Brachiopods: another piece in the puzzle of eye evolution


About 600 million years ago, or a little more, there was a population of small wormlike creatures that were the forebears of all modern bilaterian animals. They were small, soft-bodied, and simple, not much more than a jellyfish in structure, and they lived by crawling sluglike over the soft muck of the sea bottom. We have no fossils of them, and no direct picture of their form, but we know a surprising amount about them because we can infer the nature of their genes.

These animals would have been the predecessors of flies and squid, cats and starfish, and what we can do is look at the genes that these diverse modern animals have, and those that are held in common we all inherited together from that distant ancestor. So we know that flies and cats both have hearts that are initiated in early development by the same genes, nkx2.5 and tinman, and infer that our common ancestor had a heart induced by those genes…and that it was only a simple muscular tube. We know that modern animals all have a body plan demarcated by expression of Hox genes, containing muscles expressing myoD, so it's reasonable to deduce that our last common ancestor had a muscular and longitudinally patterned body. And all of us have anterior eyes demarcated by early expression of pax6, as did our ancient many-times-great grandparent worm.


We do not have fossils of these small, soft organisms, but that's no obstacle to picturing them. You just have to see the world like a modern molecular or developmental biologist. One of the graphical conceits of the Matrix movies was that the hero could see the hidden mathematical structure of the world, which was visualized as green streams of symbols flowing over everything. We aspire to the same understanding of the structure of life, only what we see are patterns of genetic circuity, shared modules that are whirring away throughout development to produce the forms we see with our eyes; and also, unfortunately, we currently only see these patterns spottily and murkily. There is no developmental biologist with the power of Neo yet, but give us a few decades.

There's another thing we know about these ancient ancestors: they had two kinds of eyes. ciliary and rhabomeric. Your eyes contain ciliary photoreceptors; they have a particular cellular structure, and they use a recognizable form of opsin. A squid has a distinctly different kind of photoreceptor, called rhabdomeric, with a different cell structure and a different form of opsin. We humans also have some rhabdomeric receptors tucked away in our retinas, while invertebrates have ciliary receptors as well, so we know the common ancestor had both.

Now this ancestral population eventually split into two great tribes, the protostomes, which includes squid and flies, and the deuterostomes, which includes cats and starfish. It should be an obvious indication of the general state of that ancestor that it represents all that those four diverse animals have in common. It also tells us that while that ancestor had eyes, they were almost certainly very simple, and could have been nothing more than a patch of light-sensitive cells, or perhaps even single cells, as we see in some larval eyes.

What we think happened at this division is that both tribes took the primitive eyes and specialized them independently. Each group evolved under similar constraints: they needed directionally-sensitive eyes that could tell what direction a source of illumination was coming from (and these would eventually form true image-forming eyes), and they also needed sensors to detect general light levels — is it day or night, are we in the open or under a rock? Think of it like a camera system: there is a part that gets all the attention, the lens and image-forming chip, but there's also a light meter that senses ambient light levels.

The two tribes made different choices, though. The protostomes pulled the rhabdomeric photoreceptor out of their toolbox, and used that to make the camera; they used the ciliary photoreceptor to make their light meter. The deuterostomes (actually, just us chordates) instead used the ciliary photoreceptor for their camera, and the rhabdomeric photoreceptor for the light meter. It's the same ancestral toolkit, but we've just specialized in different ways.

At least, that's the general model we've been exploring. A new discovery at the Kewalo Marine Laboratory, one of the premiere labs for evo-devo research, has made the interpretation a little more complex.

That discovery is that brachiopod larvae, which are protostomes, have been found to have directionally sensitive eyes…which are ciliary. A protostome should have directionally sensitive eyes that are rhabdomeric. How interesting!

Brightfield microscopy of a Terebratalia transversa larva, with red eye spots visible in the apical lobe (black arrows). (A) Dorsal view. (B) Lateral view.

In addition to being ciliary in structure, these eyes express ciliary opsin. They are also true cerebral eyes, also expressing pax6 and having a nervous connection to the central nervous system.

Notice what is going on here: a protostome is building a camera, and unlike all the other protostomes we've observed, it's pulled a ciliary photoreceptor out of its pocket to make it. This is a surprise, but it doesn't upset any theories too much — it just means we need to explore a couple of alternative explanations. We don't have answers to resolve these hypotheses yet — we need more data and experiments — but it'll be fun to watch the work roll onward.

One explanation is illustrated in A, below. The initial animal state was to build directional, cerebral eyes using rhabdomeric photoreceptors. The vertebrates are oddballs who swapped in ciliary receptors instead, while these larval eyes in brachiopods are major peculiarities, an evolutionary novelty which resembles a cerebral eye, but is actually non-homologous. This seems unlikely to me; there are multiple elements of the eye circuitry at work in these eyes, and if they're using the same gene circuitry, we ought to recognize them as homologous at the molecular level…the only one that counts.

The second explanation in B is that all of these cerebral eyes are homologous, but that the receptor type is more plastic than we thought — it's relatively easy to switch on the ciliary module vs. the rhabodmeric module, so we would expect to see multiple flip-flops in the evolutionary record.

If we accept that it's easy to switch receptor type, though, then why assume that the last common ancestor had a directional, cerebral eye that was rhabdomeric? It could have been ciliary, which is also a more parsimonious explanation, because it requires only one switch of types in the protostomes, shown in C.

(Click for larger image)

Alternative hypothesis on the evolution of photoreceptor deployment in cerebral eyes. Schematic representation of three hypotheses accounting for the deployment of ciliary photoreceptors in the cerebral eyes of Terebratalia and vertebrates, versus rhabdomeric photoreceptors in Platynereis and other protostomes. (A) Deployment of rhabdomeric photoreceptors as the ancestral state in cerebral eyes, with the larval eyes of Terebratalia, containing ciliary photoreceptors, representing an evolutionary novelty. The deployment of ciliary photoreceptors is the result of a substitution (with ciliary photoreceptors having replaced rhabdomeric photoreceptors in the cerebral eyes) early in the chordate lineage. (B) Larval eyes in Terebratalia are homologous to the cerebral eyes in other protostomes, but ciliary photoreceptors have been substituted for rhabdomeric photoreceptors, as in the vertebrates. (C) Ciliary photoreceptors in cerebral eyes represent the ancestral condition, inherited by Terebratalia and vertebrates. Deployment of rhabdomeric photoreceptors in the cerebral eyes of Platynereis and other protostomes are the result of substitution events.

Whichever hypothesis pans out, though, the important message is that photoreceptor type is a more evolutionarily labile choice than previously thought. What I want to see is more research into photoreceptor development in more exotic invertebrates — that's where we'll learn more about our evolutionary history.

I have to mention a couple of other cool features of this paper. If you ever want to see a minimalist directional eye, here it is: the larval eye sensor of brachiopods consists of two cells, a lens cell that actually does the job of light detection, and a pigment cell that acts as a shade, preventing light from one direction from striking the lens cell. That's all it takes.


I lied! That isn't a minimal directional eye at all: here it is.


This rather blew my mind. The brachiopod gastrula senses light. The figure above is of a very early stage in development, when the organism is little more than a couple of sheets of cells with no organs at all, only tisses in the process of forming up into rough structures. It definitely has no brain, no nervous tissue at all, and no eyes…and there it is, that dark blue smear is a region selectively expressing ciliary opsin as if it were a retina. Furthermore, when tested behaviorally (mind blown again…behavior, in a gastrula), populations in a light box show a statistical tendency to drift into the light. Presumably, light stimulation of the opsin is coupled to the activity of cilia used for motility in the outer epithelium of the embryo.

Amazing. It suggests how eyes evolved in multicellular organisms, as well — initially, it was just localized general expression of light-sensitive molecules coupled directly to motors in the skin, no brain required.

Passamaneck Y, Furchheim N, Hejnol A, Martindale MQ, Lüter C (2011) Ciliary photoreceptors in the cerebral eyes of a protostome larva. EvoDevo, 2:6.


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