Evolution

07
May

The Improbable—but True—Evolutionary Tale of Flatfishes

Every summer there’s a snowfall in the sea. Instead of drifting down, it falls up, and rather than flakes of ice, it’s made of innumerable diaphanous eggs that rise from the bottom of the ocean to the surface. There, they hatch into baby flatfish, each no larger than a pinhead.

For the first few weeks of life, they look and act like typical fish fry, swimming upright through sun-dappled waters, darting after plankton. Soon enough, though, these young flatfish lose all semblance of normalcy during one of the most difficult puberties of any animal on the planet. You think pimples and prom were awkward? Please.

flounder-eyes
Flatfish eyes begin in a symmetrical position before migrating to one side.

As a larval flatfish begins its passage into adulthood, it does not merely experience uneven growth spurts and mood swings. Rather, it changes from a cute, symmetrical little fish into a total anatomical disaster—like some unrecognizable object evolution made from clay in preschool and gleefully brought home to its parents, who kept it for “sentimental value.”

At the same period in our lives when the slightest blemish seems like a calamity, the flatfish is preparing to lose half of its face. The bones in its skull bend and shift as one eye forces its way to the opposite side of the head. Its whole body begins to tip over, so it has to swim at an angle. One of its flanks turns a sickly pallor; the other becomes colorfully flecked, matching the speckled sand on the seafloor. Eventually, when it is large enough, the transformed flatfish sinks and settles on its newly blind side. It is now a young adult bottomfeeder with two eyes on the same side of its head, a contorted mouth, and one fin squashed against the sand. It will spend the rest of its life this way.

“Flatfish are the most asymmetrically-shaped vertebrate to ever live on earth,” says Alexander Schreiber, a flatfish expert at St. Lawrence University. “It sounds likes a really dramatic thing to say, but as far as vertebrates go, it’s true.”

Evolutionary biologists have long struggled to explain the flatfish’s curious, asymmetrical anatomy. The prevailing story has been that modern flatfish evolved from bilateral fish, which—like goldfish and most familiar species—have right and left sides that mirror one another. But why did flatfish become flatlanders in the first place? And how does a young flatfish have the audacity to reject the manner of locomotion favored by the vast majority of fish in the ocean? Somehow, its brain ditches everything it once knew about how to swim in the open water and decides that, actually, the right thing to do is to lie sideways on the seafloor forever. Talk about cognitive dissonance.

In the past decade, biologists have hit upon some of the answers. In the process, they’ve come to realize that the flatfish is even stranger than they previously realized—an asymmetrical anomaly from the inside out.

Finned Freaks

People have been interested in flatfish for thousands of years—primarily as food. Most modern scientists who study this diverse family—which includes halibut, soles and flounders—are interested in farming the fish more efficiently. But since the time of Charles Darwin, a handful of biologists have become fascinated with the flatfish for an entirely different reason: its unique evolutionary history.

Creationists have long pointed to the finned freak as certain proof of evolution’s implausibility. If the flatfish evolved from bilateral ancestors with one eye on either side of their heads, how did it survive during its facial reconstruction, they asked, and where were the fossils to prove it? Darwin worried that the relative scarcity of such transitional fossils would doom his theory.

One of Darwin’s most vehement critics was the English zoologist St. George Jackson Mivart, a conflicted Catholic who vacillated between accepting and decrying natural selection. In his 1871 publication On the Genesis of Species, Mivart wielded the flatfish like a weapon to bludgeon Darwin’s ideas. Regarding the evolutionary origins of the flatfish’s wandering eye, Mivart wrote:

…the accidental occurrence of such a spontaneous transformation is hardly conceivable. But if this is not so, if the transit was gradual, how such transit of one eye a minute fraction of the journey towards the other side of the head could benefit the individual is indeed far from clear. It seems, even, that such an incipient transformation must rather have been injurious.

More than 130 years later, paleobiologist Matt Friedman, now at Oxford University, identified exactly the type of fossils Darwin had in mind. In the late 2000s, Friedman reexamined 45-million-year-old fish fossils that other researchers had dredged up from Monte Bolca, an ancient petrified coral reef in Italy. No one thought these fossils were related to flatfish. Using CT scans, however, Friedman took a much more detailed look at the fishes’ skeletons and showed that they were in fact primitive adult flatfishes with asymmetrical skulls and one eye only halfway through its evolutionary journey across the face.

Scientists now had tangible evidence that flatfish did, in fact, gradually evolve from bilateral ancestors. Yet several fundamental conundrums remained. Namely, why did these animals abandon their previously symmetrical situation in life? And how does an individual larval flatfish grow comfortable with going all cattywampus?

Schreiber is getting close to solving the latter puzzle. He began by studying how fish maintain a sense of direction. Two organs—the eyes and inner ears—work together to keep typical fish in an upright swimming posture, Schreiber explains. If the eyes are not receiving the same amount of light on each retina, chances are the fish is leaning one way or the other, so retinal neurons trigger the brain to tilt the entire animal and set it straight. But the brain also listens to what the inner ears have to say. When clumps of calcium known as otoliths (literally “ear stones”) roll over sensitive hairs in the inner ear in one direction, they trigger those hairs to send neuronal impulses; when otoliths roll over the hairs in the other direction, they muffle the hairs. As a fish’s vertical orientation in water changes, the brain combines information from the eyes and ears to figure out which way is up.

OLYMPUS DIGITAL CAMERA
With its left eye perched atop its head, this larval flatfish appears to be midway through its metamorphosis.

Based on his research, Schreiber thinks that although larval flatfish look and behave like ordinary symmetrical fish, they are essentially hardwired as asymmetrical freaks. Scientists have gathered preliminary evidence, for example, that one half of the brain region receiving input from the inner ears is more active than the other and that otoliths are larger in one ear than another. Schreiber has also studied some flatfish “morphant” larvae that, for unknown reasons, swim on one side practically from birth, even though they are just as anatomically symmetrical as their peers. Similarly, flatfish larvae that are deliberately blinded adopt a sideways swimming posture. All of this suggests that, from a very young age, the flatfish’s inner ears somehow begin to overrule the eyes until they become the sole organ telling the flatfish how to orient itself.

In some of his most recent experiments, Schreiber discovered something astonishing that confirmed these suspicions. In the dark, goldfish and other bilateral fish have no trouble staying in an upright position because they can rely on their inner ears, even when their eyes cannot see much of anything. Schreiber wondered if the same was true for flatfish, so he filmed typically developing larval flatfish in pitch darkness with infrared cameras—something no one had ever done before. In the absence of visible light, the baby flatfish were incapable of staying upright. Depending on their stage of metamorphosis, they either bobbed in the water with noses pointed down, as though weighted by lead, or they leaned over and drifted to the bottom of the tank like a falling leaf, landing on the same side every time—the one that would eventually become blind.

“I didn’t know what to expect,” Schreiber says. “I wanted to show that larval flatfish before metamorphosis were like goldfish, but lo and behold—Holy cow!—they are different from the get go. They are just masquerading as normal fish.”

Evolution’s Exemplars

The early dominance of the inner ears may explain how a young individual flatfish learns to stay grounded, but there’s still the question of why ancient flatfish flopped over in the first place. Did a mutation cause one of their eyes to wander, throwing off their balance and forcing them to swim askance? Or did one eye begin migrating to accommodate a new lifestyle at the bottom of the sea? Friedman and Schreiber think that the flatfish’s anatomical makeover followed a change in its behavior. When threatened, some modern fish are known to lie flat on their side on the seafloor and briefly bury themselves in the sand. Others tip over to play possum, only to leap up and snatch unsuspecting prey. Perhaps the flatfish’s predecessor was a bilateral open water fish particularly adept at this kind of stealth. And perhaps it was so successful that it made rock bottom its permanent home.

Jennifer Specker, a flatfish expert at the University of Rhode Island who has worked with Schreiber in the past, agrees with this line of reasoning. “One of the guesses we make is that there was not a lot of competition for early lie-and-wait predators on the bottom of the ocean,” she says. “It seems that habitat was a vacuum, and nature abhors a vacuum, so flatfish adapted to it.”

spotted-turbot
On this spotted turbot, you can see its sideways mouth and upright fin.

Spending so much time in that lowly position would inevitably have damaged one eye—not to mention wasting its visual powers. So ancient flatfish with eyes even a little closer together would have had a better chance of avoiding their predators’ bellies while still filling their own. Modern adult flatfish are both excellent camouflagers and insatiable predators, waiting patiently for the chance to pounce on their prey by flipping themselves up with their concealed pectoral fin and a jet of water expelled from their gills. From their new perch, the flatfish’s constantly swiveling eyes provide 360 degree vision.

On top of the unabashed asymmetry of an individual flatfish, there’s a whole extra level of lopsidedness among the entire population of flatfishes in the ocean. Different life stages inhabit very different regions of the ocean ecosystem. Just as metamorphosis has proved an enormously successful strategy for insects—separating larvae and adults so they do not compete for resources (think: nectar-slurping butterflies vs. leaf-munching caterpillars)—flatfish larvae have clung to the vestiges of symmetry in order to distance themselves from their parents. The young ‘uns need to swim upright to catch plankton near the surface of the ocean. Were they to remain at the seafloor where they hatched, they would surely be vacuumed up by a roving sideways pair of lips—perhaps even by their own parents.

Flatfish larvae require light to swim upright, so when the lights go off, they swim erratically.

Flatfish may be genuine anatomical anomalies—rebuffing nature’s devotion to symmetry—but they did not somehow evade natural selection, nor are they a counter-argument to Darwin. Quite the contrary. Flatfish are exemplars of evolution at work.

Evolution is capable of producing a wonderfully streamlined, symmetrical bottom-feeding fish: we know them as skates and rays. Stingrays and the like have pancake thin bodies oriented in a way that makes sense to us—bellies and mouths on their undersides, eyes and snout on top. But evolution did not engineer them that way on purpose. There are no deliberate designs in nature—only tenacious tinkering, marvels of serendipity, and perseverance despite frequent mishaps. When an organism’s circumstances change and demand a completely different body, evolution cannot go back to the drawing board. Instead, it works with what it has. If survival requires turning a symmetrical creature into a mish mash that looks like it was sewed together by Dr. Frankenstein, so be it. It’s weird, but it works.

And that is what biologists love about the fish—their functional freakiness. “I’ve always been drawn to really weird things different from what other people like,” Schreiber says. “If everyone is studying fruit flies and zebrafish, I’ll be damned if I am going to study them. Flatfish are just so cool. If you were to imagine what kind of fish Picasso would paint, it would be the flatfish.”