Ion regulation at gills precedes gas exchange and the origin of vertebrates

Gas exchange and ion regulation at gills have key roles in the evolution ofvertebrates(1-4). Gills are hypothesized to have first acquired these important homeostatic functions from the skin in stem vertebrates, facilitating the evolution of larger, more-active modes oflife(2,3,5). However, this hypothesis lacks functional support in relevant taxa. Here we characterize the function ofgills and skin in a vertebrate (lamprey ammocoete; Entosphen us tridentatus), a cephalochordate (amphioxus; Branch iostomafloridae) and a hemichordate (acorn worm; Saccoglossus kowaleuskii) with the presumed burrowing, filter-feeding traits ofvertebrate ancestors(6-9). We provide functional support for a vertebrate origin ofgas exchange at the gills with increasing body size and activity, as direct measurements in vivo reveal that gills are the dominant site ofgas exchange only in ammocoetes, and only with increasing body size or challenges to oxygen supply and demand. Conversely, gills of all threetaxa are implicated in ion regulation. Ammocoetegills are responsible for all ion flux at all body sizes, whereas molecular markers for ion regulation are higher in the gillsthan in the skin of amphioxus and acorn worms. This suggeststhat ion regulation at gills has an earlier origin than gas exchange that is unrelated to vertebrate size and activity-perhaps at the very inception of pharyngeal pores in stem deuterostomes.

Automated summary

Gas exchange and ion regulation are crucial in the evolution of vertebrates. Gills are involved in gas exchange and become the dominant site for larger or more active vertebrates, while all three taxa exhibit ion regulation in their gills. Ammocoete gills are responsible for all ion flux, indicating an earlier origin of ion regulation at gills than gas exchange in vertebrates.