Inner ear biomechanics reveals a Late Triassic origin for mammalian endothermy

• Published in: Nature (London) Vol. 607; no. 7920; pp. 726 - 731
• Main Authors: Araújo, Ricardo, David, Romain, Benoit, Julien, Lungmus, Jacqueline K., Stoessel, Alexander, Barrett, Paul M., Maisano, Jessica A., Ekdale, Eric, Orliac, Maëva, Luo, Zhe-Xi, Martinelli, Agustín G., Hoffman, Eva A., Sidor, Christian A., Martins, Rui M. S., Spoor, Fred, Angielczyk, Kenneth D.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 28.07.2022; Nature Publishing Group
• Subjects: 631/181/414; 631/443/376; 631/601/1737; Animals; Biodiversity; Biological Evolution; Biomechanical Phenomena; Biomechanics; Birds; Body Temperature; Canals; Ducts; Ear; Ear, Inner - anatomy & histology; Ear, Inner - physiology; Earth Sciences; Endangered & extinct species; Endolymph; Engineering Sciences; Extinct species; Extinction; Extinction, Biological; Fossils; Functional morphology; Head movement; History, Ancient; Humanities and Social Sciences; Inner ear; Life Sciences; Mammals; Mammals - anatomy & histology; Mammals - physiology; Mechanics; Metabolism; Morphology; Motility; multidisciplinary; Paleontology; Phylogenetics; Populations and Evolution; Science; Science (multidisciplinary); Sciences of the Universe; Semicircular Ducts - anatomy & histology; Semicircular Ducts - physiology; Thermogenesis; Triassic; Viscosity
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/s41586-022-04963-z

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 performance 27 . 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 instability 28 . The functional morphology of the fluid-filled semicircular ducts of the inner ear is adapted to body temperature and behavioural activity and can be used to investigate the evolution of endothermy.