The Mysterious Origin of the Wandering Eye

tags: , , , , , , ,

During the development of extant flatfishes, such as this plaice, Pleuronectes platessa, one eye has migrated round the head to lie on the same side as the other. So these fishes have an 'eyed' (up) side and a 'blind' (down) side suitable for their bottom-dwelling lifestyle.

Image: KÃ¥re Telnes.

Flounder, turbot, sole, halibut and plaice (pictured above) are more than just a tasty slab of flesh on your plate. They are flatfishes that spend their adult life lying with one side flat on the seabed, while the other side faces up and is camoflaged, so the fish can lie motionless for hours, waiting for a tasty morsel to swim by. When this happens, the flatfish lunges upwards and suddenly opens its mouth to vacuum the hapless fish inside. Since flatfish spend all their adult lives with one side up and the other side facing the seafloor, they have evolved several morphological adaptations, such as having both eyes located on one side of their head, giving them a sighted (up) side and a blind (down) side. But flatfish are not born with both eyes on one side of their heads, so how do they end up that way? How did this asymmetrical character first evolve? Even Charles Darwin, one of the co-discoverers of the theory of evolution by natural selection, was baffled by what he referred to as this "remarkable peculiarity" of flatfish morphology.

Flatfishes are born with one eye on each side of their head, but undergo larval metamorphosis where one eye migrates to the other side of the fish's head late in larval development, producing asymmetrical juvenile fishes. By the time the skull is fully ossified, the eyes are permanently fixed in place.

But there are no known transitional fossils with only partially displaced eyes that would link these asymmetrical flatfishes with their symmetrically shaped relatives. This lack of transitional fossils has been the source of tremendous scientific controversy regarding whether this asymmetry evolved gradually or through a sudden evolutionary leap that produced "hopeful monsters," as originally described by geneticist Robert Goldschmidt in the 1930s.

Of course, creationists have entered the fray as well; seizing upon this curious morphological feature as part of their argument against evolution, they insist that the flatfishes' wandering eye could not have evolved gradually through natural selection because there is no apparent evolutionary advantage to a fish with a slightly asymmetrical skull that still retained eyes on opposite sides of its head. Further, they say that no fish fossils have ever been discovered with a wandering eye that had gotten "stuck" in an intermediate position on the fish's head.

Until now, that is.

Graduate student Matt Friedman, who is on the Committee on Evolutionary Biology at the University of Chicago and who is also a member of the Department of Geology at the Field Museum, was describing and naming a new genus of fossilized fish, Heteronectes. He was comparing this new genus to another similar primitive fish fossil, Amphistium, that had first been described two centuries ago, and made a startling discovery.

He noticed that adults from both fossil genera possessed features that are intermediate between modern flatfishes and their primitive symmetrical relatives, particularly the partial displacement of one eye -- an intermediate condition predicted by evolutionary biologists for a transitional flatfish fossil, or "missing link".

"What we found was an intermediate stage between living flatfishes and the arrangement found in other fishes," said Friedman, adding that these two fossil fishes "indicate that the evolution of the profound cranial asymmetry of extant flatfishes was gradual in nature."

How did Amphistium and Heteronectes see? As modern flatfishes so often do today, these transitional forms probably lifted their bodies partially off the seafloor with their elongated dorsal and pectoral fins, which would provide a greater range of vision for their lower eye.

Curious to learn whether this misplaced eye was a freak accident in a few specimens or was a common feature of these groups, Friedman traveled to many of the great natural history museums of the world to carefully examine the fossilized remains of Heteronectes and Amphistium. In every situation, he noticed the halfway misplaced eye in all the fossils he sudied. Additionally, these asymmetrically placed eyes were present in fossils of adult and larval specimens.

"Most remarkably, orbital migration, the movement of one eye from one side of the skull to the other during the larval stage, was present but incomplete in both of these primitive flatfishes," reports Friedman. In both fossils, one eye had begun its migratory journey but had not crossed the midline from one side of the fish to the other (figure 1);

Figure 1: Skulls of primitive pleuronectiforms showing incomplete orbital migration intermediate between generalized fishes and living flatfishes. a, Heteronectes chaneti gen. et sp. nov., holotype, NHMW 1974.1639.25 (dextral morph); transfer preparation dusted with ammonium chloride and presented in right-lateral view. b, Counterpart, NHMW 1974.1639.24; transfer preparation dusted with ammonium chloride and presented in left-lateral view, showing migrated orbit. c, Amphistium paradoxum, Muséum national d'Histoire naturelle, Paris (MNHN), MNHN 10878b/Bol87 (sinistral morph); specimen presented in left-lateral view (photo credit: C. Lemzaouda, MNHN). d, Interpretive drawing. Solid grey shading indicates impression; diagonal hatching indicates damaged bone. e, Amphistium altum, Natural History Museum, London (BMNH), BMNH P. 3940 (dextral morph); silicone peel dusted with ammonium chloride and presented in left-lateral view, showing migrated orbit. f, Interpretive drawing. bsp, basisphenoid; ent, entopterygoid; f, frontal; hym, hyomandibular; la, lacrimal; le, lateral ethmoid; m.o, dorsal margin of migrated orbit; mes, mesethmoid; pmx, premaxilla; psp, parasphenoid; ri.par, parietal/epioccipital ridge; ri.pto, pterotic ridge; scl, sclerotic ring; sn, supraneural; soc, supraoccipital; names followed by 'r' or 'l' indicate right or left feature, respectively; '?' indicates uncertain identification. Scale bars, 10 mm. DOI: 10.1038/nature07108 [larger view].

Friedman's studies differed from previous work because he performed Computed Tomography scans (CT or CAT Scan) on the fossils instead of relying on traditional methodologies and this new technique revealed that both genera of fishes "unequivocally" had the cranial asymmetry.

When Friedman compared Amphistium and Heteronectes to modern flatfishes, he found they possess some characters in common with each other that are not present in modern flatfishes, while they share other characters with modern flatfishes, thereby allowing him to place them on the evolutionary tree as transitional fossils, or evolutionary "missing links" (figure 2);

Figure 2: Phylogenetic placement of Heteronectes and Amphistium and implications for the origin of cranial asymmetry in flatfishes. a, Topology arising from the analysis of a matrix comprising 19 taxa coded for 58 morphological characters (8 ordered) (number of cladograms = 1; cladogram length = 135; consistency index = 0.50; retention index = 0.74; rescaled consistency index = 0.37). Heteronectes and Amphistium are placed as successively more crownward plesions on the flatfish stem. Unordered analyses reconstruct these taxa in the same position. Numbers at nodes indicate Bremer decay index, bootstrap support and jackknife support, from top to bottom, respectively. Extinct taxa are marked (â ) and '-' indicates that bipartition occurs in fewer than half of cladograms arising from bootstrap or jackknife analysis. Previous placements of Amphistium outside Pleuronectiformes are rejected. See Supplementary Information for full details of the analysis. b, Reconstruction of Amphistium, showing sinistral (front) and dextral (back) individuals in the left lateral view (modified from ref. 20). c, Simplified cladogram adapted from a showing the progression of orbital migration across flatfish phylogeny. Neurocrania are depicted in left lateral (top), dorsal (middle) and right lateral (bottom) views. DOI: 10.1038/nature07108 [larger view].

Interestingly, there is another peculiar extant flatfish genus, Psettodes, that contains three species of flatfishes that range throughout the Indian and Pacific Oceans. As you can see in the above diagram, Psettodes has an eye that is placed near its midline, near the top of its head. These fishes swim vertically like other fishes, although they do spend some of their lives laying on the seafloor, waiting for lunch to arrive. The asymmetrical placement of their eyes provides a greater range of vision while they are prone, thereby enhancing their own ability to escape becoming another fish's lunch.

But the relationship of this genus to other modern flatfishes was mysterious, so
Friedman included Psettodes in his analysis and found that this genus is the basalmost living flatfish, while the extinct Amphistium and Heteronectes form a lineage that is paraphyletic with respect to modern flatfish.

According to Friedman, his findings "refutes these claims of radical sudden change" -- Goldschmidt's "hopeful monster" hypothesis -- "and demonstrates that the assembly of the flatfish body plan occurred in a gradual, stepwise fashion."

So once again, scientists have discovered another transitional fossil that, like Tiktaalik, provides creationists with yet another gap to demand that scientists fill with yet more fossils -- thus ensuring plenty of scientific research for centuries to come.


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

University of Chicago Medical Center press release (quotes).

More like this

Friedman included Psettodes in his analysis and found that this genus is a true "living fossil" because it diverged away from the ancestral flatfish lineage before even the extinct Amphistium and Heteronectes did.

That's not what the analysis shows. Psettodes is the basalmost living flatfish, Amphistium and Heteronectes form a paraphyletic stem to living flatfish.

Thanks for this! Coincidentally, I was just the other day trying to explain the fun-ness and funny-ness of flatfish to my six-year-olds, and I misinformed them about the timing of the eye migration. Now, I can not only give them correct information, but I can also show them your super-cool plaice photo and tell them even more fun stuff about these fish and their forebears.