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Abstract

Oxygen-sensing cells involved in the respiratory reflex develop in association with the embryonic pharyngeal arch arteries and gut endoderm. In the adult, oxygen-sensing cells are located in the carotid body and lungs of amniotes, and in the gills and orobranchial cavity of anamniotes. These cells respond to hypoxia in the blood and surrounding air/water, triggering increased ventilation via the respiratory reflex. Despite their physiological importance, little is known about their development or evolution. The oxygen-sensing cells of the gills, which develop in association with pharyngeal arch arteries, are hypothesised to be evolutionarily related to those of the carotid body, which are neural crest-derived and develop in association with the third pharyngeal arch artery. However, this relationship has never been tested. Using neural fold grafts in the chick and genetic lineage-tracing in the mouse, we confirm the neural crest origin of the carotid body, and also show that the oxygen-sensing cells of the lungs are not neural crest-derived. Using vital dye labelling, neural fold grafts, genetic lineage-tracing and analysis of zebrafish mutants lacking all neural crest cells, we show that the oxygen-sensing cells in the gills and orobranchial cavity of lamprey, zebrafish and frog are not neural crest-derived. Hence these cells cannot share an evolutionary origin with carotid body glomus cells. Our results suggest that oxygen-sensing cells in the lungs, not the carotid body, are homologous to those found in the gills and orobranchial cavity of anamniotes, and, furthermore, that the importance for the respiratory reflex of hypoxia-sensitive neural crest-derived cells seems to have evolved in association with air-breathing.