Evolution and Development of the Atrial Septum

Abstract

The complete division of the atrial cavity by a septum, resulting in a left and right atrium, is found in many amphibians and all amniotes (reptiles, birds, and mammals). Surprisingly, it is only in eutherian, or placental, mammals that full atrial septation necessitates addition from a second septum. The high incidence of incomplete closure of the atrial septum in human, so‐called probe patency, suggests this manner of closure is inefficient. We review the evolution and development of the atrial septum to understand the peculiar means of forming the atrial septum in eutherian mammals. The most primitive atrial septum is found in lungfishes and comprises a myocardial component with a mesenchymal cap on its leading edge, reminiscent to the primary atrial septum of embryonic mammals before closure of the primary foramen. In reptiles, birds, and mammals, the primary foramen is closed by the mesenchymal tissues of the atrioventricular cushions, the dorsal mesenchymal protrusion, and the mesenchymal cap. These tissues are also found in lungfishes. The closure of the primary foramen is preceded by the development of secondary perforations in the septal myocardium. In all amniotes, with the exception of eutherian mammals, the secondary perforations do not coalesce to a secondary foramen. Instead, the secondary perforations persist and are sealed by myocardial and endocardial growth after birth or hatching. We suggest that the error‐prone secondary foramen allows large volumes of oxygen‐rich blood to reach the cardiac left side, needed to sustain the growth of the extraordinary large offspring that characterizes eutherian mammals. Anat Rec, 302:32–48, 2019. © 2018 The Authors. The Anatomical Record published by Wiley Periodicals, Inc. on behalf of American Association of Anatomists.

Comparative analysis of avian hearts provides little evidence for variation among species with acquired endothermy

“…The pronounced offset in birds may reflect in part that the membranous septum of the ventricle completely myocardialises (Adams, ). In crocodylians this septum only exhibits slight myocardialization (Jensen et al, ) and mammals always have the membranous septum present in the adult heart (Rowlatt, ). We confirm the constant presence of a large left atrioventricular junction guarded by membranous leaflets anchored to papillary muscles, a feature crocodylians and birds share with mammals (Jensen et al, ; Cook et al , ).…”

“…The atrial septum of monotreme and marsupial mammals develops from the primary septum only. In eutherian mammals, the atrial septum is formed by the merger of the primary and secondary atrial septum, a process that is revealed in the adult heart by the presence of the fossa ovale (Röse, ; Runciman, Gannon, & Baudinette, ; Jensen, Wang, & Moorman, ). In contrast, the atrial septum of birds has no fossa ovale and it develops from the primary septum only (Jensen, Wang, Moorman, ).…”

Development and evolution of the metazoan heart

“…In the human population, deficient PDGF signaling is related to pulmonary vein abnormalities . A major structure in atrium development found in many amphibians and in amniotes (reptiles, birds, mammals) is the atrium septum, dividing the common atrium into left‐ and right‐sided chambers. The primary foramen is closed collaboratively by the AV cushions, the mesenchymal cap, and the DMP, tissues that can also be found in lungfish .…”

“…A major structure in atrium development found in many amphibians and in amniotes (reptiles, birds, mammals) is the atrium septum, dividing the common atrium into left‐ and right‐sided chambers. The primary foramen is closed collaboratively by the AV cushions, the mesenchymal cap, and the DMP, tissues that can also be found in lungfish . In placental mammals, septation is completed by addition of the second septum, while definitive closure of the septum is completed only after birth.…”

“…The primary foramen is closed collaboratively by the AV cushions, the mesenchymal cap, and the DMP, tissues that can also be found in lungfish. 172 In placental mammals, septation is completed by addition of the second septum, while definitive closure of the septum is completed only after birth.…”