons with Alligator mississippiensis and Gallus domesticus in [52]). The anterior outlet of the osseous braincase in Av. renestoi is also transversely broad; the prootics angle strongly medially at their anterior tips to meet dorsolaterally inclined clinoid processes of the parabasisphenoid. A brain enlarged in the way this endocast suggests is otherwise unknown in a Triassic reptile (figure 3a). Past studies correlate the enlargement of the brain in pterosaurs and maniraptorans with the adaptation of those taxa to flight—it may be that the enlargement of the drepanosaurid brain followed a similar path to an adaptation to the three-dimensional environments required by arboreality, precision grasping and enhanced stereoscopic vision [29,40,49,50,53]. The inclination of the occipital condyle relative to the long axis of the skull is unclear, owing to the disarticulation of the Av. renestoi holotype. In our reconstruction, the occipital condyle is slightly posteroventrally inclined relative to the long axis of the skull, in contrast to the strong posteroventral inclination described for Me. preonensis [40]. However, the distortion of the skull of Av. renestoi may obscure the original shape of the craniocervical articulation.

Plesiomorphic traits

The anatomy of the suspensorium and other morphologies of the braincase stand in stark contrast to the ‘advanced’ features of the skull roof and rostrum. The squamosal is a dorsoventrally tall, anteroposteriorly broad bone. It exhibits both lateral and posterior laminae that frame the quadrate on those sides, as in archaic eureptiles (e.g. Captorhinus aguti [43,54]) and diapsids (e.g. Araeoscelis gracilis [55]). This contrasts with the condition in younginiform and saurian reptiles (appendix C), in which the quadrate is only framed laterally. In younginiform and saurian taxa, the quadrate also extends dorsally to fit into a fossa on the ventral surface of the squamosal—a feature absent in Av. renestoi. The quadrate itself is dorsoventrally short and vertically oriented, lacking the posterior embayment in most early saurian reptiles (figure 3f) [33,56-58].

The braincase exhibits a number of traits more commonly found in non-saurian diapsids. The occipital condyle exhibits a deep, posterior depression (=notochordal pit) across much of its surface and the basal tubera barely extend ventrally below the condyle (similar to Ca. aguti [59], Ar. gracilis [55]) (figure 3d). The foramen ovale is extremely large and extends to the ventralmost margin of the braincase. The stapes is massive, with a footplate that entirely fills the foramen and a lateral stem that is larger in all dimensions than the paroccipital process of the opisthotic (figure 3d). Foramina ovale and stapedes of this great size are common in early amniotes [59,60], but they are substantially smaller in younginiform diapsids (e.g. Youngina capensis [61]) and early saurians (e.g. Mesosuchus browni [60], Prolacerta broomi [58]). There is no evidence of a laterosphenoid ossification, as in Archosauriformes [62-64].

The plesiomorphic diapsid characters of the skull in Av. renestoi strongly suggest a plesiomorphic ear. Extant reptiles possess a tympanic membrane framed anteriorly by the concavity of the quadrate, which medially contacts a cartilaginous extracollumella, which in turn meets a very slender, osseous stapes [65,66]. The absence of an embayed quadrate and tympanic crest in Av. renestoi suggests the absence of a tympanic membrane. The large foramen ovale with prominent contributions by parabasisphenoid and basioccipital is more common in non-younginiform and non-saurian amniotes, as is the large stapes [59,65,66]. Thus, Av. renestoi lacks the major osteological correlates of impedance-matched hearing. An atympanic condition occurs in a number of extant lepidosaurs (e.g. chameleons, Sphenodon), although these taxa exhibit a slender stapes and a condyle–cotyle articulation between quadrate and squamosal and are widely considered to have undergone secondary loss of external ears. The archaic ear morphology in Av. renestoi, in concert with the other plesiomorphic amniote traits discussed above, contrasts sharply with the comparatively ‘advanced’ condition in most Triassic Sauria [58,60,67].

Phylogenetic analysis

In the light of the extensive new data on the cranial anatomy of Drepanosauromorpha provided by AMNH FARB 30834, we integrated the taxon into a phylogenetic analysis focused on terrestrial Permo-Triassic Diapsida and early Sauria (modified from [10,11,68]). We present analysis parameters and detailed results in appendix C. In the most-parsimonious trees, Drepanosauromorpha is recovered as an extremely early-diverging clade of Diapsida, occurring outside of a clade including Permian ‘younginiform’ diapsids and Sauria (figure 4). The oldest-known younginiform diapsid (herein referred to as Tropidostoma Zone Youngina) dates to the lowermost Upper Permian [69], suggesting that the lineage including drepanosauromorphs must have originated by the end of the Middle Permian (approx. 260 Myr). This phylogeny also recovers Kuehneosauridae, typically found as the sister taxon of Lepidosauria in cladistic analyses of early Diapsida (e.g. [70-72]), as deeply nested within Archosauromorpha (postulated in [73]).

Figure 4.

Strict consensus of most-parsimonious trees based on the phylogenetic analysis presented herein. Petrolacosaurus kansensis (not shown) was designated as the outgroup. Taxa listed in all-capitals are represented by multiple species-level terminal taxa in the analysis. The complete species-level topology is presented in figures 8 and 9.

Figure 8.

Strict consensus of the primary parsimony analysis presented in this paper. Numbers above the nodes are Bremer values (=decay indices). Numbers below the nodes are frequency differences resulting from the jackknife analysis.

Figure 9.

Strict consensus of the primary parsimony analysis stratigraphically calibrated.

Discussion and conclusion

These results indicate that drepanosauromorphs represent a deep divergence within Diapsida, earlier than that of crown-group reptiles, but one that persisted through the PTE and radiated deep within the Triassic [11,27]. A number of the non-saurian diapsids included in this analysis are taxa that also survived the PTE (Weigeltisauridae per [74], Hovasaurus boulei per [75]), indicating that the survival of drepanosauromorphs among non-crown-group reptiles was not a unique event.

Our revised phylogeny, combined with the extensive character data provided by the Av. renestoi holotype, strongly supports the hypothesis that Drepanosauromorpha are non-saurian diapsids. Phylogenetic analyses have long recognized that a number of crown-group reptile lineages (mostly early archosauromorphs) had diverged by the PTE, despite their initial appearance in the fossil record in the Triassic Period [9,10,33,63]. We tested hypothetical placements of drepanosauromorphs among crown-group reptiles through constraint analyses, but found these to be substantially less parsimonious (appendix C). That result, along with the recognition of numerous other non-crown-group lineages within the Triassic indicates that the Triassic diapsid radiation was far more phylogenetically heterogeneous than traditionally realized.

The general bird-like shape of the drepanosaurid rostrum has long been recognized, owing to complete but crushed specimens from the Upper Triassic of Italy. The three-dimensional preservation of AMNH FARB 30834 adds substantially to the bird-like features of the skull, including the frontated orbits and presumed binocular vision, the absence of teeth, possible fusion of the premaxillae and the inflated endocranium. However, these features occur in conjunction with a strikingly plesiomorphic braincase, suspensorium and postcranial skeleton [27]—features that strongly support the hypothesis that these bird-like features are entirely convergent. Bird-like features have been noted in a number of small Triassic diapsids—including Longisquama insignis and the putative stem-bird Protoavis texensis—which have been used to support the hypothesis that key features of the bird skull evolved very early in the Mesozoic [76,77]. This conception of bird evolution stands at odds with the fossil record of Theropoda, which suggests the gradual acquisition of avian cranial features throughout the Jurassic and Cretaceous [78-80]. The mosaic anatomy of Av. renestoi instead supports the hypothesis that several bird-like traits first emerged in a Triassic diapsid lineage entirely outside of crown-group reptiles [36].

The brain of Av. renestoi differs greatly from that in most Permian and Triassic diapsids. The cerebrum is substantially wider than the olfactory tracts and the endocranium occupies a substantial proportion of the transverse width of the skull, distinctly similar to the brains of maniraptorans (e.g.[50,81,82]), living birds (e.g.[83-85]) and pterosaurs (e.g. [49,86]). Many authors have suggested that the proportional expansion of brain and cerebrum size in these taxa is an adaptation to the sensory complexity required for navigating three-dimensional habitats [87-89]. The anteriorly directed orbits in Av. renestoi, coupled with the hypothesized arboreal habitat for drepanosauromorphs [27,39] suggest a complex sensory life for the animal and may explain the similarities in brain shape to flying and arboreal taxa. Further testing of this hypothesis requires better preserved endocasts and reconstruction of the vestibular apparatus of other drepanosauromorphs.

This phylogenetic study, in concert with the bird-like characters of the skull of Av. renestoi, increases the known disparity achieved by terrestrial diapsid reptiles during the Triassic Period and extends the pattern of morphological convergence on later Mesozoic lineages during the Triassic beyond Archosauromorpha into a non-crown-group reptile clade. This and similar discoveries demand constant re-evaluation of the phylogenetic diversity and morphological disparity of fossil groups involved in the recovery from the PTE.