Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy

doi:10.1038/s41586-022-04963-z

. 2022 Jul;607(7920):726-731.

doi: 10.1038/s41586-022-04963-z. Epub 2022 Jul 20.

Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy

Ricardo Araújo^#^{1

2}, Romain David^#^{3

4}, Julien Benoit⁵, Jacqueline K Lungmus⁶, Alexander Stoessel^{7

8}, Paul M Barrett⁹, Jessica A Maisano¹⁰, Eric Ekdale^{11

12}, Maëva Orliac¹³, Zhe-Xi Luo¹⁴, Agustín G Martinelli¹⁵, Eva A Hoffman¹⁶, Christian A Sidor¹⁷, Rui M S Martins¹⁸, Fred Spoor^{9

7

19}, Kenneth D Angielczyk²⁰

Affiliations

¹ Instituto de Plasmas e Fusão Nuclear, Instituto Superior Técnico, Universidade de Lisboa, Lisboa, Portugal. [email protected].
² Institut des Sciences de L'Évolution de Montpellier, Université de Montpellier, Montpellier, France. [email protected].
³ Natural History Museum, London, UK. [email protected].
⁴ Max Plank Institute for Evolutionary Anthropology, Leipzig, Germany. [email protected].
⁵ Evolutionary Studies Institute, University of Witwatersrand, Johannesburg, South Africa.
⁶ Department of Paleobiology, National Museum of Natural History, Washington DC, USA.
⁷ Max Plank Institute for Evolutionary Anthropology, Leipzig, Germany.
⁸ Institute of Zoology and Evolutionary Research, Friedrich Schiller University Jena, Jena, Germany.
⁹ Natural History Museum, London, UK.
¹⁰ Jackson School of Geosciences, University of Texas at Austin, Austin, TX, USA.
¹¹ Department of Biology, San Diego State University, San Diego, CA, USA.
¹² Department of Paleontology, San Diego Natural History Museum, San Diego, CA, USA.
¹³ Institut des Sciences de L'Évolution de Montpellier, Université de Montpellier, Montpellier, France.
¹⁴ Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA.
¹⁵ Museo Argentino de Ciencias Naturales 'Bernardino Rivadavia', Buenos Aires, Argentina.
¹⁶ Division of Paleontology, American Museum of Natural History, New York, NY, USA.
¹⁷ Burke Museum and Department of Biology, University of Washington, Seattle, WA, USA.
¹⁸ Instituto de Plasmas e Fusão Nuclear, Instituto Superior Técnico, Universidade de Lisboa, Lisboa, Portugal.
¹⁹ Department of Anthropology, University College London, London, UK.
²⁰ Neguanee Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA. [email protected].

^# Contributed equally.

PMID: 35859179
DOI: 10.1038/s41586-022-04963-z

Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy

Ricardo Araújo et al. Nature. 2022 Jul.

. 2022 Jul;607(7920):726-731.

doi: 10.1038/s41586-022-04963-z. Epub 2022 Jul 20.

Authors

Affiliations

¹ Instituto de Plasmas e Fusão Nuclear, Instituto Superior Técnico, Universidade de Lisboa, Lisboa, Portugal. [email protected].
² Institut des Sciences de L'Évolution de Montpellier, Université de Montpellier, Montpellier, France. [email protected].
³ Natural History Museum, London, UK. [email protected].
⁴ Max Plank Institute for Evolutionary Anthropology, Leipzig, Germany. [email protected].
⁵ Evolutionary Studies Institute, University of Witwatersrand, Johannesburg, South Africa.
⁶ Department of Paleobiology, National Museum of Natural History, Washington DC, USA.
⁷ Max Plank Institute for Evolutionary Anthropology, Leipzig, Germany.
⁸ Institute of Zoology and Evolutionary Research, Friedrich Schiller University Jena, Jena, Germany.
⁹ Natural History Museum, London, UK.
¹⁰ Jackson School of Geosciences, University of Texas at Austin, Austin, TX, USA.
¹¹ Department of Biology, San Diego State University, San Diego, CA, USA.
¹² Department of Paleontology, San Diego Natural History Museum, San Diego, CA, USA.
¹³ Institut des Sciences de L'Évolution de Montpellier, Université de Montpellier, Montpellier, France.
¹⁴ Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA.
¹⁵ Museo Argentino de Ciencias Naturales 'Bernardino Rivadavia', Buenos Aires, Argentina.
¹⁶ Division of Paleontology, American Museum of Natural History, New York, NY, USA.
¹⁷ Burke Museum and Department of Biology, University of Washington, Seattle, WA, USA.
¹⁸ Instituto de Plasmas e Fusão Nuclear, Instituto Superior Técnico, Universidade de Lisboa, Lisboa, Portugal.
¹⁹ Department of Anthropology, University College London, London, UK.
²⁰ Neguanee Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA. [email protected].

^# Contributed equally.

PMID: 35859179
DOI: 10.1038/s41586-022-04963-z

Erratum in

Author Correction: Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy.
Araújo R, David R, Benoit J, Lungmus JK, Stoessel A, Barrett PM, Maisano JA, Ekdale E, Orliac M, Luo ZX, Martinelli AG, Hoffman EA, Sidor CA, Martins RMS, Spoor F, Angielczyk KD. Araújo R, et al. Nature. 2023 Jan;613(7945):E2. doi: 10.1038/s41586-023-05700-w. Nature. 2023. PMID: 36624295 No abstract available.

Abstract

Endothermy underpins the ecological dominance of mammals and birds in diverse environmental settings^1,2. However, it is unclear when this crucial feature emerged during mammalian evolutionary history, as most of the fossil evidence is ambiguous^3-17. 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 awareness^18-22. Increased body temperatures during the ectotherm-endotherm transition of mammal ancestors would decrease endolymph viscosity, negatively affecting semicircular duct biomechanics^23,24, while simultaneously increasing behavioural activity^25,26 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 suggestions^3-14, 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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Comment in

Evolution of thermoregulation as told by ear.
Glasauer S, Straka H. Glasauer S, et al. Nature. 2022 Jul;607(7920):661-662. doi: 10.1038/d41586-022-01943-1. Nature. 2022. PMID: 35859128 No abstract available.

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References

1. Lovegrove, B. G. Fires of Life: Endothermy in Birds and Mammals (Yale Univ. Press, 2019).
1. Benton, M. J. The origin of endothermy in synapsids and archosaurs and arms races in the Triassic. Gondwana Res. 100, 261–289 (2021). - DOI
1. Kubo, T. & Benton, M. J. Tetrapod postural shift estimated from Permian and Triassic trackways. Palaeontology 52, 1029–1037 (2009). - DOI
1. 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). - DOI
1. 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). - DOI

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

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

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

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

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

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

[7] 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). - DOI

[8] 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). - DOI

[9] 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). - DOI

[10] 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). - DOI

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Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy

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Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy

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