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The First Breath

Gogonasus

Gogonasus, the 380-million-year-old fossil sarcopterygian fish from Gogo in Western Australia, had large spiracles on its head to enable it to breathe air. Illustration: Brian Choo

By John Long

The African reedfish Polypterus has revealed how breathing first evolved in terrestrial animals, and perhaps how the structures of the ear first formed.

A 100-year-old controversy in science has recently been solved by a team of fish physiologists at the Scripps Institute of Oceanography in San Diego after careful observation of various species of African reedfishes (Polypterus) in controlled laboratory conditions. As a result, we now know more about how our ancient fish ancestors first began to breathe air and, perhaps surprisingly, how we developed our capacity to hear.

Because Polypterus is one of the most primitive of all the living bony fishes (Osteichthyes), I was asked to help out by comparing what the researchers found with other ancient fishes. The results were published in Nature Communications on 23 January 2014.

But the story really begins with Napoleon’s crushing defeat by the British at Alexandria in 1801. While the two navies were squaring off, one of Napoleon’s appointed naturalists, Etienne Geoffrey Saint-Hillaire, was busy studying a new kind of strange and primitive-looking fish that dwelt in the Nile. When things turned sour for the French, he had to conclude his work rapidly and he brought his specimens of the fish back to France with him.

He named the fish Polypterus, meaning “many fins”. It had robust fleshy limbs like the coelacanths, which are related to the Queensland lungfish. Saint-Hillaire thought Polypterus to be living relicts related to an extinct line of fossil fishes that were anatomically very close to amphibians. Naturally this caused a huge stir back in Europe.

The  evolution of the spiracle in early fossil fishes. Credit: John Long

Later research confirmed that it was one of the ray-finned fishes (Actinopterygii), the group to which most fishes today belong, but it belongs in a very primitive group that diverged from most modern fishes back in the Devonian at least 380 million years ago.

The huge interest in this fish as a possible “living fossil” caused much excitement among the naturalists of the day, and several expeditions tried to find more specimens to study. Englishman John Budgett failed to find the fishes on three expeditions, but finally met with success in 1903, only to die from black fever on his return to the motherland. Before his death he wrote a short paper in which he observed that these fishes could breathe air through holes on top of their heads, making a loud sucking noise when they surfaced to breathe.

Belgian researcher George Albert Boulenger made many observations on Polypterus in a paper published in 1907, but failed to confirm that it was breathing through the holes on the top of its head called spiracles. Much later, in 1966, Ahmed Mohamed Magid of the University of Khartoum published several experiments with Polypterus under differing environmental conditions from which he concluded that they breathed in air through the spiracles when water was low in oxygen, or after high metabolic activity.

The last word on the subject seemed to come in 1989 when a team of American physiologists led by Elizabeth Brainerd concluded adamantly in a paper in Science that polypterids “do not, as others have suggested, breathe through the spiracles”.

The late Jeffrey Graham, who worked at Scripps in California, was a leading expert on the physiology of air-breathing fishes. His landmark 1997 book on the subject is still widely used today. He wanted to solve this mystery once and for all, so he set his student Nick Wegner to test the hypothesis.

Nick went out and bought some Polypterus at a pet shop and put them in a tank with a camera to observe and record them. He noticed that when he approached the camera, the fish moved away from the surface waters as if scared off by the intrusion of a potential predator. To counter this he built a blind around the camera to isolate it from any suspicious movements perceived by the fish.

After 360 hours of observation of four species of polypterid, the evidence proved beyond doubt that these fish, when relaxed in laboratory conditions, took in up to 93% of all their air through their spiracles and the rest through their mouths.

The significance of this is that modern lungfishes, which also breathe air directly from the atmosphere into their lungs, do so through their mouths, as do all amphibians, reptiles, birds and mammals like us. As a result, it was always assumed that breathing must have originated in our distant ancestors in this way. But if primitive living fish like Polypterus breathe mostly through the top of the head using their spiracles, then this structure might also have played a role in the evolution of how fishes evolved into land animals (tetrapods).

In the Nature Communications paper I made comparisons with several ancient fossil fishes that have large spiracles on top of the head, and concluded that these must also have been used for breathing. The ability to breathe air though the spiracles is clearly seen in ancient fish like Gogonasus and Tiktaalik, both of which have very large open spiracles on top of the head. Early amphibians like Acanthostega and Ventastega also have big spiracles.

But the spiracular canal first used for breathing in these ancient fishes and tetrapods no longer had a use when the fishes finally left the water and evolved into fully terrestrial animals, the early amphibians. These creatures began breathing through their nose and mouth, as we do today. Their rib cages became more flexible and costal breathing took over.

But the spiracular canals then became useful to transmit sound from the outside world to the brain via the ear. The canal eventually became smaller and transformed into the Eustachian tube, and the remnant spiracle cover is now the tympanum or ear drum. This later sank deeper inside the ear in more advanced reptiles and mammals.

It has long been known that the stapes, incus and malleus of our human inner ear are three tiny bones that enable us to hear. They are derived from the larger hypomandibular, articular and quadrate bones, which originally served to brace the upper and lower jaw joints in the prehistoric bony fishes.

Thus the link from reedfishes that breathe through the tops of their heads back to their 380-million-year-old fossil ancestors, and from them back to us, is the very reason we have such a refined sense of hearing.

Professor John Long is Strategic Professor in Palaeontology at Flinders University’s School of Biological Sciences.