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The earliest bird-line archosaurs and the assembly of the dinosaur body plan

Naturevolume 544, pages484–487 (2017)Cite this article

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Abstract

The relationship between dinosaurs and other reptiles is well established1,2,3,4, but the sequence of acquisition of dinosaurian features has been obscured by the scarcity of fossils with transitional morphologies. The closest extinct relatives of dinosaurs either have highly derived morphologies5,6,7 or are known from poorly preserved8,9 or incomplete material10,11. Here we describe one of the stratigraphically lowest and phylogenetically earliest members of the avian stem lineage (Avemetatarsalia),Teleocrater rhadinus gen. et sp. nov., from the Middle Triassic epoch. The anatomy ofT. rhadinus provides key information that unites several enigmatic taxa from across Pangaea into a previously unrecognized clade, Aphanosauria. This clade is the sister taxon of Ornithodira (pterosaurs and birds) and shortens the ghost lineage inferred at the base of Avemetatarsalia. We demonstrate that several anatomical features long thought to characterize Dinosauria and dinosauriforms evolved much earlier, soon after the bird–crocodylian split, and that the earliest avemetatarsalians retained the crocodylian-like ankle morphology and hindlimb proportions of stem archosaurs and early pseudosuchians. Early avemetatarsalians were substantially more species-rich, widely geographically distributed and morphologically diverse than previously recognized. Moreover, several early dinosauromorphs that were previously used as models to understand dinosaur origins may represent specialized forms rather than the ancestral avemetatarsalian morphology.

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Figure 1: Geographical and stratigraphical occurrence ofTeleocrater rhadinus gen. et sp. nov. from the Ruhuhu Basin, southern Tanzania, Africa.
Figure 2: Skeletal anatomy ofTeleocrater rhadinus gen. et sp. nov.
Figure 3: Early evolution of avemetatarsalians.

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Acknowledgements

We acknowledge A. Tibaijuka for help with fieldwork logistics in Tanzania. Supported by National Geographic Society Research & Exploration grant (9606-14, S.J.N.), National Science Foundation EAR-1337569 (C.A.S.) and EAR-1337291 (K.D.A., S.J.N.), a Marie Curie Career Integration Grant (630123, R.J.B.), a National Geographic Society Young Explorers grant (9467-14 M.D.E.), and the Russian Government Program of Competitive Growth of Kazan Federal University and RFBR 14-04-00185, 17-04-00410 (A.G.S.). We thank S. Chapman, A. C. Milner, M. Lowe and S. Bandyopadhyay for access to specimens, S. Werning, G. Lloyd, R. Close and K. Padian for discussions, and H. Taylor for photographs of the holotype.

Author information

Author notes

  1. Alan J. Charig: Deceased.

Authors and Affiliations

  1. Department of Geosciences, Virginia Tech, Blacksburg, 24061, Virginia, USA

    Sterling J. Nesbitt & Michelle R. Stocker

  2. School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, B15 2TT, Birmingham, UK

    Richard J. Butler & Martín D. Ezcurra

  3. CONICET—Sección Paleontología de Vertebrados, Museo Argentino de Ciencias Naturales, Buenos, Aires, Argentina

    Martín D. Ezcurra

  4. Department of Earth Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK

    Paul M. Barrett & Alan J. Charig

  5. Integrative Research Center, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, 60605, Illinois, USA

    Kenneth D. Angielczyk

  6. Evolutionary Studies Institute, University of the Witwatersrand, PO Wits 2050, Johannesburg, South Africa

    Roger M. H. Smith

  7. Iziko South African Museum, PO Box 61, Cape Town, South Africa

    Roger M. H. Smith

  8. Burke Museum and Department of Biology, University of Washington, Seattle, 98195, Washington, USA

    Christian A. Sidor

  9. Department of Organismal Biology, Uppsala University, Norbyvägen 18A, Uppsala, 752 36, Sweden

    Grzegorz Niedźwiedzki

  10. Borissiak Paleontological Institute, Russian Academy of Sciences, Profsoyuznaya 123, Moscow, 117997, Russia

    Andrey G. Sennikov

  11. Kazan Federal University, Kremlyovskaya ul. 18, Kazan, 420008, Russia

    Andrey G. Sennikov

Authors
  1. Sterling J. Nesbitt
  2. Richard J. Butler
  3. Martín D. Ezcurra
  4. Paul M. Barrett
  5. Michelle R. Stocker
  6. Kenneth D. Angielczyk
  7. Roger M. H. Smith
  8. Christian A. Sidor
  9. Grzegorz Niedźwiedzki
  10. Andrey G. Sennikov
  11. Alan J. Charig

Contributions

S.J.N., R.J.B., M.D.E. and P.M.B. designed the research project; C.A.S. and K.D.A. designed the field project; S.J.N., C.A.S., K.D.A., R.M.H.S. and M.R.S. conducted fieldwork; S.J.N., R.J.B., M.D.E., P.M.B., M.R.S. and A.J.C. described the material; S.J.N., M.D.E. and M.R.S. conducted the phylogenetic analyses; R.J.B. conducted disparity analyses; and S.J.N., R.J.B., M.D.E., P.M.B., M.R.S., K.D.A., R.M.H.S., C.A.S., G.N. and A.G.S. wrote the manuscript.

Corresponding author

Correspondence toSterling J. Nesbitt.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer InformationNature thanks K. Padian and H.-D. Sues for their contribution to the peer review of this work.

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 Figure 1 Skeletal anatomy of the aphanosaursDongusuchus efremovi,Yarasuchus deccanensis andSpondylosoma absconditum.

a,b,D. efremovi.c–t,Y. deccanensis.u–cc,S. absconditum.a,b, Left holotype femur ofD. efremovi (Borissiak Paleontological Institute of the Russian Academy of Sciences, Moscow, Russia (PIN) 952/15-1) in posteromedial (a) and anterolateral (b) views.c–e, Right partial femur ofY. deccanensis (Indian Statistical Institute, Kolkata, India (ISIR) unnumbered) in posterolateral (c), proximal (d) and anterolateral (e) views.f,g, Left tibia ofY. deccanensis (ISIR 334) in posterior (f) and distal (g) views.h,i, Left calcaneum ofY. deccanensis (ISIR unnumbered) in proximal (h) and lateral (i) views.j, Second sacral vertebra ofY. deccanensis (ISIR BIA 45/43) in ventral view.k, Right ischium ofY. deccanensis (ISIR 334) in ventrolateral view.l,m, Posterior cervical vertebrae ofY. deccanensis (ISIR BIA 45/43) in posterior (l) and right lateral (m) views.n,o, Right humerus ofY. deccanensis (ISIR 334 53) in anterior (n) and posterior (o) views.p, Right ulna ofY. deccanensis (ISIR 334) in anterior view.q, Trunk vertebra ofY. deccanensis (ISIR BIA 45/43) in left lateral view.r,s, Posterior cervical vertebrae ofY. deccanensis (ISIR BIA 45/43) in posterior (r) and right lateral (s) views.t, Triple-headed rib ofY. deccanensis (ISIR BIA 45) in anterior view.u,x, Original condition (u) of a cervical vertebra (from Huene 1942) ofS. absconditum (Paläontologische Sammlung der Universität Tübingen, Tübingen, Germany (GPIT) 479/30) compared to that of the current condition (x).v,w,y, Original condition of a more posterior cervical vertebra ofS. absconditum (from Huene 1942) in left lateral (v) and anterior (w) views compared to that of the current condition of the same vertebra in left lateral (y) view.z, Trunk vertebra ofS. absconditum in posterior view.aa, Second sacral vertebra ofS. absconditum in dorsal view.bb,cc, Right scapula ofS. absconditum in lateral (bb) and posterior (cc) views. a., articulates with; ain, anteriorly inclined anterior margin of the neural spine; as, astragalus; ct, calcaneal tuber; dp, deltopectoral crest; fi, fibula; hy, hyposphene; mic, M. iliotrochantericus caudalis scar; mie, M. iliofemoralis externus scar; pr, posterolateral; r, ridge. Scale bars, 1 cm. Outline of Africa and Tanzania obtained from Google Maps.

Extended Data Figure 2 Histological sections of the limb bones ofT. rhadinus gen. et sp. nov.

a, Right fibula (NMT RB 488) in lateral (left) and medial (right) views.b, Photo of the histological section of the fibula (NMT RB 488) in regular transmitted light (bright field) (1 plane polarizer).c, Photo of the same section as inb using a full wave retarder (l = 530 nm).d, Left humerus (NMT RB476) in posterior (left) and anterior (right) views.e, Photo of a partial histological section of the humerus (NMT RB476) in regular transmitted light (bright field) (1 plane polarizer).f, Photo of the same section as ine using a full wave retarder (l = 530 nm). Scale bars, 1 mm. Arrows ina,d indicate where each element was sampled. Arrows inb,c,e,f indicate growth marks in the outer cortex.

Extended Data Figure 3 The relationships ofT. rhadinus gen. et sp. nov. among archosauriforms from the Nesbitt dataset.

The dataset used has been described in ref.19. Strict consensus of 36 most parsimonious trees (tree length = 1,374; consistency index = 0.3559; retention index = 0.7807). Bremer support values (first), absolute (second), and GC (third) bootstrap frequencies presented at each branch.

Extended Data Figure 4 The relationships ofTeleocrater rhadinus gen. et sp. nov. among archosauriforms from the Ezcurra dataset.

The dataset used has been described in ref.20. Strict consensus of four most parsimonious trees (tree length = 2,684; consistency index = 0.2955; retention index = 0.6284). Bremer support values (first), absolute (second), and GC (third) bootstrap frequencies presented at each branch.

Extended Data Figure 5 Phylogeny of early Avemetatarsalia illustrating the character distributions of the components of the crocodile-normal ankle configuration and showing that this ankle type was plesiomorphic for Archosauria, Avemetatarsalia, and possible less inclusive clades within Avemetatarsalia (for example, Dinosauriformes).

a, Left calcaneum of the pseudosuchianNundasuchus songeaensis (NMT RB48).b, Right calcaneum of the aphanosaurT. rhadinus gen. et sp. nov. (reversed) (NMT RB490).c, Left calcaneum of the dinosauriform silesauridA. kongwe (NMT RB159). Proximal view (left), distal view (middle) and lateral view (right). Scale bars, 1 cm. red, character state present; blue, character state absent; red and blue, basal condition could be either; ?, unknown condition. SeeFig. 3 for silhouette sources. 4th, fourth tarsal; a., articulates with; as, astragalus; ct, calcaneal tuber; fi, fibula.

Extended Data Figure 7 The relationships ofS. taylori among archosauriforms from the Nesbitt dataset.

The dataset used has been described in ref.19. Strict consensus of 792 most parsimonious trees (tree length = 1,378; consistency index = 0.3549; retention index = 0.7803) (seeSupplementary Information). Bremer support values (first), absolute (second), and GC (third) bootstrap frequencies presented at each branch.

Extended Data Figure 8 The relationships ofS. taylori among archosauriforms from the Ezcurra dataset.

The dataset used has been described in ref.20. Strict consensus of four most parsimonious trees (tree length = 2,693; consistency index = 0.2945; retention index = 0.6280) (seeSupplementary Information). Bremer support values (first), absolute (second), and GC (third) bootstrap frequencies presented at each branch.

Extended Data Figure 9 Disparity estimates for major archosaur groups and time intervals (weighted mean pairwise dissimilarity (WMPD)).

Ani, Anisian; C, Changhsingian; Car, Carnian; H, Hettangian; I, Induan; J, Jurassic; Lad, Ladinian; Lo, Lopingian; Nor, Norian; Olen, Olenekian; P, Permian; Rha, Rhaetian.

Extended Data Figure 10 New character illustrations for the phylogenetic analysis.

SeeSupplementary Information.a–c, Archosaurian iliac comparisons for character 414 in the modified dataset of ref.19.a, Left ilium ofTeleocrater rhadinus (NHMUK PV R6795) in lateral view.b, Right ilium ofAsilisaurus kongwe (NMT RB159) in lateral view.c, Left ilium ofBatrachotomus kupferzellensis (Staatliches Museum für Naturkunde Stuttgart (SMNS) 80273) in lateral view.d–g, Avemetatarsalian fibula comparisons for character 415 in the modified dataset of ref.19.d,e, Left fibula ofT. rhadinus (NHMUK PV R6795) in lateral (d) and posterior (e) views.f,g, Left fibula ofA. kongwe (NMT RB159) in lateral (f) and posterior (g) views. Arrows highlight the posterior ridge, character 415 state 1.h,i, Archosauriform femoral comparisons for character 417 in the modified dataset of ref.19.h, Right femur ofErythrosuchus africanus (NHMUK PV R3592) in ventral view.i, Right femur ofT. rhadinus (NHMUK PV R6795) in posteromedial view. White dotted regions highlight character 417, state 1.j–m, Avemetatarsalian second primordial sacral comparisons for character 416 in the modified dataset of ref.19.j,k, Second primordial sacral vertebra ofT. rhadinus (NMT RB519) in ventral (j) and posterior (k) views.l,m, The second primordial sacral vertebra ofA. kongwe (NMT RB159) in ventral (l) and dorsal (m) views. Arrows highlight the posterior process of the sacral rib, character 416, state 1. Scale bars,. 1 cm (a–g,i–m) and 5 cm (h).

Supplementary information

Supplementary Information

This file contains Supplementary Text, Supplementary Tables 1-8 and Supplementary References. (PDF 1167 kb)

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Nesbitt, S., Butler, R., Ezcurra, M.et al. The earliest bird-line archosaurs and the assembly of the dinosaur body plan.Nature544, 484–487 (2017). https://doi.org/10.1038/nature22037

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Editorial Summary

Earliest avian archosaur

The early history of the bird-line archosaurs, a group including dinosaurs, birds and pterosaurs, but excluding crocodilians, is not well defined. This is due in part to a fragmentary fossil record, but the distinctive morphology of pterosaurs has also obscured their ancestry. Sterling Nesbitt and colleagues describe a new species,Teleocraterrhadinus, from the Middle Triassic of Tanzania, that represents the most primitive known member of the bird-line archosaurs.Teleocrater provides the best guide so far to the ancestral bird-line condition. It was a lightly built, quadrupedal carnivore, so more like a crocodile than the small bipeds often depicted at this point in archosaur evolution. These are long-awaited findings onTeleocrater, which was undergoing study by the late Alan Charig of the Natural History Museum in London, and remained unpublished on his death in 1997.

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