Flatfish, in the order Pleuronectiformes, have long been an evolutionary puzzle, for all the fish in this order lie on the substrate—on their sides—with both eyes on one side of their body, like the flounder below:
Phylogenetic analysis shows that flatfish evolved from “regular” fish, fish having one eye on each side and swimming vertically, that evolved over time to lie on their sides. The bizarre thing about this evolution is that it involved genetic changes so that “normal” fish had their eyes move over the top of their head so that both eyes look upwards. Their skin changes color and texture, too, with the top half colored, as above, and the bottom half pale.
And all flatfish begin their development like “normal fish”, swimming vertically and having one eye on each side of the head. Then, as the fish gets older, one eye migrates over the top of the skull to the other side! (You can see that in the video below.)
When the eyes are both on one side, the flatfish tip onto their sides and spend the rest of their adult life lying on one side. (The side varies among species: some have 100% right-sided individuals, others 100% left-sided, and some species are random, with half of the individuals having the right eye move over (and lying on their right side), and the other half having the left eye move.
Living on the substrate like this, and often camouflaged as the flounder above, is an advantage for the fish, both protecting them from predators and, since they are predatory piscivores (fish eaters), hiding from their prey.
Here’s a video of the development of a young flatfish, showing the eye migration. Since the ancestor had both eyes on one side, like the young flatfish, this is a case of “ontogeny recapitulating phylogeny”—that is, the development of a single living fish goes through a process mimicking the evolution of their adult ancestors.
But since the weird developmental pathway is presumably an adaptation that evolved by (presumably stepwise) natural selection, two big questions immediately arise:
- What were the intermediate evolutionary stages of eye migration?
- What were the evolutionary advantages of this migration, which presumably involved a gradual evolutionary movement of the eye from the side to the top of the head, and then over the head to the other side? It’s hard to see how, for example, an eye that’s halfway around, so it’s close to the top of the skull but hasn’t moved to the other side, could leave more offspring, or survive better, than their ancestors. What would be the advantage of each small step of the migration?
It’s hard to envision a gradual Darwinian process that could produce this migration. As Carl Zimmer wrote in a new NYT article that summarizes recent flatfish findings (click below), Darwin’s critics used both questions about to cast doubt on his theory. In response, some “saltationists”, who assumed that major evolutionary changes occurred in one huge step rather than a series of gradual steps, said that a single mutation moved the eye from one side to the other. (But that would not be advantageous unless the fish had already evolved to lie on its side!)
Click below to read the Zimmer piece in the NYT here (the drawing is animated), or find it archived here.
As Carl reports, there was another weird finding that now seems doubtful: a 2001 paper by a group of Chinese researchers who, using DNA=based family trees, seemed to show that flatfish evolved twice. You can see that paper in Nature Genetics by clicking on the headline below, or read the pdf here. The discovery that flatfish seemed to be “polyphyletic”—with more than one evolutionarily independent origin—was deeply weird, because the hormone-induced eye migration, which is extraordinarily complex, would have had to evolve twice. It’s not impossible, but seemed unlikely. One of the doubters was evolutionist Matt Friedman, who got his Ph.D. here and is now a professor at the University of Michigan and director of its Museum of Paleontology.
A while back, when he was still at Chicago, Friedman published what I see as the most interesting of the three papers highlighted here. This one was in Nature, and you can read it by clicking below or seeing the pdf here
Note that this paper was a lot of work, and yet, unlike the others, Friedman was the sole author. I love to see single-person research efforts like this. That aside, what Friedman found were two fossil evolutionary intermediates between adult “normal” fishes (the presumed ancestors of flatfish) and modern flatfishes, having both eyes on one side. Friedman reanalyzed a neglected species, Amphistium paradoxum, and a described a new fossil fish, Heteronectes chaneti, both from the lower Eocene, about 50 million years ago.
Amazingly, both species (the former randomly sided and the latter lying on its left side) showed an intermediate placement of the eyes in the adult fish. Both eyes were on the same side of a vertically-oriented fish, but one eye had migrated upwards toward the top of the skull, so that the fish could presumably see both to the side and also, perhaps, a bit above them. Thus we have two evolutionary intermediates of the adult stage, likely showing that the eye movement did not occur in one big evolutionary leap.
Here’s a photo from the 2008 paper of the left and right sides of the H. chaneti skull, showing the eye sockets, which I’ve circled. The asymmetry is obvious:
And a reconstruction of the Amphistium species, showing both sides. The asymmetry is again clear, but the eyes of the adults are still on opposite sides of the head:
You’ve probably realized that this addresses question #1 above, showing that the movement was presumably gradual over evolutionary time, though we need more fossils to show that it was a continuous series of small steps. But at least the movement didn’t seem to involve one big leap.
But that leaves question #2, which I’ll address in a moment.
The reason Zimmer’s note came out now, though the papers above date from 2008 and 2021, is that a group of authors recently published another DNA based analysis in Nature Genetics showing that the Chinese group was probably wrong: flatfishes and their eye movements seem to have had a single evolutionary origin. (The Chinese group maintains that their “polyphyly” conclusion is still the best one.)
Click below to read, or find the pdf here.
Before returning to the Big Unsolved Question, I’ll show the phylogeny advanced in the 2001 paper (bottom), showing two origins of flattening and eye migration, and the newer analysis by Duarte-Ribiero et al. at the top (Friedman is the third author), showing a single origin of flatfish (I’ve circled it). This newer paper also singles out some genes that, showing signs of selection in their DNA sequence, may be involved in the evolutionary transformation, but I’ll leave that issue aside. Green silhouettes are flatfish, black are nonflat fish.
Now for the big mystery. How could there possibly be an evolutionary advantage to each step of the eye movement? Presumably the adult either laid on its side or swam “normally”, and what would be the advantage of intermediate stages when the eye gradually moved up, across the top of the skull, and settling on the other side? The movement is presumably advantageous only when the fish is already on its side, but then what would be the advantage of moving a few mm towards the top of the skull?
Well, perhaps the fish didn’t lie fully on its side. Here’s one clue in a quote from the 2008 paper:
Questions about the possible selective advantage of incomplete orbital transit arise from the discovery of stem flatfishes. Clues are given by living taxa, which often prop their bodies above the substrate by depressing their dorsal- and anal-fin rays. Similar behaviour might have permitted Amphistium and Heteronectes—both of which have long median-fin rays—the use of both eyes while on the sea floor. The unusual morphology and resting orientation of pleuronectiforms have been interpreted as adaptations for prey ambus, and it is clear that stem flatfishes, like morphologically primitive living forms, were piscivorous; one specimen of Amphistium (MCSNV V.D.91+92) contains the remains of a fish nearly half its own length.
So perhaps this happened: a normal ancestor, through behavioral evolution, adapted to hanging around the sea bottom, as they were less conspicuous and could get more prey. But they’d have a more difficult time seeing upwards with eyes on both sides of the head. Movements of the eyes toward the top of the skull could be advantageous so long as they occurred in concert with behavioral changes (first perhaps learned, then evolved) involving propping themselves up with their fins. The advantage of tilting a bit would be that the fish might become a bit less conspicuous.
This whole scenario, as I proposed it (and I’m sure others have before in some form) presumes that the eye movement is either induced by or occurs in concert with changes in the fish’s behavior, which initially could have been learned and not coded in the genes. (Ernst Mayr once said something like “all major evolutionary changes begin with a change in behavior”). I don’t know how to test the hypothesis, as even finding more fossils with intermediate stages of eye migration will tell us little about the selective pressures involved. But for sure the movement involved natural selection rather than other evolutionary forces like genetic drift, for we have a big directional change involving many genes, genes that involve both morphology and behavior.
In short, I don’t know how it happened. But seeing that modern fishes can use their fins to prop themselves up on the sea floor may give us a clue. And other scenarios may be possible; readers can entertain themselves by finding alternative ways this change could have occurred by natural selection.
Splendid post – refreshing and insightful!
“ontogeny recapitulating phylogeny”
^^^cannot unread
But can you say it 3 times, fast?
This was fascinating and I thank you, Jerry, for explaining it in a manner that even a nonscientist like me can understand (I’m not saying it wasn’t a challenge… It was). It blows my mind to consider all combined expertise and research it has to take to arrive at such discoveries. That such things are even “discoverable” is pretty crazy. Good stuff.
Very interesting post.
[ Possible typo?: “Both eyes were on the same side of a vertically-oriented fish, but one eye had migrated upwards toward the top of the skull, …”. Unless I’m misunderstanding the images, the eyes are on opposite sides of a vertically-oriented fish. ]
I wonder if the movement of the eye toward the top of the head could not have happened first, as the fish became a bottom dweller. In a vertical posture, this would allow it to keep an eye out for predators from above while hunting for prey (on one side) across the bottom sands. Once this had occurred, the transition to flat swimming occurred.
I also wonder if ever in fishy evolution, a fish evolved an extra, eye with one pointed strait up. In this case, one of the side eyes might have atrophied away leaving the present form of the flatfish.
I could see no advantage to a small, incremental movement of the eye towards the top of the head unless it was already changing towards a bottom dweller. As the developmental and fossil data show, a third eye or signs thereof did not evolve.
A plausible – to me – intermediate might be evolution from an ambush predator lurking in crevices in the rock / reef, where the utility of the eye is severely reduced in one direction, but the bottom-dwelling asymmetric swimming mode has not developed (yet). The partly migrated eye would have a field of view at less than 180° to the unmigrated eye.
Unfortunately, this is comparable to Einstein’s reason for disliking quantum mechanics, and particularly entanglement – “god throwing the dice where we cannot see them”. Because a sufficiently rocky substrate to have significant crevices is a pretty unlikely place to get the rapid burial best-suited to fossilisation.
ISTR that occasional amphibian species and some fossil relatives of the New Zealand tuatara had a small medial fossa on the braincase which would be in about the right position to allow light to penetrate to the pituitary gland. Though if this was actually sufficiently transparent, it would have been considerably inferior to the other two eyes for actual vision. But a role in thermal non-imaging detection or day-length sensing has been hypothesised. But it’s an intermittent and labile character in the fossil record.
I’m trying to remember if snakes also have “pits” or fossae in their skulls, associated with their modern heat-detecting capabilities. And crucially, if these structures are paired about the median line, or unpaired on the median line.
Any herps about?
Great post.
Great post. I wonder if the change initially could have involved both natural selection and geographic isolation, which perhaps in tandem might have resulted in a faster rate of change? Also, might studying the embryo development of a flatfish species provide clues to the evolutionary development of the species itself?
One wouldn’t need geographic isolation if the evolution was going on in a single species; you need such isolation (usually) if you are producing reproductive barriers two related species derived from a common ancestor. Natural selection within a species doesn’t require that it be geographically isolated from others.
This could be several adaptations going on at once. If bottom dwelling resulted in greater evolutionary fitness – and greater horizontal orientation resulted in greater evolutionary fitness (as an ambush predator perhaps) – and one eye looking up resulted in greater evolutionary fitness, then the other eye migrating to also look upwards is not a mystery but a consequence of the fitness of other changes.
It’s a fascinating evolutionary story. Thank you for sharing it. Apropos the change in the phylogenetic tree between Lu et al (2001) and Duarte-Ribeiro et al (2024), leading to the identification of a single evolutionary origin of flatfish, there’s been a lot of work done on building such trees from genome sequences in the last 20 years. We have many more complete genomes now than we did in 2001, for one thing.
At the Sanger Institute, where I work, there’s an ambituous ongoing project called Darwin Tree of Life which aims to sequence all 70,000 eukaryotic species that are native to the British Isles. It’s a major collaboration with several other institutes and universities. One of the latest species to have its genome published is the death-watch beetle, and the DNA was extracted from an insect found in a wooden beam on HMS Victory, as reported by the Guardian today:
https://www.theguardian.com/uk-news/article/2024/jun/22/nelson-hms-victory-gives-scientists-vital-dna-for-battle-against-deathwatch-beetle
Is it possible that the “moving” eye offered an advantage in sexual selection? Do the male fish “fan the bed” of eggs laid by females? Could the wandering eye help in a reproductive way enabling the male with a more mobile eye to pass on more genes to future generations?
Interesting stuff. A polyphyletic origin of the asymmetry does sound very unlikely, at least a priori.
A gradual migration of the eyes to one side of the head might, at first, seem to be a problem, but part of that “problem” might simply be failure on our part to accept that small changes can impact reproductive success. A similar “problem” is frequently raised in the form of the question: “What good is part of an eye?” The answer is that a lot of good can come from a small change in the way that an organism responds to light. We know this because there is a multitude of visual systems out there at all levels of sophistication. Probably the same thing is the case here—as the fossil discoveries suggest. And, adding a concomitant shift to life on the bottom creates a synergistic effect that may be all that’s needed to tip the balance.
More fossils please.
See my comment above about “crevice dwelling” ambush predation as a putative environment where the migration of the eyes from symmetry could be advantageous distinct from the adoption of a bottom-dwelling role.
Everybody talks about flatfish eyes. What I’m wondering about is – how did one side of their gill structures evolve to ventilate – exhale – stale water from the gill structure, and do it surreptitiously as befits a predator in “ambush” mode.
Bottom-dwelling sharks … actually, I’m trying to remember my “naming of parts” now. Is it the “rays and skates” which have migrated their spiracles to the upper surface of the body? With the migrated spiracle as a distinguishing characteristic of “skates and rays” versus “other cartilaginous not-fishes”?
Taxonomical delousing aside – there are a number of bottom-dwelling genera of elasmobranchs which have addressed such issues of ventilation by moving the spiracle to the upper surface of the (part-buried) body. How “flat fish” deal with the same problem, I don’t know.
My “Bloody AutoIncorrect” `assistant` tried “correcting” “elasmobranch” to “lamellibranch”. Which is quite a step away from the jawed vertebrates.
I have nothing coherent to say except: what a great article. This is one of the reasons I come back to WEIT every day, before anything else. Thank you.
+1
Every few weeks in my case, but yeah.
Very interesting. Thanks for posting.
Thanks for the huge efforts you put in to your website but especially the science.
Fascinating to the max! Thank you.
Thank you for this amazing post! More, please.
I once caught a 204lb. halibut 30 years ago- that was quite the struggle. I think halibut are the largest Pleuronectiformes. A truly formidable fish that are on record for killing some people who have caught them- flapping them to death. Again, this eye-migration illustrates how evolution is smarter than me and you. Left to right or right to left or indiscriminate migration boggles my mind in a way. Something we’ll probably never understand…some things are simply random I suppose. Biology is really tough, regardless (unless you’re a creationist, then everything is simple!). Thanks for this terrific post!
A number of fish burrow into the sand to wait for prey and to avoid predators.
eg https://www.youtube.com/watch?v=vRPXo63pxLE
These fish have tubular bodies. notably the puffer fish. Their eyes jut from above the head. No need for eyes to move to the side. The real question would seem to be: why did some fish become flat?
Most of you will have gazed into rock pools at the beach and noted that a shadow cast over the water will send fish scurrying to find cover. Some will nestle against rocks. That works ok in a rock pool, but what about outside the pool in channels where currents are strong. Having a low profile would be an advantage then. I think some comparative biology might reveal the existence of so-called in-betweens to throw light on the matter. It would be relatively easy for a flattened fish with one eye on the move to adapt to sandy bottoms.
Just thinking!
I supposed flat fish can hunker down where other fishes cannot bury themselves. Every niche gets exploited, eventually.
In my childhood I hunted flounder (as flatfish are called in NZ) with a spear in shallow waters. There were places where, indeed, a flat fish would have an advantage, especially where a layer of rock was covered by a mere couple of cm of mud. The local flounder had the remarkable ability, if trodden on, to scamper away a few meters, and disappear into the muds without creating a mud storm, and thence be difficult to find, visually. It seems to me that two rules might apply to the evolution of the ‘flatfish niche’: unlikely, the niche exclusion principle of Gause and Rmer’s rule, that an adaptation (‘pre-adaptation’) evolving for one circumstance give rise to the possibility of occupying another niche, as you suggest. I think that being flat was the pre-adaptation.
This is part of my reason for suggesting an intermediate “crevice dwelling ambush predator” stage – to prompt the development of asymmetric eyes. Followed by dispersal into a new “infaunal” econiche which drove the eye migration to completion. Turning one big evolutionary problem into two smaller intermediate problems.
Great stuff. I’d be curious to learn about the genes. Classically, the Sonic Hedgehog signaling pathway has been used to evolve left/right asymmetry in vertebrates. Maybe it’s involved here? I’m not sure that this would be too hard to evolve more than once.
Before people ask for more science posts, realize that it’s about four times more work to write one of these than a “non-science post.” That’s why I did only on substantial post yesterday. When interesting stuff about evolution comes out, I try to write about it.
Truly a fascinating discussion, prompting thought and insight into evolution generally. Indeed, evolution of the body plan must go hand-in-hand with evolution of behaviour, and small changes in body plan and behaviour must lead to advantage.
Astonishing how Jerry keeps up a huge effort day after day.
David Lillis
Here’s an interesting video on this subject: