Development of the pulmonary surfactant system in non-mammalian amniotes

Pulmonary surfactant (PS) is a complex mixture of phospholipids, neutral lipids and proteins that lines the inner surface of the lung. Here, it modulates surface tension thereby increasing lung compliance and preventing the transudation of fluid. In mammals, the PS system develops towards the end of gestation, characterized by an increase in the saturation of phospholipids in lung washings and the appearance of surfactant proteins in amniotic fluid. Birth, the transition from in utero to the external environment, is a rapid process. At this time, the PS system is important in opening and clearing the lung of fluid in order to initiate pulmonary ventilation. In oviparous vertebrates, escape from an egg can be a long and exhausting process. The young commence pulmonary ventilation and hatching by 'pipping' through the eggshell, where they remain for some time, presumably clearing their lungs. This paper relates changes in the development of the pulmonary surfactant system within the non-mammalian amniotes in response to birth strategy, lung morphology and phylogeny in order to determine the conservatism of this developmental process. Total phospholipid (PL), disaturated phospholipid (DSP) and cholesterol (Chol) were quantified from lung washings of embryonic and hatchling chickens, bearded dragons (oviparous), sleepy lizards (viviparous), snapping turtles and green sea turtles throughout the final stages of incubation and gestation. In all cases, the pattern of development of the pulmonary surfactant lipids was consistent with that of mammals. PL and DSP increased throughout the latter stages of development and Chol was differentially regulated from the PLs. Maximal secretion of both PL and DSP occurred at 'pipping' in oviparous reptiles, coincident with the onset of airbreathing. Similarly, the amount of DSP relative to total PL was maximal immediately after the initiation of airbreathing in chickens. The relative timing of the appearance of the lipids differed between groups. In the oviparous lizard, surfactant lipids were released over a relatively shorter time than that of the sleepy lizard, turtles, birds and mammals. Thus, despite temporal differences and vastly different lung morphologies, birth strategies and phylogenies, the overall development and maturation of the PS system is highly conserved amongst the amniotes.