As Many Exceptions As Rules: The Eyes Have It

Biology concepts – asymmetry, lateral polymorphism, flatfish, evolution, copepod, ecology, niche

Ray Harryhausen was the most famous of the stop

motion artists in the movies. This version of the

Cyclops was his creation for the 1958 movie, The 7^th

Voyage of Sinbad. I can’t see how the Cyclops could

catch anything with just the one eye – he had no

depth perception.

We have been talking about bilateral symmetry in the past few weeks, and this would include having two eyes, one on each half of your face. Two eyes must be a pretty important evolutionary adaptation; can you think of an animal that has just one eye – other than a cyclops, that is? (the answer is somewhere in post) Some protists have a single eyespot for sensing light – but they aren’t animals.

Predators need to catch their food, so they need depth perception. For this you need two overlapping images. You don’t do the math consciously, but your brain uses the differences in each image to tell you how far away the target prey is. To get two images simultaneously, you need both eyes to be on the front of your face.

Prey animals, usually herbivores, have to worry about being chased down by a predator. Prey animals are usually quick, but they need clues to get a good start before the predator gets too close. Their eyes are designed to pick up motion; it doesn’t matter how far away it is. If something moves in their line of sight, they assume it’s a predator and they bolt. By having their eyes on the sides of their head, they have a maximal range of vision which gives them the best chance to see that lioness coming.

Just to show you how important evolution thinks it is to have at least two eyes, let’s discuss a group of animals that have found a way to make two drastic changes work for them. Flatfish have evolved to lie on their side, but they’re predators so they can’t afford to have one eye constantly seeing nothing but the sandy ocean bottom. Consequently, they have moved one eye to the other side of their head!

This is a winter flounder (Pseudopleuronectes

americanus). Notice how it blends in to the floor. It

does more by flapping and tossing sand on its back.

The mouth points up when the fish is vertical, so the

left most eye is the one that migrated. Makes sense,

you wouldn’t want to move an eye under your chin –

that would be silly.

Flatfish are all from the order Pleuronectiformes (pleuro = toward the side), sometimes called the Heterosomata (hetero = differently, and soma = bodied). There are some 715 species of flatfish in 11 families, and they include the turbots, sole, flounder, plaice, and halibut. They are all predators that lie in wait on the ocean-, lake-, sea-, or riverbed. But they don’t start out that way.

All the Pleuronectifromes start out as fry that swim upright. Their top is at the top, and the bottom is toward the bottom. They live nearer the top of the water than the bottom, have pigment coloration on both sides of their body, and feed on phyto- and zooplankton. But the surface isn’t the safest place to live; bigger fish are always around to eat the small fry.

So, as they start to develop into adults, many changes take place. They swim down to the floor of whatever body of water they call home. One eye starts to move! It travels over the top of their head and onto the other side, like the Mr. Potato Head of some deranged child.

As you can imagine, moving an eye isn’t an easy thing to do. Their brain has to move, as do the cranial and facial bones. Their mouth has to make room for the eye coming its way. All in all, it’s a tough piece of work.

The top image is the visible side of a rock sole, the

bottom image is the lower side of the same fish. As the

fish matures and lies on its side, the coloring changes.

Pigments are energetically expensive to make, so why

waste them. The middle image shows the line where it

goes from pigmented to unpigmented. What control!

Moving an eye from one side of the head to the other seems illogical, why not just develop with both eyes on one side, or make do with one eye? Creationists have used the flatfishes as an argument against evolution. We have fish with eyes on each side of their head, and fish with both eyes on one side of their head. They argued that if natural selection was responsible for the change in flatfish, there should be fossils or fish that are intermediates.

Well, there are evolutionary intermediates – even some living examples. A paper in 2008 introduced us to two extinct species of flatfish. In each (Amphisitium and Heteronectes), one eye had migrated, making the fish asymmetric, but it had not crossed the crown of the skull and made it to the other side. These are definitely intermediate species, but we can go one better.

The Psettodes genus of flatfish (the turbots - yummy by the way) have one eye that is located right at the crown of their skull. Perhaps technically you could say that is has migrated to the other side, but just barely. And this brings us to another question, which eye moves?

Some flatfish are right-eyed (dextral) that swim left side down. Others are left-eyed (sinistral) and swim with their right side down. Some species are strict and some are more likely to have reversants (individuals that lay on their other side). A 2005 paper stated that only about 7 of the 700 species of flatfish show lateral polymorphism (lateral = side, poly = more than one, and morph = shape), ie. some right-eyed and some left-eyed individuals.

The bottom image has on the left side depicts the two

extinct species of flatfish where the migrating eye hadn’t

quite made it to its destination. The middle cartoon is

the extant Psettodidae, like the Indian Halibut on the top.

The eye has just made it to the crest of the cranium. The

right cartoon on bottom shows a species where the eye

has completely migrated. Looks like great support

for evolution.

For example, a 2009 paper describes reversants for two right-eyed flounder species which are the first left-eyed individuals ever seen in these two species (Microstomus achne and Cleisthenes pinetorum). It goes the other way too – a 2013 study describes the first right-eyed individual ever seen in a megrim (sometimes called a whiff, Lepidorhombus whiffiagonis). But in the left-eyed California halibut (Paralicythys californicus), up to 40% of the individuals are right-eyed. Perhaps right-eyed species are stricter than left-eyed species.

The exception to that rule is the starry flounder (Platichthys stellatus). It’s a member of a right-eyed family of flounders, but in some cases half of the individuals are left-eyed. In this case, there seems to be more to the story - the lateral polymorphism occurs only in populations of specific geographic areas.

A paper from 2007 looked into the mystery that 7 species that show lateral polymorphism, but only two (starry flounder and P. fleusus) show a geographical distribution in their polymorphs. Off the coasts of Japan and Russian, 100% of the starry flounders are left-eyed, but near Alaska they are only 75% sinistral and from Washington state to central California the populations are about 50/50.

The researchers looked into several questions. Was there more to being left-eyed or right eyed than just which side the eye went to? Does the side make a difference that could account for the geographic distribution? They found out – yes, and yes.

They saw that the right and left-eyed individuals have more asymmetries between them than just the side of the body that the eye migrates to. They have differences in mouth size and angle, as well as tail size of all things. Right-eyed individuals had significantly longer and wider tails than did left-eyed individuals!

The research also shows that in areas where the two groups compete the most, the differences between the dextral and sinistral individuals are the greatest. This suggested to them that the differences allow them to compete for different prey – to fill different ecological niches. The hypothesis is that the polymorphic asymmetries give them different advantages which they then exploit and this is why there is a stable geographic distribution in populations.

A very complicated but informative chart from the paper

on pitx2 reactivation during metamorphosis. Note which

side is right and left and then follow what happens for

the two species, one right-eyed and one left-eyed. The

right side shows what can happen if you block pitx2. In

the reversed individual, the left habenula (dd. l) enlarges

instead of the right.

Well, that’s cool, but how is it controlled – what makes a fish right- or left-eyed? A 2009 paper started to investigate this. During development of the embryo, certain internal asymmetries develop (will talk more about this in a few weeks). In fish and other vertebrates, this is controlled by expression of certain genes in the habenula of the brain. One of the gene products (proteins) in the habenula is called pitx2.

There are actually two habenulae, one in each hemisphere of the brain, as part of the thalamus. The researchers looked at the brains of right-eyed and left-eyed flounder species and detected some things that were the same and some things that were different.

After the pitx2 did its job in the embryo, it was turned off. But right before metamorphosis – when the eye migrates and the fish lies down on one side, pitx2 was turned back on – only in the left habenula, regardless of which way the fish’s eye was going to migrate and which way it was going to lie down.

Not only that, but the right habenula started to grow bigger than the left habenula in both dextral and sinistral species. The only thing that was different was the rotation of the brain, with the left habenula moving forward in the right-eyed species and the opposite occurring in the left-eyed species. The same changes occurred in fish no matter which eye migrated!

This copepod is about to swim into the top border of

this image. The reason for this is that he only has one eye

(the light spot between the antennae), so he has no depth

perception! By the way, he’s only 2 mm long, so he

probably will just bounce off the edge.

However, in those fish that they experimentally blocked the second round of pitx2 activity, you could get a normally turned fish or a reversant. The only difference - when you got a reversant, it was the left habenula that enlarged, not the right. I think we still have some more to learn.

By the way – at the beginning of today’s post I asked if there were any real animals with one eye. I made it sound like there aren’t but in fact there are exceptions. In some small crustaceans (arthropods) called copepods, the majority of species have a single eye right in the middle of their head! What’s more, a 1994 study showed that the holdfast of a particular copepod parasite is asymmetric (like we saw last week) and this particular copepod is a parasite of only flatfishes! How symmetric this tale of asymmetry turned out to be!

Next week - can a single tooth render an animal asymmetric? Well, that depends on the tooth, doesn't it.

MacDonald P (2013). A rare occurrence of reversal in the common megrim Lepidorhombus whiffiagonis (Pleuronectiformes: Scophthalmidae) in the northern North Sea. Journal of fish biology, 83 (3), 691-4 PMID: 23991885

Suzuki, T., Washio, Y., Aritaki, M., Fujinami, Y., Shimizu, D., Uji, S., & Hashimoto, H. (2009). Metamorphic pitx2 expression in the left habenula correlated with lateralization of eye-sidedness in flounder Development, Growth & Differentiation, 51 (9), 797-808 DOI: 10.1111/j.1440-169X.2009.01139.x

Goto T (2009). Reversals in two dextral flounder species, Microstomus achne and Cleisthenes pinetorum (Pleuronectida; Teleostei), from Japan. Journal of fish biology, 74 (3), 669-73 PMID: 20735586

BERGSTROM, C. (2007). Morphological evidence of correlational selection and ecological segregation between dextral and sinistral forms in a polymorphic flatfish, Platichthys stellatus Journal of Evolutionary Biology, 20 (3), 1104-1114 DOI: 10.1111/j.1420-9101.2006.01290.x

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

For more information or classroom activities, see:

Flatfish –

https://www.youtube.com/watch?v=L66qpRL6mfw

http://www.amnh.org/explore/news-blogs/news-posts/dawn-roje-tracing-the-metamorphosis-of-flatfishes

http://bogleech.com/flatfish.html

http://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=2&ved=0CCUQFjAB&url=http%3A%2F%2Fnefsc.noaa.gov%2Fpublications%2Fcrd%2Fcrd1415%2Fcrd1415.pdf&ei=oF32VPv4OYqaNr2agqgJ&usg=AFQjCNGvlBB3CL1rCNq29nhB3HXPSjpMGA&sig2=4gJD9UkkojsswQjJTiSBng&bvm=bv.87269000,d.eXY

http://scienceblogs.com/grrlscientist/2008/07/09/the-mysterious-origin-of-the-w-1/

http://www.pbs.org/wgbh/nova/next/evolution/flatfish-evolution/

https://www.youtube.com/watch?v=6LZftSciYNY

http://www.dtmag.com/Stories/Marine%20Life/11-03-whats_that.htm

http://mostlyopenocean.blogspot.com/2012/07/flatfish-eyes-twice-solved-mystery.html