Origin of the avian respiratory system: a CT-study of postcranial pneumaticity in basal archosaurs

Lead Research Organisation: The Natural History Museum
Department Name: Earth Sciences

Abstract

The incredible success of living birds (>9000 species) results, in part, from their unique respiratory system, which underpins the key evolutionary innovations of high metabolism and flight. This system comprises the lungs and a complex array of interconnected air sacs. The air sacs allow a unidirectional flow of air through the lungs, permitting exceptionally efficient gas-exchange. Extensions from the air sacs penetrate and pneumatize nearby bones, including vertebrae and limb elements, with the associated effect of reducing skeletal mass. In contrast, the closest living relatives of birds, crocodiles, lack air sacs and corresponding pneumatic features. There is now overwhelming evidence that birds are direct descendents of theropod dinosaurs. Many features previously regarded as uniquely avian appeared first among dinosaurs (e.g. feathers, brooding behaviour). The avian air sac system is another such feature: its presence in theropod and sauropod dinosaurs (and pterosaurs) has been inferred on the basis of pneumatic features in vertebrae that are almost identical to those seen in living birds. However, the origin of the air sac system is poorly understood: there is no consensus on whether air sacs and pneumaticity were present in the common ancestor of theropods, sauropods and pterosaurs, or whether they evolved independently in these three groups. Furthermore, possible evidence of pneumaticity has recently been identified in more distantly related Triassic archosaurs, prompting the controversial hypothesis that pneumaticity (and, by inference, air sacs and some bird-like respiratory capabilities) may have been present in the last common ancestor of birds and crocodiles, and subsequently lost in crocodilians. If true, this would require radical alteration of our understanding of the remarkable biology of birds and crocodiles and how they evolved. Understanding the origin of the avian respiratory system is clearly fundamental to explaining the success and diversity of the various archosaur lineages. However, the main alternative hypotheses have not yet been tested. We propose a pilot study to test alternative hypotheses explaining the origin of bird-like respiration. This work is timely, given recent intensive interest in dinosaur and bird respiratory systems, the availability of the research team and a new micro X-ray Computed Tomography (CT) facility at the Natural History Museum. We will determine the presence/absence of pneumatic structures in the vertebrae of selected Triassic archosaurs that lie close to the common ancestry of crocodiles and birds. The identification of pneumaticity will be based on external and internal vertebral anatomy: the latter data were previously unavailable, but will be obtained using CT scans - an entirely novel approach to this problem. The extent of pneumaticity, both within individual bones and throughout the skeleton, will be documented and the distribution of pneumatic structures will be determined by mapping the presence/absence of these features onto current archosaur evolutionary trees. This will permit us to establish: when pneumaticity appeared in archosaurs; whether the acquisition (or loss) of pneumaticity was a single event or occurred on multiple independent occasions; and the evolutionary sequence in which the different components of the air sac system appeared. Demonstrating the absence of pneumaticity in basal archosaurs would falsify hypotheses that a bird-like respiratory system was present in the ancestral archosaur, and support alternative hypotheses suggesting a later origin of air sacs. However, if pneumaticity is identified in primitive archosaurs this project will demonstrate that evolution of the air sac system is more complex than currently assumed and will facilitate future investigations into the origins of avian and crocodilian respiratory systems. This work will be of fundamental importance to palaeontologists, zoologists and physiologists.
 
Description We used CT scanning to investigate the distribution of air sacs in the skeletons of dinosaurs, pterosaurs and various other extinct reptile groups. These air sacs are an integral part of the archosaur respiratory system and this survey enabled us to investigate how early the various components of the bird respiratory system had been assembled through time. We showed that bird-like respiratory systems had a deep origin, in the Middle Triassic and characterised the majority of dinosaurs and pterosaurs, whereas this system was either absent or disappeared early in the evolution of crocodiles and their ancestors. The appearance of this respiratory system may have been a key event that sparked dinosaur (and later bird) success. In addition, we also described a new Triassic archosaur (Hyselorhachis) as an additional benefit.
Exploitation Route These results can be used in formal educational and public outreach settings as a way of explaining complex evolutionary and physiological principles through the medium of dinosaur biology.
Sectors Education,Culture, Heritage, Museums and Collections

 
Description In addition to being used among academic peers (with 90+ citations of the three that have resulted), the results have been broadly disseminated via public talks and lectures, both at the Natural History Museum and at various local institutions outside of London, as well as at undergraduate level via a number of student seminars in universities around the UK. In addition, the results of this study led to related MSc project (now also published) at the University of Bristol.
First Year Of Impact 2008
Sector Education,Culture, Heritage, Museums and Collections
Impact Types Cultural

 
Description Investigation of vertebral anatomy in the ostrich 
Organisation University of Bristol
Department School of Earth Sciences
Country United Kingdom 
Sector Academic/University 
PI Contribution My work on pneumaticity led to an invitation to collaborate on the supervision of two MSc projects, one on neck flexibility and the other on cervical pneumaticity in the ostrich. I contributed my expertise on bird and dinosaur osteology, functional morphology and on the evolution of pneumatic systems in archosaurs.
Collaborator Contribution They contributed materials for the project, space in which to carry it out and expertise in muscular reconstructions and biomechanics.
Impact Two papers resulted from these collaborations: Cobley, M. J., Rayfield, E. J. & Barrett, P. M. 2013. Intervertebral flexibility of the ostrich neck: implications for estimating sauropod neck flexibility. PLoS ONE 8(8): e72187 (doi:10.1371/journal.pone.0072187) Apostolaki, N. Rayfield, E. J. & Barrett, P. M. 2015. Osteological and soft-tissue evidence for pneumatization in the cervical column of the ostrich (Struthio camelus) and observations on the vertebral columns of non-volant, semi-volant and semi-aquatic birds. PLoS ONE 10(12): e0143834.
Start Year 2012
 
Description Dorset Naturalists Talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Talk on the advances in dinosaur biology drawing on NERC work related to dinosaur hearing and breathing. Around 200 people in the audience, comprising members of the general public. Numerous questions followed.
Year(s) Of Engagement Activity 2012
 
Description Nature Live, Natural History Museum 2011 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Talk on the evolution of archosaur respiration to at the Natural History Museum London. Around 60 students attended, with numerous questions afterward.
Year(s) Of Engagement Activity 2011
 
Description Student Society Talk (Cambridge) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact Talk on the evolution of archosaur respiration to the University of Cambridge Geological Society. Around 40 students attended, with numerous questions afterward.
Year(s) Of Engagement Activity 2013
 
Description Student Society Talk (Leicester) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact Talk on the evolution of archosaur respiration to the University of Leicester Geological Society. Around 100 students attended, with numerous questions afterward.
Year(s) Of Engagement Activity 2013
 
Description Student Talk (UCL) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact Talk on the evolution of archosaur respiration to UCLs LERN centre. Around 30 students attended, with numerous questions afterward.
Year(s) Of Engagement Activity 2013
 
Description Ulster Museum talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Professional Practitioners
Results and Impact A talk on advances in dinosaur biology drawing on advances from NERC projects on dinosaur hearing and breathing. Lengthy discussion followed, with impact on museum and educational professionals attempting to communicate science in museums.
Year(s) Of Engagement Activity 2012
 
Description World Museum Talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Professional Practitioners
Results and Impact Talk on advances in dinosaur biology drawing on NERC funded projects on hearing and respiration. Numerous questions from both the public and professionals.
Year(s) Of Engagement Activity 2011