Atmospheric oxygen remodels cardiac outflow tract in the American alligator

Abstract

The in-series circulatory systems of mammals and birds evolved from an ancestral system capable of shunting blood between the systemic and pulmonary circuits, as seen in extant amphibians and non-avian reptiles. To test whether atmospheric oxygen level can affect cardiac outflow tract morphology, we exposed hatchlings of the American alligator to chronic hypoxia (12%O2), normoxia (21%O2) and hyperoxia (30%O2). After three months, we quantified the perimeter of the left aorta (LAo), right aorta and pulmonary artery from histologic sections, and calculated their maximum (circular) cross-sectional area (CSA). Relative to the total outflow CSA, LAo fraction was 0.17 in hypoxia, 0.24 in normoxia and 0.26 in hyperoxia, suggesting the outflow tract remodels in response to blood flow distribution. In vivo recordings from juvenile alligators confirmed that shunt magnitude via LAo decreases with acute exposure to hypoxia and increases in hyperoxia. We posit that a pulmonary bypass shunt in tetrapods was maintained by global hyperoxia of the Late Carboniferous-Early Permian, but reduced by hypoxia of the Late Triassic-Early Jurassic. The latter period coincides with the appearance of mammals and theropod dinosaurs (avian ancestors). Once the shunt was lost, the mammalian and theropod cardiovascular systems would have been committed to the obligatory in-series circulation. Funded by NSF IOS 922756.