Darwin's Flatfish Flounder

And now for something completely different. Today is Darwin Day, the bicentennial of Darwin's birth, and this year is the sesquicentennial of the publication of On the Origin of Species. I don't know about you, but I think an ideal topic for today is to talk about one of the ways in which Darwin was wrong.

He was wrong about flatfish.

Flatfish, by the way, are those weird fish which have both their eyes on the same side of their head. They look sort of like they were designed by Picasso. They spend their adult lives swimming sideways, flat.

A few interesting facts: While they're usually camouflaged on top, their underside is usually just a pale white. Unlike most fish which flex side to side to swim, flatfish flex up and down (because they're sideways, of course). However, they do not look like this their entire lives. They begin their lives looking like normal fish, with one eye on each side, and then one eye migrates over to the other side. Most species are exclusively right-eyed, or exclusively left-eyed, but the more primitive forms often have a mix of left-eyed and right-eyed fish within each species.

In Darwin's day, the flatfish was used as an argument against the theory of evolution. Darwin's theory of evolution (keeping in mind that he did not know much about the mechanisms of heredity and development) required that evolution occur in small, gradual steps. Each step of the way must be evolutionarily advantageous, or it will never catch on. But then, how could flatfish evolution be possible? What possible advantage could be gained by having an eye which migrates only part way to the other side of one's head? Until the eye reaches the other side of the head, it seems like there is no advantage at all, or even a disadvantage.

Darwin, of course, had an explanation. On the Origin of Species has a chapter called Difficulties on Theory in which Darwin answers many of the contemporary objections to his theory. He devoted several paragraphs to flatfish. Let us ponder his wisdom:

The Pleuronectidae [flatfish], while very young and still symmetrical, with their eyes standing on opposite sides of the head, cannot long retain a vertical position, owing to the excessive depth of their bodies, the small size of their lateral fins, and to their being destitute of a swim-bladder. Hence, soon growing tired, they fall to the bottom on one side. While thus at rest they often twist, as Malm observed, the lower eye upward, to see above them; and they do this so vigorously that the eye is pressed hard against the upper part of the orbit. The forehead between the eyes consequently becomes, as could be plainly seen, temporarily contracted in breadth. On one occasion Malm saw a young fish raise and depress the lower eye through an angular distance of about seventy degrees.

I realize Darwin's writing is pretty dense, so allow me to parse it for you. Flatfish, when they are young, vigorously try to move their eye. Because of the extended stress, their eye eventually moves over to the other side. This behavior and condition are inherited and acted upon through natural selection.

The problem is that this explanation is rather Lamarckian (though there's a bit of natural selection in it too). Lamarckianism was a sort of alternative to Darwin's natural selection, which stated that a creature's behavior would give it new characteristics over time, and that these acquired characteristics would be inherited by later generations. For example, the Lamarckian explanation for giraffes might be that they kept on reaching for the tops of trees, and eventually, over generations, they grew long necks. Lamarckianism is currently unaccepted. Though creatures may acquire new characteristics in their lives, these acquired characteristics are not heritable unless it some how affects their genes or gene expression.

To be clear, Darwin did not reject Lamarckianism (as the example with flatfish demonstrates). In fact, he was sympathetic to it. What Darwin said was that in addition to the Lamarckian mechanism, there is also the mechanism of natural selection, which he dare says is the dominant mechanism. Darwin was too cautious a scientist to go so far as to say that Lamarckian evolution was impossible. After all, Darwin didn't know anything about genetics, so he couldn't have ruled it out.

So the question is, if Darwin couldn't explain it, have we come up with an explanation in the 150 years since that time? The answer, I found, is no. We are not sure of the explanation. However, there's a recent article in Nature which sheds some light into the question!*

The evolutionary origin of flatfish asymmetry

This paper discusses two extinct genus of flatfish, called Amphistium and Heteronectes. These are the most primitive forms of flatfish that we know of. By examining the fossil evidence, the author concluded that there was no torsion-induced damage. This suggests that the eye migration is not caused by the fish's vigorous effort, as Darwin suggested. So we know that whatever the answer, Darwin's is not the correct one.

The other interesting thing about Amphistium and Heteronectes is that their eyes do not completely migrate to the other side. Their eyes are asymmetrical, but they still remain on opposite sides, even in the adult forms. These genus' were evolutionarily stable, and existed for at least two geological stages. This shows that there was a gradual transition from having eyes on the opposite sides of the head, to having both eyes on the same side of the head. This was not the result of a sudden mutation. No punctuated equilibrium here.

Perhaps the transitional forms were not as maladaptive as we previously thought. The author suggests that primitive flatfish were still able to use the part-way migrated eye by propping up their body (as certain modern flatfish sometimes do). But we can't say for sure! I think the flatfish are mocking us.

*Some years ago, I wrote a research paper on this topic for a class, and I was pretty disappointed to find that there was no known explanation for Darwin's flatfish problem. When this Nature paper came out, I was pretty excited. If only the Nature paper had appeared before I took that class.

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