Some Assembly Required

Breath of Fresh Air
 
When Napoleon Bonaparte invaded Egypt in 1798, he brought more than ships, soldiers, and weapons with his army. Seeing himself as a scientist, he wanted to transform Egypt by helping it control the Nile, improve its standard of living, and under­stand its cultural and natural history. His team included some of France’s leading engineers and scientists. Among them was Étienne Geoffroy Saint-Hilaire (1772–1844).
 
Saint-Hilaire, at twenty-six, was a scientific prodigy. Already chair of zoology at the Museum of Natural History in Paris, he was destined to become one of the greatest anatomists of all time. Even in his twenties, he distinguished himself with his ana­tomical descriptions of mammals and fish. In Napoleon’s retinue he had the exhilarating task of dissecting, analyzing, and nam­ing many of the species Napoleon’s teams were finding in the wadis, oases, and rivers of Egypt. One of them was a fish that the head of the Paris museum later said justified Napoleon’s entire Egyptian excursion. Of course, Jean-François Champol­lion, who deciphered Egyptian hieroglyphics using the Rosetta Stone, likely took exception to that description.
 
With its scales, fins, and tail, the creature looked like a standard fish on the outside. Anatomical descriptions in Saint-Hilaire’s day entailed intricate dissections, frequently with a team of art­ists on hand to capture every important detail in beautiful, often colored lithographs. The top of the skull had two holes in the rear, close to the shoulder. That was strange enough, but the real surprise was in the esophagus. Normally, tracing the esophagus in a fish dissection is a pretty unremarkable affair, as it is a simple tube that leads from the mouth to the stomach. But this one was different. It had an air sac on either side.
 
This kind of sac was known to science at the time. Swim bladders had been described in a number of different fish; even Goethe, the German poet and philosopher, once remarked on them. Present in both oceanic and freshwater species, these sacs fill with air and then deflate, offering neutral buoyancy as a fish navigates different depths of water. Like a submarine that expels air following the call to “dive, dive, dive,” the swim bladder’s air concentration changes, helping the animal move about at vary­ing depths and water pressures.
 
More dissection revealed the real surprise: these air sacs were connected to the esophagus via a small duct. That little duct, a tiny connection from the air sac to the esophagus, had a large impact on Saint-Hilaire’s thinking.
 
Watching these fish in the wild only confirmed what Saint-Hilaire inferred from their anatomy. They gulped air, pulling it in through the holes in the back of their heads. They even exhib­ited a form of synchronized air sucking, with large cohorts of them snorting in unison. Groups of these snuffling fish, known as bichirs, would often make other sounds, such as thumps or moans, with the swallowed air, presumably to find mates.
 
The fish did something else unexpected. They breathed air. The sacs were filled with blood vessels, showing that the fish were using this system to get oxygen into their bloodstreams. And, more important, they breathed through the holes at the top of their heads, filling the sacs with air while their bodies remained in the water.
 
Here was a fish that had both gills and an organ that allowed it to breathe air. Needless to say, this fish became a cause célèbre.
 
A few decades after the Egyptian discovery, an Austrian team was sent on an expedition to explore the Amazon in celebra­tion of the marriage of an Austrian princess. The team collected insects, frogs, and plants: new species to name in honor of the royal family. Among the discoveries was a new fish that, like any fish, had both gills and fins. But inside it also had unmistakable vascular plumbing: not a simple air sac, but an organ loaded with the lobes, blood supply, and tissues characteristic of true human-like lungs. Here was a creature that bridged two great forms of life: fish and amphibians. To capture the confusion, the explorers gave it the name Lepidosiren paradoxa—Latin for “paradoxically scaled salamander.”
 
Call them what you will—fish, amphibian, or something in between—these creatures had fins and gills to live in water but also lungs to breathe air. And they weren’t just one-offs. In 1860 still another fish with lungs was discovered in Queensland, Aus­tralia. This fish also had a very distinctive set of teeth. Shaped like a flat cookie cutter, such teeth were known from the fossil record from a species that was long extinct—an animal named Ceratodus found in rocks over 200 million years old. The impli­cation was clear: lunged, air-breathing fish were global and had been living on Planet Earth for hundreds of millions of years.
 
An aberrant observation can be a game changer for how we see the world. Fish lungs and swim bladders spawned a gen­eration of scientists interested in exploring the history of life by looking both at fossils and at living creatures. Fossils show what life looked like in the distant past, and living creatures reveal how anatomical structures work, as well as how organs develop from egg to adult. As we’ll see, this is a powerful approach.
 
Linking studies of fossils and embryos was a fruitful area of inquiry for the natural scientists who followed Darwin. Bash­ford Dean (1867–1928) had an unusual distinction in academic circles—he is the only person ever to hold a curatorship at both the Metropolitan Museum of Art and, directly across Central Park, the American Museum of Natural History. He had two passions in life, fossil fish and battle armor. He founded the armor collection and displays at the Met, and he did the same for the fish collection at the Museum of Natural History. Befit­ting a person with such interests, he was a quirky individual. He designed his own armor and even took to wearing it on the streets of Manhattan.
 
When he wasn’t donning medieval faulds, Bashford Dean was studying ancient fish. Somewhere locked inside the embryo’s transformation from egg to adult, he believed, were answers to the mysteries of history and the mechanism of current fish’s descent from ancestral species. Comparing fish embryos with fossils and reviewing the work in anatomy labs at the time, Dean saw that lungs and swim bladders look essentially the same during development. Both organs bud from the gut tube and both form air sacs. The major difference is that swim bladders develop on the top of the tube, near the spine, while lungs bud from the bottom, or belly side. Using these insights, Dean argued that swim bladders and lungs were different versions of the same organ, formed by the same developmental process. Indeed, some kind of air sac is present in virtually all fish but sharks. Like many ideas in science, Dean’s comparison has a long history. Its antecedents can be seen in the work of nineteenth-century Ger­man anatomists.
 
But what do air sacs say about Mivart’s critique and Darwin’s response?
 
A surprising number of fish can breathe air for extended peri­ods of time. The six-inch-long mudskipper can walk and live on the mud for over twenty-four hours. The aptly named climbing perch can wiggle from pond to pond as needed, sometimes even climbing branches and stepping over twigs in the process. But that perch is only a single species. Hundreds of species can gulp air when the concentration of oxygen in the water they inhabit declines. How do these fish do it?
 
Some, like the mudskipper, absorb oxygen through their skin. Others have a special gas-exchange organ above their gills. Some catfish and other species absorb oxygen through their guts, gulping air like food, only to use it to breathe. And a num­ber of fish have paired lungs that look like our own. Lungfish live in water and breathe with their gills most of the time, but when the oxygen content of their stream is not sufficient to sup­port their metabolism, they will push to the surface and gulp air into their lungs. Air breathing is not some crazy exception in an oddball fish—it is the common state of affairs.
 
Recently, researchers at Cornell University revisited the com­parison of swim bladders to lungs, using new genetic techniques. Their question: What genes help build fish swim bladders dur­ing development? In looking at the catalog of genes that are active in fish embryos, they found something that would have pleased both Dean and Darwin. The genes that are used to build swim bladders in fish are the same ones used to make lungs in both fish and people. Having an air sac is common to virtually all fish; some use them as lungs, while others use them as buoyancy devices.
 
Here is where Darwin’s answer to Mivart becomes so pre­scient. DNA clearly shows that lungfish, Saint-Hilaire’s bichirs, and other fish with lungs are the closest living fish relatives to land-living creatures. Lungs aren’t some invention that abruptly came about as creatures evolved to walk. Fish were breathing air with lungs well before animals ever stepped onto terra firma. The invasion of land by descendants of fish did not originate a new organ—it changed the function of an organ that already existed. Moreover, virtually all fish have some kind of air sac, whether lung or swim bladder. Air sacs shifted from being used for a life in water to later enabling creatures to live and breathe on land. The change did not involve the origin of a new organ; instead the transformation was, as Darwin said more generally, “accompanied by a change of function.”