Origin of the unique ventilatory apparatus of turtles.
The turtle body plan differs markedly from that of other vertebrates and serves as a model system for studying structural and developmental evolution. Incorporation of the ribs into the turtle shell negates the costal movements that effect lung ventilation in other air-breathing amniotes. Instead, turtles have a unique abdominal-muscle-based ventilatory apparatus whose evolutionary origins have remained mysterious. Here we show through broadly comparative anatomical and histological analyses that an early member of the turtle stem lineage has several turtle-specific ventilation characters: rigid ribcage, inferred loss of intercostal muscles and osteological correlates of the primary expiratory muscle. Our results suggest that the ventilation mechanism of turtles evolved through a division of labour between the ribs and muscles of the trunk in which the abdominal muscles took on the primary ventilatory function, whereas the broadened ribs became the primary means of stabilizing the trunk. These changes occurred approximately 50 million years before the evolution of the fully ossified shell.
1] Department of Earth Sciences, Denver Museum of Nature and Science, Denver, Colorado 80205, USA [2] Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington DC 20560, USA [3] Evolutionary Studies Institute, University of the Witwatersrand, PO Wits 2050, Johannesburg, South Africa.
Tyler R
TR
Lyson
1] Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, Louisiana 70803, USA [2] Department of Biology, University of Utah, Salt Lake City, Utah 84112, USA.
Emma R
ER
Schachner
1] Karoo Palaeontology, National Museum, Box 266, Bloemfontein 9300, South Africa [2] Department of Zoology and Entomology, University of the Free State, Bloemfontein 9300, South Africa.
Jennifer
J
Botha-Brink
Paläontologisches Institut und Museum, Universität Zürich, Karl Schmid-Strasse 4, 8006 Zürich, Switzerland.
Torsten M
TM
Scheyer
Institut für Zoologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Poppelsdorfer Schloss, 53115 Bonn, Germany.
Markus
M
Lambertz
1] Evolutionary Studies Institute, University of the Witwatersrand, PO Wits 2050, Johannesburg, South Africa [2] New York Institute of Technology, College of Osteopathic Medicine, Old Westbury, New York 11568, USA [3] Division of Paleontology, American Museum of Natural History, New York, New York 10024, USA.
G S
GS
Bever
Evolutionary Studies Institute, University of the Witwatersrand, PO Wits 2050, Johannesburg, South Africa.
Bruce S
BS
Rubidge
Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington DC 20560, USA.
Kevin
K
de Queiroz
D000009:Abdominal Muscles / Q000033:anatomy & histology* / Q000000981:diagnostic imaging / Q000502:physiology; D000717:Anatomy, Comparative; D060105:Animal Shells / Q000033:anatomy & histology / Q000000981:diagnostic imaging / Q000502:physiology; D000818:Animals; D005075:Biological Evolution; D005260:Female; D008168:Lung / Q000033:anatomy & histology* / Q000000981:diagnostic imaging / Q000502:physiology; D010802:Phylogeny; D012123:Pulmonary Ventilation / Q000502:physiology; D012132:Respiratory Muscles / Q000033:anatomy & histology* / Q000000981:diagnostic imaging / Q000502:physiology; D012272:Ribs / Q000033:anatomy & histology* / Q000000981:diagnostic imaging / Q000502:physiology; D014057:Tomography, X-Ray Computed; D014426:Turtles / Q000033:anatomy & histology* / Q000235:genetics / Q000502:physiology