Unusual morphology in the mid-Cretaceous lizard Oculudentavis Author Bolet, Arnau Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Barcelona, Spain & School of Earth Sciences, University of Bristol, Bristol, UK Author Stanley, Edward L. Department of Natural History, Florida Museum of Natural History, Gainesville, FL, USA Author Daza, Juan D. Department of Biological Sciences, Sam Houston State University, Huntsville, TX, USA juand.daza@gmail.com Author Arias, J. Salvador Unidad Ejecutora Lillo (CONICET - Fundación Miguel Lillo), San Miguel, de Tucumán, Tucumán, Argentina Author Cernanský, Andrej Department of Ecology, Laboratory of Evolutionary Biology, Faculty of Natural Sciences, Comenius University in Bratislava, Bratislava, Slovakia Author Vidal-García, Marta Department of Cell Biology & Anatomy, University of Calgary, Calgary, AB, Canada Author Bauer, Aaron M. Department of Biology and Center for Biodiversity and Ecosystem Stewardship, Villanova University, Villanova, PA, USA Author Bevitt, Joseph J. Australian Centre for Neutron Scattering, Australian Nuclear Science and Technology Organisation, Sydney, NSW, Australia Author Peretti, Adolf GRS Gemresearch Swisslab AG and Peretti Museum Foundation, Meggen, Switzerland Author Evans, Susan E. Department of Cell and Developmental Biology, University College London, London, UK text Current Biology 2021 2021-06-14 31 1 12 journal article 10.1016/j.cub.2021.05.040 a0723a89-d4df-4e36-9da9-cc6fd438c7c3 5013953 Oculudentavis naga new species Holotype Peretti Museum Foundation, GRS-Ref-28627 , a skull and anterior postcranial skeleton ( Figures 1 , 2A–2J , 3A, 3C , and S 1 ). Three-dimensional model of new specimen available at https:// tinyurl.com/Oculudentavis-L-10420. Type locality The holotype specimen of Oculudentavis naga ( GRS-Ref-28627 ) and the holotype of O. khaungraae (HPG-15-3) were recovered from the same mine ( Aung Bar mine , 26 O 09 0 N , 96 O 34 0 E ) . Etymology Combination of Oculudentavis (oculus = eye, dentes = teeth, and avis = bird) 1 and Naga, thename of oneof the many ethnic tribes living in the Burmese amber mines area. The Naga are mentioned in historical chronicles for their prominent role in amber trading. Divided into many sub-groups scattered across the hills and jungle of India (in Nagaland and other states) and in the Tiger valley region of Burma (where amber deposits are found), the Naga tribes are also reputed for their rich and fascinating culture. Diagnosis The holotype of O. naga (skull length = 14.2 mm ) is somewhat smaller than that of O. khaungraae (skull length = 17.3 mm ). Oculudentavis naga differs from O. khaungraae in having a jugal process of the maxilla that reaches caudally to less than 25% of orbit length; in having a long squamosal process of the postorbital; in having a relatively smaller braincase, with short, distally expanded basipterygoid processes (versus longer, unexpanded processes); and in having anterior palatal rami of pterygoids parallel, diverging posteriorly just behind the fossa columellae, interpterygoid vacuity nearly rectangular (versus divergent pterygoids, heart-shaped vacuity), rostral part of premaxilla shorter and proportionally wider than that of O. khaungraae , and less conspicuous platform on the dorsolabial surface of the posterior third of the dentary. Notes There are also differences between the two specimens in the robusticity of the postorbital (greater in O. khaungraae ); the height of the premaxillary crest (greater in O. naga ); the extent of the nasal emargination of the frontal (greater in O. naga ); the presence of a large anterior palatine fenestra ( O. naga ); the length and height of the coronoid process (larger and taller in O. naga ); the shape of the quadrate conch (more angular in O. khaungraae ); and in the overall shape of the rostrum (more pointed in O. khaungraae ) and postorbital skull (more vaulted in O. khaungraae ). Oculudentavis naga also displays a very large palatal fenestra between the vomers and palatines. This region is poorly preserved in the holotype of O. khaungraae , and the presence or absence of the fenestra cannot be determined. However, it is possible that at least some of these differences between the two specimens are due to a combination of individual variation, taphonomical deformation (also rendering some elements difficult to segment precisely), and perhaps sexual dimorphism (comparing a male of one species with a female of another could exaggerate interspecific differences like the premaxillary crest height). With only a single specimen of each species, individual variation is impossible to assess.Also note that the skull of O . khaungraae was reported as measuring 14 mm in length, 1 whereas our own measurement of the specimen gives a length of 17.3 mm . Figure 2. Comparison of the two specimens of Oculudentavis , each bone digitally segmented Synchrotron HRCT of O.naga (A–J) and O . khaungraae (K–T).(Aand K) Anterior view, (B and L) posterior view, (C, M, I, and S) dorsal view,(D, N, J, and T) ventral view, (E and O) left lateral view, (F, G, P, and Q) right lateral view, and (H and R) medial view are shown. See also Figures S1–S7 and Data S1. Figure 3. Comparison of the two specimens of Oculudentavis , details of the lacrimal and dentary Right side view of the orbit showing the ring-like lacrimal bone (salmon color) in situ in (A) O . naga and (B) O . khaungraae (orbit view here is posterolateral to show the orbital elements more clearly). Dorsolingual view of the dentary in (C) O . naga and (D) O . khaungraae is shown. Scale bar represents 1 mm. Description In its bird-like shape (vaulted cranium and tapering rostrum), the skull of Oculudentavis khaungraae appears strikingly different from that of any known lizard ( Figure 4 ). The bird-like appearance is less striking in O. naga , which has a less compressed rostrum ( Figure 2 ). Despite thecompression of the rostrum,the two speciesshare many characters that distinguish them from other lizards. The nares are bounded by the premaxilla anterodorsally, the maxilla posteroventrally, and by the nasals posteriorly. The location of the nares is also the same, being placed at mid-length of the antorbital region and in having an elongated oval shape. The orbit is more intact in O. khaungraae , being nearly circular. In both species, the longest axis of the orbit is about 1/3 the total length of the skull and the orbit is complete and separated from the temporal fenestrae by a complete postorbital bar. The parietal supratemporal processes are aligned with the long and slender vertical supratemporals and fail to meet the squamosals ventrally. There is a complete circumorbital series in both specimens—jugal (ventrally), lacrimal (anteriorly), prefrontal (anterodorsally), frontal (dorsal), postfrontal (posterodorsally), and postorbital (posteriorly). Premaxilla ( Figures 2, S2A–S2B, S 2I , and S2J ). The upper jaw comprises an unpaired median premaxilla with slender, pointed teeth ( 9 in O. khaungraae and ~ 10 in O. naga ; count refers to one side of the element). The more anterior premaxillary teeth appear recurved in O. khaungraae , but the equivalent teeth in O. naga are partially obscured. Both species have a long crest along the premaxillary nasal process (the crest was considered taphonomic in O. khaungraae ), 1 which continues onto the nasals. The palatal shelf is broad and flat and has two narrow palatal processes that bound a large premaxilla-vomer fenestra in O. naga , which has a less deformed palate. The palatal processes of the premaxilla are also visible in O. khaungraae , but not the intervening fenestra (see below). Maxilla ( Figures 2, S2C–S2E, and S2K–S2M ). The maxilla of both species has a low, medially curved facial process, a long rostral component, and a suborbital ramus that does not reach the posterior margin of the orbit—extending up to one-quarter of the orbit length in O. naga and to about mid-orbit in O. khaungraae . It is excluded from the orbital rim by the jugal. The maxillary teeth are conical and pointed. There are 24 to 25 tooth maxillary loci in O. naga and 27–29 in O. khaungraae . The maxilla has two horizontal facets: one to support the prefrontal and another for the jugal. Nasal ( Figures 2, S2F, and S2N ). The paired nasals form a rhomboid plate, and combined with the maxilla, they define a long tapering rostrum with retracted narial openings. The nasals are paired, but they exhibit partial fusion along the crest and remain separated posterior to the crest. Prefrontal ( Figure 2 ).The prefrontalscomprisea flatanterodorsal plate and a weakly concave orbital plate, contacting the ringshaped lacrimal ventrally. The anterodorsal plate seems less developed in O. khaungraae than O. naga . The lateral edge of the anterodorsal plate projects as a short angular ( O. naga ) or ridgelike ( O. khaungraae ) shelf that overhangs the lacrimal and maxilla. This shelf is autapomorphic among lizards, with a ridge, crest, or boss in this position variably present (e.g., some iguanians, including chameleons; some Phrynosoma ; and some Anolis ). Figure 4. Cranial disparity of typical lepidosaurs to demonstrate the atypical skulls of Oculudentavis (A) Sphenodon punctatus , Rhynchocephalia UF 11978;(B) Anelytropsis papillosus UF-H-86708, Dibamidae ;(C) Sphaerodactylus caicosensis UF 95971,Gekkota; (D) Smaug swazicus NMB-R9201, Cordyliformes; (E) Eugongylus albofasciolatus CAS 159825, Scincidae ; (F) Varanus sp. UF71411, Varanidae ; (G) Rieppeleon brevicaudatus CAS 168891, Iguania;(H) Boaedon fuliginosus CAS 85747, Serpentes;(I) Oculudentavis naga GRS-Ref-28627;(J) O . khaungraae HPG-15-3.Scale bar represents 10 mm. Lacrimal ( Figures 3A and 3B ). The lacrimal of both species is unique among lizards and is one of several distinctive features that demonstrates their close relationship. It forms a ring, completely enclosing a large lacrimal foramen. Jugal ( Figures 2, S2G, S2H, S2O, and S2P ). In both species, the jugal forms a dorsomedially expanded flange that provides ventral support to the large eye. The orientation of the jugal is unusual for squamates, being dorsomedially inclined. The postorbital process of the jugal is short (distorted on the right side of O. naga ). Frontal ( Figures 2 , S 3A, and S3E ). In both species, the unpaired median frontal has weak sub-olfactory processes and a deep V-shaped anterior emargination that receives the nasals. The frontal is overlapped extensively by the nasals, reaching the level of the mid-orbit in O. naga and somewhat less in O. khaungraae . The supraorbital margins are subparallel and diverge posterolaterally, establishing a broad contact with the anterior margin of the parietal. The structure of the posteromedial margin of the fronto-parietal suture is unclear in both specimens ( Figure 2 , dashed lines). Parietal ( Figures 2 , S 3B, and S3F ). The parietals are short and partially fused (separated posteriorly). They have a rounded lateral profile, lack a parietal foramen, and have short supratemporal processes that curve ventrally rather than posteriorly to meet the supratemporals. This portion of the skull contacts the short paroccipital processes of the otoccipital. Li et al. 3 argued that the small opening in the midline of the parietals in the holotype of O. khaungraae corresponds to a parietal foramen, but it is irregular and appears to be an artifact of breakage. Postfrontal ( Figure 2 ). The postfrontal is a small, splint-like bone, lateral to the frontal and the parietal in O. khaungraae but of uncertain structure and position in O. naga . The postfrontals are very reduced in both species and were not noticed in the original description of O. khaungraae . Postorbital ( Figures 2 , S 3C, and S3G ). The postorbital is a strongly triradiate bone with a long ( O. naga ) or short ( O. khaungraae ) posterior process that contacts the squamosal posteriorly. The postorbital differs in the two species: the postorbital squamosal process tapers gradually in the O. naga holotype , while the tapering appears more abrupt in the O. khaungraae specimen. Due to the proportionally thicker postorbital, the right side of O. khaungraae shows a more extensive contact between the postorbital and the descending process of the parietal, entirely covering the braincase laterally and almost completely closing the upper temporal fenestra. However, on the left side, it is clear that this fenestra remained open. In O. naga , the upper temporal fenestra looks larger, but the skull table of this specimen is very depressed and the postorbital is more gracile, so the differences in configuration of the upper temporal bar may be exaggerated by taphonomic deformation. Squamosal ( Figures 2 , S 3D, and S3H ). In both species, the typically squamate hockey-stick-shaped squamosal lacks an ascending process and lies between the supratemporal, the postorbital, and the quadrate. Supratemporal ( Figures 2 , S 3B, and S3F , articulated with the parietal). The supratemporal is also reduced to a slender vertical splint of bone that contacts the lateral margin of the parietal supratemporal process, separating it from the squamosal. Palate ( Figures 2 , S 4A, and S4D ). In the palate of O. khaungraae , the premaxilla-vomer fenestra is totally obliterated (due to compression). In this respect, O. naga has a more intact rostrum, more clearly exhibiting thepremaxilla-vomer fenestra and the very large fenestra exochoanalis. The suborbital fenestra is oval in both specimens and is bounded by the same bones: palatines anteromedially, ectopterygoids laterally, and pterygoids posteriorly, although the sutures between these bones are not easy to identify. It also looks as if the ectopterygoid barely contacts the palatine in O. naga , but the degree of contact is ambiguous in O. khaungraae . The shape of the interpterygoid vacuity differs between the two species. Pterygoid teeth are present and are arranged in a row on the anteromedial process of the pterygoid, just posterior to the inferred suture with the palatine. There are about 3 to 4 on each bone in O. khaungraae ; the same area is fragmented in O. naga , but small projections on both pterygoids can be interpreted as pterygoid teeth. Quadrate ( Figures 2 , S 4B, and S4E ). The quadrate is distinctively low in position and small in size in both species. The quadrate is stouter in O. khaungraae (with a more prominent head) than in O. naga , but the overall shape is similar in both specimens, with a shallow conch, a slightly curved medial pillar, and a lateral tympanic crest that has a 90-degree angulation along its length. The quadrate suspension in both species is characteristically squamate. Braincase ( Figures 2 and S 5 ). By comparison with that of O. khaungraae , the braincase of O. naga is unevenly dorsoventrally compressed, so that the right side is more damaged than the left and the posteroventral margin is abnormally low. Nonetheless, comparison of the two braincases shows more similarities than differences, notably the well-developed crista prootica, short alar processes, slender basipterygoid processes, short basisphenoid, enclosed vidian canals opening posteriorly within the basisphenoid, robust parasphenoid rostrum (base only preserved in O. naga ), short uncrested supraoccipital with a visible processus ascendens (mineralization uncertain), and short paroccipital processes. The parasphenoid rostrum is well preserved in O. khaungraae , being longer than the basipterygoid processes, and almost entirely divides the interpterygoid vacuity. In O. naga , the parasphenoid rostrum is represented only by its base, possibly due a fracture or weak mineralization. However, there are differences in the orientation, length, and distal shape of the basipterygoid processes in the two species. Epipterygoid ( Figure 2 ). These elements are poorly preserved and displaced in both species. They are columnar and still in articulation within the fossa columellae of the pterygoid, this articulation being another uniquely squamate character. In the holotype of O. naga , a portion of the left epipterygoid remains attached to the alar process. Scleral ossicles ( Figures 1 , S 4C, and S4F ). In both species, the orbit contains a large ring of ‘‘spoon-shaped’’ scleral ossicles that supported a large eye. The ossicle count is 14 in both specimens. Due to the distinctive shape of the ossicles, they overlap at both their inner edges (which would have surrounded the iris and the pupil) and the outer edges, leaving oval gaps between ossicles in the middle of the sclerotic ring. Although the skull of O. khaungraae is 1.2X longer than that of O. naga , the scleral ossicles are proportionally larger in O. khaungraae , being 1.5X larger than those of O. naga . Dentary ( Figures 2 , 3C, 3D , and S 6 ). Both species have a long shallow mandible of which the straight dentary forms the major part ( ~ 75%) and a large number of sharp, weakly pleurodont teeth ( 29 to 30 in both specimens). Both speciesalso have a large number of lateral neurovascular foramina (10–12), and the dentary in each specimen has parallel upper and lower margins. Thesymphysealregiondoes not extendbeyondthe second tooth locus in either specimen. The lower margin of the dentary curves dorsomedially and closely approaches the subdental shelf, thus restricting the Meckelian fossa but without fusion.The Meckelian fossa remains open posteriorly, where it is overlapped by the splenial. The dorsolabial surface of the posterior one-third of the dentary bears a flattened, shelf-like surface. Splenial ( Figures 2 and S 6 ). The splenial is very slender and does not extend anteriorly beyond the posterior one-third of the dentary, closing only the posterior part of the Meckelian fossa in both species. Posteriorly, the splenial does not extend beyond the level of the coronoid eminence. Coronoid ( Figures 2 and S 6 ). The postdentary region is short, including a coronoid with a low, posteriorly set, coronoid eminence. The coronoid looks significantly larger in the holotype of O. naga than in the holotype of O. khaungraae , especially in the development of the anterolateral and anteromedial processes. However, these differences could be due to damage during deformation, making it difficult to establish clear bone boundaries (e.g., between surangular and coronoid), as this was one of the most problematic regions to segment in both specimens. Angular ( Figures 2 and S 6 ). This is a very reduced and slender bone, limited to the posteroventral side of the jaw. Compound bone ( Figures 2 and S 6 ). There is no obvious suture between the surangular and the articular or prearticular in either specimen. Both specimens have a long retroarticular process and a short, deep adductor fossa. It is uncertain whether the coronoid reached the anterior margin of the adductor fossa. Although only part of the postcranial skeleton is preserved in O. naga , it shows a short neck with eight cervical vertebrae that are amphicoelous, atlantal arches bearing posterior zygapophyses, and a pectoral region comprising a T-shaped interclavicle, medially expanded clavicles, and a typically squamate scapulocoracoid with scapular, scapulocoracoid, and primary coracoid fenestrae. Vertebrae ( Figures S7Aand S7B ). Eight cervical vertebrae are preserved, including the atlas and the axis, as well as a small number of dorsal vertebrae (using the traditional anatomical definition whereby the first dorsal vertebra is that with a rib that meets the sternum, contra Gauthier et al. 7 ). The atlantal arches are not fused, and they have well-developed postzygapophyses. The axis preserves the dens, which is already fused in place. The vertebrae are amphicoelous and notochordal, with low neural spines. There are simple semicircular intercentra visible in the anterior part of the neck, with only a weak ventromedian keel ( Figure S7 ). As in living gekkotans, these elements are free and intercentral in position. The first visible cervical rib is on cervical six, but there may have been ribs more anteriorly. There are no gastralia. Clavicle ( Figure S7C–S7E ). The clavicles are expanded medially and have a well-defined clavicular fenestra completely enclosed by bone. The clavicles are separated at the ventral midline by tip of the T-shaped interclavicle. Dorsally, the clavicles appear to extend above the level of the scapula blade, possibly meeting a suprascapular cartilage. Scapulocoracoid ( Figures S7C–S7E ). Both scapulocoracoids are preserved and display an anterior primary coracoid emargination, anemarginated scapular blade, and a large circular scapulocoracoid emargination. Dorsal to the scapula, there is an irregular mass that may represent the suprascapular cartilage. Sternum ( Figure S7D ). Only the anterior border of the cartilage sternum is preserved, suggesting it was rhomboid. Interclavicle ( Figure S7D ). The interclavicle is T-shaped and quite robust. Humerus ( Figure S7D ). The proximal portion of the left humerus is present, preserving the humeral head and the lateral tuberosity. Figure 5. Phylogenetic trees showing the position of Oculudentavis (A) Phylogenetic tree showing the position of Oculudentavis usingan amniote dataset; 6 (B) photograph of the holotypeof O . naga ; (C) simplified phylogenetic tree showing the position of Oculudentavis using a squamate dataset 7 combined with a molecular dataset 15 treating some morphological characters as ordered; (D) simplified phylogenetic tree showing the position of Oculudentavis using the same dataset as in (C) but with all characters unordered;(E) simplified phylogenetic tree showing the position of Oculudentavis using the same dataset as (C) but removing molecular data. In (C)–(E), crown groups were collapsed and are represented by silhouettes. Sphenodon punctatus , Anelytropsis papillosus ( Dibamidae ), Sphaerodactylus klauberi (Gekkota) , Smaug giganteus ( Cordylidae ), Xantusia vigilis ( Xantusiidae ), Tribolonotus gracilis ( Scincidae ), Bachia flavescens (Lacertoidea) , Lacerta bilineata (Lacertoidea) , Blanus cinereous (Amphisbaenia) , Varanus komodoensis (Anguimorpha) , Physignathus cocincinus (Iguania) , and Ophiophagus hannah (Serpentes) are shown. Node values indicate Bremer support; nodes with no support were recovered in the implied weights analyses. See also Data S1. Soft tissue ( Figure 1 ; Data S1, Gular scales in Oculudentavis ). Both specimens also preserve soft tissue. The head and body are covered in small, granular scales, with large rectangular supralabial and infralabial scales, tiny scales covering the eyelid, and a nostril placed anterior to the midpoint of each retracted narial opening ( Figures 1 and 2 ) in O. naga . There are no osteoderms. On the ventral surface of the head in O. naga , along the midline, the epidermal scales are raised and form a line of evenly spaced short ridges. Posterior to this midventral line, the skin of the gular region is thrown into a series of narrow linear folds. This folded region underlies the hyoid ceratobranchials and may demonstrate the resting anatomy of loose gular skin that could be inflated, for example in territorial display,in associationwith hyoidmovements.