Convergent evolutionary reduction of atrial septation in lungless salamanders

Abstract

Nearly two thirds of the approximately 700 species of living salamanders are lungless. These species respire entirely through the skin and buccopharyngeal mucosa. Lung loss dramatically impacts the configuration of the circulatory system but the effects of evolutionary lung loss on cardiac morphology have long been controversial. For example, there is presumably little need for an atrial septum in lungless salamanders due to the absence of pulmonary veins and the presence of a single source of mixed blood flowing into the heart, but whether lungless salamanders possess an atrial septum and whether the sinoatrial aperture is located in the left or right atrium are unresolved; authors have stated opposing claims since the late 1800s. Here, we use micro‐computed tomography (μ‐CT) imaging, gross dissection and histological reconstruction to compare cardiac morphology among lungless plethodontid salamanders (Plethodontidae), salamanders with lungs, and the convergently lungless species Onychodactylus japonicus (Hynobiidae). Plethodontid salamanders have partial atrial septa and incomplete separation of the atrium into left and right halves. Partial septation is also seen in O. japonicus. Hence, lungless salamanders from two lineages convergently evolved similar morphology of the atrial septum. The partial septum in lungless salamanders can make it appear that the sinoatrial aperture is in the left atrium, but this interpretation is incorrect. Outgroup comparisons demonstrate that the aperture is located in a posterodorsal extension of the right atrium into the left side of the heart. Independent evolutionary losses of the atrial septum may have a similar developmental basis. In mammals, the lungs induce formation of the atrial septum by secreting morphogens to neighboring mesenchyme. We hypothesize that the lungs induce atrial septum development in amphibians in a similar fashion to mammals, and that atrial septum reduction in lungless salamanders is a direct result of lunglessness.

Development and evolution of the metazoan heart

“…In these species, the atrium is only partially septated. In amphibians, the lungs induce atrial septation similar to mammals, and atrial septum reduction results directly from reduced or absent lungs . As these species lack pulmonary veins, all the blood flowing into the heart derives from the cardinal veins via the sinus venosus in the right‐sided part of the atrium, while pulmonary ostia in the left atrium are lacking.…”

“…In amphibians, the lungs induce atrial septation similar to mammals, and atrial septum reduction results directly from reduced or absent lungs. 162 As these species lack pulmonary veins, all the blood flowing into the heart derives from the cardinal veins via the sinus venosus in the right-sided part of the atrium, while pulmonary ostia in the left atrium are lacking. During normal development, the pulmonary veins become incorporated into the left atrial body wall (frog 163 ) but not the atrial appendage (human 164 ), demonstrating the close relationship between the left atrium and lung circulation.…”

Retinoic acid signaling in heart development

“…In the amphibian heart, the sinus venosus moves more anteriorly, and the pulmonary vein connects with the atrium through the dorsal mesocardium (Romer, 1971). The atrial septum is present in vertebrates with pulmonary respiration including lungfishes, amphibians, and amniotes (Lewis & Hanken, 2017;Moorman & Christoffels, 2003;Steimle et al, 2018). The atrial septum is present in vertebrates with pulmonary respiration including lungfishes, amphibians, and amniotes (Lewis & Hanken, 2017;Moorman & Christoffels, 2003;Steimle et al, 2018).…”

“…Lunged amphibians have a complete atrial septum, whereas lungless salamanders have an incomplete atrial septum, suggesting a coordinated mechanism regulating the cardiopulmonary system during development and evolution (Lewis & Hanken, 2017). …”

“…The orifice of the pulmonary vein is demarcated by DMP, part of the atrial septum originating from the posterior SHF; therefore, the pulmonary vein drains into the left side of the atrium (Tasaka et al, 1996). The atrial septum is present in vertebrates with pulmonary respiration including lungfishes, amphibians, and amniotes (Lewis & Hanken, 2017;Moorman & Christoffels, 2003;Steimle et al, 2018).…”