'Missing link' flatfish has eye that's moved halfway across its head

Imagine watching a movie where every now and then, key frames have been cut out. The film seems stilted and disjointed and you have to rely on logic to fill in the gaps in the plots. Evolutionary biologists face a similar obstacle when trying to piece together how living species arose from their common ancestors. It's like watching a film with a minimum of footage; the species alive today are just a few frames at the very end, and the fossil record represents a smattering of moments throughout the film's length.

But the gaps, while plentiful, are being slowly filled in. With amazing regularity, new fossils are being unearthed that bridge the gap between existing specimens. These "transitional fossils" are always greeted with great relish for their intermediate nature provides yet more examples of gradual evolution from one form to another. They act as handy visual aids for explaining the story of evolution to those with a dearth of imagination.

Now, Matt Friedman from the University of Chicago has described a new transitional fossil that is one of the most dramatic yet. Its name is Heteronectes (meaning "different swimmer") and it's a flatfish, but not as you know it.

You've probably eaten flatfish before but tasty fillets of plaice, sole or halibut give few hints about their extraordinary physical specialisations. They are fish that live on their sides and their flat profiles make them both efficient hunters and difficult prey. For other fish, lying sideways would give one eye a useless view of sand but flatfish have adapted accordingly. Their fry resemble those of other fish but as they grow, one of their eyes makes an amazing journey to the other side of its head. The adults look like they've swum out of a Picasso painting.

But Heteronectes is a half-committed flatfish. Like modern representatives, its skull is asymmetrical and one eye has begun migrating to the other side of its head. But it hasn't made it all the way round and stops near the midline without crossing to the other side. No living flatfish has eyes arranged in such a way. We couldn't have wished for a better intermediate form - it's a marvellous missing link between the standard fish body plan and the distorted visages of flounders and soles.

Settling the debate

The discovery of a transitional flatfish is particularly poignant because the group's grotesque faces have fuelled a significant amount of evolutionary debate. In The Blind Watchmaker, Richard Dawkins views the displaced eye as a perfect example of adaptation, an extraordinary solution to the problems posed by life on your side. But opponents of evolution have long viewed the flatfish's shifted face as proof against gradual adaptation, for what would be the point of a half-migrated eye that would still be facing into the sand?

Darwin himself was somewhat stymied by flatfish, and proposed an explanation with shades of Lamarckism - the mostly discredited idea that organisms can inherit traits that their parents acquired during their lifetimes. Robert Goldschmidt claimed the flatfish's eye as evidence for his "Hopeful Monster" hypothesis, which suggested that some features evolved extremely suddenly, bypassing the need for any intermediary forms. But Heteronectes quashes both these hypotheses and confirms that the deformed body plan of modern flatfish developed at a gradual, step-wise tempo.

Friedman also studied another intermediate flatfish called Amphistium which hailed from the same region of northern Italy.  Palaeontologists had previously dismissed Amphistium's resemblance to modern flatfish but by bringing modern scanning technology to the fore, Friedman has confirmed its membership within the group. What's more, Amphistium's asymmetrical skull, like that of Heteronectes, bears an eye that has only migrated halfway across its head.

Could these fossils simply be juvenile flatfish whose eyes haven't finished their migration? Not according to Friedman, who offers three lines of evidence to refute this interpretation. In living flatfish, the eye starts to migrate when the fry hit a centimetre or so in length, and all the known specimens of Amphistium and Heteronectes are more than ten times as long. Their skulls have completely hardened, which only happens in adult flatfish once their eyes have stopped moving. And even though specimens of Amphistium have a wide range of lengths, all of their eyes have the same alignment.  The fossils are the remains of adults.

Nor is it likely that Amphistium and Heteronectes belong to different groups of fish whose skulls have been crushed and distorted. In the Heteronectes fossil, the areas around the eyes are obviously asymmetrical but they show no signs of twisting damage and other parts of the skull have not been deformed. Their fins and tails bear features that are trademarks of the flatfish dynasty but some of these are only found in the group's most primitive member - the spiny turbot.

The spiny turbot shares another trait with Amphistium - both species are ambivalent in their asymmetry and have both right-sided and left-sided individuals. Other modern flatfish have a dominant side, and that strongly suggests that Amphistium and Heteronectes are not advanced flatfish whose eyes happen to have reverted to a state of incomplete migration. They are indeed ancestral members of the group and they site outside the lineage that includes modern species.

Life on your side

In the light of such dramatic fossils, asking about the point of half-migrated eyes isn't going to make evolution's proponents to lose much sleep. It's intuitive to suggest that such organs would be useless, but the point is moot when they clearly existed! But it's still an interesting question - how did Heteronectes cope with an eye that, while displaced, would still have had an eyeful of sand?

Friedman suggests that Heteronectes could have propped itself up by using its dorsal fin, so that its head was lifted just high enough above the surface to give it a view. That's a speculative guess, but it's not a wild one - modern flatfish can do the same trick, and both Heteronectes and Amphistium had even longer bony rays in their dorsal fins.

And what initially compelled a vertically flattened fish to start lying on its side? The prevailing theory is that it provided them with a perfect posture for springing an ambush. It's a hypothesis that neither Heteronectes nor Amphistium is in a position to confirm or deny. But at the very least, it's clear that Amphistium was a hunter of other fish, for one fossil contains the remains of a smaller fish inside its stomach. Perhaps other missing links will provide even more answers.

For more on flatfish, including a much deeper look at the history of the debate, have a look at the peerless Carl Zimmer over at Discover Blogs.

Images: courtesy of Nature

Reference: doi:10.1038/nature07108