The evolution of a physiological system: the pulmonary surfactant system in diving mammals

Pulmonary surfactant lines the alveolar air-water interface, varying surface tension with lung volume to increase compliance and prevent adhesion of respiratory surfaces. We examined whether the surfactant system of diving mammals exhibits adaptations for more efficient lung function during diving, to complement other respiratory adaptations. Here we review adaptations at the molecular, compositional, functional and cellular levels and during development for animals beginning life on land and progressing to an aquatic environment. Molecular adaptations to diving were examined in surfactant protein C (SP-C) from terrestrial, semi-aquatic and diving mammals using phylogenetic analyses. Diving species exhibited sites under positive selection in the polar N-terminal domain. These amino acid substitutions may lead to stronger binding of SP-C to the phospholipid film and increased adsorption to the air-liquid interface. The concentration of shorter chain phospholipid molecular species was greater and SP-B levels were lower in diving than terrestrial mammals. This may lead to a greater fluidity and explain the relatively poor surface activity of diving mammal surfactant. There were no consistent differences in cholesterol between diving and terrestrial mammals. Surfactant from newborn California sea lions was similar to that of terrestrial mammals. Secretory activity of alveolar type II epithelial cells of sea lions demonstrated an insensitivity to pressure relative to sheep cells. The poor surface activity of diving mammal surfactant is consistent with the hypothesis that it has an anti-adhesive function that develops after the first entry into the water, with a surfactant film that is better suited to repeated collapse and respreading.