Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy

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

Subjects

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

This article has been updated

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

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.

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

References

  1. Lovegrove, B. G. Fires of Life: Endothermy in Birds and Mammals (Yale Univ. Press, 2019).

  2. Benton, M. J. The origin of endothermy in synapsids and archosaurs and arms races in the Triassic. Gondwana Res. 100, 261–289 (2021).

    Article  ADS  Google Scholar 

  3. Kubo, T. & Benton, M. J. Tetrapod postural shift estimated from Permian and Triassic trackways. Palaeontology 52, 1029–1037 (2009).

    Article  Google Scholar 

  4. Huttenlocker, A. K. & Farmer, C. G. Bone microvasculature tracks red blood cell size diminution in Triassic mammal and dinosaur forerunners. Curr. Biol. 27, 48–54 (2017).

    Article  CAS  Google Scholar 

  5. Jones, K. E., Angielczyk, K. D. & Pierce, S. E. Stepwise shifts underlie evolutionary trends in morphological complexity of the mammalian vertebral column. Nature Commun. 10, 5071 (2019).

    Article  ADS  Google Scholar 

  6. Faure-Brac, M. G. & Cubo, J. Were the synapsids primitively endotherms? A palaeohistological approach using phylogenetic eigenvector maps. Phil. Trans. R. Soc. B 375, 20190138 (2020).

    Article  CAS  Google Scholar 

  7. Crompton, A. W. et al. Structure of the nasal region of non-mammalian cynodonts and mammaliaforms: speculations on the evolution of mammalian endothermy. J. Vertebr. Paleontol. 37, e1269116 (2017).

    Article  Google Scholar 

  8. Bajdek, P. et al. Microbiota and food residues including possible evidence of pre-mammalian hair in Upper Permian coprolites from Russia. Lethaia 49, 455–477 (2016).

    Article  Google Scholar 

  9. Farmer, C. G. Parental care, destabilizing selection, and the evolution of tetrapod endothermy. Physiology 35, 160–176 (2020).

    Article  CAS  Google Scholar 

  10. Rey, K. et al. Oxygen isotopes suggest elevated thermometabolism within multiple Permo–Triassic therapsid clades. eLife 6, e28589 (2017).

    Article  Google Scholar 

  11. Newham, E., Gill, P. G. & Corfe, I. J. New tools suggest a middle Jurassic origin for mammalian endothermy: advances in state‐of‐the‐art techniques uncover new insights on the evolutionary patterns of mammalian endothermy through time. BioEssays 44, 2100060 (2022).

    Article  Google Scholar 

  12. Angielczyk, K. D. & Schmitz, L. Nocturnality in synapsids predates the origin of mammals by over 100 million years. Proc. R. Soc. B 281, 20141642 (2014).

    Article  Google Scholar 

  13. Botha, J. & Huttenlocker, A. in Vertebrate Skeletal Histology and Paleohistology (eds. de Buffrénil, V. et al.) 550–563 (CRC Press, 2021).

  14. Grigg, G. et al. Whole‐body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians. Biol. Rev. 97, 766–801 (2022).

    Article  CAS  Google Scholar 

  15. Benoit, J. et al. The sixth sense in mammalian forerunners: variability of the parietal foramen and the evolution of the pineal eye in South African Permo–Triassic eutheriodont therapsids. Acta Palaeontol. Pol. 61, 777–789 (2016).

    Google Scholar 

  16. Benoit, J., Manger, P. R. & Rubidge, B. S. Palaeoneurological clues to the evolution of defining mammalian soft tissue traits. Sci. Rep. 6, 25604 (2016).

    Article  ADS  CAS  Google Scholar 

  17. Rowe, T. B., Macrini, T. E. & Luo, Z.-X. Fossil evidence on origin of the mammalian brain. Science 332, 955–957 (2011).

    Article  ADS  CAS  Google Scholar 

  18. Rabbitt, R. D., Damiano, E. R. & Grant, J. W. in The Vestibular System (eds. Highstein, S. M. et al.) 153–201 (Springer, 2004).

  19. David, R. et al. Assessing morphology and function of the semicircular duct system: introducing new in-situ visualization and software toolbox. Sci. Rep. 6, 32772 (2016).

    Article  ADS  CAS  Google Scholar 

  20. Highstein, S. M., Fay, R. R. & Popper, A. N. The Vestibular System (Springer, 2004).

  21. Angelaki, D. E. & Cullen, K. E. Vestibular system: the many facets of a multimodal sense. Annu. Rev. Neurosci. 31, 125–150 (2008).

    Article  CAS  Google Scholar 

  22. Fitzpatrick, R. C., Butler, J. E. & Day, B. L. Resolving head rotation for human bipedalism. Curr. Biol. 16, 1509–1514 (2006).

    Article  CAS  Google Scholar 

  23. Ten Kate, J. H. & Kuiper, J. W. The viscosity of the Pike’s endolymph. J. Exp. Biol. 53, 495–500 (1970).

    Article  Google Scholar 

  24. Oman, C. M. in The Vestibular System: Function and Morphology (ed. Gualtierotti, T.) 251–274 (Springer, 1981).

  25. Garland, T. & Albuquerque, R. L. Locomotion, energetics, performance, and behavior: a mammalian perspective on lizards, and vice versa. Integr. Comp. Biol. 57, 252–266 (2017).

    Article  Google Scholar 

  26. Hirt, M. R. et al. A general scaling law reveals why the largest animals are not the fastest. Nat. Ecol. Evol. 1, 1116–1122 (2017).

    Article  Google Scholar 

  27. Jones, G. M. & Spells, K. E. A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proc. R. Soc. Lond. B 157, 403–419 (1963).

    Article  ADS  CAS  Google Scholar 

  28. Scotese, C. R., Song, H., Mills, B. J. & van der Meer, D. G. Phanerozoic paleotemperatures: the earth’s changing climate during the last 540 million years. Earth Sci. Rev. 215, 103503 (2021).

    Article  CAS  Google Scholar 

  29. Storey, K. B. & Storey, J. M. Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Quart. Rev. Biol. 65, 145–174 (1990).

    Article  CAS  Google Scholar 

  30. Legendre, L. J. & Davesne, D. The evolution of mechanisms involved in vertebrate endothermy. Phil. Trans. R. Soc. B 375, 20190136 (2020).

    Article  CAS  Google Scholar 

  31. Woodley, R. & Buffenstein, R. Thermogenic changes with chronic cold exposure in the naked mole-rat (Heterocephalus glaber). Comp. Biochem. Phys. A 133, 827–834 (2002).

    Article  Google Scholar 

  32. Pianka, E. R. in Ecology and Natural History of Desert Lizards: Analyses of the Ecological Niche and Community Structure (ed Pianka, E. R.) 35–47 (Princetown Univ. Press, 1986).

  33. Grigg, G. C., Beard, L. A. & Augee, M. L. The evolution of endothermy and its diversity in mammals and birds. Physiol. Biochem. Zool. 77, 982–997 (2004).

    Article  Google Scholar 

  34. Bennett, A. F. & Ruben, J. A. Endothermy and activity in vertebrates. Science 206, 649–654 (1979).

    Article  ADS  CAS  Google Scholar 

  35. Spoor, F. The semicircular canal system and locomotor behaviour, with special reference to hominin evolution. Cour. Forschungsinst. Senckenberg 243, 93–104 (2003).

    Google Scholar 

  36. Kemp, A. D. & Christopher Kirk, E. Eye size and visual acuity influence vestibular anatomy in mammals. Anat. Rec. 297, 781–790 (2014).

    Article  Google Scholar 

  37. Money, K. E. et al. Physical properties of fluids and structures of vestibular apparatus of the pigeon. Am. J. Physiol. 220, 140–147 (1971).

    Article  CAS  Google Scholar 

  38. Rowe, T. Definition, diagnosis, and origin of Mammalia. J. Vertebr. Palaeontol. 8, 241–264 (1988).

    Article  Google Scholar 

  39. Nicol, S. C. Energy homeostasis in monotremes. Front. Neurosci. 11, 195 (2017).

    Article  Google Scholar 

  40. Spoor, F. & Thewissen, J. G. M. in Senses on the Threshold: Adaptations in Secondarily Aquatic Vertebrates (eds Thewissen, J. G. M. & Nummela, S.). 257–286 (Univ. California Press, 2008).

  41. Opiang, M. D. Home ranges, movement, and den use in long-beaked echidnas, Zaglossus bartoni, from Papua New Guinea. J. Mammal. 90, 340–346 (2009).

    Article  Google Scholar 

  42. Viglietti, P. A. et al. Evidence from South Africa for a protracted end-Permian extinction on land. Proc. Nat. Acad. Sci. USA 118, e2017045118 (2021).

    Article  CAS  Google Scholar 

  43. Jones, K. E. et al. Regionalization of the axial skeleton predates functional adaptation in the forerunners of mammals. Nature Ecol. Evol. 4, 470–478 (2020).

    Article  Google Scholar 

  44. Lautenschlager, S. et al. The role of miniaturization in the evolution of the mammalian jaw and middle ear. Nature 561, 533–537 (2018).

    Article  ADS  CAS  Google Scholar 

  45. Donnelly, H. T. Oxygen consumption, activity and body fat in normal and hairless mice. Lab. Animals 16, 167–171 (1982).

    Article  CAS  Google Scholar 

  46. Bal, N. C. & Periasamy, M. Uncoupling of sarcoendoplasmic reticulum calcium ATPase pump activity by sarcolipin as the basis for muscle non-shivering thermogenesis. Phil. Trans. R. Soc. B 375, 20190135 (2020).

    Article  CAS  Google Scholar 

  47. Rowland, L. A., Bal, N. C. & Periasamy, M. The role of skeletal‐muscle‐based thermogenic mechanisms in vertebrate endothermy. Biol. Rev. 90, 1279–1297 (2015).

    Article  Google Scholar 

  48. Benson, R. B., Butler, R., Close, R. A., Saupe, E. & Rabosky, D. L. Biodiversity across space and time in the fossil record. Curr. Biol. 31, R1225–R1236 (2021).

    Article  CAS  Google Scholar 

  49. Close, R. A. et al. Diversity dynamics of Phanerozoic terrestrial tetrapods at the local-community scale. Nat. Ecol. & Evol. 3, 590–597 (2019).

    Article  Google Scholar 

  50. Fernandez, V. et al. Synchrotron reveals Early Triassic odd couple: injured amphibian and aestivating therapsid share burrow. PLoS ONE 8, e64978 (2013).

    Article  ADS  CAS  Google Scholar 

  51. 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).

    Google Scholar 

  52. Mason, M. J. et al. The frog inner ear: picture perfect? J. Assoc. Res. Otolaryngol. 16, 171–188 (2015).

    Article  Google Scholar 

  53. Schulz-Mirbach, T. et al. A unique swim bladder-inner ear connection in a teleost fish revealed by a combined high-resolution microtomographic and three-dimensional histological study. BMC Biol. 11, 75 (2013).

    Article  Google Scholar 

  54. Schulz-Mirbach, T., Heß, M. & Metscher, B. D. Sensory epithelia of the fish inner ear in 3D: studied with high-resolution contrast enhanced microCT. Front. Zool. 10, 63 (2013).

    Article  Google Scholar 

  55. Schulz-Mirbach, T., Heß, M. & Plath, M. Inner ear morphology in the Atlantic molly Poecilia mexicana—first detailed microanatomical study of the inner ear of a cyprinodontiform species. PLoS ONE 6, e27734 (2011).

    Article  ADS  CAS  Google Scholar 

  56. Ghanem, T. A., Rabbitt, R. D. & Tresco, P. A. Three-dimensional reconstruction of the membranous vestibular labyrinth in the toadfish Opsanus tau. Hearing Res. 124, 27–43 (1998).

    Article  CAS  Google Scholar 

  57. Buran, B. N., Deng, X. & Popper, A. N. Structural variation in the inner ears of four deep‐sea elopomorph fishes. J. Morph. 265, 215–225 (2005).

    Article  Google Scholar 

  58. Deng, X., Wagner, H. J. & Popper, A. N. The inner ear and its coupling to the swim bladder in the deep-sea fish Antimora rostrata (Teleostei: Moridae). Deep Sea Res. 58, 27–37 (2011).

    Article  Google Scholar 

  59. Deng, X., Wagner, H. J. & Popper, A. N. Interspecific variations of inner ear structure in the deep‐sea fish family Melamphaidae. Anat. Rec. 296, 1064–1082 (2013).

    Article  Google Scholar 

  60. Evangelista, C. et al. A comparison of the external morphology of the membranous inner ear in elasmobranchs. J. Morphol. 271, 483–495 (2010).

    Google Scholar 

  61. Gauldie, R. W., Mulligan, K. & Thompson, R. K. The otoliths of a chimaera, the New Zealand elephant fish Callorhynchus milii. N. Zeal. J. Mar. Freshw. Res. 21, 275–280 (1987).

    Article  Google Scholar 

  62. Gray, A. A. The Labyrinth of Animals: Including Mammals, Birds, Reptiles and Amphibians, Vol. I (Churchill, 1907).

  63. Gray, A. A. The Labyrinth of Animals: Including Mammals, Birds, Reptiles and Amphibians, Vol. II (Churchill, 1908).

  64. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).

    Article  CAS  Google Scholar 

  65. XLSTAT statistical and data analysis solution (Addinsoft, 2021).

  66. R Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2017).

  67. Bjørn-Helge, M., Wehrens, R. & Liland, K. H. pls: partial least squares and principal component regression. R package version 2.7-3 (2020).

  68. Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis, Version 3.61 (2018).

  69. Kumar, S. et al. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819 (2017).

    Article  CAS  Google Scholar 

  70. Prum, R. O. et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015).

    Article  ADS  CAS  Google Scholar 

  71. Suh, A. et al. Ancient horizontal transfers of retrotransposons between birds and ancestors of human pathogenic nematodes. Nat. Commun. 7, 11396 (2016).

    Article  ADS  CAS  Google Scholar 

  72. Naylor, G. J. P. et al. in Biology of Sharks and Their Relatives 2 (eds. Carrier, J. C., Musick, J. A. & Heithaus, M. R.) 31–56 (2012).

  73. Bakke, I. & Steinar, J. Characterization of mitochondrial ribosomal RNA genes in gadiformes: sequence variations, secondary structural features, and phylogenetic implications. Mol. Phylogenetics Evol. 25, 87–100 (2002).

    Article  CAS  Google Scholar 

  74. Bakke, I. & Steinar, D. J. Molecular phylogenetics of Gadidae and related Gadiformes based on mitochondrial DNA sequences. Mar. Biotech. 7, 61–69 (2005).

    Article  CAS  Google Scholar 

  75. Parham, J. F. et al. Best practices for justifying fossil calibrations. Syst. Biol. 61, 346–359 (2012).

    Article  Google Scholar 

  76. Rüsch, A. & Thurm, U. Cupula displacement, hair bundle deflection, and physiological responses in the transparent semicircular canal of young eel. Pflügers Archiv. 413, 533–545 (1989).

    Article  Google Scholar 

  77. Steer, R. W. The Influence of Angular and Linear Acceleration and Thermal Stimulation on the Human Semicircular Canal. Sc.D. thesis, Massachusetts Institute of Technology (1967).

  78. Rauch, S. Biochemie das Hörorgans (Thieme Verlag, 1964).

  79. Ten Doesschate, G. De eigenschappen van de endolymph van Beenvissche. Sc. D. thesis, Utrecht University (1914).

  80. Money, K. E., Sokoloff, M. & Weaver, R. S. Specific gravity and viscosity of endolymph and perilymph. In NASA, Second Symposium on the Role of the Vestibular Organs 91–98 (NASA, 1966).

  81. Schnieder, E. A. & Schindler, K. in Biochemie des Hörorgans (ed Rauch, S.) 164–168 (Georg Thieme Verlag, 1964).

  82. Macdonald, J. A. & Wells, R. M. G. in Biology of Antarctic fish (eds di Prisco, G., Maresca, B. & Tota B.) 163–178. (Springer, 1991).

  83. Revell, L. J. phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

  84. Orme, D. et al. caper: comparative analyses of phylogenetics and evolution in R. R package version 1.0.1 (2018).

  85. Pennell, M. W. et al. geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30, 2216–2218 (2014).

    Article  CAS  Google Scholar 

  86. Schliep, K. P. phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).

    Article  CAS  Google Scholar 

  87. Papadakis, M. et al. Rfast: a collection of efficient and extremely fast R functions. R package version 2.0.1 (2020).

  88. Wilkinson, S. P. & Davy, S. K. phylogram: an R package for phylogenetic analysis with nested lists. J. Open Source Softw. 3, 790 (2018).

    Article  ADS  Google Scholar 

  89. Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).

    Article  CAS  Google Scholar 

  90. Ben-Shachar, M., Lüdecke, D. & Makowski, D. effectsize: estimation of effect size indices and standardized parameters. J. Open Source Softw. 5, 2815 (2020).

    Article  ADS  Google Scholar 

  91. Komsta, L. outliers: tests for outliers. R package version 0.14 (2011).

  92. Puttick M. et al. motmot: models of trait macroevolution on trees. R package version 2.1.3 (2019).

  93. Wickham H., François R., Henry L. & Müller K. dplyr: a grammar of data manipulation. R package version 0.7.6 (2018).

  94. Xiang, Y., Yakushin, S. B., Kunin, M., Raphan, T. & Cohen, B. Head stabilization by vestibulocollic reflexes during quadrupedal locomotion in monkey. J. Neurophysiol. 100, 763–780 (2008).

    Article  Google Scholar 

  95. Boucot A. J., Chen, X., Scotese, C. R. & Morley, R. J. in SEPM Concepts in Sedimentology and Paleontology, Vol. 11 (eds Nichols, G. J. & Ricketts, B.) 1–478 (SEPM, 2013).

  96. Rees, P. M. et al. Permian phytogeographic patterns and climate data/model comparisons. J. Geol. https://doi.org/10.1086/324203 (2002).

  97. Rey, K. et al. Global climate perturbations during the Permo–Triassic mass extinctions recorded by continental tetrapods from South Africa. Gondwana Res. 37, 384–396 (2016).

    Article  ADS  CAS  Google Scholar 

  98. Roscher, M., Stordal, F. & Svensen, H. The effect of global warming and global cooling on the distribution of the latest Permian climate zones. Palaeogeogr. Palaeoclimatol. Palaeoecol. 309, 186–200 (2011).

    Article  Google Scholar 

  99. Gibbs, M. T. et al. Simulations of Permian climate and comparisons with climate-sensitive sediments. J. Geol. 110, 33–55 (2002).

    Article  ADS  CAS  Google Scholar 

  100. Harris, R. et al. Climate change during the Triassic and Jurassic. Geol. Today 33, 210–215 (2017).

    Article  Google Scholar 

  101. Sellwood, B. W. & Valdes, P. J. Mesozoic climates: general circulation models and the rock record. Sediment. Geol. 190, 269–287 (2006).

    Article  ADS  Google Scholar 

Download references

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.

Author information

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

Authors
  1. Ricardo Araújo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Romain David
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julien Benoit
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jacqueline K. Lungmus
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexander Stoessel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paul M. Barrett
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jessica A. Maisano
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Eric Ekdale
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Maëva Orliac
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhe-Xi Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Agustín G. Martinelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Eva A. Hoffman
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Christian A. Sidor
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Rui M. S. Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Fred Spoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Kenneth D. Angielczyk
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

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

Additional information

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 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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-022-04963-z

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing