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UBC Theses and Dissertations

Ions before oxygen : ancestral origins of vertebrate gill function Sackville, Michael


Gas exchange and ion regulation at gills play many key roles in vertebrate evolution. Current hypotheses assume gills acquired these important functions from the skin along the vertebrate stem, facilitating the evolution of larger, armoured and more active modes of life. However, this assumption lacks functional support from representatives of early vertebrates and their ancestors. To better understand how and when vertebrate gills became the primary site of gas exchange and ion regulation, I characterized gill and skin function in representatives of ancestral vertebrates (lamprey ammocoete, Entosphenus tridentatus), cephalochordates (amphioxus, Branchiostoma floridae) and hemichordates (acorn worm, Saccoglossus kowalevskii). Intraspecific comparisons within ammocoetes tested the effects of size, dermal thickness and activity on gill function, and interspecific comparisons between taxa tested ancestral origins of gill function. For ammocoetes, I measured multiple gas and ion fluxes in vivo at gills and skin of different sized animals (0.02-2.00 g). Gills accounted for ~20% of gas flux in the smallest ammocoetes in normoxia at 10°C, and contributions increased with size, hypoxia and temperature. Conversely, gills accounted for 100% of ion flux in all sizes and conditions. For acorn worms, I exploited their regenerative ability to partition animals into viable halves with and without gills for respirometry. Gills did not enhance oxygen uptake or ammonia excretion despite hypoxic or thermal challenges. Morphometry by others estimates amphioxus gills also contribute negligibly to gas exchange. However, both acorn worm and amphioxus gills displayed elevated signals for ion regulation (NKA/VHA activity; CA/NHE/AE/Foxi expression). This is the first functional support in ancestral representatives for a vertebrate origin of gas exchange at gills associated with increasing size, dermal thickness and activity. However, ion regulation at gills appears unrelated to this vertebrate transition, and results instead suggest a novel and much earlier deuterostome origin near the inception of pharyngeal arches.

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