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Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy

Nature volume 607, pages 726–731 (2022)Cite this article

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An Author Correction to this article was published on 09 January 2023

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Abstract

Endothermy underpins the ecological dominance of mammals and birds in diverse environmental settings1,2. However, it is unclear when this crucial feature emerged during mammalian evolutionary history, as most of the fossil evidence is ambiguous3,4,5,6,7,8,9,10,11,12,13,14,15,16,17. Here we show that this key evolutionary transition can be investigated using the morphology of the endolymph-filled semicircular ducts of the inner ear, which monitor head rotations and are essential for motor coordination, navigation and spatial awareness18,19,20,21,22. Increased body temperatures during the ectotherm–endotherm transition of mammal ancestors would decrease endolymph viscosity, negatively affecting semicircular duct biomechanics23,24, while simultaneously increasing behavioural activity25,26 probably required improved performance27. Morphological changes to the membranous ducts and enclosing bony canals would have been necessary to maintain optimal functionality during this transition. To track these morphofunctional changes in 56 extinct synapsid species, we developed the thermo-motility index, a proxy based on bony canal morphology. The results suggest that endothermy evolved abruptly during the Late Triassic period in Mammaliamorpha, correlated with a sharp increase in body temperature (5–9 °C) and an expansion of aerobic and anaerobic capacities. Contrary to previous suggestions3,4,5,6,7,8,9,10,11,12,13,14, all stem mammaliamorphs were most probably ectotherms. Endothermy, as a crucial physiological characteristic, joins other distinctive mammalian features that arose during this period of climatic instability28.

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Fig. 1: Three-dimensional visualizations of bony and membranous labyrinths.
Fig. 2: Relationships between the TMI and body temperature.
Fig. 3: Phylogenetic distribution of the TMI in tetrapods.
Fig. 4: Temporal distribution of the TMI in synapsids.

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Data availability

The raw datasets used in this study are available in the Supplementary Dataset. Links for CT scan datasets and bony labyrinth 3D meshes obtained from https://www.morphosource.org/ can be found in Supplementary Data 3. Some bird skull measurements and fish lengths were obtained from https://skullsite.com/ and fishbase.org, respectively (Supplementary Data 2). Time calibrations between most extant species were obtained from timetree.org. Body mass and Tb of some extant species were obtained from https://eol.org/traitbank (Supplementary Data 2). Source data are provided with this paper.

Code availability

The R scripts used in this study are available in the Supplementary Dataset.

Change history

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Acknowledgements

Funding for this project was provided by the Fundação para a Ciência e a Tecnologia postdoctoral fellowship SFRH/BPD/96205/2013, FCT–AGA KHAN Development Network grant number 333206718, National Geographic Society grant number CP-109R-17, the Field Museum, NSF EAR-1337291, the Max Planck Society and the Calleva Foundation. We acknowledge intellectual contributions from discussions with R. Rabbitt. We thank J. White, S. Walsh, P. Campbell, S. Pierce, C. Capobianco, S. Chapman, J. D. Cundiff, A. Wynn, P. Gill, E. Rayfield, J. Hopson, R. Asher, A. Neander, W. Simpson, A. Stroup, A. Resetar, J. Mata, J.-J. Hublin, D. Plotzki, H. Temming, W. van Gestel, J. Jansen, R. Allain, D. Silvestro, F. Condamine, C. Scotese, R. Mundry, S. W. Evers, M. J. Mason, P.-O. Antoine, S. Hellert, C. Schultz, M. B. Soares and A. Schmitt. We also thank the Institute of Veterinary Pathology and the Veterinary Clinic for Birds and Reptiles at Leipzig University, the Leibniz Institute for Zoo and Wildlife Research and the German Primate Center at Göttingen. We acknowledge the MRI platform member of the national infrastructure France-BioImaging supported by the French National Research Agency (ANR-10-INBS-04, «Investments for the future»), the labex CEMEB (ANR-10-LABX-0004) and NUMEV (ANR-10-LABX-0020). We acknowledge the European Synchrotron Radiation Facility for provision of synchrotron radiation facilities and we would like to thank V. Fernandez and P. Tafforeau for assistance in using beamline BM05 and ID17. IPFN activities received financial support from through projects UIDB/50010/2020 and UIDP/50010/2020. Some silhouettes were obtained from Phylopic.org.

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Author notes

  1. These authors contributed equally: Ricardo Araújo, Romain David

Authors and Affiliations

  1. Instituto de Plasmas e Fusão Nuclear, Instituto Superior Técnico, Universidade de Lisboa, Lisboa, Portugal

    Ricardo Araújo & Rui M. S. Martins

  2. Institut des Sciences de L’Évolution de Montpellier, Université de Montpellier, Montpellier, France

    Ricardo Araújo & Maëva Orliac

  3. Natural History Museum, London, UK

    Romain David, Paul M. Barrett & Fred Spoor

  4. Max Plank Institute for Evolutionary Anthropology, Leipzig, Germany

    Romain David, Alexander Stoessel & Fred Spoor

  5. Evolutionary Studies Institute, University of Witwatersrand, Johannesburg, South Africa

    Julien Benoit

  6. Department of Paleobiology, National Museum of Natural History, Washington DC, USA

    Jacqueline K. Lungmus

  7. Institute of Zoology and Evolutionary Research, Friedrich Schiller University Jena, Jena, Germany

    Alexander Stoessel

  8. Jackson School of Geosciences, University of Texas at Austin, Austin, TX, USA

    Jessica A. Maisano

  9. Department of Biology, San Diego State University, San Diego, CA, USA

    Eric Ekdale

  10. Department of Paleontology, San Diego Natural History Museum, San Diego, CA, USA

    Eric Ekdale

  11. Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA

    Zhe-Xi Luo

  12. Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Buenos Aires, Argentina

    Agustín G. Martinelli

  13. Division of Paleontology, American Museum of Natural History, New York, NY, USA

    Eva A. Hoffman

  14. Burke Museum and Department of Biology, University of Washington, Seattle, WA, USA

    Christian A. Sidor

  15. Department of Anthropology, University College London, London, UK

    Fred Spoor

  16. Neguanee Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA

    Kenneth D. Angielczyk

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  1. Ricardo Araújo
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  2. Romain David
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  3. Julien Benoit
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  16. Kenneth D. Angielczyk
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R.A., R.D. and K.D.A. designed the study and interpreted the data. R.A. and R.D. collected and analysed the data and wrote the manuscript, with specific input by F.S., K.D.A. and P.M.B. R.D. developed the thermo-motility index and wrote the code. K.D.A. and R.A. reviewed time divergence dates and last occurrence data. R.D., F.S. and A.S. collected specimens for membranous labyrinth analysis. All authors contributed raw and/or processed data, discussed the results, and commented on the draft manuscript.

Corresponding authors

Correspondence to Ricardo Araújo, Romain David or Kenneth D. Angielczyk.

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Competing interests

The authors declare no competing interests.

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Nature thanks Michael Benton and the other, anonymous, reviewers for their contribution to the peer review of this work. Peer review reports are available.

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Extended data figures and tables

Extended Data Fig. 1 Selected computed-tomography sections of inner ears of non-mammalian synapsids.

a-e, Anterior (ASC), posterior (PSC), and lateral (LSC) semicircular canals, vestibule (Ve), and crus communis (CC). Scale bar is 5 mm. a, horizontal section of the dicynodont Kawingasaurus (GPIT/RE/9272). b, coronal section of the dicynodont Aulacephalodon (NHCC LB335). c, horizontal section of the probainognathian Chiniquodon (MCZ 3778). d, coronal section of the mammaliamorph Pseudotherium (PVSJ 882). e, horizontal section of the therocephalian Mupashi (NHCC LB44).

Extended Data Fig. 2 Examples of measurements used in this study.

a-i, Views of the bony labyrinth (grey) and the membranous semicircular duct system (red) of an alpaca (a-c, CEB 130038), a domestic turkey (d-f, CEB 130069), and a false gharial (g-i, CEB140070), in the plane of the anterior (a, d, g), posterior (b, e, h), and lateral (c, f, i) semicircular canals. DM a, DM p, and DM l, major axes of the anterior, posterior, and lateral canal tori; Dm a, Dm p, and Dm l, minor axes of the anterior, posterior, and lateral canal tori; dS a, dS p, and dS l, cross-sectional thicknesses of the slender portion of the anterior, posterior, and lateral canals; LS a, LS p, and LS l, lengths of the slender portion of the anterior, posterior and lateral canals; Sa, Sp, and Sl, slender portions of the anterior, posterior, and lateral semicircular ducts; Aa, Ap, and Al, anterior, posterior, and lateral ampullae; Ua, anterior utriculus; CC, common crus; Ve, vestibule.

Extended Data Fig. 3 Distribution of morphological parameters measured on the anterior semicircular canals of tetrapods.

a-d, Boxplots of the radius of curvature relative to body mass (a), average cross-sectional thickness (b), and length (c) of the slender portion relative to the radius of curvature, and eccentricity of the semicircular canal tori (d). Arrows represent the direction of adaptations theoretically expected for endotherms. Boxplot centre, median; box boundaries, first and third quartiles; whiskers, 1.5 × IQR from boundaries. b, The outlier Caecilia has been omitted to standardize the plot area.

Extended Data Fig. 4 Phylogenetic distribution of uncontrolled parameters of the TMI.

a, Optimization of the residual variation of bony/membranous correlations on a time calibrated tree of extant tetrapods. Branch colours reflect the value of the residual variation according to the colour scale. b, Scatterplot of endolymph viscosity against Tb showing all data available (see Methods). Mammals are in blue, euteleosteans in green and birds in red. Dashed curves represent endolymph physicochemical properties that are water-like (large dashes), near water-like (medium dashes) or relatively viscous (small dashes). Animal silhouettes were either created by Ricardo Araújo (guinea pig, whiting, haddock, bald notothen) or are available at phylopic (http://phylopic.org/) under Public Domain license.

Source data

Extended Data Fig. 5 Probability distributions of body temperatures of fossil synapsids predicted from the TMI.

a-c, Note the elevated Tb of non-mammalian mammaliamorphs (NMM) and relatively low Tb of non-mammaliamorph probainognathians (NMP, b-c). Overlaps between distributions should be interpreted carefully because predicted temperatures are phylogenetically-dependent (see Table 1). Vertical dashed line represents the lowest Tb observed in extant endotherms (31 °C). Predicted Tb for endotherm and ectotherm (a), phylogenetic clusters best summarizing the data (b), and major groups (c) of fossil synapsids. c, Note that predicted Tb of non-mammaliamorph synapsids conform to a stochastic process.

Extended Data Fig. 6 Phylogenetic distribution of the TMI in fossil tetrapods.

Optimization of the TMI on a time-calibrated tree of major tetrapod clades and all of the extinct tetrapods analysed in this study. Branch colours reflect the likelihood of being endothermic according to the probability colour scale.

Extended Data Fig. 7 Relationship between thermo-motility indices of the lateral and anterior canals.

The solid line represents the PGLS regression for synapsids. The lateral canal best reflects behavioural agility and its TMI, calculated from the saturating velocity, is the least related to Tb (Supplementary Note 2). Note that non-mammalian synapsids mostly plot above extant ectotherms, suggesting increased locomotor activity for similar Tb. Additionally, while non-mammalian mammaliamorphs plot with endotherms for the anterior canal TMI (the main TMI used in this study), they are intermediate between endotherms and ectotherms for the lateral canal TMI, suggesting their locomotor activity was intermediate between basal synapsids and mammals. Animal silhouettes were either created by Ricardo Araújo (Oligokyphus, Cynognathia) or are available at phylopic (http://phylopic.org/) under Public Domain license.

Source data

Extended Data Table 1 Probabilities of endothermy for extinct synapsids
Full size table
Extended Data Table 2 Probabilities of endothermy for synapsid nodes
Full size table
Extended Data Table 3 Probabilities of endothermy for groups of non-mammalian synapsids
Full size table

Supplementary information

Supplementary Information

Supplementary Methods, including: sampling rationale; biomechanics of the thermo-motility index; discussion on the endolymph viscosity in vertebrates and a step-by-step summary of the analyses. Supplementary Notes 1–3, including: definitions; description of the statistical analyses; Dimetrodon photogrammetry and divergence times and last occurrence datum.

Reporting Summary

Supplementary Data 1

Data on stride frequency, maximum aerobic and anaerobic speeds with body temperature and body mass for a vertebrate sample.

Supplementary Data 2

Measurements; body temperature; body size variables; thermo-motility indices; details on PLS regressions.

Supplementary Data 3

Scan data and specimen provenience.

Supplementary Data 4

Data on the age, palaeolatitude and palaeoclimate for sites of non-mammaliamorph synapsids; with predicted body temperature and interpretations of thermoregulatory strategies; data on climate of today’s locations.

Supplementary Data 5

Reproducibility and repeatability tests.

Supplementary Data 6

Phylogenetic tree of all specimens used in the study.

Supplementary Dataset

R custom code and associated datasets.

Peer Review File

Source data

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Araújo, R., David, R., Benoit, J. et al. Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy. Nature 607, 726–731 (2022). https://doi.org/10.1038/s41586-022-04963-z

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