A non-avian dinosaur with a streamlined body exhibits potential adaptations for swimming Author Lee, Sungjin School of Earth and Environmental Sciences, Seoul National University, Seoul, Korea. Author Lee, Yuong-Nam School of Earth and Environmental Sciences, Seoul National University, Seoul, Korea. ynlee@snu.ac.kr Author Currie, Philip J. Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada. Author Sissons, Robin Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada. Author Park, Jin-Young School of Earth and Environmental Sciences, Seoul National University, Seoul, Korea. Author Kim, Su-Hwan School of Earth and Environmental Sciences, Seoul National University, Seoul, Korea. Author Barsbold, Rinchen Institute of Paleontology, Mongolian Academy of Sciences, Ulaanbaatar, Mongolia. Author Tsogtbaatar, Khishigjav Institute of Paleontology, Mongolian Academy of Sciences, Ulaanbaatar, Mongolia. text Communications Biology 2022 2022-12-01 5 1 1 9 journal article 10.1038/s42003-022-04119-9 b49b6ede-730b-460a-a2c1-f1b7f221399d 7390392 Natovenator polydontus gen. et sp. nov. Holotype . MPC-D 102/114 (Institute of Paleontology, Mongolian Academy of Sciences, Ulaanbaatar, Mongolia) is a mostly articulated skeleton with a nearly complete skull (See Supplementary Table 1 for measurements). Locality and horizon . Baruungoyot Formation (Upper Cretaceous) , Hermiin Tsav , Omnogovi Province , Mongolia 13 (Supplementary Fig. 5 ) . Fig. 1 Natovenator polydontus (MPC-D 102/114, holotype). Photographs ( a , c ) and line drawings ( b , d ) of the main block containing most of the specimen in opposite views. cav caudal vertebra, co coracoid, cv cervical vertebra, d dentary, dc distal carpal, dv dorsal vertebra, fem femur, fu furcula, h humerus, mx maxilla, ph phalanx, pm premaxilla, r radius, ul ulna. (2022) 5:1185 | https://doi.org/10.1038/s42003-022-04119-9 | www.nature.com/commsbio Fig. 2 Skull of Natovenator polydontus (MPC-D 102/114, holotype). a – d Skull in left lateral ( a ), right lateral ( b ), dorsal ( c ), and ventral ( d ) views. e µ CTrendered image sliced at the point marked on a , showing a cross-section of the premaxillary and anterior maxillary teeth in dorsal view. f Micro-computed tomography ( µ CT) rendered image of the occipital region in posterior view. g µ CT-rendered image of the pterygoid and quadrate.?bm possible bite mark, d dentary, f frontal, h humerus, l lacrimal, m5 5th maxillary tooth, mx maxilla, na nasal p parietal, p13 13th premaxillary tooth, pl palatine, pm premaxilla, pop paroccipital process, pt pterygoid, q quadrate, rt replacement tooth, sq squamosal, so supraoccipital. Etymology . Natovenator , from the Latin nato (swim) and venator (hunter), in reference to the hypothesized swimming behaviour and piscivorous diet of the new taxon; polydontus , from the Greek polys (many) and odous (tooth) in reference to the unusually many teeth. Diagnosis . A small halszkaraptorine dromaeosaurid with the following autapomorphies: wide groove delimited by a pair of ridges on the anterodorsal surface of the premaxilla, premaxilla with an elongated internarial process that overlies nasal and extends posterior to the external naris, 13 premaxillary teeth with large and incisiviform crowns, first three anteriormost maxillary teeth are greatly reduced and are clustered together with the following tooth without any separations by interdental septa, anteroposteriorly long external naris (about 30% of the preorbital skull length), paroccipital process with a anteroposteriorly broad dorsal surface, elongate maxillary process of the palatine that extends anteriorly beyond the middle of the antorbital fenestra, pterygoid with a deep fossa on the medial surface of the quadrate ramus, distinct posterolaterally oriented projection on the lateral surface of atlas, absence of pleurocoels in cervical vertebrae (not confirmed in the missing fifth cervical centrum), posterolaterally oriented and nearly horizontal proximal shafts in the dorsal ribs, hourglass-shaped metacarpal II with distinctly concave medial and lateral surfaces. Description . The skull of Natovenator is nearly complete, although the preorbital region has been affected by compression and is slightly offset from the rest of the skull ( Figs. 1c, d , 2a–d and Supplementary Figs. 1 , 2 ). Near the tip of the snout, the premaxilla is marked by a broad groove. The body of the premaxilla is also dorsoventrally low and is perforated by numerous foramina that lead into a complex network of neurovascular chambers (Supplementary Fig. 1b ) as in Halszkaraptor 4. Similarly, the external naris is positioned posteriorly and is level with the premaxilla-maxilla contact ( Fig. 2a, b ), although it is marginally behind this position in Halszkaraptor 4 . It is also dorsally placed compared to those of other non-avian theropods and faces dorsolaterally. The exceptionally long external naris and accordingly elongated internarial process of Natovenator ( Fig. 2c ) are unique among dromaeosaurids but comparable to those in aquatic toothed birds 14 as well as in therizinosaurs 15 , 16 . The frontal is similar to those of other halszkaraptorines 4 , 17 in that it is vaulted to accommodate a large orbit and has little contribution to the supratemporal fossa. A sharp nuchal crest is formed by the parietal and the squamosal (Supplementary Fig. 2a–e ). The latter also produces a shelf that extends over the quadrate head as in other dromaeosaurids 18 . The paroccipital process curves gently on the occiput and has a broad dorsal surface that tapers laterally ( Fig. 2f and Supplementary Fig. 2b, e ). Its ventrolateral orientation is reminiscent of Mahakala 17 but is different from the more horizontal paroccipital process of Halszkaraptor 4 . The occipital condyle is long and constricted at its base. A shallow dorsal tympanic recess on the lateral wall of the braincase is different from the deep one of Mahakala 17 . The palatine is tetraradiate with a greatly elongated maxillary process, which extends anteriorly beyond the level of the mid-antorbital fenestra. The pterygoid is missing its anterior portion ( Fig. 2g and Supplementary Fig. 2a–e ). A deep fossa on the medial surface of the thin quadrate ramus is not seen in any other dromaeosaurids. The mandibles of Natovenator preserve most of the elements, especially those on the left side ( Fig. 1a, b, d and Supplementary Figs. 1a , 2 ). Each jaw is characterized by a slender dentary with nearly parallel dorsal and ventral margins, a surangular partially fused with the articular, a distinctive surangular shelf, and a fan-shaped retroarticular process that protrudes dorsomedially. The upper dentition of Natovenator is heterodont as the premaxillary teeth are morphologically distinct from the maxillary teeth ( Fig. 2a, b, e and Supplementary Fig. 1a, c ). There are unusually numerous premaxillary teeth tightly packed without any separation of the alveoli by bony septa. The roots of the teeth are long, and the crowns are tall and incisiviform as in Halszkaraptor 4 . Moreover, the large replacement teeth in the premaxilla suggest that the replacement of the premaxillary teeth was delayed as in Halszkaraptor 4 . However, the number of teeth in each premaxilla is 13 in Natovenator , whereas it is only 11 in Halszkaraptor 4 . In the maxilla, the three most anterior maxillary teeth are markedly shorter than the premaxillary teeth and the more posterior maxillary teeth. This pattern is also observed in Halszkaraptor , although the number of shorter maxillary teeth differs as it has two reduced ones 7 . Both the maxillary and dentary teeth have sharp fang-like crowns that lack serrations. Although posteriormost parts are poorly preserved, there are at least 23 alveoli in each of the maxilla and dentary, which suggests high numbers of teeth in both elements. (2022) 5:1185 | https://doi.org/10.1038/s42003-022-04119-9 | www.nature.com/commsbio Fig. 3 Postcranial elements and phylogenetic position of Natovenator polydontus (MPC-D 102/114, holotype). a Anterior cervical vertebrae in left lateral view. b Axis and third cervical vertebra in dorsal view. c Fourth cervical vertebra in dorsal view. d Posterior cervical vertebrae in right lateral view. e Dorsal series in right lateral view. f Anterior caudal vertebrae in right lateral view. g Left forearm elements in medial view and manus in ventral view. h Right foot in ventral view. i Phylogenetic position of Natovenator in Dromaeosauridae . Numbers at each node indicate Bremer support values. at atlas, c3 third cervical vertebra, c4 fourth cervical vertebra, c7 seventh cervical vertebra, c9 ninth cervical vertebra, ch chevron, d7 seventh dorsal vertebra, fem femur, mc I metacarpal I, mt III metatarsal III, mt IV metatarsal IV, poz postzygapophysis, prz prezygapophysis, r radius, r7 seventh dorsal rib, ul ulna, I-2 pedal phalanx I-2. (2022) 5:1185 | https://doi.org/10.1038/s42003-022-04119-9 | www.nature.com/commsbio Fig. 4 Body plan of Natovenator polydontus (MPC-D 102/114, holotype) and dorsal rib morphology of various diving birds and terrestrial taxa. a Dorsal series of Natovenator in ventral view. b Reconstruction of dorsal vertebrae and ribs of Natovenator in left lateral view. c Skeletal reconstruction of Natovenator with missing parts in dark grey. d – i Dorsal rib morphology of Natovenator ( d ), diving birds ( e – i ), common ostrich ( j ), and Shri devi , a likely terrestrial dromaeosaurid from the Baruungoyot Formation ( k ) in ventral view (not to scale). l Reconstruction of the fourth dorsal vertebra with corresponding ribs in anterior view. d2 second dorsal vertebra, r2 second dorsal rib, r3 third dorsal rib, r4 fourth dorsal rib. The neck of Natovenator , as preserved, is twisted and includes ten elongated cervical vertebrae, although most of the 5th cervical is missing ( Figs. 1 , 3a–d ). This elongation of the cervicals results in a noticeably longer neck than those of most dromaeosaurids and is estimated to be longer than the dorsal series. It is, however, proportionately shorter than that of Halszkaraptor , which has a neck as long as its dorsal and sacral vertebra combined 4 . Another peculiarity in the neck of the Natovenator is a pronounced posterolaterally extending projection on the neurapophysis of the atlas ( Fig. 3a and Supplementary Fig. 2b, c, e ). The postzygapophyses of each anterior cervical are fused into a single lobe-like process as in Halszkaraptor 4 . Pleurocoels are absent in the cervical vertebrae. In contrast, Halszkaraptor has pleurocoels on its 7th–9th cervicals 4 . A total of 12 dorsal vertebrae are preserved ( Figs. 1a, b , 3e , 4a and Supplementary Figs. 3a–d ). They all lack pleurocoels, and their parapophyses on the anterior and middorsals are placed high on the anterodorsal end of each centrum. Interestingly, the positions of the parapophyses are similar to those of hesperornithiforms 19 – 21 rather than other dromaeosaurids such as Deinonychus 22 or Velociraptor 23 . The preserved dorsal ribs, articulated with the second to seventh dorsals, are flattened and posteriorly oriented ( Figs. 1 , 3e , 4a–d ). The proximal shafts are also nearly horizontal, which is indicative of a dorsoventrally compressed ribcage. Each proximal caudal vertebra has a long centrum and horizontal zygapophyses with expanded laminae ( Fig. 3f and Supplementary Fig. 3e–i ), all of which are characters shared with other halszkaraptorines 4 , 17 . The forelimb elements are partially exposed ( Figs. 1a, b , 2a–d , 3e, g ). The nearly complete right humerus is proportionately short and distally flattened like that of Halszkaraptor 4 . The shaft of the ulna is mediolaterally compressed to produce a sharp posterior margin as in Halszkaraptor 4 and Mahakala 17 . Metacarpal III is robust and is only slightly longer than metacarpal II. Similarly, metacarpal III is almost as thick and long as other second metacarpals of other halszkaraptorines 4 , 17 . The femur has a long ridge on its posterior surface, which is another characteristic shared among halszkaraptorines 4 . Typically for a dromaeosaurid, metatarsals II and III have ginglymoid distal articular surfaces ( Fig. 3h and Supplementary Fig. 4f, h ). The ventral surface of metatarsal III is invaded by a ridge near the distal end, unlike other halszkaraptorines ( Fig. 3h ) 4 , 5 , 17 , 24 . (2022) 5:1185 | https://doi.org/10.1038/s42003-022-04119-9 | www.nature.com/commsbio Phylogenetic analysis . The phylogenetic analysis found more than 99,999 most parsimonious trees (CI = 0.23, RI = 0.55) with 6574 steps. Deinonychosaurian monophyly is not supported by the strict consensus tree (Supplementary Fig. 6). Instead, Dromaeosauridae was recovered as a sister clade to a monophyletic clade formed by Troodontidae and Avialae, which is consistent with the results of Cau et al. 4 and Cau 7 . Halszkaraptorinae is positioned at the base of Dromaeosauridae as in Cau et al. 4 , although there are claims that dromaeosaurid affinities of halszkaraptorines are not well supported 25 . Nine (seven ambiguous and two unambiguous) synapomorphies support the inclusion of Halszkaraptorinae in Dromaeosauridae . The two unambiguous synapomorphies are the anterior tympanic recess at the same level as the basipterygoid process and the presence of a ventral flange on the paroccipital process. A total of 20 synapomorphies (including one unambiguous synapomorphy) unite the four halszkaraptorines, including Natovenator (Supplementary Fig. 7). In Halszkaraptorinae, Halszkaraptor is the earliest branching taxon, and the remaining three taxa form an unresolved clade supported by three ambiguous synapomorphies (characters 121/ 1, 569/0, and 1153/1). Two of these synapomorphies are related to the paroccipital process (characters 121 and 569), which is not preserved in Hulsanpes 5 , 24 . The other is the presence of an expansion on the medial margin of the distal half of metatarsal III, which is not entirely preserved in the Natovenator . When scored as 0 for this character, Natovenator branches off from the unresolved clade. It suggests that the medial expansion of the dorsal surface of metatarsal III could be a derived character among halszkaraptorines.