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The origin of squamates revealed by a Middle Triassic lizard from the Italian Alps

Naturevolume 557pages706709 (2018) | Download Citation

Abstract

Modern squamates (lizards, snakes and amphisbaenians) are the world’s most diverse group of tetrapods along with birds1 and have a long evolutionary history, with the oldest known fossils dating from the Middle Jurassic period—168 million years ago2,3,4. The evolutionary origin of squamates is contentious because of several issues: (1) a fossil gap of approximately 70 million years exists between the oldest known fossils and their estimated origin5,6,7; (2) limited sampling of squamates in reptile phylogenies; and (3) conflicts between morphological and molecular hypotheses regarding the origin of crown squamates6,8,9. Here we shed light on these problems by using high-resolution microfocus X-ray computed tomography data from the articulated fossil reptile Megachirella wachtleri (Middle Triassic period, Italian Alps10). We also present a phylogenetic dataset, combining fossils and extant taxa, and morphological and molecular data. We analysed this dataset under different optimality criteria to assess diapsid reptile relationships and the origins of squamates. Our results re-shape the diapsid phylogeny and present evidence that M. wachtleri is the oldest known stem squamate. Megachirella is 75 million years older than the previously known oldest squamate fossils, partially filling the fossil gap in the origin of lizards, and indicates a more gradual acquisition of squamatan features in diapsid evolution than previously thought. For the first time, to our knowledge, morphological and molecular data are in agreement regarding early squamate evolution, with geckoes—and not iguanians—as the earliest crown clade squamates. Divergence time estimates using relaxed combined morphological and molecular clocks show that lepidosaurs and most other diapsids originated before the Permian/Triassic extinction event, indicating that the Triassic was a period of radiation, not origin, for several diapsid lineages.

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Acknowledgements

We are grateful for funding from the Vanier Canada and the Izaak Walton Killam Memorial PhD scholarships to T.R.S.; Euregio Science Fund (call 2014, IPN16) to M.B.; Midwestern University Intramural Funds to R.L.N.; Natural Science and Engineering Research Council of Canada Discovery Grant to M.W.C. (23458); Alberta Ukrainian Centennial Scholarship to O.V.; and National Science Centre grant 2014/13/N/NZ8/02467 to M.T.; and E. Kustatscher for access to the holotype of M. wachtleri.

Reviewer information

Nature thanks M. Baron, J.-C. Rage and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Affiliations

  1. Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada

    • Tiago R. Simões
    • , Michael W. Caldwell
    •  & Oksana Vernygora
  2. Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta, Canada

    • Michael W. Caldwell
  3. Department of Palaeobiology and Evolution, Faculty of Biology, Biological and Chemical Research Centre, University of Warsaw, Warsaw, Poland

    • Mateusz Tałanda
  4. MUSE, Museo delle Scienze di Trento, Trento, Italy

    • Massimo Bernardi
  5. School of Earth Sciences, University of Bristol, Bristol, UK

    • Massimo Bernardi
  6. College of Science and Engineering, Flinders University, Adelaide, South Australia, Australia

    • Alessandro Palci
  7. Museo Storico della Fisica e Centro di Studi e Ricerche Enrico Fermi, Roma, Italy

    • Federico Bernardini
  8. The Abdus Salam International Centre for Theoretical Physics, Trieste, Italy

    • Federico Bernardini
  9. Elettra Sincrotrone Trieste S.C.p.A., Trieste, Italy

    • Lucia Mancini
  10. Department of Anatomy, Arizona College of Osteopathic Medicine, Midwestern University, Glendale, AZ, USA

    • Randall L. Nydam

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Contributions

T.R.S. conducted phylogenetic data collection and analyses; M.W.C. conceived the project; F.B., L.M., M.B., T.R.S. and A.P. conducted micro-CT scans and computed tomography segmentations; T.R.S. and O.V. performed molecular sequence alignment; T.R.S., M.B., M.T., A.P. and R.L.N. performed morphological description; all authors contributed to writing and discussions.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Tiago R. Simões.

Extended data figures and tables

  1. Extended Data Fig. 1 Cranial anatomy of M. wachtleri (PZO 628) based on personal examination and micro-CT scan data.

    a, Skull in dorsal view. b, Skull in posteroventral view. c, Skull in anteroventral view. d, Skull in right ventrolateral view. e, Skull in left dorsal lateral view. f, Line drawing of the skull in dorsal view. g, Reconstruction of the skull in dorsal view. h, Detailed view of right lateral side of the skull. i, Drawing of the view in h. San, surangular. Scale bars, 5 mm (ag).

  2. Extended Data Fig. 2 Cranial and postcranial anatomy of M. wachtleri (PZO 628) based on personal examination and micro-CT scan data.

    a, Cross-section of the skull at the level of the frontals in anterior view. b, Details of the anterior end of the left dentary in occlusal view. c, Left quadrate. d, Whole body of the holotype as preserved in the slab (dorsal view). e, Anterior cervical vertebrae in left lateral view. f, Longitudinal section of the anterior cervicals in ventral view. g, Last cervicals and anterior dorsals in dorsal view. h, Pectoral girdle in ventral view. i, Pectoral girdle in left ventrolateral view. j, Right humerus in ventral view. k, Right manus in dorsal view. l, Line drawing of right manus in dorsal view. Ax.R., axis rib; Ce.Pl., cervical, pleurocentrum; Co, cotyle; C.V.3, third cervical vertebra; dc2–5, distal carpals 2–5; DPC, deltopectoral crest; D.R., dorsal rib; D.T., dentary teeth; Epi.St., epiphysial suture; H.Epi., humeral epiphysis; i, intermedium; lc, lateral centrale; McI–V, metacarpals I–V; N.A., neural arch; Olf.Tr., olfactory tract; Po.Co., posterior cotyle; Qj.Fr., quadratojugal foramen; Qj.St., quadratojugal suture; r, radiale; Sbd.Sh., subdentary shelf; Sof.Pr., subolfactory processes; u, ulnare. Scale bars, 1 mm (a, b), 5 mm (c, eh, jl), 10 mm (d, i).

  3. Extended Data Fig. 3 Equal weights maximum parsimony analysis, morphological data only.

    Strict consensus of 621 most parsimonious trees (2,268 steps each). Numbers at nodes indicate Bremer indices.

  4. Extended Data Fig. 4 Implied weighting maximum parsimony analysis, morphological data only.

    Strict consensus of the five best feet trees (fit = 91.768892).

  5. Extended Data Fig. 5 Bayesian inference analysis, morphological data only.

    Bayesian majority-rule consensus tree. Numbers at nodes indicate posterior probabilities.

  6. Extended Data Fig. 6 Bayesian inference analysis, combined morphological and molecular data.

    Bayesian majority-rule consensus tree. Numbers at nodes indicate posterior probabilities.

  7. Extended Data Fig. 7 Relaxed-clock Bayesian inference analysis with total-evidence tip dating using the fossilized birth–death tree model, combined morphological and molecular data.

    Bayesian majority-rule consensus tree. Numbers at nodes indicate posterior probabilities.

  8. Extended Data Fig. 8 Relaxed-clock Bayesian inference analysis with total-evidence tip and node dating using the fossilized birth–death tree model, combined morphological and molecular data.

    Bayesian majority-rule consensus tree. Numbers at nodes indicate median estimates for the divergence times, and node bars indicate the 95% highest posterior density for divergence times.

  9. Extended Data Fig. 9 Taxon stability plotted against taxon completeness in the analysis combining both morphological and molecular data.

    a, Taxon stability in uncalibrated Bayesian inference analysis. b, Taxon stability in relaxed-clock Bayesian inference analysis with tip dating. Taxon stability increases directly proportional to taxon completeness. M. wachtleri (taxon 67, in red) has a stability slightly above average for uncalibrated Bayesian inference, and well above average for Bayesian inference with tip dating. All taxa are identified in Supplementary Table 3 (n = 129 taxa). Regression line in blue and 95% confidence interval in grey. Labels for extant taxa (~100% completeness) are omitted for simplicity.

Supplementary information

  1. Supplementary Information

    This file contains Supplementary Discussions on the morphology of M. wachtleri, Supplementary Methods including taxon sampling and character list and Supplementary Tables 1-3

  2. Reporting Summary

  3. Supplementary Data 1

    Morphological phylogenetic dataset

  4. Supplementary Data 2

    Molecular phylogenetic dataset

  5. Supplementary Data 3

    Combined phylogenetic dataset with Mr. Bayes commands used for uncalibrated Bayesian analysis.

  6. Supplementary Data 4

    Combined phylogenetic dataset with Mr. Bayes commands used for relaxed clock Bayesian analysis calibrated with tip dating.

  7. Supplementary Data 5

    Combined phylogenetic dataset with Mr. Bayes commands used for relaxed clock Bayesian analysis calibrated with tip and node dating.

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