Plastic loss of motile cilia in the internal gills of Polypterus in response to high CO₂ or terrestrial environments

Abstract

The evolutionary transition of vertebrates from water to land during the Devonian period was accompanied by major changes in animal respiratory systems in terms of physiology and morphology. Indeed, the fossil record of the early tetrapods has revealed the existence of internal gills, which are vestigial fish-like traits used underwater. However, the fossil record provides only limited data to elucidate the process of the evolutionary transition of internal gills from fish to early tetrapods. This study investigated the internal gills of Polypterus senegalus, a basal ray-finned/amphibious fish which shows many ancestral features of stem Osteichthyes. Based on scanning electron microscopy observations and transcriptome analysis, the existence of motile cilia in the internal gills was revealed which may create a flow on the internal gill surface leading to efficient respiration. Interestingly, these cilia were observed to disappear after rearing in terrestrial or high CO₂ environments, which mimics the environmental changes in the Devonian period. The cilia re-appeared after being returned to the original aquatic environment. The ability of plastic loss of internal gills in Polypterus revealed in this study may allow them to survive in fluctuating environments, such as shallow swamps. The ancestor of Osteichthyes is also expected to have possessed such plasticity in the internal gills, which may be one of the driving forces behind the transition of vertebrates from water to land.