Flatfish eyes: The twice solved mystery

You know it's particularly mysterious when a puzzle stumps Charles Darwin and all the egghead evolutionary biologists that have come since. But, how both eyes of flatfish came to be on the same side of the head was such a bafflingly mysterious puzzle that it needed to be solved twice. By the same person.

The turbot, Psetta maxima (image Wikipedia)

In 2008, Matt Friedman was able to show that the transition to both eyes on the same side of the head was gradual. Now, in 2012, Matt Friedman has done it again and solved the mystery of the flatfish head by demonstrating that the transition to both eyes on the same side of the head was gradual. Or perhaps, in both instances the journalists overcooked the story and tried to make an interesting incremental step in our understanding of the evolution head asymmetry in flatfish into a revolution in understanding.

But, behind every popular science article beat-up of stumped boffins and puzzling riddles, there's usually some interesting science. And that's the case here. 

Flatfish are fascinating creatures. Adults live on the bottom, lying on one side, with both eyes gazing up from the same side of their head. At hatching, though, their larvae look unremarkable in comparison to other fish larvae. Their eyes are on opposite sides of their head and they swim vertically. But, late in their larval development one eye begins to migrate upwards and over the top of the head until it sits near the other eye.

Larval stages of the summer flounder Paralichthys dentatus. Each letter denotes a stage in development and 'early' and 'late' indicate the position withing the stage. The migrating eye is in grey. The migration begins during stage F, with the eye crossing the midline in stage H (image from Martinez & Bolker 2003).

Far from being stumped, several scientists put forward their explanations, including Darwin. Saltationists, such as Goldschmidt, saw it as evidence that some speciation events were the result of large mutations that revolutionised morphology. While others thought that the eye must have gradually migrated, as it does at the end of the larval period.

The evidence seems to have been more strongly in the gradualist camp. And not only because the new synthesis largely killed off the idea of saltation in evolution. It was already known that the more ancestral flatfish groups, such as spiny turbot and flounder, were less asymmetrical and less strongly associated with the bottom than the more derived groups, such as sole. The only thing that was lacking was truly smoking gun evidence.

Three species of flatfish. From top to bottom,  the spiny turbot, Psettodes belcheri, the flounder, Citharus linguatula, and the sole, Achirus klunzingeri. As you move top to bottom, the wandering eye moves further down the head (Pictures from FAO, via FishBase).

Enter Matt Friedman. He found several examples of fossilised flatfish species from two genra that were about 50 million years old. One genus, Amphistium, had been previously described, but had not been placed within the flatfish group. The other genus, Heteronectes, was previously undescribed. They were in the collections of European museums that, like most museums, had a heap of fossils that nobody had really looked at before. 

The two sides of the fossil fish Heteronectes chaneti. Note the eye on the left side (right hand image) is higher than the eye on the right (from Friedman 2012).

The reason that Amphistium had not been placed within the flatfish was that, although the eyes were not in symmetrical positions, the asymmetry was put down to distortion during fosilisation. Friedman was able to show in his 2008 Nature paper that the eye asymmetry was not as a result of distortion that that, therefore, Amphistium and Heteronectes were transitional between the symetrical ancestors and modern flatfish. 

A simplified phylogeny of flatfish showing the progression of eye migration over history. Next to each fish is a diagram of their skull from the left (top), top (middle) and right (bottom). The two rightmost fish are the modern genera Psettodes and Citharus, examples of which are shown above (image modified from Friedman 2008).

Interestingly, Amphistium and Heteronectes were alive at them same time as flatfish with the modern asymmetrical morphology. Which indicates that they aren't the direct ancestors of the modern flatfish and that the origins of flatfish are much older. This, in turn, suggests that the transitional morphology provided some advantages, since it persisted for so long in the presence of more modern eye arrangements.

The fossil flatfish Eobothus that was alive at about the same time as Amphistium and Heteronectes, but, like modern flatfish, had both eyes on the same side of its head (image the Fossil Forum).

How Heteronectes and Amphistium were so successful with one eye pointing at the bottom is not clear. However, extant species provide some clues. The less asymmetrical species spend more time hunting prey away from the bottom, where a downward pointing eye would be more useful. In addition, Friedman speculates in his 2008 paper that like many modern flatfish, Heteronectes and Amphistium may have used their dorsal an anal fins to lift their downwards facing eye into a position where it could be used. But, of course, all this assumes that lying on one side came before eye migration, which is not clear.

The European plaice, Pleuronectes platessa, using its dorsal and anal fins to lift itself off the bottom (image EOL).

Friedman's 2012 paper in the Journal of Vertebrate Paleontology, provides a much more detailed description of the morphology of Heteronectes. Because Heteronectes represents a transitional form, it may also share more characters with the common ancestor. The aim of the paper was, therefore, to use the described characters of Heteronectes to clarify the relationships between the flatfish and other groups of fish.

The analysis suggested that the Latids are the most closely related family of fish. But, Friedman cautions that his analysis was necessarily coarse. Some of the characters identified as uniquely shared by the Latids and Heteronectes may actually be general to a larger group of fish. And, because Friedman didn't examine other flatfish in the study (he must have another paper in the works), the characters identified in Heteronectes may not be shared with other flatfish.


So, two interesting papers. But, although we now know that evolution of the asymmetrical flatfish eye was gradual and, therefore, that transitional flatfish morphologies clearly were not useless, a lot of questions remain. For instance, we can only speculate about the selective pressures that drove eye migration and we don't yet know what the flatfish common ancestor looked like. 


References

Friedman, M. (2008). The evolutionary origin of flatfish asymmetry Nature, 454 (7201), 209-212 DOI: 10.1038/nature07108

Friedman, M. (2012). Osteology of †Heteronectes chaneti (Acanthomorpha, Pleuronectiformes), an Eocene stem flatfish, with a discussion of flatfish sister-group relationships The Journal of Vetebrate Paleontology, 32 (4), 735-756 DOI: 10.1080/02724634.2012.661352

Martinez, G. M. and Bolker, J. A. (2003). Embryonic and Larval Staging of Summer Flounder (Paralichthys dentatus) Journal of Morphology, 255, 162-176