Pterosaurs were the first vertebrates to evolve powered flight1 and comprised one of the main evolutionary radiations in terrestrial ecosystems of the Mesozoic era (approximately 252–66 million years ago), but their origin has remained an unresolved enigma in palaeontology since the nineteenth century2,3,4. These flying reptiles have been hypothesized to be the close relatives of a wide variety of reptilian clades, including dinosaur relatives2,3,4,5,6,7,8, and there is still a major morphological gap between those forms and the oldest, unambiguous pterosaurs from the Upper Triassic series. Here, using recent discoveries of well-preserved cranial remains, microcomputed tomography scans of fragile skull bones (jaws, skull roofs and braincases) and reliably associated postcrania, we demonstrate that lagerpetids—a group of cursorial, non-volant dinosaur precursors—are the sister group of pterosaurs, sharing numerous synapomorphies across the entire skeleton. This finding substantially shortens the temporal and morphological gap between the oldest pterosaurs and their closest relatives and simultaneously strengthens the evidence that pterosaurs belong to the avian line of archosaurs. Neuroanatomical features related to the enhanced sensory abilities of pterosaurs9 are already present in lagerpetids, which indicates that these features evolved before flight. Our evidence illuminates the first steps of the assembly of the pterosaur body plan, whose conquest of aerial space represents a remarkable morphofunctional innovation in vertebrate evolution.
This is a preview of subscription content
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
The data matrices for the phylogenetic analyses in NEXUS and/or TNT formats have been deposited in MorphoBank at http://morphobank.org/permalink/?P3773. Three-dimensional models of lagerpetid bones in STL format are available in MorphoSource at http://www.morphosource.org/Detail/ProjectDetail/Show/project_id/1095 under the following DOIs: https://doi.org/10.17602/M2/M157269, https://doi.org/10.17602/M2/M157271, https://doi.org/10.17602/M2/M157273, https://doi.org/10.17602/M2/M157275, https://doi.org/10.17602/M2/M157280, https://doi.org/10.17602/M2/M157282, https://doi.org/10.17602/M2/M157283 and https://doi.org/10.17602/M2/M157284. Source data are provided with this paper.
Padian, K. The origins and aerodynamics of flight in extinct vertebrates. Palaeontology 28, 413–433 (1985).
Padian, K. in Third Symposium on Mesozoic Terrestrial Ecosystems: Short Papers (eds Reif, W.-E. & Westphal, F.) 163–166 (Atempto, 1984).
Sereno, P. C. Basal archosaurs: phylogenetic relationships and functional implications. Soc. Vertebr. Paleontol. Mem. 2, 1–53 (1991).
Benton, M. J. Scleromochlus taylori and the origin of dinosaurs and pterosaurs. Phil. Trans. R. Soc. Lond. B 354, 1423–1446 (1999).
Gauthier, J. A. Saurischian monophyly and the origin of birds. Mem. Calif. Acad. Sci. 8, 1–55 (1986).
Nesbitt, S. J. The early evolution of archosaurs: relationships and the origin of major clades. Bull. Am. Mus. Nat. Hist. 352, 1–292 (2011).
Ezcurra, M. D. The phylogenetic relationships of basal archosauromorphs, with an emphasis on the systematics of proterosuchian archosauriforms. PeerJ 4, e1778 (2016).
Nesbitt, S. J. et al. The earliest bird-line archosaurs and the assembly of the dinosaur body plan. Nature 544, 484–487 (2017).
Witmer, L. M., Chatterjee, S., Franzosa, J. & Rowe, T. Neuroanatomy of flying reptiles and implications for flight, posture and behaviour. Nature 425, 950–953 (2003).
Wellnhofer, P. The Illustrated Encyclopedia of Pterosaurs (Salamander Books, 1991).
Witton, M. P. Pterosaurs: Natural History, Evolution, Anatomy (Princeton Univ. Press, 2013).
Dalla Vecchia, F. M. in Anatomy, Phylogeny and Palaeobiology of Early Archosaurs and their Kin (eds Nesbitt, S. J. et al) 119–155 (Geological Society London, 2013).
Britt, B. B. et al. Caelestiventus hanseni gen. et sp. nov. extends the desert-dwelling pterosaur record back 65 million years. Nat. Ecol. Evol. 2, 1386–1392 (2018).
Butler, R. J., Brusatte, S. L., Andres, B. & Benson, R. B. How do geological sampling biases affect studies of morphological evolution in deep time? A case study of pterosaur (Reptilia: Archosauria) disparity. Evolution 66, 147–162 (2012).
Padian, K. Osteology and functional morphology of Dimorphodon macronyx (Buckland) (Pterosauria: Rhamphorhynchoidea) based on new material in the Yale Peabody Museum. Postilla 189, 1–44 (1983).
Benton, M. J. Classification and phylogeny of the diapsid reptiles. Zool. J. Linn. Soc. 84, 97–164 (1985).
Peters, D. A reexamination of four prolacertiforms with implications for pterosaur phylogenesis. Riv. Ital. Paleontol. Stratigr. 106, 293–336 (2000).
Bennett, S. C. Reassessment of the Triassic archosauriform Scleromochlus taylori: neither runner nor biped, but hopper. PeerJ 8, e8418 (2020).
Renesto, S. & Binelli, G. Vallesaurus cenensis Wild 1991, a drepanosaurid (Reptilia, Diapsida) from the Late Triassic of northern Italy. Riv. Ital. Paleontol. Stratigr. 112, 77–94 (2006).
Langer, M. C., Nesbitt, S. J., Bittencourt, J. S. & Irmis, R. B. in Anatomy, Phylogeny and Palaeobiology of Early Archosaurs and their Kin (eds Nesbitt, S. J. et al.) 156–186 (Geological Society London, 2013).
Cabreira, S. F. et al. A unique Late Triassic dinosauromorph assemblage reveals dinosaur ancestral anatomy and diet. Curr. Biol. 26, 3090–3095 (2016).
Kammerer, C. F., Nesbitt, S. J., Flynn, J. J., Ranivoharimanana, L. & Wyss, A. R. A tiny ornithodiran archosaur from the Triassic of Madagascar and the role of miniaturization in dinosaur and pterosaur ancestry. Proc. Natl Acad. Sci. USA 117, 17932–17936 (2020).
Dalla Vecchia, F. M. Gli Pterosauri Triassici (Edizioni del Museo Friulano di Storia Naturale, 2014).
Dalla Vecchia, F. M. Seazzadactylus venieri gen. et sp. nov., a new pterosaur (Diapsida: Pterosauria) from the Upper Triassic (Norian) of northeastern Italy. PeerJ 7, e7363 (2019).
Codorniú, L., Paulina-Carabajal, A., Pol, D., Unwin, D. & Rauhut, O. W. M. A Jurassic pterosaur from Patagonia and the origin of the pterodactyloid neurocranium. PeerJ 4, e2311 (2016).
Goloboff, P. A. & Catalano, S. A. TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics 32, 221–238 (2016).
Spoor, F. & Zonneveld, F. Comparative review of the human bony labyrinth. Am. J. Phys. Anthropol. 107, 211–251 (1998).
Winship, I. R. & Wylie, D. R. Zonal organization of the vestibulocerebellum in pigeons (Columba livia): I. Climbing fiber input to the flocculus. J. Comp. Neurol. 456, 127–139 (2003).
Birn-Jeffery, A. V., Miller, C. E., Naish, D., Rayfield, E. J. & Hone, D. W. Pedal claw curvature in birds, lizards and mesozoic dinosaurs—complicated categories and compensating for mass-specific and phylogenetic control. PLoS ONE 7, e50555 (2012).
Kubo, T. & Kubo, M. O. Associated evolution of bipedality and cursoriality among Triassic archosaurs: a phylogenetically controlled evaluation. Paleobiology 38, 474–485 (2012).
Andres, B. & Padian, K. in Phylonyms: A Companion to the PhyloCode (eds de Queiroz, K. et al.) 1201–1204 (CRC, 2020).
Langer, M. C., Ezcurra, M. D., Bittencourt, J. S. & Novas, F. E. The origin and early evolution of dinosaurs. Biol. Rev. Camb. Philos. Soc. 85, 55–110 (2010).
Nesbitt, S. J. et al. Ecologically distinct dinosaurian sister group shows early diversification of Ornithodira. Nature 464, 95–98 (2010).
Langer, M. C., Novas, F. E., Bittencourt, J., Ezcurra, M. D. & Gauthier, J. A. in Phylonyms: A Companion to the PhyloCode (eds de Queiroz, K. et al.) 1209–1217 (CRC, 2020).
Clarke, J. A. et al. in Phylonyms: A Companion to the PhyloCode (eds de Queiroz, K. et al.) 1247–1253 (CRC, 2020).
Fedorov, A. et al. 3D Slicer as an image computing platform for the quantitative imaging network. Magn. Reson. Imaging 30, 1323–1341 (2012).
David, R. et al. Motion from the past. A new method to infer vestibular capacities of extinct species. C. R. Palevol 9, 397–410 (2010).
Evers, S. W. et al. Neurovascular anatomy of the protostegid turtle Rhinochelys pulchriceps and comparisons of membranous and endosseous labyrinth shape in an extant turtle. Zool. J. Linn. Soc. 187, 800–828 (2019).
Neenan, J. M. et al. Evolution of the sauropterygian labyrinth with increasingly pelagic lifestyles. Curr. Biol. 27, 3852–3858 (2017).
Adams, D., Collyer, M. & Kaliontzopoulou, A. Geomorph: software for geometric morphometric analyses. R package version 3.2.1 https://cran.r-project.org/package=geomorph (2020).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).
Butler, R. J., Ezcurra, M. D., Liu, J., Sookias, R. B. & Sullivan, C. The anatomy and phylogenetic position of the erythrosuchid archosauriform Guchengosuchus shiguaiensis from the earliest Middle Triassic of China. PeerJ 7, e6435 (2019).
Ezcurra, M. D. et al. Deep faunistic turnovers preceded the rise of dinosaurs in southwestern Pangaea. Nat. Ecol. Evol. 1, 1477–1483 (2017).
Ezcurra, M. D. & Butler, R. J. The rise of the ruling reptiles and ecosystem recovery from the Permo-Triassic mass extinction. Proc. R. Soc. Lond. B 285, 20180361 (2018).
Ronquist, F., van der Mark, P. & Huelsenbeck, J. P. in The Phylogenetic Handbook: a Practical Approach to Phylogenetic Analysis and Hypothesis Testing (eds Lemey, P. et al) 210–266 (Cambridge Univ. Press, 2009).
Ezcurra, M. D., Scheyer, T. M. & Butler, R. J. The origin and early evolution of Sauria: reassessing the Permian saurian fossil record and the timing of the crocodile-lizard divergence. PLoS ONE 9, e89165 (2014).
Benton, M. J. et al. Constraints on the timescale of animal evolutionary history. Palaeontol. Electronica 18, 1–106 (2015).
Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901–904 (2018).
We thank C. Alsina and F. De Cianni (MACN) for repreparation, M. B. Epele and M. Cipollone for μCT scanning and F. Tricárico for scanning-electron microscopy microphotographs of PVL 4625; M. Colbert for μCT scanning TMM 31100-1334; D. Cavallari for μCT scanning ULBRA-PVT059; V. Radermacher and J. Choiniere for providing access to the μCT scan of a Heterodontosaurus specimen scanned at ESRF, and ESI and SAHRA for permits for that work; A. Paulina-Carabajal for allowing access to the μCT scan of Allkaruen; S. Chapman, H. Furrer, Z. Gasparini, M. Moser, G. Muscio, P. Ortíz, A. Paganoni, J. Powell, O. Rauhut, E. Ruigómez, R. Stecher and A. Tintori for access to specimens; J. Gauthier for discussion and suggestions about phylogenetic nomenclature; D. Boyer for assisting us during the uploading of the three-dimensional models of specimens to MorphoSource; S. Hartman allowed the use and modification of the lagerpetid skeletal reconstruction; and S. Brusatte and N. Fraser for comments that improved the overall quality of the manuscript. R. Nogueira digitally assembled and reconstructed the lagerpetid skull and created the life reconstruction. University of Antananarivo, Madagascar, allowed access to three-dimensional data and first-hand study of Kongonaphon. This study was supported by the Sepkoski Grant of the Paleontological Society (to M.D.E.), Agencia Nacional de Promoción Científica y Técnica (PICT 2018-01186; to M.D.E.), The Coleman and Susan Burke Foundation (to F.E.N.), Financiadora de Estudos e Projetos, Brazilian Federal Government (project CT-INFRA 01/2013), and São Paulo Research Foundation (FAPESP 2014/03825-3 to M.C.L. and 2018/18145-9 to M.B.).
The authors declare no competing interests.
Peer review information Nature thanks Stephen Brusatte, Nicholas Fraser and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
Extended Data Fig. 1 Life reconstruction and three-dimensional reconstruction of the skull of the lagerpetid I. polesinensis (ULBRA-PVT059, holotype) with additions of cranial bones of other lagerpetids.
a–i, Images are shown in right lateral (a, f, i), anterior (b, g), posterior (c), ventral (d), dorsal (e) and anterodorsolateral (h) views. f–h, Images show transparent inferred bones to show the braincase and skull roof bones through them. Bones of I. polesinensis are indicated in yellow and those of K. kely (UA 10618, holotype), D. gregorii (TMM 31100-1334, referred specimen) and L. chanarensis (PVL 4625, referred specimen) in red, and inferred bones in light blue. Arrows indicate the anterior direction. Complete scale bar, 5 cm. Life and skull reconstruction by R. Nogueira.
Extended Data Fig. 2 Lagerpetid L. chanarensis (PVL 4625, referred specimen), three-dimensional reconstruction from the μCT scan of articulated dentaries and magnifications of dentary tooth crowns.
a–h, Images are shown in left lateral (a), right dorsolateral (b), ventral (c), dorsal (d), anterodorsal (e), apicolingual (f) and lingual (g, h) views. Horizontal arrows indicate the anterior direction (a–d, f–h) and diagonal arrows point to accessory cusps (f, h). a–e, Three-dimensional models based on μCT scan data. f, Scanning electron microscopy photograph. g, h, Binocular microscopy photographs. Scale bars, 5 mm (a–e), 0.2 mm (f) and 0.5 mm (g, h).
a, Partial skull roof and braincase of the lagerpetid D. gregorii (TMM 31100-1334) in left lateral view. b, Right hemipelvis of the lagerpetid L. chanarensis (PVL 4619) in lateral view. c, Left hemipelvis and articulated proximal end of femur of the pterosaur Dimorphodon macronyx (NHMUK PV OR 41212, reversed) in lateral view. d, Right femur of the pterosaur D. macronyx (YPM 9182) in anterolateral view. Arrows indicate the anterior direction. Scale bars, 3 mm (a) and 5 mm (b–d).
Extended Data Fig. 4 Phylogenetic relationships of pterosaurs and lagerpetids among pan-archosaurs using discrete characters.
Strict consensus of the 280 most-parsimonious trees (tree length = 5,002; consistency index = 0.21431; retention index = 0.65014). Absolute (left) and GC (group present/contradicted) (right) bootstrap frequencies are indicated above each branch and Bremer support values are shown below each branch. The position of Scleromochlus in the secondary analysis is indicated with a dotted line.
Strict reduced consensus of the same most-parsimonious trees of Extended Data Fig. 4 after a posteriori pruning of Spondylosoma, Dongusuchus and PVSJ 883 to avoid reduction of Bremer support values because of missing data in these taxa. Bremer support values are indicated on each branch.
Extended Data Fig. 6 Majority rule tree recovered from the unconstrained Bayesian phylogenetic analysis.
Branch colours indicate character state transition rates (that is, the evolutionary rates), numbers at the nodes indicate posterior probabilities, the thin black horizontal line segments indicate the 95% probability distribution of node ages, and dotted vertical lines indicate the boundaries between the Carboniferous, Permian, Triassic and Jurassic geological periods. Thick black vertical bars indicate polytomies and, as a result, transition rates could not be calculated.
Extended Data Fig. 7 Majority rule tree recovered from the constrained Bayesian phylogenetic analysis.
The topology of this tree has been constrained a priori after selecting randomly one of the most-parsimonious trees recovered after forcing the position of lagerpetids as the earliest branching dinosauromorphs in the maximum parsimony analysis. Branch colours indicate character state transition rates, the black horizontal line segments indicate the 95% probability distribution of node ages and the dotted vertical lines indicate the boundaries between the Carboniferous, Permian, Triassic and Jurassic geological periods. Posterior probabilities at the nodes are not shown because the topology is fully constrained.
Extended Data Fig. 8 Phylogenetic relationships of pterosaurs and lagerpetids among pan-archosaurs using discrete characters and the three-dimensional morphogeometric configuration of the inner ear.
Strict consensus tree generated from the 256 most-parsimonious trees (tree length = 4,927.67960; consistency index = 0.77624; retention index = 0.85756).
Extended Data Fig. 9 Single most-parsimonious tree found when analysing only the three-dimensional morphogeometric configuration of the inner ear and three-dimensional examples of how distances and angles were measured in the three-dimensional endosseous labyrinth models.
a, Tree rooted with T. buettneri. b, Three-dimensional model of the left endosseous labyrinth of Plateosaurus sp. (HMN R1937) in dorsolateral view. c, Labyrinth with reference plane for sectioning indicated. d, Landmark scheme for semicircular canal length measurements. e, Landmark scheme for asc circumference and labyrinth height measurements. f, Landmark scheme for labyrinth width measurements in ventral view on the reference plane. g, Landmark constellation explanation. asc, anterior semicircular canal; cc, common crus; enla, endosseous labyrinth; lsc, lateral semicircular canal; psc, posterior semicircular canal; ve, vestibule.
Extended Data Fig. 10 Single most-parsimonious tree found when analysing only the three-dimensional morphogeometric configuration of the inner ear and alternative rooting, and morphospace plot of archosauromorph labyrinths.
a, Tree rooted with M. browni. b, Landmark constellation explanation. c, Principal component (PC) analyses (n = 22 species) with variation in PC1 plotted against PC2 (showing deformations along PC1–PC2), in which grey dots are non-pan-avian archosauromorphs, pink dots are non-pterosauromorph pan-avians, garnet dots are pterosaurs and orange dots are lagerpetids.
About this article
Cite this article
Ezcurra, M.D., Nesbitt, S.J., Bronzati, M. et al. Enigmatic dinosaur precursors bridge the gap to the origin of Pterosauria. Nature 588, 445–449 (2020). https://doi.org/10.1038/s41586-020-3011-4