Respiratory evolution in archosaurs

Abstract

The Archosauria are a highly successful group of vertebrates, and their evolution is marked by the appearance of diverse respiratory and metabolic strategies. This review examines respiratory function in living and fossil archosaurs, focusing on the anatomy and biomechanics of the respiratory system, and their physiological consequences. The first archosaurs shared a heterogeneously partitioned parabronchial lung with unidirectional air flow; from this common ancestral lung morphology, we trace the diverging respiratory designs of bird- and crocodilian-line archosaurs. We review the latest evidence of osteological correlates for lung structure and the presence and distribution of accessory air sacs, with a focus on the evolution of the avian lung-air sac system and the functional separation of gas exchange and ventilation. In addition, we discuss the evolution of ventilation mechanics across archosaurs, citing new biomechanical data from extant taxa and how this informs our reconstructions of fossils. This improved understanding of respiratory form and function should help to reconstruct key physiological parameters in fossil taxa. We highlight key events in archosaur evolution where respiratory physiology likely played a major role, such as their radiation at a time of relative hypoxia following the Permo-Triassic mass extinction, and their evolution of elevated metabolic rates. This article is part of the theme issue ‘Vertebrate palaeophysiology’.

Vertebrate palaeophysiology

“…Modifications to these systems in the synapsid and archosaur lineages, which include wide-ranging foragers and terrestrial cursors, probably promoted the expansion of aerobic scope and athleticism previously unseen in vertebrates prior to the Permo-Triassic boundary. Brocklehurst et al [10] analyse the evolution of ventilation mechanics, as well as the osteological correlates for lung structure and distribution of air sacs, in archosaurs.…”

“…'Vertebrate palaeophysiology' will promote a better understanding of how organism-environment interactions have evolved in terms of energy budgets, predator-prey relationships and sensitivity to environmental change. The research areas covered by this theme issue include: phospho-calcic metabolism [2], acid-base homeostasis [3,4], thermometabolism [4][5][6][7][8][9], respiratory physiology [10], skeletal growth [11], palaeopathophysiology [12,13], genome size and metabolic rate [14], and a concluding historical perspective [15]. Sometimes, the two components ( physiological mechanism and palaeobiological inference) are proposed in separate papers (for instance, three contributions devoted to mechanisms of thermogenesis mechanisms [5][6][7] and three papers dealing with the thermometabolic inferences in extinct taxa [4,8,9]).…”

A new Heterodontosaurus specimen elucidates the unique ventilatory macroevolution of ornithischian dinosaurs

“…Osteological evidence of air sacs or pulmonary diverticula ( O'Connor and Claessens, 2005 ; O'Connor, 2006 ; Wedel, 2006 ; O'Connor, 2009 ), and functionally decoupled non-compliant and fixed gas-exchanging regions of the lung ( Wang et al, 2018 ; Perry and Reuter, 1999 ; Schachner et al, 2009 ; Schachner et al, 2011 ; Brocklehurst et al, 2018 ) in the major lineages Theropoda and Sauropodomorpha, have led to the modern consensus that most dinosaurs had a ‘proto avian-like’ respiratory system. Pulmonary anatomy similar to the avian-like respiratory system is also hypothesized to have been present in pterosaurs ( Butler et al, 2009 ; Claessens et al, 2009 ), leading to the hypothesis that aspects of proto-avian respiration, including air sacs, are plesiomorphic for the clade Ornithodira (Pterosauria + Dinosauromorpha) ( Wedel, 2006 ; Brocklehurst et al, 2020 ).…”

The evolution of mechanisms involved in vertebrate endothermy

“…In lamnids, the axial RM ( part of the muscle blocks that surround the vertebral column and supply most of the propulsive force for swimming) are located in a more medial position than in closely related taxa, allowing them to be better insulated, and are associated with retia. The brain region is heated by blood vessels carrying warm blood from the axial RM [89,123,124]. Cranial and pectoral-fin retia have also been detected in several species of the devil and manta rays (Mobulidae), but their heat production strategy is so far unknown [47].…”