How Flounder Wound Up With an Epic Side-Eye

A flounder looks like a hallucination of a fish. Its body is flat as a pancake, its head permanently tilted to one side, and instead of having one eye on each side of its head, both eyes are crowded on one side.

This anatomy, as weird as it may be, is one of evolution’s remarkable success stories. Flounder, like more than 800 other species of flatfish, lie flat on the sea floor, their two eyes gazing up at the water overhead. When a smaller fish swims by, a flatfish shoots up and strikes. One species, the Pacific halibut, can grow to the size of a barn door.

The bizarre bodies of flatfish have long puzzled biologists. In fact, Charles Darwin’s critics used it as evidence against his theory of evolution.

In “The Origin of Species,” Darwin argued that natural selection favors tiny variations. Each little increment benefited an organism. Over countless generations, he said, those increments gradually added up to large-scale transformations.

Darwin’s critics rejected the idea that such changes could actually happen. St. George Jackson Mivart, a British biologist, used flatfish as Exhibit A: It seemed impossible to him that the slow migration of the eye around the fish’s head would be advantageous at every stage along the way.

“How such transit of one eye a minute fraction of the journey toward the other side of the head could benefit the individual is indeed far from clear,” Mivart wrote in 1871. The idea that natural selection could gradually create a flatfish, he added, “seems to contradict not imagination, but reason.”

Darwin’s theory survived Mivart’s assaults, but the conundrum of the flatfish remained. For decades, scientists puzzled over what sort of ancestor they evolved from. Flounder, halibut, sole and all the other flatfishes had very similar bodies, indicating that they were closely related to one another. But they were all so strange that it was impossible to identify their closest living cousins.

The mystery began to unravel in the early 2000s, when biologists found that the closest genetic relatives of flatfish looked nothing like them. Their cousins included big, fast swimmers that spent their lives in the open ocean, including tunas, barracudas and marlins.

“That is kind of shocking,” said Ricardo Betancur-R., a marine biologist at Scripps Institution of Oceanography, who discovered the connection in 2013.

Flatfish DNA offered some clues to how the transformation happened. By counting up the mutations that flatfish and their relatives had accumulated, researchers could estimate when their evolutionary branches split apart. It turned out that flatfish and their fast-swimming cousins split not long after Earth went through a huge catastrophe 66 million years ago.

At that time, a six-mile-wide asteroid slammed into the planet and turned the sky black, wiping out over half of species both on land and in the ocean. The mass extinction opened up ecological opportunities for the survivors. One surviving lineage split apart, with some individuals finding opportunities in the open ocean and others settling on the sea floor.

Flatfish DNA looks like what you’d expect if they evolved as Darwin envisioned. Natural selection favored a series of mutations that gradually altered the body of an ordinary-looking ancestor, creating the flatfish anatomy.

Fossils are also providing glimpses into this transformation. In 2008, Matt Friedman, now the director of the Museum of Paleontology at the University of Michigan, discovered that fossils of two early species of flatfish had eyes on both sides of their heads. But one of the eyes was close to the top of the skull. The fossils documented exactly the kind of transitional form that Darwin predicted — and that Mivart claimed was impossible.

To understand how flatfish eyes changed so drastically, some biologists are watching flatfish eggs hatch and develop into adult fish. The larvae start off looking like normal fish. Only when they go through metamorphosis into adults does one eye migrate to the other side of the head. The fish then settle down on the sea floor to lie in wait for prey.

Hormones from the thyroid gland trigger larvae to go through this metamorphosis. The hormones switch on genes in the flatfish skull that cause it to change shape, helping to push one eye into a new position. Inside the eye itself, other genes stimulate the growth of neurons so that it can stay connected to the brain as it travels to a new place.

The new flatfish discoveries have provided some answers to questions about their evolution — and led to new debates. In 2021, a team of researchers in China created a new evolutionary tree of flatfish by looking at 1,700 DNA segments in 13 species of flatfish and their relatives. The researchers concluded that the flatfish body evolved twice. One of these transitions gave rise to a group of flatfish species that live in tropical oceans, known as spiny turbots, and the other transition produced all the other flatfish, including flounder.

Dr. Friedman was skeptical. All flatfish share many of the same extreme changes to their anatomy, made possible by dramatic changes to their larvae. Dr. Friedman found it hard to believe that ordinary fish would gain the bizarre flatfish body twice. “I’m pretty sure that that innovation evolved once,” he said.

Because flatfish evolved so quickly after the asteroid hit 66 million years ago, their evolutionary tree was tricky to reconstruct. Dr. Friedman tried to do so with Dr. Betancur-R. and Emanuell Duarte-Ribeiro, an evolutionary biologist at the University of Basel in Switzerland. They focused on certain DNA segments that they predicted would be more likely to provide a more accurate picture. They also expanded their analysis to compare more than 400 species of flatfish and their relatives.

Last month, the researchers reported that their new analysis pointed to just one origin of flatfish. “We’re happy to find the single origin, because it’s the simpler explanation,” Dr. Duarte-Ribeiro said. “There are so many genes that are potentially involved in this transition that it’s quite unlikely that it happened twice.”

The Chinese researchers published a response in which they stood by their results. Three members of the team did not respond to emails seeking comment.

Dr. Betancur-R. and his colleagues are now pulling together more data from flatfish DNA to see whether their finding of a single origin holds up. “That’s what I think would happen,” he said. “But it’s hard to tell, because these are difficult problems.”

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