Evolution of the in‐series circulation in tetrapods: form follows function

Abstract

The ancestral in‐parallel circulation of tetrapods combines a single ventricle and two systemic aortae, which allow central vascular shunting. Loss of the shunt and evolution of the in‐series circulatory design, as exemplified by extant mammals and birds, involved independent acquisition of two anatomic features: a complete interventricular septum, and a single aorta. Extent and location of the interventricular septum is dictated by the expression gradient of Tbx transcription factors in the myocardium. Loss of an aorta, however, has yet to be addressed by developmental studies. Our experimental work on the American alligator suggests that the heart's outflow tract is remodelled by changes in blood flow distribution in response to environmental stressors. Flow capacity of the left aorta (a conduit for the pulmonary bypass shunt) was significantly reduced (−27%) in alligator hatchlings chronically exposed for three months to atmospheric hypoxia (12%O2), when compared to conspecifics reared in normoxia (21%O2) or hyperoxia (30%O2). In contrast, outflow tract capacities did not differ in juvenile alligators subject to 15 months of different exercise regimina (sedentary, running or swimming). We suggest that a global hypoxic episode, rather than increased activity, may have been the driving pressure behind loss of the shunt and origin of the in‐series circulation. Funded by NSF IOB0445680 and IOS922756 to JWH.