How the Pufferfish Got Its Puff

By Carl Zimmer|Monday, September 01, 1997
The puzzle--and joy--of evolutionary biology is to find the lost paths that life took to arrive at the strange forms it has today. Take, for example, the pufferfish. At first sight, it seems miserably adapted to the tropical waters where it makes its home: it is an unassuming, small fish, so slow you can easily catch it by hand. But when a predatory fish or bird attacks, a pufferfish goes through a unique transformation: it rapidly gulps water and swells into a huge, spiky, hard-shelled ball three times its normal size. How could anything like this evolve from an ordinary fish?

Given that fossils are too scant and scrappy to offer any clues, biologists have been reluctant to hazard a guess. But fossils aren’t the only way to reconstruct evolutionary history. In the past few years researchers have learned much about how pufferfish puff and have found some striking similarities in the behavior of their relatives. They’ve discovered that pufferfish are yet another example of a surprisingly common pattern in evolution: features that look like radically new innovations turn out to be, on a fundamental level, a matter of minor tinkering.

Pufferfish belong to an order of fishes known as Tetraodontidae. These tropical fish include the pufferfish’s closest relatives, species like triggerfish and tripodfish. Using the evolutionary tree of pufferfish and their relatives illustrated on this page, you can trace the development of the pufferfish’s unique anatomy. And, according to Peter Wainwright, a Florida State University biologist, along the way you can see how the remarkable trait of pufferfish inflation was created out of nothing more than coughing.

Before the tetraodontiforms branched away, they probably resembled the sunfish that Wainwright studies in his lab. We often feed them earthworms, and earthworms have this slimy mucus on them. After eating a couple of earthworms, every sunfish I’ve seen will pause--and it’s almost as if you see it going, ahem, ahem--and it’ll cough up a bunch of this mucus that has gotten entangled in its gills. Wainwright has made a careful study of the muscle activity patterns in fish and can make out the timing of individual muscles down to less than a thousandth of a second. Fish, he has found, typically cough by closing off the gill slits through which the water would normally flow and then compressing the cheeks inward. The increase in pressure expels the water in the mouth cavity and whatever gunk may be floating in it.

The first tetraodontiforms to branch away on their own were probably much like today’s tripodfish. Wainwright has found only minor changes among them associated with coughing: their mouths (which are smaller than those of other fishes their size) open wide for a fifth of a second--letting more water rush in--before they close their gills and squeeze their cheeks in. As minor as these changes may be, the smaller mouth has a strong effect on the flow of water in a cough. If you exhale the same volume of water through a small aperture, you get a more directed, controlled flow, which can be aimed and which has a higher velocity, says Wainwright.

Tripodfish don’t take advantage of this jet of water, but if you take another step along the tree, you find a group of fish--triggerfish and their close relatives--that do. Wainwright first encountered their skill while scuba diving in the Caribbean. I noticed that triggerfish will attack sea urchins by grabbing one by a single spine, lifting the animal off the bottom, ducking under the animal, and then blowing at it to turn it over. In this way the fish expose the soft, fleshy underside of the urchin that they then tear into. These spurts can be aimed at other targets as well. Two other species of triggerfish I’ve seen in Hawaii eat by exposing invertebrates in the sand by shooting these jets of water, says Wainwright.

Yet as different as coughing and water-blowing may seem, Wainwright can find only one difference associated with the change from one to the other. During water-blowing, the muscles compressing a triggerfish’s cheekbones squeeze a little harder and for a longer time; otherwise the complex pattern of muscle contractions is the same. There’s no reason the tripodfish can’t blow water, but they don’t, says Wainwright. I’ve worked on tripodfish and I’ve tried everything I could to seduce them into a situation where a blowing behavior would be useful, and they would never do it.

The next step along the tree carries the ancestors of pufferfish past the point where they branched away from the triggerfish lineage. It was at this stage of their evolution that they gained the ability to inflate themselves. Pufferfish typically pump themselves up by taking 35 gulps or so in the course of 14 seconds. Each gulp draws in a big load of water thanks to some peculiar anatomic changes in their muscles and bones. Most fish, for example, have shoulder bones that anchor firmly to the back of their head, but in pufferfish the connection is hinged. When a pufferfish opens its mouth, it can therefore rotate its shoulders back and increase the size of its mouth cavity, pulling in even more water. Once a pufferfish has taken in water, its gill slits clamp shut and a powerful valve flips up over the inside of its mouth, acting as a seal. Now when the pufferfish compresses its mouth cavity, the water flows down its esophagus rather than out its gills or mouth.

Elizabeth Brainerd, a biologist at the University of Massachusetts at Amherst, has recently shown that a pufferfish’s stomach is an exquisite water balloon. As water pours into it, the stomach expands to 100 times its normal volume. The ribs that might get in the way of this expansion are missing in pufferfish. The stomach expands easily into the abdominal cavity, which is lined with folded tissue that opens like accordion pleats. Pufferfish skin is also uniquely suited for ballooning. It is made of wavy fibers that straighten out as the fish inflates, allowing the skin to expand. As the skin expands, it engulfs the fish’s tail and fins, forming a nearly perfect sphere. When the wavy fibers finally pull tight, they suddenly become hard, giving the pufferfish a tough shell that predators have a hard time penetrating. And some species of pufferfish have spines anchored in these fibers; normally the spines lie flat on the fish’s body, but when the fibers are pulled taut, the spines flip up.

Certainly many of these features must have arisen with the first pufferfish, since their close triggerfish relatives lack them. But by measuring the muscle activity in pufferfish, Wainwright has found that the way they fill their stomachs isn’t an out-of-the-blue innovation. It’s really just a modest modification of water-blowing, which is in turn just a minor variation on coughing. There is one minor muscle-activation difference between inflation behavior and water-blowing, he explains. During water-blowing the muscle that’s used to open the mouth opens really early and stays open through the compressive stage, because you want to keep the mouth open the whole time so water can be shot out. But in inflation you want to close the mouth. So that muscle’s not open very long. That’s the single difference. Otherwise the sequence is the same.

Wainwright sees the origin of pufferfish puffing as less of a huge leap across the evolutionary landscape than an easy stroll. It probably wouldn’t take much experimentation with water-blowing for an animal to discover that it could make itself a bit larger and tougher by swallowing a few mouthfuls of water, Wainwright says. Being a bit larger and tougher would also tend to make puffers a bit less likely to be eaten, and natural selection would eventually have shaped their current form, making their stomachs and skin more elastic, shrinking their ribs, and facilitating the growth of spines.

From coughing to water-blowing to inflating, the anatomy and behavior of the pufferfish lineage have been dramatically refashioned by evolution, but the sequence of nerve impulses that control these traits has barely changed. This is the third time in my career that I’ve discovered that the thing we’re looking at involves many morphological changes, not the muscle activity pattern, says Wainwright. And he’s not alone: Other researchers have found cases in which evolution holds on to an old neuromuscular pattern while changing part of the body it controls, thus creating a new behavior. Birds, for example, fire some of their shoulder muscles in much the same pattern as reptiles. The pufferfish is not simply a marine oddity. It’s living proof of the beautiful subtlety and economy of natural selection.
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