Fish May Not Have Evolved Gills to Breathe

Mystery solved? The gills of this rainbow trout embryo may have evolved to exchange ions, not oxygen.

Why did fish evolve gills? If you said, "To breathe," then you probably passed Biology 101. But you--and the textbooks--may not be right. A new study argues that the structures really emerged to help keep fish in chemical balance with their environment.

The first person to suggest that fish develop gills to breathe was Nobel Prize–winning physiologist August Krogh in the 1940s. Later, other researchers expanded the theory, arguing that, as fish became larger and more predatory hundreds of millions of years ago, their rudimentary gills became larger and more complex to help them draw more oxygen from the water.

Studies over the past decade have hinted at a different explanation. In order to keep from shriveling like your fingers in the bathtub, fish must constantly exchange ions, such as sodium and potassium, with the water. Larval fish can exchange ions through their skin, and early fish likely used rudimentary gill structures known as branchial baskets. But when the salinity of the water changes rapidly--as happened when fish invaded freshwater habitats--fish would have needed a much more efficient way of exchanging ions with their environment. That means large, complex gills. "It's always hard not to believe what a Nobel Prize winner has put forward," says Peter Rombough, a biologist at Brandon University in Manitoba, Canada. "But we began to accumulate evidence, and it didn't seem to fit with the theory."

In the new study, Rombough and colleagues looked at rainbow trout, a common laboratory animal. The researchers wanted to know if the fledgling gills first exchange ions or oxygen--a clue to which activity evolved first.

The team placed the rainbow trout larvae in a box with two compartments: one for the head, where gills develop, and one for the tail. Clarice Fu, then a graduate student at the University of British Columbia in Canada, measured ion and oxygen levels at both ends of the larvae. After about 15 days, gills were exchanging more ions than the tail was. It took another 10 days or so for the same thing to happen with oxygen, the researchers report online this week in the Proceedings of the Royal Society B. To Rombough and Fu, this suggests that gills first evolved to transfer ions.

Greg Goss, a biologist at the University of Alberta in Canada, says the study has made him much more confident in the hypothesis that gills evolved to exchange ions. But he'd still like to know which genes turn on first--those involved in oxygen exchange or those involved in ion exchange. And Pung-Pung Hwang, a zoologist at the Academia Sinica in Taipei, says the team also needs to look at more-ancient fish, such as lamprey and sturgeon, as well as fish living in saltwater.

Meanwhile, the study raises concerns for the modern day, Rombough says. Industrial runoff and other pollution has filled Earth's oceans with metals that poison fish. With fish larvae relying on gills to exchange ions at just 2 weeks of age, fish may be more vulnerable to these pollutants than scientists realize. If ion exchange is blocked in fish, he says, "eventually they're just as dead as if they didn't have oxygen."

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