During the embryo and early larval stages, fish are small enough to sustain metabolism by simply diffusing O2 across their skin. However, as the fish grows this becomes inefficient and a special structure with a larger surface area for extracting O2 is required. At this crucial moment, fish begin to develop gills, the quintessential characteristic we associate with fish and their ability to ‘breathe’ in watery habitats. However, gills have many more functions. Adult fish also use gills to dispose of metabolic carbon dioxide and for pH and water balance, which is done largely via ion regulation pathways. This is important because the ion concentrations of a fish's body fluids are very different from those of the water in which it lives, allowing essential ions to leak either into or out of the fish's body to create ionic imbalances that disrupt crucial physiological processes. Initially fish use the enzymes and transporters associated with special mitochondrion-rich cells (MRCs) on their skin to move ions into and out of their bodies. However, as the fish's ion regulation requirements exceed the capacity of the MRCs on the skin and the surface area of the fish's body is too small to accommodate further MRCs, the site of ion regulation moves to the high surface area gills. Given that both gill duties – ensuring that the proper ions enter and leave the body, and O2 extraction – are crucial to the fish, Clarice Fu and her colleagues from Universities in Canada and Portugal developed a hypothesis to directly test, for the first time, which function needed the gills to develop first.
Fu and her colleagues selected trout embryos for the study and built specialized chambers so that the newly hatched larvae's heads could be isolated from their bodies, to enable them to compartmentalize the duties of the gills and the skin. At various points in development, which they tracked as ‘days post-hatch’, the team measured the fish's O2 extraction and ion (Na+) uptake rates from the water. Because they had isolated the head (gills) from the body (skin), they could determine the proportion of each job that was performed by each body part. When the proportion of the job performed by the skin decreased and the proportion performed by the gills increased, they would know that it was time for the gills to take over the function from the skin.
The team determined that O2 extraction transitioned from a job that was performed predominantly by the skin to one undertaken by the gills 23 to 28 days post-hatch. However, this transition occurred earlier for ion regulation; the job site switched from the skin to the gills at 15 to 16 days post-hatch. This indicated to the team that ion regulation was a bigger issue to a developing fish: the development of gill structures for ion regulation is required earlier than for O2 extraction. Fu and her team found that this trend remained when experiments were performed in ion-rich hard water and ion-poor soft water, suggesting that the timing of gill development is intrinsic. The team's conclusions regarding gill development give scientists an insight into the evolution of primitive fishes and the kinds of fishes that may have existed. It may have been that the invasion of freshwater was what gave rise to gills, more so than a dire need for O2.
